Abstract
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New species of Cladosporium associated with human and animal infections
Abstract
Cladosporium is mainly known as a ubiquitous environmental saprobic fungus or plant endophyte, and to date, just a few species have been documented as etiologic agents in vertebrate hosts, including humans. In the present study, 10 new species of the genus were isolated from human and animal clinical specimens from the USA. They are proposed and characterized on the basis of their morphology and a molecular phylogenetic analysis using DNA sequences from three loci (the ITS region of the rDNA, and partial fragments of the translation elongation factor 1-alpha and actin genes). Six of those species belong to the C. cladosporioides species complex, i.e., C. alboflavescens, C. angulosum, C. anthropophilum, C. crousii, C. flavovirens and C. xantochromaticum, three new species belong to the C. herbarum species complex, i.e., C. floccosum, C. subcinereum and C. tuberosum; and one to the C. sphaerospermum species complex, namely, C. succulentum. Differential morphological features of the new taxa are provided together with molecular barcodes to distinguish them from the currently accepted species of the genus.
INTRODUCTION
The genus Cladosporium (Cladosporiaceae, Capnodiales) is a large genus of the Ascomycota. It comprises 189 species, mostly saprobes with a worldwide distribution and isolated from a wide range of substrates (David 1997, Bensch et al. 2012, 2015, Crous et al. 2014). The genus also includes common endophytes, plant pathogens often causing leaf spots or other lesions, as well as hyperparasites of other fungi (Bensch et al. 2012). Certain species are relevant as potential biocontrol agents for plant diseases (Köhl et al. 2015) or, in the food industry, as fruit contaminants causing spoilage in low temperature storage or on cereals such as barley, oat, rye and wheat (Samson et al. 2010, Kulik et al. 2014, Frasz & Miller 2015). The role of cladosporia is not well understood in human pathology. Their small conidia are easily dispersed, making them one of the most common air-borne microorganisms (David 1997, De Hoog et al. 2011). They are among the most important allergenic fungi linked to allergic rhinitis and respiratory arrest in asthmatic patients (Black et al. 2000, Sellart-Altisent et al. 2007). Some species are described as a cause of opportunistic phaeohyphomycosis, including subcutaneous and deep infections in humans and animals (De Hoog et al. 2011, Sandoval-Denis et al. 2015), although, their ubiquitous nature suggests that in some reports they may be mere colonizers.
Species identification in Cladosporium has always relied on the morphology of the conidiogenous apparatus together with data on host ranges (Crous et al. 2007b, Bensch et al. 2012). Traditionally, those dematiaceous fungi showing branched acropetal chains of aseptate to septate conidia were included in Cladosporium, which has made it a large and complex group of fungi difficult to differentiate (Bensch et al. 2012). However, recent phylogenetic studies have helped to clarify the taxonomy of these fungi and demonstrated that most of the well-known morphologically-defined species comprises several phylogenetically cryptic species practically impossible to identify using morphological criteria alone (Braun et al. 2003, 2008; Crous et al. 2007b, Zalar et al. 2007, Schubert et al. 2007, 2009, Bensch et al. 2010, 2012, 2015). In its current circumscription, the genus Cladosporium includes dematiaceous fungi with solitary to fasciculate conidiophores, proliferating mostly sympodially and forming unbranched or branched acropetal conidial chains. However, the most characteristic feature is the presence of a thick refractive to darkened cladosporioid or coronate scar, defined as a raised periclinal rim with a central convex dome (Schubert et al. 2007, Bensch et al. 2012). The sexual morph (previously assigned to the genus Davidiella) is characterised by pseudothecial ascomata, 8-spored obovoid to subcylindrical asci, and hyaline, obovoid to ellipsoid ascospores showing irregular luminar inclusions (Schubert et al. 2007).
In recent years, the survey of unexplored habitats and sources by using molecular techniques has expanded our knowledge of fungal diversity. Similarly, clinical specimens have become an important source of undescribed fungi, including both true pathogens and/or also contaminants/colonizers (Gilgado et al. 2005, Perdomo et al. 2013, Giraldo et al. 2014, Guinea et al. 2015, Sandoval-Denis et al. 2015) that had not been recognizable previously because of their poor morphological differentiation (De Hoog et al. 2015).
In order to assess the real prevalence of Cladosporium in the clinical setting and the spectrum of species associated with clinical samples, we studied a large set of Cladosporium isolates from human and animal clinical origin using both molecular characterisation and phenotypic features (Sandoval-Denis et al. 2015). Surprisingly, we found that nearly 40 % of the isolates could not be assigned to any known species and probably represented new species for the genus. The objective of the present study is therefore to determine the phylogenetic relationships of those previously unidentified isolates by using the criteria currently accepted in the taxonomy of this genus.
