Stud Mycol. 2015 Sep; 82: 23–74.
Published online 2015 Nov 18. doi: 10.1016/j.simyco.2015.10.001
PMCID: PMC4774271
This article has been cited by other articles in PMC.
Abstract
The genus Cladosporium (Cladosporiaceae, Dothideomycetes),
which represents one of the largest genera of dematiaceous
hyphomycetes, has been intensively investigated during the past decade.
In the process, three major species complexes (C. cladosporioides, C. herbarum and C. sphaerospermum) were resolved based on morphology and DNA phylogeny, and a monographic revision of the genus (s. lat.) published reflecting the current taxonomic status quo.
In the present study a further 19 new species are described based on
phylogenetic characters (nuclear ribosomal RNA gene operon, including
the internal transcribed spacer regions ITS1 and ITS2, as well as
partial actin and translation elongation factor 1-α gene sequences) and
morphological differences. For a selection of the species with
ornamented conidia, scanning electron microscopic photos were prepared
to illustrate the different types of surface ornamentation.
Surprisingly, during this study Cladosporium ramotenellum was
found to be a quite common saprobic species, being widely distributed
and occurring on various substrates. Therefore, an emended species
description is provided. Furthermore, the host range and distribution
data for several previously described species are also expanded.
Key words: Cladosporiaceae, Emendation, Phylogeny, Taxonomic novelties, Taxonomy
Taxonomic novelties: New species: Cladosporium aciculare Bensch, Crous & U. Braun, C. aggregatocicatricatum Bensch, Crous & U. Braun, C. angustiherbarum Bensch, Crous & U. Braun, C. angustiterminale Bensch, Crous & U. Braun, C. austroafricanum Bensch, Crous & U. Braun, C. austrohemisphaericum Bensch, Crous & U. Braun, C. ipereniae Bensch, Crous & U. Braun, C. limoniforme Bensch, Crous & U. Braun, C. longicatenatum Bensch, Crous & U. Braun, C. longissimum Bensch, Crous & U. Braun, C. montecillanum Bensch, Crous & U. Braun, C. parapenidielloides Bensch, Crous & U. Braun, C. penidielloides Bensch, Crous & U. Braun, C. pseudochalastosporoides Bensch, Crous & U. Braun, C. puyae Bensch, Crous & U. Braun, C. rhusicola Bensch, Crous & U. Braun, C. ruguloflabelliforme Bensch, Crous & U. Braun, C. rugulovarians Bensch, Crous & U. Braun, C. versiforme Bensch, Crous & U. Braun
Introduction
Members of the genus Cladosporium
are dematiaceous hyphomycetes characterised by a unique coronate
structure of the conidiogenous loci and conidial hila, consisting of a
central convex dome surrounded by a raised periclinal rim (David 1997). The genus belongs in a separate family, the Cladosporiaceae, which is a sister family to Mycosphaerellaceae and Teratosphaeriaceae, residing in the Capnodiales (Dothideomycetes) (Schoch et al., 2006, Schoch et al., 2009a, Schoch et al., 2009b, Crous et al., 2009b, Quaedvlieg et al., 2014). Based on comprehensive revisions of numerous cladosporioid genera, Cladosporium
is now both phylogenetically and morphologically defined and delimited
against numerous morphologically similar but distinct genera to which
various excluded former Cladosporium species have been reallocated (Crous et al., 2006, Crous et al., 2007a, Schubert et al., 2007a, Braun et al., 2008). Furthermore, a polyphasic approach was undertaken to establish species entities in the three major species complexes within Cladosporium, viz. C. herbarum s. lat., C. sphaerospermum s. lat. and C. cladosporioides s. lat. (Zalar et al., 2007, Schubert et al., 2007b, Bensch et al., 2010).
A surprising result of these studies was the high diversity of species
and genotypes that exist in nature in formerly accepted, morphologically
defined species. Most recently, a monographic revision of Cladosporium s. lat. has been published, comprising about 170 true Cladosporium species and reflecting the current status quo (Bensch et al. 2012).
However, examination of the diversity, phylogeny and taxonomy of Cladosporium
on various host substrates from different geographical regions is still
ongoing, and the present paper represents an additional contribution
highlighting the huge biodiversity in Cladosporium. A
multilocus DNA sequence typing approach, employing three loci (the
internal transcribed spacers of the rDNA genes (ITS), and partial actin
and translation elongation factor 1-α gene sequences), as well as
morphological examinations and cultural characteristics were used for
the identification and delimitation of several new species.
Material and methods
Isolates
Isolates
included in this study were obtained from the culture collection of the
Centraalbureau voor Schimmelcultures (CBS-KNAW Fungal Biodiversity
Centre), Utrecht, Netherlands, and from several other collections (Table 1),
or were freshly isolated from a range of different substrates and
placed in the working collection of Pedro Crous (CPC), housed at CBS.
Single-conidial isolates were obtained using techniques outlined in Crous et al. (1991).
Isolates were inoculated onto 2 % potato-dextrose agar (PDA), synthetic
nutrient-poor agar (SNA), 2 % malt extract agar (MEA) and oatmeal agar
(OA) (Crous et al. 2009c),
and incubated under continuous near-ultraviolet light at 25 °C to
promote sporulation. All cultures in this study are maintained at the
CBS (Table 1). Nomenclatural novelties and descriptions were deposited in MycoBank (www.MycoBank.org; Crous et al. 2004).
Cladosporium isolates included for sequence and morphological analyses.
DNA isolation, amplification and sequence analysis
Fungal colonies were established on agar plates, and genomic DNA was isolated as described in Groenewald et al. (2013).
DNA amplification of the internal transcribed spacer regions and
intervening 5.8S rRNA gene (ITS) of the nrDNA cistron, partial actin (act) and translation elongation factor 1-alpha (tef1) followed Groenewald et al., 2005, Groenewald et al., 2013.
Representative isolates and / or species were selected from the NCBI
nucleotide database mainly based on degree of nucleotide similarity and /
or morphological similarity to the strains examined in this study.
Phylogenetic analyses consisted of parsimony analyses of an alignment
representing the C. cladosporioides complex and a separate alignment for the combined C. herbarum / sphaerospermum complexes. The analyses were performed as described by Lombard et al. (2014). Novel sequences were deposited in NCBI's GenBank nucleotide database (Table 1) and the alignments and trees in TreeBASE (study accession number S18262).
Morphology
Light
microscopy (LM). Microscopic observations of isolates were made from
colonies cultivated for 7 d under continuous nearultraviolet light at
25 °C on SNA. Preparations were mounted in Shear's solution (Crous et al. 2009c).
To study conidial development and branching patterns of conidial
chains, squares of transparent adhesive tape (Titan Ultra Clear Tape,
Conglom Inc., Toronto, Canada) were placed on conidiophores growing in
the zone between the colony margin and 2 cm inwards, and mounted between
two drops of Shear's solution under a glass cover slip. Conidial
terminology follows Schubert et al. (2007b) and Bensch et al. (2012)
where the different types of conidia are shown and discussed. Wherever
possible, 50 measurements (× 1 000 magnification, differential
interference contrast microscopy, Zeiss Axioscope 2 PLUS) were made of
conidia with outliers given in parentheses. Average values and standard
deviations are also listed. Photographic images were captured with a
Zeiss Axio Imager 2 light microscope using differential interference
contrast (DIC) illumination and an AxioCam MRc5 camera and ZEN software.
For cultural characteristics, colonies were cultivated on PDA, SNA, OA
and MEA for 14 d at 25 °C in the dark, after which the surface and
reverse colours were rated using the charts of Rayner (1970).
Low-temperature scanning electron microscopy (SEM)
Isolates of Cladosporium
spp. were grown on SNA with 30 g agar/L for 3–4 d at room temperature
under black light. Relevant parts of the small colonies with
conidiophores and conidia were selected under a binocular, excised with a
surgical blade as small agar (3 × 3 mm) blocks, and transferred to a
copper cup for snap-freezing in nitrogen slush. To prevent disruption of
the intricate structure of the conidiophores by liquid nitrogen, a
piece of Scotch tape was placed lightly over the opening of the copper
cup. Agar blocks were glued to the copper surface with frozen tissue
medium (KP-Cryoblock, Klinipath, Duiven, Netherlands) mixed with 1 part
colloidal graphite (Agar Scientific, Stansted, UK). Samples were
examined in a JEOL 5600LV scanning electron microscope (JEOL, Tokyo,
Japan) equipped with an Oxford CT1500 Cryostation for cryo-electron
microscopy (cryoSEM). Electron micrographs were acquired from uncoated
frozen samples, or after sputter-coating by means of a gold target for
three times during 30 s. Micrographs of uncoated samples were taken at
an acceleration voltage of 3 kV, and consisted out of 30 averaged fast
scans (SCAN 2 mode), and at 5 kV in case of the coated samples (PHOTO
mode).
Results
DNA phylogeny
To
simplify layout of the trees and to maximise the quality of the
alignment, two separate alignments were created: one alignment
representing the C. cladosporioides complex and the other the combined C. herbarum / sphaerospermum
complexes. Novel sequences generated in this study were added to
sequences deposited in the NCBI's GenBank nucleotide database (mainly
representing the data from Schubert et al., 2007b, Zalar et al., 2007, and Bensch et al., 2010, Bensch et al., 2012).
The manually adjusted alignment of the C. cladosporioides
complex contained 120 sequences (including the outgroup sequence) and
the three loci were represented by a total of 957 characters (ITS: 493, tef1: 261, act:
203) including alignment gaps, which were used in the analysis. Of the
957 characters, 292 were parsimony-informative (ITS: 11, tef1: 179, act: 102), 188 were variable and parsimony-uninformative (ITS: 122, tef1: 40, act: 26), and 477 were constant (ITS: 360, tef1: 42, act:
75). Ninety-six equally most parsimonious trees (TL = 2 202 steps;
CI = 0.415; RI = 0.784; RC = 0.325), the first of which is shown in Fig. 1,
were obtained from the parsimony analysis of the combined genes. The
ITS sequences were the least successful in resolving species with only
three out of the 44 species resolved, followed by tef1 with 38 out of 44 species and act being slightly more suitable with 39 out of 44 species (data not shown, single gene trees available in TreeBASE).
The
first of 96 equally most parsimonious trees obtained from a heuristic
search with 100 random taxon additions of the combined ITS, tef1 and act sequence alignment of the cladosporioides complex using PAUP v. 4.0b10. The scale bar shows 20 changes, ...
The manually adjusted alignment of the C. herbarum / sphaerospermum
complexes contained 112 sequences (including the outgroup sequence) and
the three loci were represented by a total of 965 characters (ITS: 496,
tef1: 270, act: 199) including alignment gaps which
were used in the analysis. Of the 965 characters, 406 were
parsimony-informative (ITS: 79, tef1: 206, act: 121), 146 were variable and parsimony-uninformative (ITS: 89, tef1: 28, act: 29), and 413 were constant (ITS: 328, tef1: 36, act:
49). One thousand equally most parsimonious trees (TL = 2 535 steps;
CI = 0.453; RI = 0.825; RC = 0.374), the first of which is shown in Fig. 2, were obtained from the parsimony analysis of the combined genes. In the sphaerospermum complex (as delimited in Fig. 2), the ITS sequences were the least successful in resolving species with only 10 out of the 14 species resolved, followed by act with 13 out of 14 species and tef1 being slightly more suitable in resolving all species (data not shown, single gene trees available in TreeBASE). In the herbarum complex (as delimited in Fig. 2), the ITS sequences were the least successful in resolving species with only three out of the 19 species resolved, followed by tef1 with 18 out of 19 species and act being slightly more suitable in resolving all species (data not shown, single gene trees available in TreeBASE).
The
first of 1 000 equally most parsimonious trees obtained from a
heuristic search with 100 random taxon additions of the combined ITS, tef1 and act sequence alignment of the herbarum / sphaerospermum complexes using PAUP v. 4.0b10. The scale ...
Taxonomy
The
status of numerous unidentified isolates included in this study was
resolved, which revealed several novel species. The circumscriptions and
delimitations of these species are mainly based on quantitative as well
as qualitative morphological features and on molecular data. Features
that proved to be diagnostic at species rank were discussed in Bensch et al. (2012)
and have been also applied here. The new taxa are treated in
alphabetical order below. Detailed descriptions, illustrations and
comments as well as the species complex they are belonging to, are
given. Additional comments on species complexes are further provided in
the Discussion.
Some previously described species, for which updated information on
species concept, host range and / or geographic distribution are
available, are also included.
Cladosporium aciculare
(CBS 140488). A–C. Conidiophores and conidial chains. D–F. Tip of
conidiophores and numerous conidia. G. Ramoconidium and conidia. Scale
bars = 10 μm.
Etymology:
Named after the typical form of the conidiophores being acicular,
needle-shaped, with a broader base and pointed towards the apex.
Mycelium
sparingly formed, short cylindrical, usually unbranched, 2–4.5 μm wide,
sometimes swollen up to 6 μm, with swellings and constrictions, pale to
often medium olivaceous-brown, sometimes subhyaline, smooth or
asperulate, sometimes verruculose towards the base of conidiophores,
walls slightly thickened. Conidiophores macro- or
semimacronematous, solitary or in loose groups of up to three arising
terminally or laterally from hyphae, sometimes as short and narrow
lateral prolongations, about 1.5 μm wide, straight or somewhat flexuous,
neither nodulose nor geniculate, but usually subuliforme, awl-like with
a wider base, 3–4 μm, and slightly to distinctly attenuated towards the
apex, (1.5–)2–2.5(–3) μm, 28–250 μm long, usually unbranched,
multiseptate, not constricted, pale to medium olivaceous-brown, paler
towards the apex, micronematous ones subhyaline, smooth or almost so,
sometimes asperulate, walls slightly thickened. Conidiogenous cells
integrated, mainly terminal, often seceding as ramoconidia,
cylindrical, 15–40 μm long, with 2–4(–5) distal conidiogenous loci
crowded at the outermost apex, loci subdenticulate, (0.8–)1–1.5 μm diam,
thickened and darkened-refractive. Ramoconidia commonly
formed, narrowly cylindrical, 22–40 × 2–2.5 μm, 0(–1)-septate, pale
olivaceous, walls unthickened, base about 2(–3) μm wide, not attenuated
towards the base, sometimes hardly distinguishable from secondary
ramoconidia. Conidia numerous, catenate, branching in all
directions, 1–3(–5) conidia in the terminal unbranched part of the
chain; small terminal conidia obovoid, ellipsoid, 3–4 × (1.5–)1.8–2 μm
[av. (± SD) 3.6 (± 0.4) × 1.9 (± 0.2)], aseptate, distinctly attenuated
towards the base; intercalary conidia ellipsoid to fusiform,
4–10 × 2–2.5 μm [av. (± SD) 6.5 (± 2.0) × 2.2 (± 0.2)], aseptate, with
1–3 distal hila, attenuated towards apex and base; secondary ramoconidia
ellipsoid or cylindrical, 5–18(–23) × 2–2.5(–3) μm [av. (± SD) 12.8 (±
5.0) × 2.3 (± 0.3)], 0–1-septate, with 2–4(–5) distal hila, subhyaline
or pale olivaceous-brown, smooth or almost so, walls unthickened, hila
protuberant, conspicuous, subdenticulate, 0.5–1.5 μm diam, thickened and
darkened-refractive; microcyclic conidiogenesis not occurring.
Culture characteristics:
Colonies on PDA attaining 38–57 mm after 14 d, olivaceous-grey to
iron-grey, grey-olivaceous towards margins, reverse olivaceous-black,
velvety to fluffy; margins white, somewhat feathery, narrow, regular,
aerial mycelium loose, diffuse to more dense in some spots, fluffy,
growth flat, without prominent exudates, sporulation profuse. Colonies
on MEA reaching 34–47 mm, glaucous-grey to pale greenish grey,
grey-olivaceous due to profuse sporulation, olivaceous-black towards
margin, reverse iron-grey to greenish black, powdery to fluffy, margins
white, narrow, somewhat feathery, regular, aerial mycelium fluffy,
dense, glaucous-grey, high, covering large parts of the colony, growth
low convex. Colonies on OA attaining 40–53 mm, pale greenish grey,
iron-grey at margins, olivaceous due to abundant sporulation, reverse
leaden-grey to leaden-black, powdery to fluffy, margins regular,
glabrous, aerial mycelium loose, diffuse to loosely fluffy, high, growth
flat.
Specimen examined: Australia, New South Wales, North Washpool State Forest, isol. from Syzygium corynanthum (Myrtaceae), 1 Mar. 2009, P.W. Crous (CBS H-22359, holotype; ex-type culture CBS 140488 = CPC 16547).
Substrate and distribution: On Syzygium; Australia.
Notes: Cladosporium aciculare clusters with species belonging to the sphaerospermum
species complex, even in the clade of the eponymous species, but the
conidial shape departs from the globose to subglobose shape typical for
members of the sphaerospermum species complex. Phylogenetically it is allied to C. fusiforme (Fig. 2) but the shape and length of conidiophores and width of conidia are quite different from that species (Zalar et al., 2007, Bensch et al., 2012).
Its morphology reminds one of C. subuliforme, a species isolated from an Arecaceae in Thailand and belonging to the cladosporioides species complex (Bensch et al. 2010).
The conidia of the latter species are somewhat longer and wider [[small
terminal conidia 2.5–4.5(–5.5) × 2–2.5 μm, intercalary conidia
5.5–12(–13) × 2–3(–3.5) μm, secondary ramoconidia
(6–)8–25(–28) × 2–3(–3.5) μm] and the conidiophores are longer (up to
330 μm long) having a wider swollen base up to 8(–10) μm wide].
Cladosporium aggregatocicatricatum Bensch, Crous & U. Braun, sp. nov. MycoBank MB814622. Fig. 4, Fig. 5.
Cladosporium aggregatocicatricatum
(CBS 140493). A–B, D, F. Conidiophores and conidia. C, E. Macronematous
conidiophores with conidiogenous loci situated at about the same level
on lateral prolongations or round about the stalk at about the same ...
Cladosporium aggregatocicatricatum
(CBS 140493). A. Part of a colony showing substrate hyphae, aerial
hyphae and sparse elongated conidiophores. B–D. Conidiophores with
conidial chains. Note the highly elongated secondary ramoconidia in (B)
with ...
Etymology:
Name refers to the conidiogenous zone of the conidi-ophores with
conidiogenous loci often being crowded and situated at about the same
level on lateral prolongations or round about the stalk at the same
height (see Fig. 4C, E, G).
Mycelium
unbranched or sparingly branched forming long ropes, infertile hyphae
0.5–1.5 μm wide, subhyaline to pale olivaceous-brown, septate, smooth or
asperulate, fertile hyphae 2–3 μm wide, pale to medium
olivaceous-brown, multiseptate, verruculose or irregularly rough-walled,
granulate, walls unthickened or almost so. Conidiophores
solitary, macronematous, occasionally micronematous, arising from
plagiotropous or ascending hyphae, narrowly cylindrical-oblong, once or
several times slightly to distinctly, loosely to densely
geniculate-sinuous or subnodulose with unilateral swellings or lateral
prolongations, after Conidi-ogenous growth sometimes continuing in a
30–45° angle, unbranched, occasionally branched, 30–550 μm long or even
longer, 2–3.5(–4) μm wide, multiseptate, pale to medium
olivaceous-brown, often somewhat paler towards the apex, smooth,
asperulate or verruculose, walls unthickened or slightly thickened. Micronematous conidiophores short, narrow, pale olivaceous, with a single terminal conidiogenous locus. Conidiogenous cells
integrated, terminal and intercalary, intercalary cells often separated
by non-conidiogenous cells, cylindrical, up to 70 μm long, slightly to
distinctly geniculate, sometimes several geniculations in short
succession, loci often situated at about the same level on lateral
prolongations or round about the stalk at the same height or subnodulose
with loci formed on lateral shoulders, with 1–6 loci per cell, loci
crowded, sometimes forming sympodial clusters of pronounced scars,
subdenticulate, 1–2 μm diam, thickened and darkened-refractive. Ramoconidia occasionally formed. Conidia
catenate, in short branched chains with 1–2 conidia in the terminal
unbranched part of the chain, small terminal conidia subglobose, obovoid
to ellipsoid, apex rounded, often with an additional hilum near the
base, (3–)4–8 × 3–3.5(–4.5) μm [av. (± SD) 5.3 (± 1.4) × 3.0 (± 0.6)],
aseptate, intercalary conidia ovoid, ellipsoid, 6.5–15 × (3–)3.5–4 μm
[av. (± SD) 10.0 (± 2.8) × 3.3 (± 0.4)], 0–1-septate, septa often not
very conspicuous, with 1–3(–4) distal scars, secondary ramoconidia
ellipsoid to subcylindrical, 11–27 × (3–)3.5–4.5 μm [av. (± SD) 17.1 (±
5.1) × 3.5 (± 0.5)], 0–2(–3)-septate, with (1–)2–4(–5) distal scars,
attenuated towards apex and base, pale olivaceous-brown, verruculose to
short spinulose, spines up to 0.5 μm high, walls more or less
unthickened, hila conspicuous, subdenticulate, 0.5–2 μm diam, thickened
and darkened-refractive; microcyclic conidiogenesis occurring forming
secondary conidiophores.
In vivo (on Asteriscus sericeus): Conidiophores
cylindrical-oblong, subnodulose with small lateral shoulders, or
slightly geniculate-sinuous, sometimes once branched towards the apex,
very long, up to 425 μm or even longer, at the base about 7–8 μm wide,
slightly attenuated towards the apex and somewhat paler, 4–6.5 μm wide,
medium to dark brown at the base, almost smooth to often asperulate or
minutely verruculose, walls thickened, two-layered, 1–1.5 μm thick. Ramoconidia up to 54 μm long, aseptate, asperulate or slightly verruculose. Conidial chains
somewhat longer than in culture, small terminal conidia globose,
subglobose or obovoid, 3–5 × (2–)2.5–4 μm, almost smooth to irregularly
rough-walled, intercalary conidia 4.5–15 × 3–4.5(–5) μm, secondary
ramoconidia up to 25 μm long, 4–6 μm wide, occasionally swollen up to
8 μm, 0–2(–3)-septate, septa becoming sinuous with age, pale to medium
brown, almost smooth to asperulate or densely minutely verruculose;
microcyclic conidiogenesis occurring.
Culture characteristics:
Colonies on PDA reaching 53–63 mm after 14 d, pale olivaceous-grey to
olivaceous-grey, reverse iron-grey to olivaceous-black, floccose to
fluffy; margins grey-olivaceous, feathery, narrow; aerial mycelium
abundant, pale olivaceous-grey, fluffy to floccose; growth effuse with
somewhat elevated colony centre. Colonies on MEA attaining 41–45 mm,
grey-olivaceous, pale olivaceous-grey towards margins, reverse
iron-grey, velvety to floccose; margins white, feathery, narrow; aerial
mycelium sparse, smoke-grey, floccose; growth effuse. Colonies on OA
reaching up to 59 mm, grey-olivaceous, olivaceous-grey towards margins,
reverse olivaceous-grey, with pale greenish grey margins, velvety to
floccose; margins narrow, glabrous; aerial mycelium floccose, loose;
growth effuse, flat; without prominent exudates, sporulation profuse.
Specimens examined: Germany, Nordrhein-Westfalen, Essen, isol. from Asteriscus sericeus (Asteraceae), 10 Sep. 2006, coll. N. Ale-Agha, isol. P.W. Crous, CPC 13365–13367. Netherlands, isol. from tempeh, isol. by J.P.A. Stevense, CBS 284.84. New Zealand, contaminant on culture plate, 1 Aug. 2007, C.F. Hill (CBS H-22364, holotype; ex-type culture CBS 140493 = CPC 14709 = ICMP 170869). Slovenia, Sečovlje, 45.4767, 13.623, saltern, hypersaline water from precrystalisation pond, 2004, P. Zalar, CPC 12055 = EXF-2288. USA, isolated from grape berry, F.M. Dugan lab, CBS 113751.
Substrate and distribution:
On plant material, tempeh, fruits and hypersaline water; Australasia
(New Zealand), Europe (Germany, Netherlands, Slovenia), North America
(USA).
Notes: With its ornamented conidia and the geniculate subnodulose conidiophores this species belongs to the herbarum species complex. It resembles C. stanhopeae, a species described by Allescher (1895) from faded leaves of Stanhopea (Orchidaceae)
from the botanical garden in Munich. The latter species also possesses
quite long conidiophores with the conidiogenous loci often arranged at
about the same level (like a garland around the stalk) and very similar
conidial measurements (Bensch et al. 2012). However, we hesitate in using this name for the isolates cited above since C. stanhopeae is only known from the type specimen and none of the strains listed above were isolated from a host belonging to the Orchidaceae. Therefore, we prefer to introduce a new name. The conidiophores of C. aggregatocicatricatum are longer (both in vivo and in vitro) and somewhat wider than in C. stanhopeae.
Cladosporium allicinum (Fr.: Fr.) Bensch et al., Stud. Mycol. 72: 50. 2012.
Specimens examined: Bulgaria, Hubavene, isol. from bean, food, Jan. 2007, B.A. Andersen, CPC 14303 = BA 1702. France, Larnas, isol. from an unidentified tree, 21 Aug. 2007, P.W. Crous, CPC 14268. Germany, isol. from Robinia pseudoacacia (Fabaceae),
leaf on ground, 11 Jan. 2015, coll. R. Jarling & R. Schumacher,
isol. P.W. Crous, CPC 21906; Gerolstein, Roter Hecke, isol. from leaf
spot of Acer campestre (Sapindaceae), 1 Jul. 1992, H.A. van der Aa, CBS 420.92; Bavaria, Munich, park of Nymphenburg palace, isol. from aecia of Puccinia bromina subsp. symphyti-bromarum var. paucispora, 2006, K. Schubert, CPC 13146. Japan, isol. from unknown substrate by Kurata, CBS 188.53 = IFO 5267. Netherlands, isol. from sputum of man, CBS 160.59; Delft, isol. from metal, CBS 155.60; Nijmegen, isol. from Alnus glutinosa (Betulaceae), 2 Jun. 2009, W. Quadvlieg, CPC 16759; Rotterdam, isol. from frozen Phaseolus vulgaris (Fabaceae),
isol. by J.C. Mooi, CBS 121.47 = VTT D-76045; Zwolle, isol. from
outside air, 1 Jul. 2007, Applied and Industrial Mycology group at CBS,
CPC 14194. Senegal, Louga, from Arachis hypogaea (Fabaceae), 2011, M.P. Sarr, CPC 21646. South Africa, Western Cape Province, Fernkloof, isol. from Nivenia stokoei (Iridaceae), 4 May 2010, P.W. Crous, CPC 18260. Switzerland, Kt. Graubünden, Val Tuors, isol. from Centaurea rhapontica = Rhaponticum scariosum subsp. rhaponticum (Asteraceae), isol. by E. Müller on 21 Jul. 1953, CBS 374.53 = IMI 163999.
Cladosporium angustiherbarum (CBS 140479). A–G, I. Conidiophores and conidial chains. H. Tip of a conidiophore and ornamented conidia. Scale bars = 10 μm.
Cladosporium angustiherbarum
(CBS 140479). A. View on the agar surface showing conidiophores
sprouting from structures beneath the agar surface or arising from
aerial hyphae with conidial chains. B. Running hyphae with a number of
conidia. Note the visibility ...
Etymology: Name refers to its morphological similarity with C. herbarum but also to its narrower conidiophores and conidia.
Mycelium
loosely branched, 1–3(–5) μm wide, septate, subhyaline or pale
olivaceous-brown, smooth or verruculose, with constrictions and
swellings, walls unthickened. Conidiophores macro-, semimacro- and micronematous, arising terminally or laterally from hyphae, solitary, erect. Macronematous conidiophores
mostly arising laterally from hyphae, with a cylindrical stipe, towards
the apex once or several times subnodulose, sometimes in short
succession giving the upper part a knotty / gnarled appearance, or with
lateral prolongations or swollen shoulders, unbranched, occasionally
once branched, branchlets also with swellings,
5–60 × (2–)2.5–3.5(–4) μm, swellings 3–6.5 μm diam, septate, septa
neither constricted nor darkened, pale or medium olivaceous-brown,
smooth, walls somewhat thickened. Conidiogenous cells
integrated, mainly terminal, occasionally intercalary, nodulose, mostly
with a single swelling at the apex or per cell in intercalary ones, or
laterally prolongating and swollen at the apex or with few swellings and
lateral shoulders and geniculations in short succession with up to
seven loci crowded towards the apex, somewhat constricted at nodules,
cells 5–19 μm long, loci protuberant, subdenticulate, 1–1.5 μm diam. Micro- and semimacronematous conidiophores
commonly formed either as short lateral outgrowth of hyphae or filiform
and longer, maximum length ambiguous, often arising terminally from
hyphae, 3–100 μm long or even longer, 1–2 μm wide, mostly without
distinct swellings, multiseptate, some septa distinctly thickened and
darkened, smooth or minutely verruculose or verruculose, subhyaline or
pale olivaceous, walls unthickened. Conidiogenous cells integrated, terminal or intercalary, narrowly cylindrical or subnodulose, up to 22 μm long, with up to four loci per cell. Ramoconidia with a truncate, non-cladosporioid base (sensu Bensch et al. 2012) not observed. Conidia
catenate, in branched or short unbranched chains with up to 4(–5)
conidia in the terminal unbranched part of the chain, small terminal
conidia subglobose, obovoid or ellipsoid, occasionally globose,
(3.5–)4–9 × 3.5–4.5(–5) μm [av. (± SD) 6.1 (± 1.5) × 4.1 (± 0.5)],
aseptate, intercalary conidia limoniform, ellipsoid,
5–9 × (3.5–)4–4.5(–5) μm [av. (± SD) 7.5 (± 1.3) × 4.3 (± 0.4)],
0(–1)-septate, with 1(–2) distal hila, secondary ramoconidia ellipsoid
or subcylindrical, sometimes obclavate often formed by semimacronematous
conidiophores, (7–)8–21 × (3–)4–6(–6.5) μm [av. (± SD) 14.1 (±
4.8) × 5.1 (± 0.9)], obclavate ones up to 25 μm long and 4 μm wide,
0–1(–2)-septate, with 1–2(–3) distal hila, pale or medium
olivaceous-brown, minutely verruculose to verrucose, walls slightly
thick-walled, hila protuberant, 1–1.5 μm diam, thickened and
darkened-refractive; microcyclic conidiogenesis occurring, secondary
conidiophores up to 30 μm long.
Culture characteristics:
Colonies on PDA attaining 57–70 mm after 14 d, iron-grey,
olivaceous-grey towards margins, grey-olivaceous, reverse greyish blue
to iron-grey, fluffy; margin feathery; aerial mycelium loose, diffuse,
sometimes high and fluffy; growth flat, few prominent exudates formed,
sporulation profuse. Colonies on MEA reaching 58–63 mm, olivaceous,
iron-grey towards margins, reverse iron-grey, velvety; margin white,
feathery; aerial mycelium loose diffuse, rarely forming small white
fluffy patches; colony centre radially furrowed, wrinkled, without
prominent exudates, sporulation profuse. Colonies on OA attaining up to
65 mm, iron-grey, olivaceous due to sporulation, reverse leaden-grey to
iron-grey, velvety or felty; aerial mycelium loose diffuse to denser and
felty, mainly in colony centre, growth flat, without exudates.
Specimen examined: USA, Utah, Escalante National Monument, Grand Staircase, isol. from Pinus ponderosa (Pinaceae), Oct. 2009, coll. W. Quaedvlieg, isol. P.W. Crous (CBS H-22351, holotype; ex-type culture CBS 140479 = CPC 17814).
Notes: The conidia and conidiophores of this new species, which belongs to the herbarum species complex, remind one of C. herbarum but it differs in having shorter and narrower conidiophores as well as narrower conidia. Phylogenetically it is allied to C. phlei, albeit with low support, but morphologically C. phlei differs in having longer and wider conidiophores and conidia. Furthermore, the conidia in C. phlei are formed singly in vivo (in vitro solitary or in short chains).
There are three other species that have been reported from Argentina from the same host, Pinus ponderosa, namely C. pini-ponderosae, C. chubutense and C. cladosporioides s. lat. (Schubert et al., 2009, Bensch et al., 2010, Bensch et al., 2012). Cladosporium pini-ponderosae
can be readily distinguished by having wider, non-nodulose
conidiophores, longer and somewhat wider intercalary conidia and
secondary ramoconidia; C. chubutense forms subcylindrical ramoconidia, longer conidiophores and longer and somewhat narrower secondary ramoconidia; and C. cladosporioides has non-nodulose conidiophores as well as longer and smooth conidia.
Cladosporium angustiterminale
(CBS 140480). A–F. Conidiophores and conidial chains. G. Peculiar
conidiogenesis characterised by forming several conidiogenous loci at
about the same level, followed by continuing growth with narrower
conidiophores ...
Etymology:
Name refers to the peculiar conidiogenesis characterised by forming
several conidiogenous loci, followed by proliferated, narrower
conidiophores (Fig. 8G).
Mycelium sparse, branched, 1.5–3 μm wide, septate, subhyaline or pale olivaceous, smooth or often verruculose. Conidiophores
macronematous or semi-macronematous, cylindrical-oblong, non-nodulose,
geniculate-sinuous, occasionally continuing growth with up to an 90°
angle, unbranched or once branched, up to 175 μm long, 3–4.5(–5) μm
wide, semimacronematous conidiophores narrower, 2–2.5 μm wide,
multiseptate, usually 1–5-septate, pale olivaceous to medium
olivaceous-brown, smooth or almost so, occasionally asperulate or
minutely verruculose, especially towards the base, walls unthickened or
slightly thickened. Conidiogenous cells terminal and
intercalary, cylindrical, non-nodulose but often geniculate-sinuous at
or towards the apex, loci crowded at the apex and also at a lower level
forming clusters of pronounced scars, 2–5 conidiogenous loci formed at
about the same level, after conidiogenesis conidiophores can start
growing again with stalks often being narrower and at a higher level
additional loci may be formed, loci often situated at lateral shoulders
due to sympodial proliferation or displaced to the side of stalks, with
up to seven loci per cell, 12–25(–45) μm long, loci protuberant, 1–2 μm
diam, thickened and darkened-refractive. Ramoconidia commonly
formed, cylindrical-oblong, 19–35 × 2.5–4 μm, 0–1(–2)-septate, smooth,
with (2–)3–5 distal hila, base unthickened, 2.5–3 μm wide, somewhat
refractive, differentiation between ramoconidia and secondary
ramoconidia under light microscopy sometimes not evident. Conidia
catenate, in branched chains, branching in all directions, with 1–3
conidia in the terminal unbranched part of the chain, small terminal
conidia subglobose, obovoid or ellipsoid, 2.5–5 × 2–2.5 μm [av. (± SD)
3.7 (± 0.7) × 2.2 (± 0.2)], aseptate, apex rounded, intercalary conidia
ellipsoid or limoniform, 4–9.5(–13.5) × (2–)2.5–3(–3.5) μm [av. (± SD)
7.4 (± 2.7) × 2.9 (± 0.4)], aseptate, rarely 1-septate, with 1–3(–5)
distal hila, crowded at the distal end, (0.5–)0.8–1.2 μm diam, secondary
ramoconidia ellipsoid, subcylindrical or cylindrical,
(7–)8–25 × (2.5–)3–3.5(–4) μm [av. (± SD) 15.5 (± 6.1) × 3.4 (± 0.8)],
occasionally swollen up to 6.5 μm, 0–1-septate, septum median, pale
olivaceous or pale olivaceous-brown, smooth or almost so, walls
unthickened or only slightly thickened, with (2–)3–5(–6) hila at the
apex forming clusters of pronounced scars, 1–2(–2.5) μm diam,
subdenticulate, thickened and darkened-refractive.
Culture characteristics:
Colonies on PDA attaining 46–64 mm after 14 d, olivaceous-grey to pale
olivaceous-grey, grey-olivaceous towards margins, reverse
olivaceous-black, fluffy, margins white, somewhat feathery, broad,
aerial mycelium loose diffuse to denser and fluffy, growth flat.
Colonies on MEA reaching 37–47 mm, grey-olivaceous to olivaceous-grey,
sometimes pale olivaceous-grey at margins, reverse olivaceous-grey to
iron-grey, fluffy, margins white, somewhat feathery, aerial mycelium
fluffy, growth low convex, radially furrowed and folded. Colonies on OA
50–57 mm, olivaceous-grey to pale olivaceous-grey, reverse leaden-grey
to iron-grey, powdery to fluffy, margins crenate, glabrous, aerial
mycelium loose diffuse to fluffy, abundant, growth flat. Without
prominent exudates; sporulation profuse on all media.
Specimen examined: Australia, Western Australia, Augusta, isol. from Banksia grandis (Proteaceae), 2 Aug. 2008, coll. A.R. Wood, isol. P.W. Crous (CBS H-22352, holotype; ex-type culture CBS 140480 = CPC 15564).
Notes: This species, which belongs to the cladosporioides species complex (Fig. 1),
has an interesting conidiogenesis with conidiophores proliferating
after giving rise to conidia in being distinctly narrower or somewhat
constricted above the conidiogenous zone. In C. rectoides the
conidiophores sometimes also proceed to grow at an angle of 45–90° but
its ramoconidia, intercalary conidia and secondary ramoconidia are
longer than in C. angustiterminale.
Cladosporium asperulatum Bensch et al., Stud. Mycol. 67: 21. 2010.
Specimen examined: Mexico, Tlacotepec, isol. from seeds of Glycine max (Fabaceae), 16 Sep. 2008, coll. M. de Jesús Yáñez-Morales, isol. P.W. Crous, CPC 15614.
Notes: This Mexican isolate fits the species concept of Cladosporium asperulatum (Bensch et al. 2010),
but the conidia are mostly smooth or almost so, rarely asperulate, and
small terminal and intercalary conidia are somewhat narrower than
described in the type in being 1.5–2.5(–3) μm wide. Cladosporium asperulatum is thus far known from India and Portugal, and was isolated from hosts belonging to Myrtaceae and Proteaceae.
Cladosporium austroafricanum (CBS 140481). A–F. Conidiophores and conidial chains. G. Conidia. Scale bars = 10 μm.
Etymology: Name refers to the country of origin, South Africa.