MATERIALS AND METHODS
Fungal isolates
A total of 48 isolates from clinical origin and belonging to the genus Cladosporium were included in this study, 35 of which corresponded to putatively undescribed species (Table 1). All the isolates were obtained from human and animal clinical specimens from the United States, submitted to the Fungus Testing Laboratory at the University of Texas Health Science Center at San Antonio (UTHSCSA) from different geographic regions of the country for either identification purposes and/or antifungal susceptibility studies.
Table 1
Speciesa | Strain numberb | Substratec | GenBank accession numbers | ||
---|---|---|---|---|---|
ITS | tef1 | ActA | |||
Cercospora beticola | CBS 116456 | Beta vulgaris | NR_121315 | AY840494 | AY840458 |
Cladosporium acalyphae | CBS 125982T | Acalypha australis | HM147994 | HM148235 | HM148481 |
Cladosporium aciculare | CBS 140488T | Syzygium corynanthum | KT600411 | KT600509 | KT600607 |
Cladosporium aggregatocicatricatum | CBS 140493T | Culture contaminant | KT600448 | KT600547 | KT600645 |
Cladosporium alboflavescens | CBS 140690T = UTHSC DI-13-225 = FMR 13338 | Animal, BAL | LN834420 | LN834516 | LN834604 |
Cladosporium allicinum | CBS 121.47 | Food, frozen Phaseolus vulgaris | KT600364 | KT600461 | KT600560 |
CBS 121624T | Hordeum vulgare | EF679350 | EF679425 | EF679502 | |
CBS 160.59 | Human, sputum | KT600366 | KT600463 | KT600562 | |
CBS 374.53 | Centaurea rhapontica = Rhaponticum scariosum subsp. rhaponticum | KT600368 | KT600465 | KT600564 | |
CPC 16759 | Alnus glutinosa | KT600374 | KT600471 | KT600570 | |
UTHSC DI-13-170 = FMR 13295 | Human, toenail | LN834409 | LN834505 | LN834593 | |
UTHSC DI-13-173 = FMR 13298 | Human, lung | LN834353 | LN834449 | LN834537 | |
Cladosporium allii | CBS 101.81 | Allium porrum | JN906977 | JN906983 | JN906996 |
Cladosporium angulosum | CBS 140692T = UTHSC DI-13-235 = FMR 13348 | Human, BAL | LN834425 | LN834521 | LN834609 |
CPC 11526 | Acacia mangium | HM148127 | HM148371 | HM148616 | |
CPC 14566 | Corymbia foelscheana | HM148147 | HM148391 | HM148636 | |
CPC 18494 | Ananas comosus | KT600413 | KT600511 | KT600609 | |
CPC 18496 | Ananas comosus | KT600414 | KT600512 | KT600610 | |
Cladosporium angustiherbarum | CBS 140479T | Pinus ponderosa | KT600378 | KT600475 | KT600574 |
Cladosporium angustisporum | CBS 125983T | Alloxylon wickhamii | HM147995 | HM148236 | HM148482 |
UTHSC DI-13-240 = FMR 13353 | Human, nail | LN834356 | LN834452 | LN834540 | |
Cladosporium angustiterminale | CBS 140480T | Banksia grandis | KT600379 | KT600476 | KT600575 |
Cladosporium antarcticum | CBS 690.92T | Caloplaca regalis | EF679334 | EF679405 | EF679484 |
Cladosporium anthropophilum | CBS 117483 | Unknown | HM148007 | HM148248 | HM148494 |
CBS 140685T = UTHSC DI-13-269 = FMR 13382 | Human, BAL | LN834437 | LN834533 | LN834621 | |
CPC 11122 | Phytolacca americana | HM148019 | HM148260 | HM148506 | |
UTHSC DI-13-168 = FMR 13293 | Human, BAL | LN834407 | LN834503 | LN834591 | |
UTHSC DI-13-169 = FMR 13294 | Human, BAL | LN834408 | LN834504 | LN834592 | |
UTHSC DI-13-178 = FMR 13303 | Animal, abscess | LN834410 | LN834506 | LN834594 | |
UTHSC DI-13-179 = FMR 13304 | Human, hand | LN834411 | LN834507 | LN834595 | |
UTHSC DI-13-207 = FMR 13320 | Human, CSF | LN834413 | LN834509 | LN834597 | |
UTHSC DI-13-226 = FMR 13339 | Human, BAL | LN834421 | LN834517 | LN834605 | |