Mycelium
loosely branched, (1–)2–5 μm wide, multiseptate, sometimes slightly
swollen, subhyaline, pale olivaceous to medium olivaceous-brown, densely
verruculose, sometimes almost smooth, walls unthickened or slightly
thick-walled, sometimes aggregated and forming loose hyphal
aggregations. Conidiophores macro- or semimacronematous, erect,
arising solitarily from hyphae or in loose groups from loose hyphal
aggregations, more or less straight, cylindrical-oblong, neither
nodulose nor geniculate, up to 210 μm long, 3–5 μm wide, mostly
unbranched, sometimes branched, when branched then branchlets often
quite long, multiseptate, sometimes slightly constricted at septa and
attenuated towards the base, pale olivaceous to medium olivaceous-brown,
smooth, walls unthickened or thickened; semimacronematous conidiophores
paler and narrower, about 2–2.5 μm wide. Conidiogenous cells
integrated, mainly terminal, cylindrical or cylindrical-oblong, mostly
neither nodulose nor geniculate, rarely geniculate-sinuous,
11–30(–45) μm long, usually with (1–)2–3 conspicuous loci at the
outermost apex, subdenticulate, 1–2.5 μm diam, thickened and
darkened-refractive. Ramoconidia occasionally formed, base 3–3.5 μm wide, unthickened or slightly thickened, somewhat refractive. Conidia
catenate, in branched chains, branching in all directions, with 1–4
conidia in the terminal unbranched part of the chain, small terminal
conidia obovoid or ellipsoid, 2.5–5 × (1.5–)2–2.5 μm [av. (± SD) 3.9 (±
0.7) × 2.1 (± 0.3)], intercalary conidia limoniform, ovoid or ellipsoid,
4–12 × 2–3(–3.5) μm [av. (± SD) 7.3 (± 2.7) × 2.7 (± 0.5)], aseptate,
with 1–4 distal hila, secondary ramoconidia ellipsoid, subcylindrical or
cylindrical-oblong, (8–)11–40 × (2.5–)3–4 μm [av. (± SD) 21.8 (±
9.9) × 3.4 (± 0.5)], 0–1(–2)-septate, septum median or often in the
upper half, somewhat darkened, with (2–)3–4(–6) distal hila, pale
olivaceous or olivaceous-brown, smooth, walls unthickened or almost so,
hila conspicuous, subdenticulate, 0.5–2.5 μm diam, thickened and
darkened-refractive; microcyclic conidiogenesis not occurring.
Culture characteristics:
Colonies on PDA attaining 70–83 mm after 14 d, smoke-grey to pale
olivaceous-grey, grey-olivaceous towards margins, reverse
olivaceous-black, fluffy to wooly-felty; margins feathery; aerial
mycelium abundant, covering almost the whole colony; growth flat;
several very small exudates formed. Colonies on MEA reaching 67–72 mm,
pale olivaceous-grey to smoke-grey, reverse olivaceous-grey, wooly-felty
or fluffy; margins white, glabrous and narrow; aerial mycelium
abundantly formed, covering large parts of the colony, dense; growth
flat, radially furrowed and somewhat folded or wrinkled, without
exudates. Colonies on OA attaining 60–68 mm, smoke-grey or white,
grey-olivaceous at margins, reverse leaden-grey to olivaceous-grey,
fluffy due to abundant, dense and high aerial mycelium; margins regular,
glabrous; without prominent exudates. Sporulation profuse on all media.
Specimen examined: South Africa,
Western Cape Province, Cape Town, next to M3 road, leaf litter, 2 Jun.
2009, coll. M. Gryzenhout, isol. P.W. Crous (CBS H-22349, holotype; ex-type culture CBS 140481 = CPC 16763).
Notes: Conidiophores and conidia resemble those of C. cladosporioides but the two species are phylogenetically distinct and in C. austroafricanum
the unbranched upper part of the conidial chain is much shorter with
only 1–4 conidia, its secondary ramoconidia are more frequently
1-septate and somewhat longer, and ramoconidia are only occasionally
formed.
Cladosporium austrohemisphaericum
(CBS 140482). A–F. Micro-, semimacro- and macronematous conidiophores
and conidial chains. G. Ramoconidium and conidia. H. Conidia. Scale
bars = 10 μm.
Etymology: From the Latin “auster” (= south) and “hemisphaerium”, referring to the Southern Hemisphere, the origin of this species.
Mycelium
immersed, sparingly branched, 1–4 μm wide, septate, subhyaline to very
pale olivaceous-brown, asperulate, minutely verruculose, verruculose or
even verrucose, walls unthickened, without any swellings and
constrictions. Conidiophores micro- to semimacronematous or
macronematous, arising terminally and laterally from erect or ascending
hyphae, erect, solitary, straight to flexuous, filiform to narrowly
cylindrical-oblong, sometimes once geniculate at or towards the apex,
unbranched or once branched, branches often only as short lateral
peg-like prolongations just below a septum,
20–135(–180) × (2–)2.5–3.5 μm, at the base up to 4.5 μm wide, septate,
often only with up to four not very conspicuous septa, sometimes
disarticulating at septa and forming ramoconidia and fragments,
subhyaline to pale or medium olivaceous-brown, minutely verruculose,
asperulate, sometimes verrucose or irregularly rough-walled especially
towards the base and almost smooth at or towards the apex, walls
unthickened or slightly thick-walled, slightly attenuating towards the
apex, sometimes conidiophores reduced to conidiogenous cells. Conidiogenous cells
integrated, mostly terminal, sometimes intercalary, filiform to
narrowly cylindrical-oblong, sometimes once geniculate, non-nodulose,
(6–)13–45(–60) μm long, with 1–3(–4) apical loci, conspicuous,
subdenticulate to denticulate, 1–2 μm diam, thickened
and darkened-refractive. Ramoconidia cylindrical-oblong,
12–36 × 2–3(–3.5) μm, 0–1(–2)-septate, subhyaline to pale
olivaceous-brown, almost smooth to asperulate or minutely verruculose,
base broadly truncate, 2–3 μm wide, neither thickened nor darkened. Conidia
numerous, catenate, formed in branched chains, branching in all
directions, in younger chains often dichotomously branched, 1–3 conidia
in the terminal unbranched part of the chain, small terminal conidia
globose, subglobose to obovoid or ovoid, 2–5(–7) × (1–)1.5–3 μm
(av. ± SD: 3.3 ± 1.0 × 2.1 ± 0.5), aseptate, subhyaline to pale or
medium olivaceous-brown, minutely verruculose to verruculose or
verrucose, hila 0.5–0.8 μm diam or narrower, intercalary conidia ovoid
to ellipsoid-ovoid, 4–11 × 2–3.5 μm (av. ± SD: 7.1 ± 2.1 × 2.6 ± 0.4),
0(–1)-septate, septa sometimes not very conspicuous, surface
ornamentation as in small terminal conidia, rounded or only very
slightly attenuated towards the ends, with 2–4 distal hila, 0.5–1 μm
diam, secondary ramoconidia ellipsoid to subcylindrical,
(8–)10–27(–30) × 2–3.5(–4) μm (av. ± SD: 18.5 ± 6.2 × 2.9 ± 0.4),
0–1(–2)-septate, with age constricted at septa, septum median or in the
upper half, 1–3(–4) distal hila, subhyaline to pale olivaceous-brown,
almost smooth to loosely verruculose or irregularly rough-walled, not or
only slightly attenuated towards apex and base, hila conspicuous,
subdenticulate, 1–2 μm diam, thickened and darkened-refractive;
microcyclic conidiogenesis not occurring.
Culture characteristics:
Colonies on PDA attaining 35–45 mm after 14 d, grey-olivaceous to dull
green or iron-grey, reverse greyish blue to olivaceous-black, velvety to
powdery, margin white, narrow, glabrous to feathery, regular, aerial
mycelium absent or sparse, loose, diffuse, growth flat or low convex,
without prominent exudates, sporulation profuse. Colonies on MEA
reaching 26–44 mm, grey-olivaceous to greenish grey or glaucous-grey at
margins, paler in the centre, reverse olivaceous to olivaceous-grey or
iron-grey, velvety to powdery, margin white, very narrow, feathery,
radially furrowed, growth flat to low convex with slightly elevated
colony centre, wrinkled and folded, few prominent exudates formed,
sporulation profuse. Colonies on OA attaining 26–34 mm, grey-olivaceous
or iron-grey, smoke-grey due to abundant sporulation, reverse
leaden-grey to leaden-black, powdery, margin white, very narrow,
glabrous, slightly undulate, aerial mycelium absent or diffuse, without
prominent exudates.
Specimens examined: Australia, Queensland, Brisbane, Brisbane Botanical Garden, isol. from Musa sp. (Musaceae), 14 Jul. 2009, P.W. Crous, CPC 17029. South Africa, Western Cape Province, Betty's bay, isol. from Cussonia thyrsiflora (Araliaceae), 14 Jan. 2009, P.W. Crous, CPC 16250. New Zealand, Auckland, Morrin Reserve, −37.00, 175.00, isolated from black mould on the surface of a fruit of Lagunaria patersonia (Malvaceae), 18 Apr. 2005, C.F. Hill, Hill 1163 (CBS H-22350, holotype; ex-type culture CBS 140482 = CPC 12068).
Substrate and distribution: On plant material and fruits of different hosts; Australasia (Australia, New Zealand), South Africa.
Notes: With its ornamented globose, subglobose or ovoid terminal conidia and the non-nodulose conidiophores C. austrohemisphaericum belongs to the sphaerospermum species complex but doesn't cluster with C. sphaerospermum, the eponymous species. Both morphologically and phylogenetically it is allied to C. langeronii and C. psychrotolerans which form a separate clade distant from C. sphaerospermum. However, C. langeronii
differs in having usually shorter and wider ramoconidia,
(10–)11–22(–42) × (3–)3.5–4.5(–5) μm, wider and darker, often medium or
dark brown conidia; and C. psychrotolerans deviates in having
longer and wider ramoconidia, 19–43(–47) × (2–)3–4(–4.5) μm, and smooth
or minutely verruculose conidia. Conidial measurements of C. dominicanum are also similar but ramoconidia are rarely formed in that species and its conidia are smooth or almost so (Zalar et al., 2007, Bensch et al., 2012).
Cladosporium cladosporioides (Fresen.) G.A. de Vries, Contr. Knowl. Genus Cladosporium: 57. 1952.
Specimens examined: Mexico,
Mexico State, forest garden, isol. from pine needles plus insects, 22
Mar. 2010, coll. M. de Jesús Yáñez-Morales, isol. P.W. Crous, CPC 18138;
Montecillo, isol. from a wild plant, 1 Oct. 2008, coll. M. de Jesús
Yáñez-Morales, isol. P.W. Crous, CPC 15626; Tlacotepec, isol. from Rumex sp. (Polygonaceae),
22 Sep. 2008, coll. M. de Jesús Yáñez-Morales, isol. P.W. Crous, CPC
15610; isol. from a wild tree, 16 Sep. 2008, coll. M. de Jesús
Yáñez-Morales, isol. P.W. Crous, CPC 15615.
Cladosporium delicatulum Cooke, Grevillea 5: 17. 1876.
Specimen examined: Mexico, Tlacotepec, isol. from Juglans regia (Juglandaceae), 16 Sep. 2008, coll. M. de Jesús Yáñez-Morales, isol. P.W. Crous, CPC 15612.
Notes: Conidiophores, ramoconidia and conidia of the Mexican isolate fit the species concept of C. delicatulum very well (Bensch et al. 2010). It is the first record of this species for Mexico.
Cladosporium dominicanum Zalar et al., Stud. Mycol. 58: 169. 2007.
Specimens examined: Philippines, isol. from Dracaena fragrans (Asparagaceae), 2008, coll. C.J.R. Cumagun, isol. P.W. Crous, CPC 15932. Taiwan, FIRDI campus, isol. from unknown vine, 17 Dec. 2011, P.W. Crous, CPC 20109.
Notes: Until now Cladosporium dominicanum
has been isolated from fruit surfaces and hypersaline waters in
(sub)tropical climates of Asia (Iran) and Central America (Dominican
Republic) (Zalar et al., 2007, Bensch et al., 2012). With these two isolates it is now also reported from the Philippines and Taiwan.
Cladosporium gamsianum Bensch et al., Stud. Mycol. 67: 49. 2010.
Specimen examined: Mexico, South region, Tamanlipas, isol. from soybean seeds (Glycine max, Fabaceae), 1 Dec. 2007, coll. M. de Jesús Yáñez-Morales, isol. P.W. Crous, CPC 15617.
Notes: The morphology of this Mexican isolate fits the species concept of C. gamsianum.
The conidiophores with the typical annellations at the apex are formed
solitarily or fasciculate with up to four conidiophores in small
fascicles. They are smooth to asperulate. The conidia, especially
secondary ramoconidia, are somewhat longer [10–20 × 2.5–3(–3.5) μm,
0–1-septate], with up to five conidia in the terminal unbranched part of
the conidial chains.
Until now C. gamsianum
was only known from the type locality in South Africa. This is the first
record from Mexico, where it was also isolated from a new host, which
implies that C. gamsianum may probably be more widely distributed.
Cladosporium inversicolor Bensch et al., Stud. Mycol. 67: 55. 2010.
Specimen examined: South Africa, Cape, Kirstenbosch Botanical Garden, isol. from Freylinia lanceolata (Scrophulariaceae), 8 May 2010, P.W. Crous, CPC 18238.
Note: Previously reported from Europe, North and South America, the species is now also recorded from South Africa.
Cladosporium ipereniae
(CBS 140483). A–D. Unbranched or branched macronematous conidiophores
and conidial chains. E–G. Tip of conidiophores and conidia with variable
surface ornamentation. Scale bars = 10 μm. ...
Cladosporium ipereniae
(CBS 140483). A. Overview of conidiophores and hyphae. B, D.
Conidiophores arising from plagiotropous hyphae or sprouting from
structures beneath the agar surface with conidial chains. C. Branched
conidiophore arising from a plagiotropous ...
Etymology:
Named after Arien van Iperen, technician at the Centraalbureau voor
Schimmelcultures, who collected the type specimen, and for her valuable
work on maintaining the numerous Cladosporium isolates.
Mycelium
loosely branched, 1.5–5 μm wide, multiseptate, subhyaline to medium
olivaceous-brown, smooth, verruculose or irregularly rough-walled,
unthickened or somewhat thickened, sometimes aggregated forming ropes of
several hyphae or loose stromatic hyphal aggregations of swollen cells,
swollen cells 6–9 μm diam, sometimes only a single cell distinctly
swollen at the base of conidiophore. Conidiophores macro- and
micronematous; macronematous ones solitary, in pairs of two or loosely
fasciculate with 3–6 conidiophores in a fascicle, arising terminally or
laterally from hyphae or from swollen hyphal cells or from small
stromatic hyphal aggregations, subcylindrical or cylindrical, slightly
attenuated towards the apex, unbranched, occasionally once or twice
branched, non-nodulose, occasionally once geniculate-sinuous at the
apex, (10–)35–85 μm long, 2.5–3.5 μm wide at the apex, 3.5–4.5(–5) μm
towards or at the base, 1–3-septate, slightly constricted at septa, pale
or medium olivaceous or olivaceous-brown, smooth or almost so,
sometimes verruculose or irregularly rough-walled, especially towards
the base, walls slightly thickened. Micronematous conidiophores subhyaline or pale olivaceous, narrower, 2–3 μm wide. Conidi-ogenous cells
integrated, terminal, occasionally intercalary, non-nodulose, sometimes
once geniculate at the apex, 11–35 μm long, with (1–)2–4 distal scars,
mostly crowded at the outermost apex, loci conspicuous, subdenticulate,
1–1.5 μm diam, thickened and darkened-refractive. Ramoconidia rarely formed. Conidia
catenate, branching in all directions or dichotomously branched,
1–4(–5) conidia in the terminal unbranched part of the chain; small
terminal conidia subglobose, obovoid, (2.5–)3–4(–5) × (2–)2.5–3(–3.5) μm
[av. (± SD) 3.5 (± 0.7) × 2.6 (± 0.4)], apex broadly rounded,
distinctly attenuated towards the base, intercalary conidia ovoid,
limoniform or ellipsoid, (4–)4.5–8(–10) × (2–)2.5–3.5 μm [av. (± SD) 6.1
(± 1.7) × 3.0 (± 0.4)], aseptate, with 1–2(–4) distal hila, attenuated
towards apex and base, secondary ramoconidia ellipsoid or
subcylindrical, (5–)6.5–18(–22) × 2.5–3.5(–4.5) μm [av. (± SD) 11.7 (±
4.1) × 3.1 (± 0.4)], aseptate, rarely 1-septate, pale olivaceous-brown
or subhyaline, surface ornamentation variable, lightmicroscopically
smooth or almost so or often loosely verruculose or sometimes verrucose
or irregularly rough-walled, under SEM delicately ornamented showing a
somewhat irregularly reticulate surface or slightly to distinctly
embossed stripes probably caused by diminishing turgor and shriveling of
tender young conidia, walls unthickened or slightly thickened, usually
with 3 distal hila, hila subdenticulate, 0.5–1.5(–1.8) μm diam,
thickened and darkened-refractive. Microcyclic conidiogenesis usually
not occurring, but intercalary and small terminal conidia especially
those formed by micronematous conidiophores germinating or rostrate.
Culture characteristics:
Colonies on PDA reaching 10–44 mm after 14 d, iron-grey to
olivaceous-black, reverse olivaceous-black, velvety or powdery; margins
narrow, white, glabrous or feathery, regular, aerial mycelium pale
olivaceous-grey, loose to dense, wooly-felty, covering larger parts,
mainly in colony centre, growth flat, forming numerous small to large
exudates. Colonies on MEA reaching 28–35 mm, greenish grey,
glaucous-grey at margins, pale olivaceous-grey due to aerial mycelium,
reverse olivaceous-grey, velvety to wooly, margins white, narrow,
regular, glabrous, aerial mycelium forming some dense patches in colony
centre, growth flat but radially furrowed or wrinkled and folded,
without exudates. Colonies on OA attaining 24–33 mm, olivaceous-grey to
iron-grey, with patches of white due to dense wooly aerial mycelium,
reverse leaden-grey to iron-grey, margins glabrous, regular, growth
flat, without exudates; sporulation profuse on all media.
Specimens examined: Chile, La Serrana, isol. from Puya sp. (Bromeliaceae), 7 Dec. 2008, coll. A. van Iperen, isol. P.W. Crous (CBS H-22353, holotype; ex-type culture CBS 140483 = CPC 16238; CPC 16239). USA, California, Oakland, Huckleberry Botanic Regional Preserve, isol. from Arctostaphylos pallida (Ericaceae), 6 Mar. 2009, P.W. Crous, CPC 16855.
Substrate and distribution: On plant material; Chile, USA.
Notes: Cladosporium ipereniae belongs to the cladosporioides species complex and is morphologically and phylogenetically close to C. phyllophilum, C. phyllactiniicola and C. licheniphilum. However, Cladosporium phyllophilum, a species occurring on woody host plants usually associated with Taphrina species, possesses longer and smooth conidia. In C. phyllactiniicola, a mycophilic species occurring on chasmothecia of Phyllactinia guttata, and C. licheniphilum,
a species growing on thalli and apothecia of lichens, the conidiogenous
loci and conidial hila are wider, 1–2 μm diam, and the conidia are
smooth or almost so or sometimes finely asperulate, but never loosely
verruculose, verrucose or irregularly rough-walled as sometimes
occurring in C. ipereniae. Cladosporium puyae, a new
species introduced below, is described from the same host genus from
Colombia, but differs in having longer conidia and wider conidiogenous
loci and hila.
Cladosporium limoniforme (CBS 140484). A–E. Micronematous conidiophores forming large amounts of conidia. F–H. Conidial chains. Scale bars = 10 μm.
Cladosporium limoniforme
(CBS 140484). A. Overview of a cluster of conidiophores that seem to
originate from one base, illustrating the density of conidial chains.
B–C, E. Conidiophores and conidial chains either sprouting from
structures beneath ...
Etymology: Named after the shape of the limoniform intercalary conidia.
Mycelium
sparingly formed, usually unbranched, 1.5–3 μm wide, pale
olivaceous-brown or subhyaline, asperulate to minutely verruculose,
walls unthickened, sometimes forming small ropes of a few hyphae. Conidiophores
micronematous to semimacronematous, sometimes macronematous, short,
sometimes only as very short lateral branches of hyphae, not very
prominent, sometimes hardly distinguishable from hyphae, usually reduced
to conidiogenous cells or 1(–2)-septate, terminally arising from
hyphae, occasionally laterally arising from plagiotropous hyphae,
unbranched, usually neither geniculate nor nodulose, rarely once
geniculate, 5–90(–130) × (1–)2–3(–4) μm, mostly only up to 60 μm long,
subhyaline, pale brown to pale olivaceous-brown, concolourous with
hyphae, smooth or almost so to asperulate or somewhat irregularly
rough-walled. Conidiogenous cells integrated, terminal,
occasionally intercalary, narrowly cylindrical, neither geniculate nor
nodulose, 15–34(–50) μm long, with 1–3 pronounced scars at the apex or
situated on short lateral outgrowths at the apex in terminal cells, in
intercalary cells a single or two loci situated on small lateral
prolongations just below a septum, conidiogenous loci 1–1.5 μm diam,
somewhat thickened and darkened-refractive. Ramoconidia 15–34 μm long, 0(–1)-septate, base 2–2.5 μm wide, somewhat refractive. Conidia
catenate, very numerous, usually 3–7(–8) conidia in the terminal
unbranched part of the chain, relatively short, pale olivaceous-brown or
pale brown, ornamentation variable, loosely verruculose, sometimes
somewhat spiny or irregularly rough-walled, walls unthickened, small
terminal conidia obovoid to subglobose, apex rounded, attenuated towards
the base, 3–4 × 2–2.5 μm [av. (± SD) 4.0 (± 0.7) × 2.4 (± 0.4)],
aseptate, intercalary conidia limoniform, ovoid to ellipsoid, sometimes
fusiform, sometimes rostrate, 4–10(–12) × 2.5–3(–3.5) μm [av. (± SD) 7.6
(± 2.2) × 2.9 (± 0.4)], aseptate, rarely 1-septate, attenuated towards
apex and base, with 1–3 distal hila, secondary ramoconidia ellipsoid,
fusiform to subcylindrical, (8–)9.5–23(–30) × 3–3.5 μm [av. (± SD) 15.7
(± 4.8) × 3.2 (± 0.3)], 0–1-septate, pale olivaceous-brown or pale
brown, surface ornamentation variable, loosely verruculose, sometimes
somewhat spiny or irregularly rough-walled, walls unthickened, with
2–3(–4) distal hila, hila protuberant, 0.5–1(–1.5) μm diam, slightly
thickened and somewhat darkened-refractive; microcyclic conidiogenesis
occasionally occurring.
Culture characteristics:
Colonies on PDA attaining 34–65 mm after 14 d, smoke-grey, iron-grey to
dark grey-olivaceous, sometimes dull green due to abundant sporulation,
reverse iron-grey to olivaceous-black, velvety to granular or floccose;
margins regular, broad, white, glabrous to feathery; aerial mycelium
sparse, diffuse, sometimes more abundantly formed in colony centre and
then villose to densely tufted; growth flat, regular, sometimes with
numerous small to large prominent exudates. Colonies on MEA reaching
39–57 mm, grey-olivaceous, greenish olivaceous to smoke-grey or
glaucous-grey towards margins, sometimes large parts smoke-grey to
glaucous-grey or whitish due to aerial mycelium, reverse
olivaceous-grey, iron-grey to black, granular, velvety to floccose;
margins regular, narrow to broad, white, feathery to glabrous; aerial
mycelium sparse or covering large parts of the colony; growth flat with
somewhat elevated colony centre, radially furrowed, sporulation profuse.
Colonies on OA attaining up to 69 mm, grey-olivaceous to olivaceous due
to abundant sporulation forming concentric zones, reverse pale
olivaceous-grey to olivaceous-grey or leaden-grey, velvety, floccose to
felty; margins regular, narrow to broad, glabrous to feathery, greenish
olivaceous; aerial mycelium absent, sparse or more abundantly formed
covering large parts of the colony, smoke-grey; growth flat, without
prominent exudates, sporulation profuse.
Specimens examined: Cyprus, Polis, isol. from Eucalyptus sp. (Myrtaceae), 18 Mar. 2007, coll. A. van Iperen, isol. P.W. Crous, CPC 13923. Egypt, isolated from Musa acuminata (Musaceae), 2005, coll. R.S. Summerbell, isol. P.W. Crous (CBS H-22354, holotype; ex-type culture CBS 140484 = CPC 12039). Israel,
Dead Sea, Ein Bokek, isol. from hypersaline water, 2004, P. Zalar,
EXF-1062 = CPC 12049; Ein Gedi, 31.45, 35.3833, isol. from hypersaline
water, 2004, P. Zalar, EXF-1060 = CPC 12048, EXF-1081 = CPC 12050. USA, isolated from grape berry, F.M. Dugan lab, CBS 113737. Unknown, from tomato, CPC 18086 = KSU C1.
Substrate and distribution: Isolated from plant material and hypersaline water; Africa (Egypt), Asia (Israel), Europe (Cyprus) and North America (USA).
Notes: Cladosporium limoniforme
is well characterised by its few micronematous conidiophores forming
large amounts of conidia and its limoniform intercalary conidia.
Conidial surface ornamentation is typical for species belonging to the herbarum complex. It is phylogenetically but not morphologically allied to C. aggregatocicatricatum.
The latter species clearly differs in having much longer macronematous
conidiophores being once or several times slightly to distinctly
geniculate-sinuous or subnodulose with clusters of pronounced scars at
apices or intercalary. Morphologically C. limoniforme resembles C. subtilissimum and C. salinae. However, Cladosporium subtilissimum possesses slightly wider conidiophores, longer and wider conidia as well as wider conidiogenous loci and hila. Cladosporium salinae also forms micronematous conidiophores with similar measurements, but the conidiophores in C. salinae
are usually slightly or distinctly geniculate-sinuous at or towards the
apex forming sympodial clusters of pronounced denticulate
Conidi-ogenous loci. Furthermore, the conidia are usually smooth (Zalar et al., 2007, Bensch et al., 2012).
Cladosporium longicatenatum
(CBS 140485). A, C–E. Conidiophores with long, dichotomously branched
conidial chains. B. Ramoconidium with conidial chains. F–G. Tip of
conidiophores with conidia attached. Scale bars = 10 μm. ...
Cladosporium longicatenatum
(CBS 140485). A. Overview of hyphae and clusters of rounded cells
visible on the agar surface that give rise to slender elongated
conidiophores and conidia. B. Very elongated smooth secondary
ramoconidia give rise to intercalary ...
Etymology: Name refers to the very long conidial chains, with up to 20 or even more conidia in a branched chain.
Mycelium
abundant, loosely branched, filiform, 1–3 μm wide, multiseptate,
without swellings and constrictions, subhyaline, pale or medium
olivaceous or olivaceous-brown, surface ornamentation variable, smooth,
verruculose or irregularly rough-walled, walls unthickened or slightly
thick-walled, sometimes forming small stromatic hyphal aggregations of
few swollen cells. Conidiophores micro- or semimacronematous,
sometimes hardly distinguishable from hyphae, erect, straight or
somewhat flexuous, filiform or narrowly cylindrical, neither nodulose
nor geniculate, usually unbranched, rarely once branched,
13–250 × 2.5–3(–4) μm, sometimes up to 650 μm long, multiseptate, pale
olivaceous or medium olivaceous-brown, smooth, verruculose, verrucose or
irregularly rough-walled, especially towards the base of conidiophores,
walls somewhat thickened, about 0.5 μm thick. Conidiogenous cells
integrated, usually terminal, cylindrical, 12–53 μm long, neither
geniculate nor nodulose, usually with 2–3 loci at the outermost apex,
sometimes up to five loci situated at the laterally proliferated apex,
loci protuberant, subdenticulate, 1–1.5(–2) μm diam, somewhat thickened
and darkened-refractive. Ramoconidia cylindrical,
22–42 × 2.5–3(–4) μm, 0(–1)-septate, base broadly truncate, 2.5–3(–4) μm
wide, not thickened, slightly refractive. Conidia catenate, in
very long, usually loosely dichotomously branched chains, up to 12
conidia in the terminal unbranched part, up to 20 conidia or more in a
chain, small terminal conidia narrowly ellipsoid, sometimes fusiform,
(3.5–)5.5–7 × 2–2.5 μm [av. (± SD) 6.0 (± 1.0) × 2.2 (± 0.2)],
subhyaline or pale olivaceous, attenuated towards apex and base,
intercalary conidia narrowly ellipsoid or subcylindrical,
7–17 × 2–2.5(–3) μm [av. (± SD) 11.0 (± 3.4) × 2.4 (± 0.3)],
0(–1)-septate, with 1–2(–3) distal hila, 0.5–1 μm diam, secondary
ramoconidia subcylindrical or cylindrical, 10–30(–38) × 2.5–3.5 μm [av.
(± SD) 18.8 (± 7.4) × 2.9 (± 0.4)], 0(–2)-septate, with (1–)2–3 distal
hila, pale olivaceous or pale olivaceous-brown, lightmicroscopically
smooth or almost so, verruculose or loosely irregularly rough-walled,
outer wall seemingly detached, with SEM smooth or almost so or
delicately irregularly reticulate, walls unthickened or almost so, hila
1–2 μm diam, thickened and darkened-refractive; microcyclic
Conidi-ogenous not observed.
Culture characteristics:
Colonies on PDA attaining 45–59 mm after 14 d, iron-grey to
olivaceous-black, reverse leaden-black to olivaceous-black, felty,
margins white, narrow, glabrous to somewhat feathery, regular, aerial
mycelium loose, diffuse to fluffy, growth flat, few prominent exudates
formed. Colonies on MEA reaching 29–37 mm, olivaceous-grey to iron-grey
with patches of smoke-grey, reverse olivaceous-grey to iron-grey,
velvety to fluffy, margins white, narrow, glabrous, aerial mycelium
loose diffuse to more densely and fluffy, growth low convex with
somewhat elevated colony centre, radially furrowed, wrinkled, without
exudates. Colonies on OA attaining 43–54 mm, grey-olivaceous to
olivaceous-grey with patches of white or smoke-grey, reverse leaden-grey
to iron-grey, velvety to fluffy, margins hyaline, glabrous, narrow,
aerial mycelium fluffy, white to smoke-grey, low to high, growth flat,
without exudates; sporulation profuse on all media.
Specimen examined: Australia, Queensland, Noosa Bay, isol. from an unknown host, 27 Jul. 2009, P.W. Crous (CBS H-22355, holotype; ex-type culture CBS 140485 = CPC 17189).
Substrate and distribution: On plant material; Australia.
Notes: Cladosporium longicatenatum, an element of the cladosporioides species complex, clusters with C. exasperatum,
which also possesses a reticulate conidial surface ornamentation which
is, however, much more prominent with often distinctly embossed stripes.
Furthermore, the latter species deviates in having shorter
conidiophores, 15–100 μm long, shorter conidial chains with only up to
six conidia in the terminal unbranched part of the chain and wider
conidia, 3–4.5(–5) μm (Bensch et al. 2010).
Cladosporium parapenidielloides
(CBS 140487), which is also phylogenetically closely allied, differs in
having shorter conidi-ophores, sparse mycelium and a different surface
ornamentation. The conidial chains are shorter, ramoconidia are absent,
conidial measurements are similar but intercalary and secondary
ramoconidia somewhat shorter, but more commonly septate.
Cladosporium longissimum
(CBS 300.96). A–C. Macronematous conidiophores and conidial chains. D.
Branchlet of a conidiophore and conidia. E. Tip of a conidiophore and
conidia. Scale bars = 10 μm.
Etymology: Name refers to the very long conidiophores, up to 512 μm long.
Mycelium
immersed and superficial; hyphae loosely to densely branched,
1–4(–5) μm wide, septate, sometimes with swellings and constrictions,
smooth to minutely verruculose, walls unthickened or almost so,
sometimes forming ropes, subhyaline to pale olivaceous-brown, at the
base of conidiophores darker and somewhat swollen, especially the longer
ones, sometimes forming stromatic hyphal aggregations. Conidiophores
macronematous to micronematous, solitary, arising terminally and
laterally from hyphae, erect, flexuous, filiform to narrowly
cylindrical-oblong, neither nodulose nor geniculate. Macronematous conidiophores
unbranched or branched, branches mostly only as short denticle-like
lateral prolongations, often very long, up to 512 μm, 2.5–3.5(–4) μm
wide, multiseptate, 4–19 septa, not constricted at septa, regularly
septate, pale to medium or even dark olivaceous-brown, smooth, walls
unthickened or slightly thickened, somewhat wider at the base, up to
4 μm wide. Conidiogenous cells integrated, terminal or
intercalary, neither geniculate nor nodulose, 13–39 μm long, with up to
four loci crowded at the apex, closely aggregated, subdenticulate,
1–1.5 μm diam, thickened and darkened-refractive. Micronematous conidiophores
numerous, as short peg-like lateral prolongations or longer, filiform,
narrower, shorter and paler, sometimes geniculate, less septate, with up
to nine septa, not constricted, subhyaline to pale olivaceous-brown,
smooth, walls unthickened. Conidiogenous cells filiform to
narrowly cylindrical-oblong, occasionally geniculate, 9–16 μm long,
often with a single apical locus, sometimes with up to three loci,
subdenticulate, 1–1.2 μm diam. Ramoconidia frequently formed
both from macro- and micronematous conidiophores, 15–52 × 2–3 μm,
0–1(–3)-septate, narrowly cylindrical-oblong, with up to four apical
hila, not attenuated towards the base. Conidia catenate, in
branched chains, up to four conidia in the unbranched part, branching in
all directions, sometimes irregular in outline due to lateral
denticulate hila, small terminal conidia numerous, globose to
subglobose, 2–4 × 2–3 μm (av. ± SD: 3.1 ± 0.8 × 2.5 ± 0.4), aseptate,
intercalary conidia subglobose, ovoid to narrowly ellipsoid,
4–7(–8) × 2.5–3(–3.5) μm (av. ± SD: 5.4 ± 1.2 × 2.8 ± 0.3),
0(–1)-septate, secondary ramoconidia ovoid, narrowly ellipsoid to
subcylindrical, (6–)8–25(–28) × 2–3(–4) μm (av. ± SD:
15.4 ± 6.3 × 2.7 ± 0.5), 0–1(–2)-septate, not constricted at septa,
subhyaline to pale or medium olivaceous-brown, smooth to asperulate or
irregularly rough-walled, walls unthickened or only slightly thickened,
attenuated towards apex and base, with up to five distal hila,
subdenticulate to denticulate, 0.5–1.5 μm diam, thickened and
darkened-refractive; microcyclic conidiogenesis occasionally occurring.
Conidia formed by micronematous conidiophores often paler and slightly
narrower, 2–25 × 1.5–2 μm, 0–1(–2)-septate.
Culture characteristics:
Colonies on PDA iron-grey, olivaceous-grey to grey-olivaceous or
olivaceous due to sporulation and mycelium, reverse leaden-grey to
iron-grey or olivaceous-black, velvety to fluffy, margin whitish,
feathery, narrow, aerial mycelium abundant, loose to dense, high,
fluffy, growth convex to raised, few very small, not prominent exudates
formed, sporulating. Colonies on MEA olivaceous-grey to grey-olivaceous,
greenish olivaceous towards margins, reverse olivaceous-grey to
iron-grey, velvety to wooly-fluffy, margin white, narrow, glabrous to
feathery, aerial mycelium high, fluffy, without prominent exudates,
sporulation profuse. Colonies on OA smoke-grey to olivaceous, reverse
pale mouse-grey to mouse-grey or olivaceous-grey, wooly-felty, margin
hyaline to white, glabrous, aerial mycelium high, fluffy to felty,
without exudates, sporulating.
Specimen examined: Papua New Guinea, Madang, Jais Aben, isol. from soil along coral reef coast, Nov. 1995, coll. A. Aptroot, isol. A. van Iperen (CBS H-22356, holotype; ex-type culture CBS 300.96).
Substrate and distribution: Isolated from soil; Papua New Guinea.
Notes: The new species clusters close to C. sphaerospermum
but the latter species differs in having shorter and wider
conidi-ophores with darkened septa in dense succession, minutely
verruculose or verrucose, wider small terminal conidia, 3–5 × 3–3.5 μm,
and wider more frequently septate conidia, 3–4(–5) μm wide, 0–3-septate (Zalar et al. 2007). Zalar et al. (2007)
hesitated to introduce this isolate as a new species since it is only
known from a single isolate, but morphological and phylogenetic
differences are sufficient enough to justify its recognition as a
distinct species.
Cladosporium cycadicola, described from Australia on Cycas and also belonging to the sphaerospermum species complex (Crous et al. 2014),
is morphologically similar in having macro- and micronematous
conidiophores and similar conidial measurements. The conidiophores in vitro
can be also quite long, up to 600 μm, but the transition between
conidiophores and conidia is often not very evident. However, it
deviates from C. longissimum in having shorter ramoconidia, shorter conidial chains and somewhat longer intercalary conidia, 4–11(–13) × 2–2.5(–2.8) μm.
Cladosporium macrocarpum Preuss, in Sturm, Deutsch. Fl. 3(26): 27. 1848.
Specimens examined: Iran, isol. from Hordeum sp. (Poaceae), 12 May 2009, isol. by P.W. Crous, CPC 19063. Morokko, Rabat, isol. from Diospyros kaki (Ebenaceae), isol. by L. Najim, CBS H-10355, CBS 108.85. Netherlands, isol. from Hordeum vulgare (Poaceae), Oct. 1962, Bierbrouwerij Amstel, isol. by A.C. Stolk, CBS 175.62.
Notes: Cladosporium versiforme (CBS 140491), introduced below, was also isolated from Hordeum sp. in Iran as was CPC 19063, which proved to be C. macrocarpum. Cladosporium versiforme
differs, however, in having narrower macronematous conidiophores,
3–4 μm, with narrower swellings, 5–7 μm. Its conidia are very variable
in shape, size and colour, and two different types are formed. The
intercalary and secondary ramoconidia of the herbarum-like type formed
by macronematous conidiophores are narrower than in C. macrocarpum.
Cladosporium montecillanum (CBS 140486). A–G. Conidiophores and conidial chains. Scale bars = 10 μm.
Etymology: Named after the place where it was collected, Montecillo, Mexico.