UTHSC DI-13-228 = FMR 13341 | Human, foot skin | LN834423 | LN834519 | LN834607 | |
UTHSC DI-13-244 = FMR 13357 | Human, BAL | LN834428 | LN834524 | LN834612 | |
UTHSC DI-13-246 = FMR 13359 | Human, BAL | LN834430 | LN834526 | LN834614 | |
UTHSC DI-13-271 = FMR 13384 | Human, BAL | LN834439 | LN834535 | LN834623 | |
Cladosporium aphidis | CBS 132182ET | Echium pininana | JN906978 | JN906984 | JN906997 |
Cladosporium arthropodii | CBS 124043ET | Leaf lesions of rock lily | JN906979 | JN906985 | JN906998 |
Cladosporium asperulatum | CBS 126339 | Eucalyptus leaf litter | HM147997 | HM148238 | HM148484 |
CBS 126340T | Protea susannae | HM147998 | HM148239 | HM148485 | |
Cladosporium australiense | CBS 125984T | Eucalyptus moluccana | HM147999 | HM148240 | HM148486 |
Cladosporium austroafricanum | CBS 140481T | Leaf litter | KT600381 | KT600478 | KT600577 |
Cladosporium austrohemisphaericum | CBS 140482T | Lagunaria patersonia, black mould on fruit surface | KT600382 | KT600479 | KT600578 |
Cladosporium basiinflatum | CBS 822.84T | Hordeum vulgare | HM148000 | HM148241 | HM148487 |
Cladosporium chalastosporioides | CBS 125985T | Fruiting bodies of T. proteae-arboreae on leaves of Protea arborea | HM148001 | HM148242 | HM148488 |
Cladosporium chubutense | CBS 124457T | Needles of Pinus ponderosa | FJ936158 | FJ936161 | FJ936165 |
Cladosporium cladosporioides | CBS 113738 | Grape bud | HM148004 | HM148245 | HM148491 |
CBS 112388T | Indoor air | HM148003 | HM148244 | HM148490 | |
CPC 14292 | Soil, pea field | HM148046 | HM148287 | HM148533 | |
UTHSC DI-13-215 = FMR 13328 | Human, sputum | LN834360 | LN834456 | LN834544 | |
Cladosporium colocasiae | CBS 386.64T | Colocasia antiquorum | HM148067 | HM148310 | HM148555 |
CBS 119542 | Leaf of Colocasia esculanta | HM148066 | HM148309 | HM148554 | |
Cladosporium colombiae | CBS 274.80BT | Dead leaf, Cortaderia | FJ936159 | FJ936163 | FJ936166 |
Cladosporium crousii | CBS 140686T = UTHSC DI-13-247 = FMR 13360 | Human, BAL | LN834431 | LN834527 | LN834615 |
Cladosporium cucumerinum | CBS 171.52ET | Fruit of Cucumis sativus | HM148072 | HM148316 | HM148561 |
CBS 173.54 | Fruit of Cucumis sativus | HM148074 | HM148318 | HM148563 | |
Cladosporium cycadicola | CPC 17251T | Leaves of Cycas media | KJ869122 | KJ869236 | KJ869227 |
Cladosporium delicatulum | CBS 126342 | Indoor building material | HM148079 | HM148323 | HM148568 |
CBS 126344 | Leaves of Tilia cordata | HM148081 | HM148325 | HM148570 | |
Cladosporium dominicanum | CBS 119415T | Hypersaline water | DQ780353 | JN906986 | EF101368 |
Cladosporium echinulatum | CBS 123191 | Leaf of Dianthus barbatus | JN906980 | JN906987 | JN906999 |
Cladosporium exasperatum | CBS 125986T | Eucalyptus tintinnans | HM148090 | HM148334 | HM148579 |
Cladosporium exile | CBS 125987T | Chasmothecia of P. guttata on leaves of Corylus avellana | HM148091 | HM148335 | HM148580 |
Cladosporium flabelliforme | CBS 126345T | Melaleuca cajuputi | HM148092 | HM148336 | HM148581 |
UTHSC DI-13-267 = FMR 13380 | Human, sputum | LN834361 | LN834457 | LN834545 | |
Cladosporium flavovirens | CBS 140462T = UTHSC DI-13-273 = FMR 13386 | Human, toenails | LN834440 | LN834536 | LN834624 |
Cladosporium floccosum | CBS 140463T = UTHSC DI-13-212 = FMR 13325 | Human, ethmoid sinus | LN834416 | LN834512 | LN834600 |
Cladosporium funiculosum | CBS 122128 | Ficus carica | HM148093 | HM148337 | HM148582 |
CBS 122129T | Leaf of Vigna umbellata | HM148094 | HM148338 | HM148583 | |