Mycelium
sparingly formed and branched, 1–4 μm wide, septate, sometimes with
swellings and constriction especially at septa, subhyaline or pale
olivaceous, medium olivaceous-brown at the base of conidiophores and
sometimes swollen up to 7 μm, verruculose, walls unthickened. Conidiophores
macro- or semimacronematous, erect, straight or somewhat flexuous,
arising from hyphae or swollen hyphal cells, cylindrical-oblong, often
subnodulose at the apex, occasionally slightly geniculate, unbranched,
25–130 × 2.5–4 μm, sometimes up to 5.5 μm at the base and attenuated
towards the apex, semimacronematous ones 2–2.5 μm wide, 0–6-septate,
septa often not very conspicuous, pale to medium olivaceous-brown,
smooth, sometimes verruculose towards the base, walls unthickened or
somewhat thickened, about 0.5 μm thick. Conidiogenous cells
integrated, mainly terminal, occasionally intercalary, cylindrical,
sometimes subnodulose at the apex or intercalary and slightly geniculate
due to sympodial proliferation, 11–40 μm long, with mainly 1–4 loci per
cell, loci conspicuous, 1–1.5(–2) μm diam, thickened and
darkened-refractive. Ramoconidia with a truncate, non-cladosporioid base not observed. Conidia
numerous, catenate, in branched chains with 1–4(–6) conidia in the
terminal unbranched part, branching in all direction, small terminal
conidia subglobose, obovoid or ellipsoid, 3–5(–6) × (1.5–)2–2.5 μm [av.
(± SD) 4.1 (± 0.7) × 2.3 (± 0.3)], apex broadly rounded, intercalary
conidia ellipsoid, more or less attenuated towards apex and base,
4–9(–11) × (2–)2.5–3(–3.5) μm [av. (± SD) 6.7 (± 2.0) × 2.7 (± 0.4)],
aseptate, with 1–3(–4) distal hila, some of them seem to have a halo
since the wall being paler than the lumen, secondary ramoconidia
ellipsoid or subcylindrical, 6.5–22(–27) × 2.5–3.5(–4) μm [av. (± SD)
14.1 (± 5.5) × 3.2 (± 0.4)], 0(–1)-septate, with 2–4 distal hila, pale
olivaceous or pale olivaceous-brown, smooth, walls unthickened, hila
conspicuous, 0.5–1.5(–2) μm diam, thickened and darkened-refractive;
microcyclic conidiogenesis occasionally observed.
Culture characteristics:
Colonies on PDA reaching 65–77 mm after 14 d, grey-olivaceous,
olivaceous to olivaceous-black, grey-olivaceous at margins, reverse
olivaceous-black, powdery to fluffy, margins white, feathery, regular,
aerial mycelium loose diffuse to fluffy, growth flat. Colonies on MEA
attaining 70 mm, greenish grey, grey-olivaceous, iron-grey at margins,
reverse olivaceous-grey to iron-grey, velvety to fluffy, margins white,
glabrous to somewhat feathery, aerial mycelium sparse, diffuse or more
commonly formed, white, fluffy, growth flat to low convex, radially
furrowed or folded. Colonies on OA reaching 55–70 mm, olivaceous to
olivaceous-grey or smoke-grey, reverse leaden-grey to iron-grey, powdery
to fluffy, margins glabrous, narrow, aerial mycelium loose diffuse, in a
few patches denser, fluffy, smoke-grey, growth flat. On all media
sporulation profuse but without prominent exudates.
Specimens examined: Mexico, Montecillo, Texcoco, isol. from pine needles (Pinus sp., Pinaceae),
12 Oct. 2009, coll. M. de Jesús Yáñez-Morales, isol. P.W. Crous, CPC
17804; from same substrate and locality, 26 Nov. 2009, coll. M. de Jesús
Yáñez-Morales, isol. P.W. Crous (CBS H-22357, holotype; ex-type culture CBS 140486 = CPC 17953); Montecillo, isol. from Taraxacum sp. (Asteraceae), 1 Oct. 2008, coll. M. de Jesús Yáñez-Morales, isol. P.W. Crous, CPC 15605.
Substrate and distribution: On plant material; Mexico.
Notes: This species reminds one of C. cladosporioides, C. tenuissimum and C. pseudocladosporioides but these three species possess somewhat longer intercalary conidia and secondary ramoconidia, form ramoconidia and in C. cladosporioides and C. tenuissimum the conidiophores are distinctly longer (Bensch et al. 2012).
Cladosporium myrtacearum (CPC 16319). A–C. Conidiophores and conidial chains. D–E. Tips of conidiophores and conidia. Scale bars = 10 μm.
Cladosporium myrtacearum
(CPC 16319). A. Overview on agar surface with conidiophores arising
from the surface. B. Running hyphae giving rise to several
conidiophores. C–F. Tips of conidiophores with conidial chains. Note
that the reticulate surface ...
Mycelium
abundantly formed, superficial hyphae branched, 1.5–5 μm wide,
multiseptate, sometimes slightly constricted at septa or intercalarily
swollen, subhyaline, pale or medium olivaceous-brown, minutely
verruculose, verruculose or verrucose, sometimes irregularly
rough-walled or appearing to be covered by a halo, walls somewhat
thickened in wider, fertile hyphae, sometimes forming ropes of a few
hyphae. conidi-ophores macronematous, arising solitarily or in
small groups of 2–4, arising terminally or laterally from hyphae,
cylindrical-oblong, often geniculate towards the apex or apex swollen,
capitate, unbranched or once branched, branchlets often quite long,
(35–)55–220(–320) × 3.5–4.5 μm, multiseptate (with 3–9 usually not very
conspicuous septa), pale to medium olivaceous-brown, smooth, minutely
verruculose or irregularly rough-walled towards the base, walls somewhat
thickened. Conidiogenous cells integrated, mainly terminal but
also intercalary, in terminal cells apex often slightly swollen,
capitate, in intercalary ones geniculate due to sympodial proliferation,
9–35 μm long, with 2–4 loci per cell, loci conspicuous, (1–)1.5–2 μm
diam, thickened and darkened-refractive. Ramoconidia cylindrical-oblong, 20–55 × 3.5–4.5 μm, 0–3-septate, base 2–3 μm wide, somewhat refractive. Conidia
catenate with 1–4 conidia in the terminal unbranched part of the chain,
straight, small terminal conidia obovoid or ellipsoid,
4.5–8.5 × (2.5–)3–3.5(–4.5) μm [av. ± SD, 6.0 (± 1.3) × 3.1 (± 0.6) μm],
aseptate, intercalary conidia ellipsoid, fusiform,
6–13(–15) × 3–4(–4.5) μm [av. ± SD, 9.4 (± 2.5) × 3.6 (± 0.5) μm],
0(–1)-septate, with 1–3(–4) distal hila, secondary ramoconidia
ellipsoid, subcylindrical or fusiform, 10–21(–23.5) × 3.5–4.5(–5) μm
[av. ± SD, 15.9 (± 3.5) × 4.0 (± 0.5) μm], 0–1(–2)-septate, septum
median, not very conspicuous, becoming sinuous with age, with
(1–)2–3(–5) distal hila, hila 1–2 μm diam, pale olivaceous-green or
olivaceous-brown, surface ornamentation variable, usually irregularly
rough-walled due to reticulate surface or embossed stripes, coarsely
verruculose, rugose or verrucose (LM), sometimes outer wall seemingly
detaching, in intercalary and small terminal conidia surface
ornamentation more prominent, secondary ramoconidia sometimes appearing
to be almost smooth or minutely verruculose, hila conspicuous, 0.5–2 μm
diam, thickened and darkened-refractive; microcyclic conidiogenesis
occurring.
Specimen examined: South Africa, North West Province, Magaliesberg, south of Mooinooi, isol. from Indigofera sp. (Fabaceae), 25 Jan. 2009, coll. A.R. Wood, isol. P.W. Crous, CPC 16319.
Substrate and distribution: On Myrtaceae (Corymbia, Eucalyptus) and Fabaceae (Indigofera); Australia, South Africa.
Notes: The description given above is based on CPC 16319 from South Africa. This isolate clusters with C. myrtacearum which is known from two isolates from Australia, the ex-type isolated from Corymbia and an additional isolate from Eucalyptus, with both hosts belonging to the Myrtaceae (Braun et al., 2005, Bensch et al., 2010). These three isolates form a highly supported subclade (see Fig. 1).
Morphologically, CPC 16319 deviates from the isolates from Australia in
forming longer conidiophores and ramoconidia and a more prominent
surface ornamentation. Whether these morphological differences represent
intraspecific variation can only be clarified with additional isolates.
Therefore, the biology, host range and distribution of C. myrtacearum still remain unclear as already stated in Bensch et al. (2010).
Cladosporium parapenidielloides Bensch, Crous & U. Braun, sp. nov. MycoBank MB814632. Fig. 21, Fig. 22.
Cladosporium parapenidielloides (CBS 140487). A–D. Conidiophores and conidial chains. E–G. Tip of conidiophores and conidia. Scale bars = 10 μm.
Cladosporium parapenidielloides
(CBS 140487). A, D. Overview of a part of a colony showing a dense
field of conidiophores that arise from cells at the level of the agar
surface and forming conidial chains. B. Dislodged conidial chains on the
agar surface. ...
Etymology: Name refers to the morphological similarity to Cladosporium penidielloides, but the conidia are shorter and narrower in C. penidielloides.
Mycelium
sparingly formed and branched, 1.5–3(–4) μm wide, septate, subhyaline,
pale olivaceous, walls unthickened or almost so, smooth, verruculose or
irregularly rough-walled, sometimes slightly swollen at the base of
conidiophores. Conidiophores macro- and semimacronematous,
solitary, rarely in pairs of two, arising terminally and laterally from
hyphae, erect, straight or somewhat flexuous, non-nodulose, sometimes
once geniculate towards the apex, unbranched, 13–67 × 2.5–3.5(–4) μm,
subcylindrical or cylindrical, 1–2(–3)-septate, septa often not very
conspicuous, pale to medium olivaceous-brown, smooth or partly
verruculose, sometimes loosely verrucose, walls unthickened or almost
so, slightly attenuated towards the apex. Conidiogenous cells
integrated, terminal, 12–32 μm long, with (1–)2–3 distal loci or once
geniculate towards the apex with a single locus on a small lateral
shoulder, loci conspicuous but small, often subdenticulate, 0.8–1.5 μm
diam, thickened and darkened-refractive. Ramoconidia (sensu Bensch et al. 2012) not observed. Conidia
catenate, in branched chains, usually dichotomously branched, with 1–6
conidia in the terminal unbranched part, small terminal conidia narrowly
ellipsoid, 4–6 × 2(–2.2) μm [av. (± SD) 5.3 (± 0.8) × 2.0 (± 0.1)],
intercalary conidia fusiform or narrowly ellipsoid,
5.5–12(–14) × (1.5–)2–2.5(–3) μm [av. (± SD) 8.4 (± 2.6) × 2.3 (± 0.4)],
0–1-septate, attenuated towards apex and base, with 1–2 distal hila,
secondary ramoconidia subcylindrical, narrowly ellipsoid, sometimes
fusiform, 10–19 × (2–)2.5–3 μm [av. (± SD) 13.8 (± 2.5) × 2.6 (± 0.3)],
0–1-septate, septum median, subhyaline or pale olivaceous, smooth or
almost so, loosely verruculose or slightly irregularly rough-walled,
walls unthickened, with 2–3 distal hila, hila conspicuous,
0.5–1.5(–1.8) μm diam, distinctly darkened-refractive and thickened;
microcyclic conidiogenesis not observed.
Culture characteristics:
Colonies on PDA attaining 39–55 mm after 14 d, iron-grey to
olivaceous-black, reverse leaden-black to olivaceous-black, felty,
margins white, narrow, glabrous to somewhat feathery, regular, aerial
mycelium loose, diffuse to fluffy, growth flat. Colonies on MEA reaching
23–32 mm, olivaceous-grey to iron-grey, grey-olivaceous due to abundant
sporulation, somewhat zonate. Colonies on OA reaching 42–55 mm,
grey-olivaceous, aerial mycelium loose diffuse.
Specimen examined: Australia, Queensland, Fraser Island, isol. from Eucalyptus sp. (Myrtaceae), 29 Jul. 2009, P.W. Crous (CBS H-22358, holotype; ex-type culture CBS 140487 = CPC 17193).
Substrate and distribution: On Eucalyptus; Australia.
Notes: Cladosporium parapenidielloides was named after C. penidielloides due to its similar morphology although the two species are phylogenetically not allied. Cladosporium penidielloides, which clusters with C. salinae, deviates in having more frequently septate, somewhat wider and longer conidia. Cladosporium ipereniae is also similar but has wider conidia, 2.5–4(–4.5) μm, and shorter small terminal and intercalary conidia.
Cladosporium parapenidielloides, which belongs in the cladosporioides species complex, clusters with C. exasperatum, also described from Australia on Eucalyptus, but the conidia of the latter species are shorter and narrower with a different surface ornamentation. Cladosporium australiense, another species on Eucalyptus
in Australia, is distinct in having longer conidiophores, wider
conidiogenous loci and hila [(0.5–)0.8–2 μm diam] as well as smooth,
longer and wider secondary ramoconidia [(7–)11–25(–27) × 3–4 μm] (Bensch et al. 2010). Morphological differences between C. parapenidielloides and the closely allied C. longicatenatum are discussed under the latter species.
Cladosporium penidielloides (CBS 140489). A–F. Macro- and micronematous conidiophores and conidial chains. G. Ramoconidium and conidia. Scale bars = 10 μm.
Cladosporium penidielloides
(CBS 140489). A. Overview on the agar surface also containing slender
conidiophores. B–D, F, H. Short and long conidiophores erumpent from
structures beneath the agar or arising from plagiotropous hyphae with
conidial ...
Etymology: This species was provisionally placed in the genus Penidiella on the basis of morphology. Name refers to its morphological similarity and this initial identification.
Mycelium
loosely branched, filiform to subcylindrical, 1–3.5(–5) μm wide,
septate, neither constricted nor swollen, but often with a short lateral
outgrowth, subhyaline to pale olivaceous-brown, smooth or minutely
verruculose in wider hyphae, walls unthickened, forming ropes of a few
hyphae. conidi-ophores macro- and micronematous, arising
terminally and laterally from hyphae, solitary, filiform to narrowly
cylindrical-oblong, sometimes with unilateral swellings or short lateral
prolongations at the apex, then appearing somewhat irregular in
outline, unbranched or branched, branches mostly as short lateral
outgrowths, 8–55(–80) × (2–)2.5–4 μm, septate, sometimes densely
multiseptate, sometimes seceding at one of these septa and forming
ramoconidia, subhyaline or pale olivaceous-brown, smooth or almost so,
walls unthickened. Conidiogenous cells integrated, mostly
terminal, but also intercalary, loci situated at the apex, on short
peg-like lateral prolongations or on small lateral shoulders, sometimes
forming a small cluster of up to six pronounced conidiogenous loci,
8–25 μm long, loci protuberant, 1–1.5(–2) μm diam, thickened and
darkened-refractive. Ramoconidia occurring, often multiseptate, 8–25 μm long. Conidia
catenate, in unbranched or often dichotomously branched chains, 1–6
conidia in the terminal unbranched part of the chain, straight,
sometimes swollen, small terminal conidia obovoid or ellipsoid,
4–6.5(–7.5) × 2.5–3.5 μm [av. (± SD) 5.8 (± 0.8) × 3.0 (± 0.4)],
0–1-septate, apex rounded, intercalary conidia ellipsoid,
5–13 × 2.5–3.5 μm [av. (± SD) 9.6 (± 2.5) × 3.1 (± 0.3)],
0–1(–2)-septate, secondary ramoconidia ellipsoid or subcylindrical,
7–22(–29) × 3–4 μm [av. (± SD) 16.4 (± 6.0) × 3.4 (± 0.4)],
(0–)1–3(–6)-septate, septa refractive, becoming sinuous with age, some
conidia with up to 12 septa, with 1–3 distal hila, smooth or almost so
or loosely verruculose, smooth or occasionally irregularly reticulate
under SEM, pale olivaceous-brown, walls unthickened or slightly
thick-walled; microcyclic conidiogenesis occasionally occurring.
Culture characteristics:
Colonies on PDA, OA and MEA attaining 15–20 mm after 14 d. On PDA
surface and reverse olivaceous-grey. On MEA surface grey-olivaceous,
reverse olivaceous-grey. On OA surface grey-olivaceous. Colonies
spreading with aerial mycelium sparse to absent, and smooth, even
margins.
Specimen examined: Australia, Victoria, Melbourne, stop 2 in the vicinity of the Twelve Apostles, isol. from Acacia verticillata (Fabaceae), 18 Oct. 2009, P.W. Crous, as ‘Penidiella’ (CBS H-22360, holotype; ex-type culture CBS 140489 = CPC 17674).
Substrate and distribution: On Acacia; Australia.
Notes: The genus Penidiella (Capnodiales, Teratosphaeriaceae)
is a cladosporium-like genus which is characterised by penicillate
conidiophores with a quite distinct branching system consisting of a
single terminal conidiogenous cell giving rise to several ramoconidia
that form several secondary ramoconidia or the branched apparatus is
composed of several terminal and sometimes lateral conidiogenous cells
giving rise to sequences of ramoconidia (Crous et al. 2007a). Cladosporium penidielloides is reminiscent of this genus and was originally identified as a Penidiella.
Phylogenetically it is allied to C. salinae which clusters with C. halotolerans and together with a few other species they form a sister clade to C. sphaerospermum and closely allied species (Fig. 2). In previous phylogenetic analyses, C. salinae had a more separate position within the genus Cladosporium being distantly related to any other described species (Zalar et al. 2007) which is also true for C. aphidis (Bensch et al. 2012). The phylogenetic position of C. salinae is sensitive to the species sampling included in the phylogenetic analysis and might be an example of long-branch attraction.
Cladosporium penidielloides and C. salinae
have usually short, poorly differentiated conidiophores sometimes
forming small clusters of pronounced scars and smooth conidia but
globose or subglobose terminal conidia typical for members of the sphaerospermum species complex are lacking. They rather resemble species of the genus Fusicladium. Cladosporium penidielloides is distinguishable from C. salinae by longer and more frequently septate intercalary conidia and secondary ramoconidia.
Cladosporium perangustum Bensch et al., Stud. Mycol. 67: 65. 2010.
Specimens examined: Panama, isol. from Ananas comosus (Bromeliaceae), CPC 18494 = 97.1; from the same plant, CPC 18496 = 110.1.
Note: These isolates represent the first records of C. perangustum from Central America.
Cladosporium pseudochalastosporoides (CBS 140490). A–E. Conidiophores and conidial chains. F–G. Tip of conidiophores and conidia. Scale bars = 10 μm.
Etymology: Name refers to its morphological similarity to Cladosporium chalastosporoides.
Mycelium
sparingly branched, filiform or cylindrical, 2.5–5.5 μm wide, septate,
in wider hyphae constricted at septa, pale to medium olivaceous-brown,
smooth to verruculose, walls somewhat thickened, occasionally swollen at
the base of conidi-ophores. Conidiophores macronematous,
solitary or in pairs, formed terminally or laterally from hyphae,
cylindrical or slightly to distinctly attenuated towards the apex,
non-nodulose, sometimes once geniculate towards or at the apex, rarely
up to three times, unbranched, 20–120 μm long, 2.5–3.5 μm wide at the
apex, 3.5–5.5 μm towards the base, 1–4(–5)-septate, not constricted at
septa, pale to medium olivaceous-brown, somewhat paler towards the apex,
smooth or minutely verruculose, walls slightly thickened, apex
sometimes swollen, slightly capitate, reminding one of species belonging
to the herbarum species complex. Conidiogenous cells
integrated, terminal, subcylindrical, sometimes geniculate due to
sympodial proliferation, 20–33 μm long, with 1–3 loci around the apex,
loci 1–1.5 μm diam, slightly thickened and refractive. Ramoconidia
occasionally formed, subcylindrical or cylindrical, 20–39 × 3–4 μm,
0–1-septate, base broadly truncate, 3–3.5 μm wide, not thickened,
somewhat refractive. Conidia catenate, in long, often
dichotomously branched chains, up to 10 conidia in the terminal
unbranched part of the chain, small terminal conidia obovoid or
ellipsoid, (4–)5–7 × (1.5–)2–2.5(–3) μm [av. (± SD) 6.0 (± 0.8) × 2.4 (±
0.3)], aseptate, basal hilum 0.8–1 μm diam, intercalary conidia
fusiform or subcylindrical, 6.5–10(–12.5) × 2–3 μm [av. (± SD) 8.2 (±
1.7) × 2.7 (± 0.4)], aseptate, with 1–2(–3) distal hila, 0.8–1(–1.2) μm
diam, secondary ramoconidia ellipsoid or subcylindrical,
9–16(–27) × 3–4 μm [av. (± SD) 13.9 (± 4.1) × 3.5 (± 0.4)],
0(–1)-septate, pale olivaceous or pale olivaceous-brown, smooth, walls
unthickened or slightly thick-walled in secondary ramoconidia, with
1–3(–5) distal hila, 1–1.5(–2) μm diam, somewhat thickened and
darkened-refractive; microcyclic Conidiogenous not observed.
Culture characteristics:
Colonies on PDA reaching 45–52 mm after 14 d, iron-grey to
olivaceous-black, reverse olivaceous-black, fluffy due to aerial
mycelium, margins white, glabrous or somewhat feathery, narrow, aerial
mycelium olivaceous-grey, dense, high, growth flat to low convex,
without prominent exudates, sporulation profuse. Colonies on MEA
attaining 43–50 mm, olivaceous-grey to pale olivaceous-grey, reverse
olivaceous-grey, fluffy, margins white, glabrous, radially furrowed,
aerial mycelium abundant, covering almost the whole colony, dense,
growth flat to low convex, sporulating. Colonies on OA reaching
34–37 mm, olivaceous-grey to pale olivaceous-grey, reverse leaden-grey
to olivaceous-grey, fluffy to wooly, margins glabrous, regular, white,
aerial mycelium loose diffuse to fluffy, growth flat, without exudates,
sporulating.
Specimen examined: Mexico, isol. from pine needles (Pinus sp., Pinaceae), 30 Nov. 2009, coll. M. de Jesús Yáñez-Morales, isol. P.W. Crous (CBS H-22361, holotype; ex-type culture CBS 140490 = CPC 17823).
Substrate and distribution: Isolated from pine needles; Mexico.
Notes: This species, which belongs to the cladosporioides species complex, is both morphologically and phylogenetically close to C. chalastosporoides (Bensch et al. 2010)
but differs in having longer conidiophores which are wider at the base
(3.5–5.5 μm) and attenuated towards the apex (2.5–3.5 μm), and longer
ramoconidia, 20–39 μm. Furthermore, secondary ramoconidia are not
distinctly darker than small terminal and intercalary conidia, and
microcyclic conidiogenesis seems to be lacking. The name C. chalastosporoides refers to the fusiform conidia formed in long, mostly unbranched chains which are reminiscent of the genus Chalastospora, especially the species Ch. gossypii (with Alternaria malorum as a synonym) representing an asexual lineage in the Pleosporales, Pleosporaceae (Simmons 2007, Crous et al., 2009a).
Cladosporium pseudocladosporioides Bensch et al., Stud. Mycol. 67: 71. 2010.
Specimen examined: South Africa, isol. from Rooibos (Aspalathus linearis, Fabaceae), wild population, code R 8263K, 8 Sep. 2009, G. Marais, CPC 18014.
Cladosporium puyae (CBS 274.80A). A–G. Conidiophores and conidial chains. Scale bars = 10 μm.
Cladosporium puyae
(CBS 274.80A). A. Survey of colony development with numerous
conidiophores arising from the agar surface. B–C, E. Conidiophores,
hyphae and conidial chains. D. Conidial chain showing the characteristic
dispersed surface ornamentation. ...
Etymology: Named after the host from which it was isolated, Puya.
Mycelium
loosely branched, plagiotropous and ascending, cylindrical-oblong,
sometimes with swellings and slightly constricted at septa, 2–5 μm wide,
septate, pale to medium olivaceous-brown, smooth or almost so to
minutely verruculose or loosely verrucose or irregularly rough-walled,
walls slightly thickened. Conidiophores macronematous,
solitary, in pairs or in loose groups, arising from plagiotropous and
ascending hyphae, cylindrical-oblong, non-nodulose, often once or a few
times geniculate-sinuous at the outermost apex, unbranched or once
branched, 8–140 × (2–)2.5–4.5 μm, up to 4-septate, septa often somewhat
darkened where ramoconidia are seceded, pale to medium olivaceous-brown,
somewhat paler towards the apex, almost smooth to asperulate or
verruculose, walls slightly thickened. Conidiogenous cells
integrated, mostly terminal but also intercalary, terminal ones often
seceding, forming ramoconidia, in intercalary ones loci situated on
small lateral prolongations just below the septum, cylindrical-oblong,
with two or few conidiogenous loci crowded at or towards the apex,
sometimes once or a few times geniculate due to sympodial proliferation,
10–41 μm long, loci conspicuous, 1–2(–2.5) μm diam, thickened and
darkened-refractive. Ramoconidia up to 35 μm long, 3–4 μm wide,
base 2.5–3.5 μm wide, 0–1-septate, base usually unthickened and not
darkened, however delimitation from secondary ramoconidia sometimes
difficult with light microscopy. Conidia catenate, in branched
chains, up to 4(–5) conidia in the terminal unbranched part of the
chain, asperulate to verruculose, several of the verrucae irregularly
enlarged (SEM, Fig. 27D),
small terminal conidia ovoid, obovoid to ellipsoid, 3.5–6 × 2.5–3 μm
[av. (± SD) 4.9 (± 0.8) × 2.8 (± 0.3)], aseptate, apex rounded,
intercalary conidia ellipsoid to subcylindrical, only slightly
attenuated towards apex and base, 5.5–16(–19) × 2.5–3.5(–4) μm [av. (±
SD) 9.8 (± 3.8) × 3.3 (± 0.4)], 0(–1)-septate, with 1–3 distal hila,
secondary ramoconidia ellipsoid to cylindrical, 10–33 × (3–)3.5–4(–5) μm
[av. (± SD) 20.4 (± 6.7) × 3.7 (± 0.5)], 0–1(–2)-septate, with 2–3(–4)
distal hila, not constricted at septa, pale olivaceous-brown, walls more
or less unthickened, hila conspicuous, protuberant, (0.5–)1–2.5 μm
diam, thickened, darkened-refractive.
Culture characteristics:
Colonies on PDA attaining 34–38 mm after 14 d, greenish olivaceous to
grey-olivaceous due to abundant sporulation, olivaceous-black, reverse
olivaceous-black, velvety to powdery, margins white, somewhat feathery,
narrow, regular, aerial mycelium loose, diffuse, growth flat,
sporulation profuse. Colonies on MEA reaching 23–35 mm, grey-olivaceous,
olivaceous-black towards margins, reverse olivaceous-grey to iron-grey,
velvety to powdery, margins white, narrow, somewhat feathery, regular,
aerial mycelium sparse, diffuse, growth flat, radially furrowed and
folded in colony centre, sporulation profuse. Colonies on OA
grey-olivaceous, olivaceous-black towards margins, reverse leaden-grey
to leaden-black, velvety to powdery, margins regular, entire edge,
glabrous, aerial mycelium loose, diffuse, growth flat, and sporulation
profuse.
Specimen examined: Colombia, Páramo de Boquerón, alt. 3 420 m, isol. from Puya goudotiana (Bromeliaceae) coll. by W. Gams, depos. May 1980, ident. as “C. tenuissimum” (CBS H-10372, holotype; ex-type culture CBS 274.80A).
Substrate and distribution: On Puya; Colombia.
Notes: Cladosporium puyae resembles C. cladosporioides and C. tenuissimum but differs in having asperulate to verruculose conidia, which is typical for species belonging to the herbarum species complex. It clusters close to C. spinulosum
but the conidia of the latter species are shorter and wider [small
terminal and intercalary conidia 4–7(–8) × 3–4.5(–5) μm and secondary
ramoconidia (6–)7–15(–18) × 4–5(–6) μm] as well as conspicuously
digitate (Zalar et al., 2007, Bensch et al., 2012).
Two
other CBS strains were isolated from Colombian plant material, both
collected in the same year, CBS 274.80B and CBS 274.80C. CBS 274.80B,
isolated from a dead leaf of Cortaderia, represents the ex-type of Cladosporium colombiae (Schubert et al. 2009)
which differs in having macro- and micronematous conidiophores, conidia
formed in long branched chains with up to 10 conidia in the terminal
unbranched part of the chain and shorter intercalary conidia and
secondary ramoconidia. CBS 274.80C, isolated from the same host as C. puyae, clusters close to C. lycoperdinum and is tentatively maintained in that species although the morphology is slightly different (Bensch et al. 2010).
Cladosporium ramotenellum K. Schub. et al., Stud. Mycol. 58: 137. 2007, emend.
Holotype: Slovenia, Sečovlje, isolated from hypersaline water from reverse ponds, salterns, 2005, P. Zalar, CBS H-19862. Isotype: HAL 2026 F. Ex-type culture: CBS 121628 = CPC 12043 = EXF-454.
Mycelium
unbranched or only sparingly branched, 1.5–4 μm wide, septate, without
swellings and constrictions, hyaline or subhyaline, smooth, sometimes
irregularly rough-walled, walls unthickened. Conidiophores
solitary, macronematous and micronematous, arising as lateral branches
of plagiotropous hyphae or terminally from ascending hyphae, erect,
straight or slightly flexuous, cylindrical, neither geniculate nor
nodulose, without capitate apices or intercalary swellings, unbranched,
sometimes branched, branches often only as short lateral prolongations,
mainly formed below a septum, 14–120(–230) × 2–4(–5) μm, septate, not
constricted at the septa, subhyaline to pale olivaceous or brown, smooth
to minutely verruculose, walls unthickened, sometimes guttulate. Conidiogenous cells
integrated, terminal, sometimes also intercalary, cylindrical, not
geniculate, non-nodulose, 10–28(–50) μm long, proliferation sympodial,
sometimes swollen, up to 7 μm wide, with few conidiogenous loci, mostly
1–3, loci sometimes situated on small lateral prolongations,
protuberant, 0.5–1.5(–2) μm diam, thickened and somewhat
darkened-refractive. Ramoconidia cylindrical-oblong, 15–50 ×
2–4(–5) μm, 0–1(–3)-septate, rarely up to 4-septate, subhyaline to very
pale olivaceous, smooth or almost so, with a broadly truncate base
lacking a dome and raised rim, 2–3 μm wide, not thickened but somewhat
refractive. Conidia numerous, polymorphous, catenate, in
branched chains with 2–5 conidia in the terminal unbranched part of the
chain, straight, sometimes slightly curved, small terminal conidia
numerous, globose, subglobose or ovoid, obovoid or limoniform,
2.5–7 × 2–4(–4.5) μm [av. ± SD, 4.5 (± 1.2) × 2.9 (± 0.6) μm], aseptate,
without distal hilum or with a single apical hilum, intercalary conidia
ellipsoid, limoniform to subcylindrical, 5–12(–15) × 3–4(–5) μm
[av. ± SD, 8.8 (± 2.5) × 3.7 (± 0.4) μm], 0–1-septate; secondary
ramoconidia ellipsoid, subcylindrical to cylindrical-oblong,
(7–)13–30(–39) × 3–4(–5) μm [av. ± SD, 17.8 (± 6.0) × 4.1 (± 0.5) μm],
sometimes swollen up to 7 μm, 0–1(–3)-septate, usually not constricted
at septa, sometimes distinctly constricted at the median septum,
subhyaline to very pale olivaceous, minutely verruculose (granulate
under SEM), walls unthickened or almost so, apex broadly rounded or
slightly attenuated towards apex and base, sometimes guttulate, hila
protuberant, conspicuous, 0.8–1.5(–2) μm diam, somewhat thickened and
darkened-refractive; microcyclic conidiogenesis occurring.
Culture characteristics:
Colonies on PDA reaching 46–49 mm diam after 14 d, olivaceous to
grey-olivaceous due to abundant sporulation, appearing zonate in forming
concentric zones, margin entire edge to slightly undulate, white,
glabrous, aerial mycelium absent or sparse, growth flat with a somewhat
folded and wrinkled colony centre, without prominent exudates,
sporulation profuse. Colonies on MEA reaching 48–49 mm diam,
grey-olivaceous to olivaceous-grey, velvety, olivaceous-grey to
iron-grey reverse, margin entire edge to undulate, radially furrowed,
glabrous to feathery, aerial mycelium sparse, diffuse, growth flat with
slightly elevated colony centre, distinctly wrinkled, prominent exudates
not formed, abundantly sporulating. Colonies on OA attaining 40 mm
diam, grey-olivaceous, margin entire edge, hyaline or white, glabrous,
aerial mycelium absent or sparse, growth flat, without exudates,
sporulation profuse.
Specimens examined: Australia, Victoria, Geelong, Sheraton Hotel, isol. from Eucalyptus sp. (Myrtaceae), 1 Oct. 2005, P.W. Crous, CPC 12385. Cyprus, Polis, Akamas Nature Reserve, isol. from Quercus infectoria (Fagaceae), 20 Mar. 2007, coll. A. van Iperen, isol. P.W. Crous, CPC 13943. Denmark,
isol. from food, garfish gill, 2007, B.A. Andersen, CPC 14306 = BA1705;
isol. from indoor building material, school, 2007, B.A. Andersen, CPC
14300 = BA 1699; isol. from cheese, J. Frisvad, deposited in CBS in Oct.
2000, CBS 109031 = JBT 13731, identified as C. cladosporioides. Germany, Essen, Botanical Garden, isol. from Rosa sp. (Rosaceae), 2005, N. Ale-Agha, CPC 12313. Italy, isol. from Paeonia sp. (Paeoniaceae) by M. Curzi as C. paeoniae, CBS 118.24 = ATCC 36972 = MUCL 10098. New Zealand, Auckland, −37.00, 175.00, isol. from leaf spots of Yucca gigantea (= Y. elephantipes) (Asparagaceae), 20 May 2005, C.F. Hill, CPC 12126 = Hill 1192. Portugal, Aveiro, Aveiro campus, isol. from Ginkgo biloba (Ginkgoaceae), 11 Oct. 2006, P.W. Crous, CPC 13407–13409. Slovenia, Ljubljana, isol. from an air conditioning system (bathroom), 2004, M. Butala, CBS 121627 = CPC 12047 = EXF-967. South Korea, isol. from Dioscorea tenuipes (Dioscoreaceae), 2004, coll. H.D. Shin, isol. P.W. Crous, CPC 11395; isol. from Weigela subsessilis (Caprifoliaceae), 2004, coll. H.D. Shin, isol. P.W. Crous, CPC 11401. Spain,
isol. from margarine, depos. by A.M. Jansen, CBS 261.80; Tenerife,
isol. from an unknown plant, 1 Mar. 2007, P.W. Crous, CPC 13792; isol.
from leaves of Leucadendron sp. (Proteaceae), 1 Mar., P.W. Crous, CPC 13798; isol. from Leucospermum sp. (Proteaceae), 1 Mar. 2007, P.W. Crous, CPC 13795, 13801; isol. from Protea sp. (Proteaceae), 1 Mar. 2007, P.W. Crous, CPC 13789. Turkey, Istanbul, isol. from man, deep mycosis of patient, isol. by A.S. Kantarcioglu, CBS 109501 = dH 12343. UK, Kew, isol. from Arundo leaf (Poaceae) by G.R. Bisby, CBS H-6933, CBS 169.54 = CBS 170.54 = IMI 025324 = NCTC 6740 = dH 15462. USA, Washington, Seattle, University of Washington campus, isol. from chasmothecia of Phyllactinia guttata (Erysiphales) on leaves of Corylus sp. (Betulaceae), 2 Dec. 2004, D. Glawe, CPC 11826, 11827, 11832. Unknown, isol. from leaf spot of Populus tremuloides (Salicaceae), dep. by C.L. Shear in Aug 1929, CBS 133.29 = ATCC 36970.
Substrate and distribution:
Hypersaline water, air, indoor environments, food and plant material;
Australasia (Australia, New Zealand), Asia (South Korea), Europe
(Cyprus, Denmark, Germany, Italy, Portugal, Slovenia, Spain, Turkey,
UK), North America (USA).
Notes: Cladosporium ramotenellum was previously only known from two Slovenian isolates (Schubert et al. 2007b),
one being the type isolated from hypersaline water and an additional
strain isolated from an air conditioning system. Since present molecular
and morphological studies indicate that this species is a quite common
saprobic species occurring on various substrates with a wider geographic
distribution, its species description needs to be emended. Bensch et al. (2012) and Jang et al. (2013) already drew attention to a broadening of the range of several characters for C. ramotenellum. Jang et al. (2013) recorded the species for Korea in a study on moulds inhabiting wood. Furthermore, it was also reported from Korea by Lee et al. (2011) causing sapwood discoloration. Samson (2014) recently showed that C. ramotenellum is also quite common in indoor environments.
Strain CBS 169.54 = CBS 170.54, Bisby's “standard culture”, which was invalidly and erroneously chosen by de Vries (1952) as lectotype for C. cladosporioides, proved to belong to C. ramotenellum. It deviates from typical C. ramotenellum
in having geniculate conidiophores with numerous conidiogenous loci
crowded at the apex, missing ramoconidia and somewhat narrower small
terminal and intercalary conidia.
Cladosporium rhusicola
(CBS 140492). A–D, F–G. Macro-, semimacro- and micronematous
conidiophores and conidial chains. E. Conidial chains. Scale
bars = 10 μm.
Cladosporium rhusicola
(CBS 140492). A. Survey of colony development with swollen hyphal cells
that give rise to young conidiophores. The ornamentation, most probably
of conidia, is also visible. B. Overview on agar surface with several
intact conidiophores ...
Etymology: Epithet composed of the name of the host genus, Rhus, and -cola, dweller.