UTHSC DI-13-175 = FMR 13300 | Human, BAL | LN834362 | LN834458 | LN834546 | |
Cladosporium fusiforme | CBS 119414T | Hypersaline water | DQ780388 | JN906988 | EF101372 |
Cladosporium gamsianum | CBS 125989T | Strelitzia sp. | HM148095 | HM148339 | HM148584 |
Cladosporium globisporum | CBS 812.96T | Meat stamp | HM148096 | HM148340 | HM148585 |
Cladosporium grevilleae | CBS 114271T | Leaves of Grevillea sp. | JF770450 | JF770472 | JF770473 |
Cladosporium halotolerans | CBS 119416T | Hypersaline water | DQ780364 | JN906989 | EF101397 |
UTHSC DI-13-250 = FMR 13363 | Human, scalp | LN834374 | LN834470 | LN834558 | |
Cladosporium herbaroides | CBS 121626T | Hypersaline water | EF679357 | EF679432 | EF679509 |
Cladosporium herbarum | CBS 121621ET | Hordeum vulgare | EF679363 | EF679440 | EF679516 |
UTHSC DI-13-220 = FMR 13333 | Human, BAL | LN834378 | LN834474 | LN834562 | |
Cladosporium hillianum | CBS 125988T | Leaves of Grevillea sp. | HM148097 | HM148341 | HM148586 |
Cladosporium inversicolor | CBS 143.65 | Leaf of Tilia sp. | HM148100 | HM148344 | HM148589 |
CBS 401.80T | Leaf of Triticum aestivum | HM148101 | HM148345 | HM148590 | |
Cladosporium ipereniae | CBS 140483T | Puya sp. | KT600394 | KT600491 | KT600589 |
CPC 16855 | Arctostaphylos pallida | KT600395 | KT600492 | KT600590 | |
Cladosporium iranicum | CBS 126346T | Leaf of Citrus sinensis | HM148110 | HM148354 | HM148599 |
Cladosporium iridis | CBS 138.40ET | Leaf of Iris sp. | EF679370 | EF679447 | EF679523 |
Cladosporium langeronii | CBS 189.54NT | Man | DQ780379 | JN906990 | EF101357 |
Cladosporium licheniphilum | CBS 125990ET | From P. orbicularis and Physcia sp. on Acer platanoides | HM148111 | HM148355 | HM148600 |
Cladosporium limoniforme | CBS 113737 | Grape berry | KT600396 | KT600493 | KT600591 |
CBS 140484T | Musa acuminata | KT600397 | KT600494 | KT600592 | |
Cladosporium longicatenatum | CBS 140485T | Unknown plant | KT600403 | KT600500 | KT600598 |
Cladosporium longissimum | CBS 300.96T | Soil along coral reef coast | DQ780352 | EU570259 | EF101385 |
Cladosporium lycoperdinum | CBS 574.78C | Aureobasidium caulivorum | HM148115 | HM148359 | HM148604 |
CBS 126347 | From galls of Apiosporina morbosa on Prunus sp. | HM148112 | HM148356 | HM148601 | |
Cladosporium macrocarpum | CBS 121623NT | Spinacia oleracea | EF679375 | EF679453 | EF679529 |
UTHSC DI-13-191 = FMR 13316 | Human, face | LN834379 | LN834475 | LN834563 | |
Cladosporium montecillanum | CBS 140486T | Pine needles | KT600406 | KT600504 | KT600602 |
CPC 15605 | Taraxacum sp. | KT600407 | KT600505 | KT600603 | |
Cladosporium myrtacearum | CBS 126350ET | Corymbia foelscheana | HM148117 | HM148361 | HM148606 |
Cladosporium ossifragi | CBS 842.91ET | Narthecium ossifragum | EF679381 | EF679459 | EF679535 |
Cladosporium oxysporum | CBS 125991 | Soil | HM148118 | HM148362 | HM148607 |
CBS 126351 | Indoor air | HM148119 | HM148363 | HM148608 | |
Cladosporium paracladosporioides | CBS 171.54T | Unknown | HM148120 | HM148364 | HM148609 |
Cladosporium parapenidielloides | CBS 140487T | Eucalyptus sp. | KT600410 | KT600508 | KT600606 |
Cladosporium penidielloides | CBS 140489T | Acacia verticillata | KT600412 | KT600510 | KT600608 |
Cladosporium perangustum | CBS 125996T | Cussonia sp. | HM148121 | HM148365 | HM148610 |
CBS 126365 | Chasmothecia of Phyllactinia guttata on leaves of Corylus avellana | HM148123 | HM148367 | HM148612 | |
CPC 11663 | Oncoba spinosa | HM148128 | HM148372 | HM148617 | |
CPC 11815 | Chasmothecia of Phyllactinia guttata on leaves of Corylus sp. | HM148130 | HM148374 | HM148619 | |
CPC 11819 | Chasmothecia of Phyllactinia guttata on leaves of Corylus sp. | HM148131 | HM148375 | HM148620 | |
CPC 11821 | Chasmothecia of Phyllactinia guttata on leaves of Corylus sp. | HM148132 | HM148376 | HM148621 | |
CPC 11831 | Chasmothecia of Phyllactinia guttata on leaves of Corylus sp. | HM148133 | HM148377 | HM148622 | |
CPC 12216 | Morus rubra | HM148135 | HM148379 | HM148624 | |
CPC 13727 | Teratosphaeria maculiformis | HM148139 | HM148383 | HM148628 | |
CPC 13730 | Protea caffra | HM148140 | HM148384 | HM148629 | |
CPC 13774 | Protea caffra | HM148141 | HM148385 | HM148630 | |
CPC 13870 | Teratosphaeria fibrillosa | HM148142 | HM148386 | HM148631 | |
UTHSC DI-13-208 = FMR 13321 | Canine, BAL | LN834380 | LN834476 | LN834564 | |
Cladosporium phaenocomae | CBS 128769T | Leaf bracts of Phaenocoma prolifera | JF499837 | JF499875 | JF499881 |
Cladosporium phlei | CBS 358.69ET | Phleum pratense | JN906981 | JN906991 | JN907000 |
Cladosporium phyllactiniicola | CBS 126353 | Chasmothecia of P. guttata on leaves of Corylus avellana | HM148151 | HM148395 | HM148640 |
CBS 126355T | Chasmothecia of P. guttata on leaves of Corylus avellana | HM148153 | HM148397 | HM148642 | |
Cladosporium phyllophilum | CBS 125992ET | Fruits of Prunus cerasus | HM148154 | HM148398 | HM148643 |
Cladosporium pini-ponderosae | CBS 124456T | Pinus ponderosa | FJ936160 | FJ936164 | FJ936167 |
Cladosporium pseudiridis | CBS 116463T | Iris sp. | EF679383 | EF679461 | EF679537 |
Cladosporium pseudochalastosporioides | CBS 140490T | Pine needles | KT600415 | KT600513 | KT600611 |
Cladosporium pseudocladosporioides | CBS 667.80 | Malus sylvestris | HM148165 | HM148409 | HM148654 |
CBS 125993T | Outside air | HM148158 | HM148402 | HM148647 | |
CPC 13683 | Eucalyptus placita | HM148173 | HM148417 | HM148662 | |
CPC 14020 | Wheat | HM148185 | HM148429 | HM148674 | |
CPC 14295 | Soil | HM148188 | HM148432 | HM148677 | |
UTHSC DI-13-165 = FMR 13290 | Human, arm drainage | LN834406 | LN834502 | LN834590 | |
UTHSC DI-13-190 = FMR 13315 | Human, CSF | LN834412 | LN834508 | LN834596 | |
UTHSC DI-13-210 = FMR 13323 | Human, skin | LN834414 | LN834510 | LN834598 | |
Cladosporium pseudocladosporioides | UTHSC DI-13-218 = FMR 13331 | Human, BAL | LN834418 | LN834514 | LN834602 |
(cont.) | UTHSC DI-13-227 = FMR 13340 | Human, sputum | LN834422 | LN834518 | LN834606 |
UTHSC DI-13-234 = FMR 13347 | Human, sputum | LN834424 | LN834520 | LN834608 | |
UTHSC DI-13-238 = FMR 13351 | Human, leg | LN834426 | LN834522 | LN834610 | |
UTHSC DI-13-241 = FMR 13354 | Human, foot | LN834427 | LN834523 | LN834611 | |
UTHSC DI-13-245 = FMR 13358 | Human, toe | LN834429 | LN834525 | LN834613 | |
UTHSC DI-13-251 = FMR 13364 | Human, BAL | LN834432 | LN834528 | LN834616 | |
UTHSC DI-13-261 = FMR 13374 | Human, sputum | LN834384 | LN834480 | LN834568 | |
UTHSC DI-13-265 = FMR 13378 | Human, BAL | LN834435 | LN834531 | LN834619 | |
UTHSC DI-13-268 = FMR 13381 | Human, toenail | LN834436 | LN834532 | LN834620 | |
UTHSC DI-13-270 = FMR 13383 | Human, nail | LN834438 | LN834534 | LN834622 | |
Cladosporium psychrotolerans | CBS 119412T | Hypersaline water | DQ780386 | JN906992 | EF101365 |
Cladosporium puyae | CBS 274.80AT | Puya goudotiana | KT600418 | KT600516 | KT600614 |