Mycelium
sparingly branched, filiform to cylindrical-oblong, 1–4 μm wide,
subhyaline to pale olivaceous-brown, smooth to asperulate or
verruculose, walls unthickened, sometimes irregular in outline due to
small swellings and constrictions, some cells distinctly swollen, up to
8 μm diam. Conidiophores micronematous, semimacronematous to
macronematous, arising terminally or laterally from plagiotropous or
ascending hyphae or from bulbous swollen hyphal cells, starting as very
short lateral outgrowths of hyphae; macronematous ones straight to
somewhat flexuous, cylindrical, unbranched, usually with a somewhat
capitate apex, sometimes once geniculate-sinuous,
6–45(–95) × 2.5–3.5 μm, aseptate or only a few septa, septa neither
darkened nor thickened, medium olivaceous-brown, smooth or almost so,
walls unthickened; micronematous to semimacronematous ones filiform to
narrowly cylindrical-oblong, occasionally subnodulose at the apex,
rarely branched, not geniculate, length variable, 1.5–2.5 μm wide,
septate, septa not constricted but often distinctly darkened and
appearing somewhat thickened, subhyaline to pale olivaceous-brown,
minutely verruculose to verruculose or somewhat irregularly
rough-walled, walls unthickened. Conidiogenous cells
integrated, terminal, sometimes intercalary in semi- and macronematous
conidiophores, often slightly swollen at the apex, sometimes once
geniculate-sinuous with conidiogenous loci being situated on unilateral
or multilateral small swellings, in semimacronematous ones apex not or
only slightly swollen, conidiogenous loci conspicuous, protuberant,
1–1.5 μm diam, thickened and darkened-refractive. Conidia
catenate in branched chains, (1–)2–5 conidia in the terminal unbranched
part of the chain, small terminal conidia globose, subglobose, obovoid
to ellipsoid, 3–9 × 2.5–4 μm [av. (± SD) 5.3 (± 1.9) × 3.3 (± 0.5)],
aseptate, apex usually broadly rounded, intercalary conidia broadly
ellipsoid-ovoid, limoniform, 6–13 × (3–)3.5–4.5(–5) μm [av. (± SD) 8.9
(± 2.3) × 3.9 (± 0.5)], 0(–1)-septate, with 1–2(–3) distal hila,
secondary ramoconidia ellipsoid to subcylindrical or obclavate,
obclavate ones commonly formed by semimacronematous conidiophores,
9–18.5(–21) × (3.5–)4–6 μm [av. (± SD) 14.1 (± 3.3) × 4.5 (± 0.7)],
0–1-septate, septa median or often somewhat in the upper half, not very
conspicuous, with (1–)2–3 distal hila, pale to medium olivaceous-brown,
verruculose to verrucose or echinulate, walls slightly thickened, hila
conspicuous, 0.5–1.5 μm diam, thickened and darkened-refractive;
microcyclic conidiogenesis occasionally occurring.
Culture characteristics:
Colonies on PDA attaining 40–58 mm after 14 d, olivaceous-grey to
iron-grey, grey-olivaceous towards margins, reverse greyish blue or
olivaceous-black, fluffy; margins regular, white, narrow, glabrous to
somewhat feathery; aerial mycelium abundantly formed, fluffy, dense and
high; sporulating. Colonies on MEA reaching 42–63 mm, grey-olivaceous to
pale olivaceous-grey or olivaceous-grey at margins, reverse
olivaceous-grey or iron-grey, velvety to wooly-felty; margins regular to
undulate, glabrous, narrow to broad, white; aerial mycelium abundant,
pale olivaceous-grey, loose to dense, fluffy, growth flat, radially
furrowed and wrinkled, sporulation profuse. Colonies on OA attaining
38–50 mm, grey-olivaceous, pale olivaceous-grey to smoke-grey due to
aerial mycelium, reverse leaden-grey to iron-grey, fluffy to
wooly-felty; margins regular, narrow, glabrous; aerial mycelium
abundant, fluffy, loose to dense, covering large parts of the colony;
growth flat; sporulation profuse.
Specimen examined: South Africa, Western Cape Province, Stellenbosch, Assegaaibos, isol. from Rhus sp. (Anacardiaceae), 16 Apr. 2008, coll. F. Roets, isol. P.W. Crous (CBS H-22363, holotype; ex-type culture CBS 140492 = CPC 15219).
Substrate and distribution: On Rhus; South Africa.
Notes: Cladosporium rhusicola, a member of the herbarum species complex, reminds one of C. herbarum
with the conidiophores having terminal swellings. However, the conidial
surface ornamentation in the new species is more prominent than in C. herbarum being verrucose to echinulate, and conidi-ophores and conidia are shorter (Schubert et al., 2007b, Bensch et al., 2012).
Cladosporium ruguloflabelliforme Bensch, Crous & U. Braun, sp. nov. MycoBank MB814637. Fig. 30, Fig. 31.
Cladosporium ruguloflabelliforme
(CBS 140494). A–E. Conidiophores with conidial chains. F. Tip of a
conidiophore with dichotomously branched conidial chains. G. Conidial
chain. Scale bars = 10 μm.
Cladosporium ruguloflabelliforme
(CBS 140494). A. Conidiophore showing several secondary ramoconidia
with hila. Note the shape and loci on the conidiophore itself. Note also
the irregularly reticulate surface ornamentation of conidia. B.
Terminal conidia ...
Etymology: Named after its morphological similarity with Cladosporium flabelliforme and the surface ornamentation of its conidia being rugulose or distinctly rugose (visible with SEM).
Mycelium
unbranched or sparingly branched, 1–3.5 μm wide, subhyaline, pale or
pale medium olivaceous-brown, with scattered irregular loose, rugulose
to rugose structures, sometimes outer walls seem to detach; sometimes
forming anastomoses between two hyphae. Conidiophores macro-,
semimacro- and micronematous, solitary, arising terminally or laterally
from hyphae, narrowly cylindrical-oblong, sometimes once
geniculate-sinuous towards the apex due to sympodial proliferation,
somewhat flexuous, unbranched, occasionally once branched,
40–140(–250) × (2–)2.5–3.5 μm, multiseptate, not constricted,
subhyaline, pale or pale medium olivaceous-brown, almost smooth, loosely
verruculose or irregularly rough-walled, walls somewhat thickened;
micro- and semimacronematous hyphae hardly distinguishable from hyphae. Conidiogenous cells
integrated, usually terminal, occasionally intercalary when geniculate
due to sympodial proliferation, then conidiogenous cells with a single
conidiogenous locus situated on a small lateral shoulder, terminal cells
with (1–)2–3(–4) loci at the apex giving rise to a whirl of secondary
ramoconidia, subcylindrical, 10–24 μm long, loci 1–1.5 μm diam.,
thickened and darkened-refractive. Ramoconidia 19–35 × 3–3.5 μm, often 1-septate, base somewhat darkened-refractive. Conidia
catenate, in long, mostly basely dichotomously branched chains, up to
12 conidia per chain, 2–9 conidia in the unbranched part of the chain;
small terminal conidia ovoid or narrowly ellipsoid, 5.5–7(–8) × 2–3 μm
[av. (± SD) 6.6 (± 0.7) × 2.3 (± 0.4)], intercalary conidia ellipsoid or
fusiform, 6–14 × (2–)2.5–3.5(–4) μm [av. (± SD) 9.2 (± 2.4) × 3.0 (±
0.6)], 0–1-septate, with 1–2 distal hila, secondary ramoconidia
ellipsoid, fusiform or subcylindrical, (8–)11.5–22(–26) × (2.5–)3–4 μm
[av. (± SD) 16.6 (± 4.7) × 3.5 (± 0.6)], 0–2(–3)-septate, septum median
or somewhat in the upper half, septa somewhat darkened, with 1–2(–3)
distal hila, pale or pale medium olivaceous-brown, surface ornamentation
variable, almost smooth, minutely rugulose to rugose, distinctly
reticulate with SEM, walls slightly thickened in larger ones, attenuated
towards apex and base, hila 0.5–1.5(–2) μm diam, slightly thickened and
darkened-refractive; microcyclic Conidi-ogenous occasionally occurring.
Culture characteristics:
Colonies on PDA attaining 40–47 mm after 14 d, olivaceous-grey to
iron-grey, olivaceous-black at margins, reverse iron-grey, greyish blue
at margins, velvety to fluffy-felty; margins hyaline, somewhat feathery,
colony centre somewhat elevated, radially furrowed and folded; aerial
mycelium low or high, fluffy-felty, abundantly formed; numerous small
but prominent exudates formed; sporulation profuse. Colonies on MEA
reaching 45–51 mm, greenish black, shiny, in colony centre
olivaceous-grey due to aerial mycelium and sporulation, reverse
olivaceous-grey, velvety; margin white, narrow, glabrous, radially
furrowed, colony centre wrinkled and folded, elevated; aerial mycelium
dense, fluffy-felty, a single prominent exudate formed. Colonies on OA
reaching 35–43 mm, greenish black, olivaceous-grey due to dense and
fluffy aerial mycelium and sporulation, reverse leaden-grey to
iron-grey; margin narrow, glabrous; growth low convex, without prominent
exudates.
Specimen examined: South Africa, Eastern Cape Province, Grahamstown, Grahamstown Botanical Garden, isol. from Diatrapaceae sp. on Aloe sp. (Xanthorrhoeaceae), 26 Jul. 2011, P.W. Crous (CBS H-22365, holotype; ex-type culture CBS 140494 = CPC 19707).
Substrate and distribution: Isolated from Diatrapaceae on Aloe; South Africa.
Notes: The conidial chains of this species are reminiscent of C. flabelliforme, but the conidia are smooth in the latter species. In the phylogenetic analyses it clusters close to C. dominicanum but based on its morphology it is not a member of the sphaerospermum but the cladosporioides species complex. Cladosporium dominicanum
differs in having subglobose and shorter small terminal conidia
[(2–)3–3.5(–5.5) μm long] and shorter intercalary conidia (3–8.5 μm
long) (Bensch et al. 2012).
Cladosporium rugulovarians
(CBS 140495). A–C. Conidiophores with conidial chains. D–E. Branched
conidiophores. F–H. Tips of conidiophores, with ramoconidia, secondary
ramoconidia and conidia. Scale bars = 10 μm. ...
Cladosporium rugulovarians
(CBS 140495). A. Overview of a colony with a fascicle of long
conidiophores arising from the agar. B. Conidiophore with dislodged
conidia and conidium initial. C. Conidiophores with secondary
ramoconidia forming large amounts ...
Etymology: Name refers to the rugulose surface ornamentation of conidia (visible with SEM) and its morphological similarity to C. varians.
Mycelium sparsely formed, 4–5.5 μm wide, septate, medium or dark olivaceous-brown, verruculose. Conidiophores
macronematous, erect, arising terminally and laterally from hyphae,
very long, geniculate, several times dichotomously branched towards the
apex, branchlets also one or several times dichotomously branched,
mostly at an angle of 5–45°, up to 475 μm long or even longer, at the
base 3.5–5 μm wide and dark olivaceous-brown, becoming distinctly
narrower and paler towards the apex, at the apex about 2 μm wide and
subhyaline, multiseptate, often seceding at one of the lower septa,
smooth, walls thickened at the base, thin-walled at the apex. Conidiogenous cells
integrated, terminal and intercalary, often geniculate, initiation of
conidiogenesis connected with onset of formation of several secondary
ramoconidia (2–4), then growth stopping, often laterally succeeding
after resurgent sympodial proliferation, loci then situated on small
lateral shoulders, up to 60 μm long, conidiogenous loci prominent,
subdenticulate, 1–1.5 μm diam, somewhat thickened and
darkened-refractive. Ramoconidia commonly formed, 20–55 × 3–4.5 μm, 0–1-septate, base 2.5 μm wide. Conidia
numerous, formed in branched chains, straight, small terminal conidia
globose, subglobose, obovoid, 3–6.5 × 3–5 μm [av. (± SD) 4.6 (±
1.1) × 3.8 (± 0.8)], intercalary conidia ovoid or ellipsoid,
5–8.5(–10) × 3.5–5(–6) μm [av. (± SD) 7.1 (± 1.4) × 4.4 (± 0.9)],
aseptate, very rarely 1-septate, with 1–3 distal hila, secondary
ramoconidia narrowly or broadly ellipsoid or subcylindrical, width
depending on the place of formation at the conidiophore, those formed at
narrower and paler apical parts also narrower and paler,
(9–)11–24(–30) μm long, (3–)4–5(–5.5) μm wide when formed at the lower
and wider parts of conidiophores, (2–)2.5–3 μm wide when formed at
apical parts of conidiophores [av. (± SD) 17.9 (± 5.6) × 3.7 (± 1.0)],
subhyaline or pale olivaceous, (1–)2–4(–5) distal hila, 0–2-septate,
sometimes constricted at the median septum; surface ornamentation
variable, reaching from smooth or almost so to verruculose–rugulose,
verrucose–rugose or irregularly rough-walled (LM), with light microscopy
reminiscent of C. verrucocladosporioides (irregularly
wrinkled-striate, reticulate structures in SEM), pigmentation variable,
wider conidia medium or even dark olivaceous-brown, narrower ones
subhyaline or pale olivaceous, walls thickened in wider conidia,
unthickened in narrower ones, conidiogenous hila conspicuous, 0.5–1.5 μm
diam; microcyclic conidiogenesis occurring.
Culture characteristics:
Colonies on PDA olivaceous-grey to iron-grey, reverse olivaceous-black
to leaden-black, velvety to floccose; margins feathery; aerial mycelium
loose, diffuse; growth low convex to convex; without prominent exudates;
sporulation profuse. Colonies on MEA grey-olivaceous, pale
olivaceous-grey due to aerial mycelium, reverse iron-grey to
olivaceous-grey, velvety to floccose; margins white, somewhat feathery,
narrow; aerial mycelium mainly in colony centre, loose, fluffy; growth
low convex to convex, radially furrowed and folded; without prominent
exudates; sporulation profuse. Colonies on OA grey-olivaceous or
olivaceous-grey, pale olivaceous-grey due to aerial mycelium, reverse
leaden-grey to olivaceous-grey, velvety to floccose or fluffy; margins
glabrous, sometimes somewhat rhizoid; aerial mycelium loosely floccose;
growth flat; without prominent exudates; sporulation profuse.
Specimen examined: Brazil, Mato Grosso, Chapada dos Guimarães, Salgadeira, isol. from leaf sheaths of unidentified Poaceae, 18 Aug. 2010, P.W. Crous (CBS H-22366, holotype; ex-type culture CBS 140495 = CPC 18444).
Substrate and distribution: Isolated from leaf sheaths of unidentified Poaceae; Brazil.
Notes: Cladosporium rugulovarians is quite unique and only comparable with C. varians.
In both species, the conidiophores are very long and several times
dichotomously branched towards the apex. However, the conidia in C. varians
are usually smooth with small terminal conidia being narrower, 2.5–3 μm
wide, and secondary ramoconidia being longer [(8–)11–33(–40) μm]. The
surface ornamentation in C. rugulovarians reminds one of C. verrucocladosporioides, which displays rugulose as well as verrucose ornamentation (Bensch et al. 2012). In the phylogenetic analyses it forms a basal sister species to the cladosporioides species complex; based on ITS it is identical to numerous other species belonging to the cladosporioides species complex (Fig. 1). In the individual gene trees it is included within the complex but at a basal position (see TreeBASE).
Cladosporium sinuosum K. Schub. et al., Stud. Mycol. 58: 141. 2007, emend. Fig. 34, Fig. 35, Fig. 36.
Cladosporium sinuosum
(CPC 14000 and CPC 17632). A–G, I–M (CPC 17632). Geniculate-sinuous
conidiophores and conidia, either formed solitary or in short chains. H.
Conidia. Scale bars = 10 μm.
Cladosporium sinuosum
(CPC 14000). A. Overview of a part of a colony on SNA, with numerous
aerial hyphae. B. Detailed overview with hyphae, aerial hyphae,
conidiophores and ornamented conidia. Note the continuous growth of the
conidiophore that forms ...
Mycelium
loosely branched, 1–5(–7) μm wide, irregular in outline due to
swellings and constrictions, sometimes swollen up to 7 μm, subhyaline to
pale olivaceous-brown, smooth, minutely verruculose or irregularly
rough-walled, walls unthickened, sometimes forming loose stromatic
hyphal aggregations of swollen hyphal cells, hyphal cells up to 15 μm
diam, medium brown or olivaceous-brown, walls somewhat thickened;
sterile hyphae sometimes forming ropes. Conidiophores
macronematous, erect, straight to often flexuous, arising terminally and
laterally from hyphae or from swollen bulbous hyphal cells, long,
subnodulose or nodulose, with uni- or multilateral swellings, several
times slightly to distinctly geniculate-sinuous due to sympodial
proliferation, sometimes even zig-zag-like (see Bensch et al. 2012,
fig. 282B), unbranched or branched, up to 380 μm long, (3.5–)4–6(–7) μm
wide, swellings up to 10 μm wide, multiseptate, medium
olivaceous-brown, smooth or minutely verruculose, walls thickened,
sometimes even distinctly two-layered, 1(–1.5) μm thick. Conidiogenous cells
integrated, terminal and intercalary, cylindrical-oblong, with 1–2 uni-
or multilateral swellings per cell, rarely more, geniculate-sinuous,
8–31(–45) μm long, loci confined to swellings, up to four loci per
nodule, loci conspicuous, prominent, 1–2(–2.2) μm diam, thickened and
darkened-refractive. Conidia solitary or in short unbranched or
branched chains, up to four conidia in a chain, conidia without a
distal hilum ovoid, obovoid to broadly ellipsoid or doliiform,
(5–)8–15 × (4–)5–8(–9) μm [av. (± SD) 10.9 (± 2.8) × 6.8 (± 1.1)],
0–1-septate, basal and intercalary conidia ellipsoid–ovoid to
subcylindrical, 11–19(–24) × (5–)6–9(–11) μm [av. (± SD) 16.0 (±
2.8) × 7.7 (± 1.0)], 0–1(–2)-septate, septa median or somewhat in the
upper half, becoming curved or sinuous with age, pale olivaceous to
medium olivaceous-brown or pale greyish brown, densely verrucose to
echinulate, walls appearing to be thick-walled due to surface
ornamentation, 1–2 μm wide, with 1–2(–3) distal hila, hila protuberant,
more or less conspicuous, sometimes immersed in surface ornamentation
and therefore not very prominent, 1–2 μm diam, thickened and
darkened-refractive; microcyclic Conidi-ogenous not observed on SNA but
occurring while growing on PDA, MEA and OA.
Culture characteristics:
Colonies on PDA attaining 28–47 mm after 14 d, smoke-grey to pale
olivaceous-grey due to aerial mycelium, grey-olivaceous towards margins,
reverse leaden-grey or olivaceous-black, fluffy-felty, margins somewhat
feathery, aerial mycelium high, loose to dense, fluffy, growth low
convex, without prominent exudates. Colonies on MEA reaching 38–55 mm,
greenish grey to grey-olivaceous, white or smoke-grey due to abundant
aerial mycelium, reverse olivaceous-grey, wooly-felty, margins white,
narrow, glabrous to somewhat feathery, radially furrowed and folded,
aerial mycelium loose to dense, fluffy to wooly or diffuse, growth flat
or effuse, sporulation profuse. Colonies on OA attaining 18–37 mm,
white, smoke-grey to pale olivaceous-grey, olivaceous-grey at margins,
reverse iron-grey or leaden-grey, wooly-felty, margins crenate, aerial
mycelium abundant, covering almost the whole colony, wooly-felty, dense,
low to high, growth flat, sporulation profuse.
Specimens examined: France, isol. from an unidentified moss, isol. by J. Nicot-Toulouse, CBS 164.48 = ATCC 11285, stored as C. macrocarpum. Germany, Dierhagen, isol. from Eryngium maritimum (Asteraceae), 2 Oct. 2009, U. Damm, CPC 17632. Netherlands, Schiermonnikoog, isol. from air, isol. by A. Kikstra, CBS 393.68, stored as C. macrocarpum; Utrecht, De Uithof, isol. from Iris pseudacorus (Iridaceae), 26 Jun. 2010, P.W. Crous, CPC 18365. New Zealand, South Canterbury, Fairlie, State Highway 8, isol. from Crocus sativus (Iridaceae), 14 Jul. 2008, J. Rennie, CPC 15454. South Africa, Free State, Bethlehem, isol. from wheat (Poaceae), 1982, MRC 02998 = CPC 14000.