Cladosporium ramotenellum | CBS 121628T | Hypersaline water | EF679384 | EF679462 | EF679538 |
UTHSC DI-13-166 = FMR 13291 | Human, nasal tissue | LN834385 | LN834481 | LN834569 | |
Cladosporium rectoides | CBS 125994T | Vitis flexuosa | HM148193 | HM148438 | HM148683 |
Cladosporium rhusicola | CBS 140492T | Rhus sp. | KT600440 | KT600539 | KT600637 |
Cladosporium ruguloflabelliforme | CBS 140494T | Diatrapaceae sp. on Aloe sp. | KT600458 | KT600557 | KT600655 |
Cladosporium rugulovarians | CBS 140495T | Leaf sheaths of unidentified Poaceae | KT600459 | KT600558 | KT600656 |
Cladosporium salinae | CBS 119413T | Hypersaline water | DQ780374 | JN906993 | EF101390 |
Cladosporium scabrellum | CBS 126358T | Ruscus hypoglossum | HM148195 | HM148440 | HM148685 |
Cladosporium silenes | CBS 109082 | Silene maritima | EF679354 | EF679429 | EF679506 |
Cladosporium sinuosum | ATCC 11285 | Unidentified moss | KT600441 | KT600540 | KT600638 |
CBS 393.68 | Air | KT600442 | KT600541 | KT600639 | |
CBS 121629T | Fuchsia excorticata | EF679386 | EF679464 | EF679540 | |
CPC 14000 | Wheat | KT600443 | KT600542 | KT600640 | |
CPC 15454 | Crocus sativus | KT600444 | KT600543 | KT600641 | |
CPC 18365 | Iris pseudacorus | KT600446 | KT600545 | KT600643 | |
Cladosporium soldanellae | CBS 132186NT | Soldanella alpina | JN906982 | JN906994 | JN907001 |
Cladosporium sphaerospermum | CBS 193.54NT | Human, nail | DQ780343 | EU570261 | EU570269 |
UTHSC DI-13-237 = FMR 13350 | Human, BAL | LN834390 | LN834486 | LN834574 | |
Cladosporium spinulosum | CBS 119907T | Hypersaline water | EF679388 | EF679466 | EF679542 |
Cladosporium subinflatum | CBS 121630T | Hypersaline water | EF679389 | EF679467 | EF679543 |
UTHSC DI-13-189 = FMR 13314 | Human, toenail | LN834391 | LN834487 | LN834575 | |
Cladosporium subtilissimum | CBS 113754T | Grape berry | EF679397 | EF679475 | EF679551 |
Cladosporium subuliforme | CBS 126500T | Chamaedorea metallica | HM148196 | HM148441 | HM148686 |
UTHSC DI-13-214 = FMR 13327 | Human, BAL | LN834394 | LN834490 | LN834578 | |
Cladosporium subcinereum | CBS 140465T = UTHSC DI-13-257 = FMR 13370 | Human, sputum | LN834433 | LN834529 | LN834617 |
Cladosporium succulentum | CBS 140466T = UTHSC DI-13-262 = FMR 13375 | Dolphin, bronchus | LN834434 | LN834530 | LN834618 |
Cladosporium tenellum | CBS 121634T | Hypersaline water | EF679401 | EF679479 | EF679555 |
Cladosporium tenuissimum | CBS 125995ET | Fruits of Lagerstroemia sp. | HM148197 | HM148442 | HM148687 |
CPC 10882 | Gnaphalium affine | HM148204 | HM148449 | HM148694 | |
CPC 11555 | Citrus sinensis | HM148205 | HM148450 | HM148695 | |
CPC 11805 | Strelitzia sp | HM148207 | HM148452 | HM148697 | |
CPC 12795 | Musa sp. | HM148209 | HM148454 | HM148699 | |
CPC 13222 | Callistemon viminalis | HM148210 | HM148455 | HM148700 | |
CPC 14250 | Magnolia sp. | HM148211 | HM148456 | HM148701 | |
UTHSC DI-13-258 = FMR 13371 | Human, thorancentesis fluid | LN834404 | LN834500 | LN834588 | |
Cladosporium tuberosum | CBS 140693T = UTHSC DI-13-217 = FMR 13330 | Human, nasal | LN834417 | LN834513 | LN834601 |
UTHSC DI-13-219 = FMR 13332 | Human, foot | LN834419 | LN834515 | LN834603 | |
Cladosporium variabile | CBS 121635ET | Spinacia oleracea | EF679402 | EF679480 | EF679556 |
Cladosporium varians | CBS 126362T | Catalpa bungei | HM148224 | HM148470 | HM148715 |
Cladosporium velox | CBS 119417T | Bamboo | DQ780361 | JN906995 | EF101388 |
Cladosporium verrucocladosporioides | CBS 126363T | Rhus chinensis | HM148226 | HM148472 | HM148717 |
Cladosporium versiforme | CBS 140491T | Hordeum sp. | KT600417 | KT600515 | KT600613 |
Cladosporium xantochromaticum | CBS 140691T = UTHSC DI-13-211 = FMR 13324 | Human, BAL | LN834415 | LN834511 | LN834599 |
CBS 126364 | Erythrophleum chlorostachys | HM148122 | HM148366 | HM148611 | |
CPC 11133 | Eucalyptus sp. | HM148126 | HM148370 | HM148615 | |
CPC 11609 | Musa sp. | EF679356 | EF679431 | EF679508 | |
CPC 11806 | Strelitzia sp. | HM148129 | HM148373 | HM148618 | |
CPC 11856 | Acacia mangium | HM148134 | HM148378 | HM148623 | |
CPC 12792 | Musa sp. | HM148136 | HM148380 | HM148625 | |
Cladosporium xylophilum | CBS 125997T | Picea abies | HM148230 | HM148476 | HM148721 |
a New species described in this study are in bolditalic.
b ATCC, American Type Culture Collection, Manassas, VA, USA; CBS, CBS-KNAW Fungal Biodiversity Centre, Utrecht, the Netherlands; CPC, collection of Pedro Crous at CBS; FMR, Facultat de Medicina, Universitat Rovira i Virgili, Reus, Spain; UTHSC, Fungus Testing Laboratory at the University of Texas Health Science Center, San Antonio, Texas, USA.
c BAL fluid, bronchoalveolar lavage fluid specimen; CSF, cerebrospinal fluid.
T Ex-type strain.
ET Ex-epitype strain.
NT Ex-neotype strain.
Phenotypic studies
Macroscopic cultural characteristics of the isolates were recorded after incubation for 14 d at 25 °C, using oatmeal agar (OA) (30 g of filtered oat flakes, 20 g of agar, water 1 L), potato dextrose agar (PDA: Pronadisa, Spain) and synthetic nutrient-poor agar (SNA; KH2PO4 1 g, KNO3 1 g, MgSO4 × 7H2O 0.5 g, KCl 0.5 g, glucose 0.2 g, sucrose 0.2 g, agar 14 g, water 1 L) with and without pieces of sterilised paper as carbon source. In descriptions, colour notations of the colonies were from Kornerup & Wanscher (1978). Observations and measurements of the microscopic structures were carried out from colonies on SNA after incubation for 7 d at 25 °C, mounted on Shear’s solution (Schubert et al. 2007, Zalar et al. 2007, Crous et al. 2009, Bensch et al. 2012). Photographs were made using a Zeiss Axio Imager M1 light microscope (Zeiss, Oberkochen, Germany) with a mounted DeltaPix Infinity X digital camera using Nomarski differential interference contrast and phase contrast optics. Scanning electron microscope (SEM) micrographs were obtained with a Jeol JSM-6400 apparatus, following the protocols described by Figueras & Guarro (1988). Cardinal temperatures of growth were determined culturing the isolates on PDA for 14 d at temperatures ranging from 15 °C to 35 °C at intervals of 5 °C.
DNA extraction, PCR amplification and sequencing
Total genomic DNA was extracted, amplified and sequenced in a previous work, using protocols described elsewhere (Bensch et al. 2012, Sandoval-Denis et al. 2015). Briefly, the primer pair ITS5/ITS4 (White et al. 1990) was used to amplify a region spanning the internal transcribed spacers 1 and 2 and the 5.8S gene of the rRNA (ITS), and the primer pairs EF-728F/EF-986R and ACT-512F/ACT-783R (Carbone & Kohn 1999) were used to amplify a partial fragment of the translation elongation factor 1-α gene (tef1) and the actin gene (actA), respectively.
Sequences were generated using the same PCR primers at Macrogen Europe (Macrogen Inc. Amsterdam, The Netherlands). Consensus sequences were assembled using SeqMan v. 7.0.0 (DNAStar Lasergene, Madison, WI, USA).