Substrate and distribution: Isolated from various plants, air and mosses; Europe (France, Germany, Netherlands), New Zealand and South Africa.
Notes: Cladosporium sinuosum, introduced by Schubert et al. in 2007 as a member of the herbarum species complex, was described on living leaves of Fuchsia excorticata from New Zealand. It is a heterosporium-like species, morphologically similar to C. macrocarpum
but its conidia are formed either singly or in short unbranched chains
being 0–1(–2)-septate. Terminal conidia without a distal hilum are
longer and wider, broadly ellipsoid-ovoid and doliiform and
micronematous conidiophores as occurring in C. macrocarpum are missing. Cladosporium herbarum
differs in having distinctly narrower conidia. Until now, it was only
known from the type. In the present phylogenetic study, several isolates
from different substrates from Europe and South Africa are shown to
belong to this species (see Fig. 2). Therefore, the species description, host range and distribution of C. sinuosum need to be emended.
Cladosporium subinflatum K. Schub. et al., Stud. Mycol. 58: 153. 2007.
Specimen examined: Ukraine, Svjatie Gory, isol. from Iris sp. (Iridaceae), 18 Jul. 2008, coll. A. Akulov, isol. P.W. Crous, CPC 15565.
Notes: Until now C. subinflatum has only been known from hypersaline environments, but it can also be saprobic as shown by the isolate from Iris sp. The isolate fits the species concept of C. subinflatum although the small swellings of the conidiophores are not as prominent as in the type.
Cladosporium subuliforme Bensch et al., Stud. Mycol. 67: 77. 2010.
Specimens examined: Brazil, Mato Grosso, on cotton (Gossypium sp.) leaves, coll. D.B. da Silva, isol. P.W. Crous, CPC 18243. Mexico, Tamanlipas, isol. from Agave tequilana var. azul (Agavaceae), 16. Oct. 2009, coll. M. de Jesús Yáñez-Morales, isol. P.W. Crous, CPC 15838; isol. from orange (Citrus sp., Rutaceae), 16 Oct. 2008, coll. M. de Jesús Yáñez-Morales, isol. P.W. Crous, CPC 15833. South Africa, Western Cape Province, Jonkershoek, isol. from Eucalyptus sp. (Myrtaceae), 12 Jan. 2009, coll. A.R. Wood, isol. P.W. Crous, CPC 16318.
Notes: Until now, this species has been recorded only from the type locality in Thailand (Bensch et al. 2010).
It is herewith reported from Mexico and South Africa and probably has
an even wider distribution. The conidiophores are macro-, semimacro- or
micronematous, 2–3.5(–4) μm wide with the base up to 5 μm, occasionally
they can be subnodulose or nodulose, both intercalary or at the apex.
Superficial mycelium is abundantly formed, and the hyphae are up to 6 μm
wide at the base of conidiophores. Secondary ramoconidia of the
isolates cited above are slightly longer than in the type specimen
[(6–)8–27(–31) μm].
Cladosporium velox Zalar et al., Stud. Mycol. 58: 181. 2007.
Specimen examined: Brazil, Chapada dos Guimaraes, Capim colonias, stop 1, −15.3621°, −55.0322°, isol. from Zea mays (Poaceae), 18 Aug. 2010, P.W. Crous, CPC 18450.
Notes: This is the first record of C. velox
for South America, which has until now been known from Europe and Asia.
In the specimen from Brazil, which fits the species circumscription of C. velox very well, ramoconidia were observed being 28–50 × 2.5–3 μm, 0–1-septate with a base of about 2.5 μm width.
Cladosporium versiforme (CBS 140491). A–G. Macro-, semimacro- and micronematous conidiophores and conidial chains. Scale bars = 10 μm.
Cladosporium versiforme
(CBS 140491). A. Conidiophores sprouting from hyphae or swollen
intercalary cells on the agar surface or arising from an aerial hypha.
B–D. Conidiophores with a characteristic rounded shape on which
relatively narrow loci ...
Etymology:
Name refers to the different polymorph shapes of conidiophores and
conidia and the variable forms of conidial surface ornamentation.
Mycelium
commonly formed, creeping or ascending, unbranched or loosely branched,
narrow or broad, 1–6 μm wide, subhyaline or pale olivaceous-brown,
surface ornamentation variable, almost smooth or loosely verruculose,
walls unthickened, sometimes forming ropes of a few hyphae, rarely
anastomosing. Conidiophores polymorphic, arising terminally
from ascending hyphae or laterally, solitary, shape, colour and surface
ornamentation very variable, macro-, semimacro- and micronematous,
filiform or narrowly cylindrical, mainly unbranched, occasionally once
branched at a lower level, in macronematous ones apex usually broadened
or swollen, laterally proliferated, occasionally with additional
intercalary swellings or lateral shoulders, in micro- and
semimacronematous conidiophores usually without lateral shoulders or
swellings, sometimes apically subnodulose, maximum length ambiguous
especially in conidiophores arising terminally from hyphae, up to 150 μm
long or even longer, with few septa, those arising laterally from
hyphae usually shorter, 7–61 μm long, 1–2-septate, macronematous
conidiophores 3–4 μm wide, swellings or shoulders 5–7 μm wide, micro-
and semimacronematous conidiophores 2–3 μm wide, subhyaline, pale or
medium olivaceous-brown, smooth, minutely verruculose or loosely
verruculose, walls unthickened, slightly thick-walled in macronematous
ones. Conidiogenous cells variable in shape, mainly terminal,
sometimes intercalary, in terminal cells subnodulose, capitate or with
lateral proliferation and therefore irregular in shape, conidiogenous
loci confined to these proliferations and swellings, usually 3–6 loci,
rarely more, crowded at the apex, in unswollen cells usually 1–2 loci at
the apex, 7–30 μm long, loci conspicuous, prominent, sometimes
subdenticulate, 1–2 μm diam, thickened and darkened-refractive. Ramoconidia up to 45 μm long and with up to five septa, hardly distinguishable from secondary ramoconidia of the second type (see below). Conidia
very variable in shape, size and colour, two different types formed in
unbranched or loosely branched chains with 2–5 conidia in the terminal
unbranched part of the chain, conidia of the first type herbarum-like
usually formed by macronematous conidiophores, broader and darker,
medium or dark olivaceous-brown, small terminal conidia globose,
subglobose, broadly obovoid, 4.5–9 × 4–7 μm [av. ± SD, 6.9 (± 1.5) × 5.4
(± 1.0) μm], aseptate, intercalary conidia broadly ellipsoid,
7–15 × (4–)4.5–6(–7) μm [av. ± SD, 9.9 (± 1.9) × 5.7 (± 0.9) μm],
0(–1)-septate, secondary ramoconidia broadly ellipsoid or
subcylindrical, 9–30 × 5–7.5 μm [av. ± SD, 17.9 (± 5.8) × 6.3 (±
0.8) μm], 0–3-septate; conidia of the second type paler and narrower,
more commonly septate, pale olivaceous-brown or subhyaline, small
terminal conidia subglobose, ovoid or ellipsoid, 4–18 × 3–5 μm
[av. ± SD, 8.4 (± 5.9) × 3.7 (± 0.4) μm], intercalary conidia ellipsoid
or subcylindrical, 6–21 × 3.5–5 μm [av. ± SD, 14.9 (± 6.1) × 3.7 (±
0.3) μm], 0–1-septate, secondary ramoconidia subcylindrical or
cylindrical, often curved, 14–38 × 4–6 μm [av. ± SD, 28.2 (± 8.3) × 4.6
(± 0.6) μm], 1–4-septate, sometimes slightly to distinctly constricted
at single septa in both types, becoming sinuous with age, surface
ornamentation ranging from almost smooth to minutely verruculose,
verruculose or verrucose, walls unthickened or slightly thick-walled,
hila conspicuous, 0.5–2 μm diam, thickened and darkened-refractive;
microcyclic conidiogenesis occurring with conidia forming secondary
conidiophores.
Culture characteristics:
Colonies on PDA reaching up to 70 mm after 14 d, olivaceous-black,
olivaceous-grey due to sporulation, pale vinaceous due to aerial
mycelium, releasing a vinaceous pigment into the agar, reverse
olivaceous-grey or dark vinaceous, fluffy-felty; margins feathery;
aerial mycelium dense, covering large parts oft he colony surface,
felty; very small exudates formed. Colonies on MEA attaining 62–72 mm,
grey-olivaceous or olivaceous where sporulating profusely, whitish or
rosy buff due to abundant, felty or fluffy aerial mycelium, reverse
olivaceous-grey, brick or cinnamon; margin broad, somewhat feathery,
radially furrowed, colony centre folded and wrinkled; small exudates
start to be formed after 14 d. Colonies on OA reaching 55–62 mm,
grey-olivaceous or olivaceous where sporulating abundantly, smoke-grey
or rosy-vinaceous due to felty aerial mycelium, releasing some vinaceous
soluble pigment into the agar, reverse dark vinaceous and livid-red,
olivaceous-grey towards margins, velvety to fluffy-felty; margins
glabrous, regular, growth flat, without prominent exudates.
Specimen examined: Iran, isol. from Hordeum sp. (Poaceae), 12 May 2009, P.W. Crous (CBS H-22362, holotype; ex-type culture CBS 140491 = CPC 19053).
Substrate and distribution: On Hordeum; Iran.
Notes: Shape of conidia and conidiophores is very polymorphic in C. versiforme, which is also true for surface ornamentation and colour. This new species belongs to the herbarum species complex (Fig. 2). Cladosporium herbaroides,
isolated from hypersaline water in Israel, is characterised by also
having two different types of conidia but is easily distinguishable from
the new species in having longer and somewhat wider conidiophores
(30–230 μm long or even longer, 3–5 μm wide), longer conidiogenous
cells, and narrower conidia in both conidial types [(2–)3–6(–7) μm and
2–3.5 μm] (Schubert et al., 2007b, Bensch et al., 2012). Cladosporium basiinflatum, isolated from Hordeum in Germany, and C. herbarum, epitypified by material isolated from Hordeum in Belgium, are morphologically and phylogenetically quite distinct.
Cladosporium xylophilum Bensch et al., Stud. Mycol. 67: 77. 2010.
Specimen examined: Mexico, Chiapas, isol. from banana (Musa sp., Musaceae), 16 Dec. 2008, coll. M. de Jesús Yáñez-Morales, isol. P.W. Crous, CPC 16356.
Notes:
With its typical clusters of pronounced conidiogenous loci in
intercalary conidia and secondary ramoconidia, this specimen matches the
species concept of C. xylophilum. It is the first report of this species from Mexico.
Discussion
Cladosporium
represents one of the most common, widely distributed genera of fungi,
occurring in and on all kinds of materials, from soil to plants, food,
paint, textiles and air, even causing human infections (Bensch et al., 2012, Sandoval-Denis et al., 2015). The first DNA phylogeny of Cladosporium s. lat. (Braun et al. 2003), clearly confirmed the genus as polyphyletic. Sexual morphs of Cladosporium s. str. were originally included in Mycosphaerella, but later the genus Davidiella (Davidiellaceae) was subsequently introduced to accommodate them (Schoch et al. 2006). Species of Davidiella have ascospores with irregular cellular inclusions (lumina), which are absent in species of Mycosphaerella (Aptroot 2006), along with periphysoids and pseudoparaphyses (Schubert et al. 2007b).
Since this study, the International Code of Nomenclature for algae,
fungi and plants changed, having profound implications for fungi, most
importantly being the end of dual nomenclature (Wingfield et al., 2012, Crous et al., 2015), meaning that Davidiella is no longer recognised, being a synonym of Cladosporium (Cladosporiaceae). Cladosporiaceae took preference over the younger Davidiellaceae (Bensch et al. 2012), while Mycosphaerella has become a synonym of Ramularia (Mycosphaerellaceae) (Videira et al. 2015). Other major changes that occurred related to the separation of cladosporium-like genera into separate entities, e.g.
Seifert et al. (2004) established Devriesia (Teratosphaeriaceae, Crous et al. 2007b) to accommodate a group of heat-resistant species. Heuchert et al. (2005), separated Digitopodium (incertae sedis) and Parapericoniella (incertae sedis), while Crous et al. (2006) introduced Metulocladosporiella (Chaetothyriales, Herpotrichiellaceae) for the taxa causing freckle disease of banana. Further studies separated several species into newly established genera, e.g. Penidiella (Capnodiales, Teratosphaeriaceae), Rachicladosporium (Capnodiales, Cladosporiaceae), Toxicocladosporium (Capnodiales, Cladosporiaceae), Verrucocladosporium (Capnodiales, Cladosporiaceae), Hyalodendriella (Helotiales, incertae sedis), Ochrocladosporium (Pleosporales, incertae sedis), Rhizocladosporium (Helotiales, incertae sedis) (Crous et al. 2007c) and Graphiopsis (Capnodiales, Cladosporiaceae) (Schubert et al., 2007a, Braun et al., 2008). Seifert et al. (2007) also delineated Amorphotheca (Leotiomycetes, Myxotrichaceae) and Hormodendrum (as Sorocybe; Chaetothyriales, incertae sedis) from Cladosporium. Finally, Quaedvlieg et al. (2014) allocated several lineages that were penidiella- and devriesia-like to novel genera, namely Neopenidiella (Capnodiales, Mycosphaerellaceae), Neodevriesia (Capnodiales, Neodevriesiaceae), Apenidiella, Eupenidiella, Myrtapenidiella, Queenslandipenidiella and Xenopenidiella (Capnodiales, Teratosphaeriaceae). Several species originally placed in Cladosporium also proved to belong to Passalora s. lat., Pseudocercospora, and Zasmidium s. lat., respectively (Crous and Braun, 2003, Schubert and Braun, 2005a, Schubert and Braun, 2005b, Schubert and Braun, 2007, Braun and Schubert, 2007).
Although Cladosporium
has always been recognised as one of the largest and most heterogeneous
genera of hyphomycetes encompassing more than 772 names (Dugan et al. 2004), the recent monographic treatment by Bensch et al. (2012) only recognised 170 true Cladosporium
species. In spite of this, revisions of established morphological
species revealed some of them to represent species complexes, namely C. herbarum s. lat., C. sphaerospermum s. lat. and C. cladosporioides s. lat. (Zalar et al., 2007, Schubert et al., 2007b, Bensch et al., 2010).
The description of several novel species in the present study is
therefore not that surprising. These are the result of continuous
isolations from a range of substrates, collected in various continents.
The polyphasic approach delineated by Bensch et al. (2012), employing morphology and a range of phylogenetic markers has proven to work well for species delimitation within the genus Cladosporium.
The
current concept of the three species complexes is based on morphology
only and does not always agree with the phylogenetic position of the
included species. The concept of species complexes is used for practical
purposes to indicate a morphological similarity of species and not to
divide the genus into smaller phylogenetic entities. Furthermore, a
species complex is not a taxonomic term ruled by the ICN but can freely
be defined and used. Morphological features describing the three
recognised species complexes within Cladosporium can be summarised as follows:
Species belonging to the herbarum
complex are characterised by possessing conidia which are ornamentated
ranging from minutely verruculose to verrucose, echinulate or spinulose.
The surface ornamentation varies based on the length of surface
protuberances and in the density of ornamentation. Most of the species
possess nodulose conidiophores with the Conidi-ogenous confined to the
usually lateral swellings. However, this phenetic trend is not expressed
in all of the species belonging to the herbarum complex, e.g. C. subtilissimum and C. limoniforme (Schubert et al. 2007b). The ITS locus is not very successful in distinguishing species in this complex (3 / 19 species resolved), whereas act and tef1 are more or less equal in their ability to distinguish species in the complex (19 / 19 and 18 / 19, respectively).
Species of the cladosporioides
species complex usually have narrowly cylindrical or
cylindrical-oblong, non-nodulose, mostly non-geniculate conidiophores.
Nodose conidiophores with distinct regular, more pronounced swellings,
clearly separated and distant from each other, are formed only in C. colocasiae, C. oxysporum and partly also in C. tenuissimum. However, the process of conidiogenesis differs from that in the herbarum
complex where the conidiophores often possess multilateral swellings
round about the stalks, usually formed in quick succession which give
the conidiophores a somewhat gnarled or knotty appearance. Surface
ornamentation of conidia in the cladosporioides complex is quite variable ranging from smooth or almost so to irregularly verrucose–rugose or rough-walled (Bensch et al. 2010). The most prominent surfaces are formed by C. acalyphae, C. exasperatum, C. rugulovarians and C. verrucocladosporioides.
What appears to be lightmicroscopically verrucose–rugose represents
irregularly reticulate structures or embossed stripes (ridges) under
SEM. True verrucose conidia are not known for species belonging to the cladosporoides
complex until now. The ITS locus is not very successful in
distinguishing species in this complex (3 / 44 species resolved),
whereas act and tef1 are more or less equal in their ability to distinguish species in the complex (39 / 44 and 38 / 44, respectively).
The most remarkable feature of species belonging to the sphaerospermum
complex is the formation of numerous globose or subglobose terminal and
intercalary conidia. Surface ornamentation is very variable; all types
of ornamentation occurring in the other two species complexes are
expressed here ranging from almost smooth (C. dominicanum) to minutely verruculose (C. fusiforme, C. langeronii), verrucose (C. halotolerans) or rugose (C. ruguloflabelliforme).
Conidiophores of all sphaerospermum-like species, are usually
ascending, neither nodulose nor geniculate and can sometimes be poorly
differentiated from their supporting hyphae. The ITS locus is rather
successful in distinguishing species in this complex (10 / 14 species
resolved), whereas act and tef1 are more or less equal in their ability to distinguish species in the complex (13 / 14 and 14 / 14, respectively).
Although all species belonging to the herbarum and cladosporioides complex are also phylogenetically allied, species of the sphaerospermum
complex are phylogenetically not monophyletic. The complex is becoming
increasingly more paraphyletic as more species with these morphological
features are added to the molecular phylogeny, which means that this
type of morphology has evolved several times. This is also mirrored in
the resolution of ITS for the identification of a species to the species
complex level in Cladosporium – ITS is actually quite successful in resolving individual species in the sphaerospermum species complex, whereas it fares rather poorly in the other two species complexes, which indicates that species of the sphaerospermum species complex are genetically quite diverse compared to the other two species complexes.
Based on their morphology most of the Cladosporium species can be referred to one of the three species complexes. There are however, a few exceptions, e.g. C. aciculare which is phylogenetically allied to C. sphaerospermum or C. ruguloflabelliforme which clusters with C. dominicanum. These two species morphologically rather resemble species of the cladosporioides complex.
In
spite of the novel taxa introduced here, the continuous collection of
isolates also meant that the species concepts, host ranges and
distributions of some species could be emended and expanded, most
notably that of C. ramotenellum and C. sinuosum. Furthermore, as we continue to collect and culture more isolates of Cladosporium
spp., we expect to reveal even more species within the genus. Further
collections would hopefully also shed more light on their ecology, as
species of Cladosporium exhibit an interesting range of life
styles, ranging from saprobes to endophytes, mycophylic species,
biocontrol agents, as well as human and plant pathogens.
Acknowledgements
The
authors thank the technical staff, Mieke Starink-Willemse and Patrick
Arensman (DNA isolation and sequencing), Arien van Iperen (cultures),
Trix Merkx (deposit of isolates) and Marjan Vermaas (photographic
plates) for their invaluable assistance.
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