Sequence alignment and phylogenetic analyses
Multiple sequence alignments of each locus were performed with MEGA v. 6.06 (Tamura et al. 2013), using the ClustalW algorithm (Thompson et al. 1994) and refined with MUSCLE (Edgar 2004) or manually if necessary. The alignment included sequences from the clinical isolates complemented with sequences representing all the available ex-types and numerous reference strains of Cladosporium spp. retrieved from GenBank and mainly published by Bensch et al. (2012, 2015). These latter sequences were selected on the basis of sequence similarity with the putative new taxa as determined by BLAST searches on the NCBI database using ITS, tef1 and actA loci (Table 1).
Phylogenetic reconstructions were performed using the maximum-likelihood (ML) and Bayesian Inference (BI) approaches under MEGA v. 6.06 and MrBayes v. 3.2 (Huelsenbeck & Ronquist 2001), respectively. MrModelTest v. 2.3 (Nylander 2004) was used to determine the best nucleotide substitution model for each dataset (SYM+G for ITS and GTR+G+I for tef1 and actA). Sequence alignments generated in this study were deposited in TreeBASE (http://treebase.org).
For the ML analyses, support for the internal branches was assessed by a search of 1 000 bootstrapped sets of data. A bootstrap support (bs) of ≥ 70 % was considered significant. For BI analyses, four Markov chains were performed in two simultaneous runs for 10 000 000 generations with a sampling rate of 1 000 generations. Once checked for the convergence of the runs (average standard deviation of split frequencies parameter below 0.01), the 50 % majority-rule consensus tree and posterior probability values (pp) were calculated after discarding 2 500 trees for burn-in. A pp value ≥ 0.95 was considered significant. Phylogenetic concordance of the ITS, tef1 and actA gene datasets was evaluated with the partition-homogeneity test implemented with PAUP v. 4.0b10 (Swofford 2003) and also by visual comparison of the individual phylogenies in order to assess for any incongruent results between nodes with high statistical support. Taxonomic novelties were deposited in MycoBank (Crous et al. 2004).
RESULTS
Phylogeny
The different partitions were congruent as determined by visual comparison of the individual phylogenies (data not shown) and by the partition homogeneity test (p = 0.16). Phylogenies obtained by ML and BI also showed topological congruence. The final combined analysis of the three mentioned loci datasets encompassed 197 sequences representing 101 taxa, including Cercospora beticola (CBS 116456) as the outgroup, and comprised 1 026 bp (ITS 448 bp, tef1 357 bp and actA 221 bp) from which 546 bp were variable (ITS 108 bp, tef1 291 bp and actA 147 bp) and 399 bp phylogenetically informative (ITS 42 bp, tef1 234 bp and actA 123 bp). Unique site pattern values for the Bayesian analyses were 92, 322 and 167 for ITS, tef1 and actA datasets, respectively (Fig. 1). Of the 35 unidentified isolates, 21 clustered into ten groups that received strong statistical support with the exception of two monotypic lineages (CBS 140465 and CBS 140466), which, however, were genetically and morphologically differentiated from their closest phylogenetic relatives. The remaining 14 isolates were identified here as C. pseudocladosporioides (13 isolates) and C. allicinum (one isolate). The isolates representing putative new taxa grouped mainly in the C. cladosporioides species complex in which 16 isolates were distributed in three terminal clades and three monotypic linages. Five isolates belonged to the C. herbarum species complex, two of them (CBS 140693 and UTHSC DI-13-219) grouped in a terminal clade, located in a basal position to the remaining species of the complex, while three isolates formed monotypic lineages. The C. sphaerospermum species complex included a single unidentified isolate (CBS 140466) forming a genetically and morphologically distinct lineage. The 10 phylogenetic groups are thus considered new species of Cladosporium and are described in the taxonomy section below.
TAXONOMY
Cladosporium alboflavescens Sandoval-Denis, Gené & Cano, sp. nov. — MycoBank MB815332; Fig. 2
Etymology. From Latin albus ‘white’ flavus ‘yellow’, referring to the colony colour of the species.
Colonies on OA attaining 20–23 mm diam after 14 d at 25 °C, white to grey-yellow (4A1/C4), flat, velvety, margin regular and with abundant submerged mycelium; reverse olive brown (4D5/F8), without diffusible pigments. On PDA attaining 34–36 mm diam after 14 d at 25 °C, yellow-grey to olive brown (4B2/D4), with prominent light yellow (3A4) exudate, flat or umbonate, folded, margin regular; reverse grey-yellow to olive brown (4B4/F4) to black. On SNA reaching 22–25 mm after 14 d at 25 °C, obverse and reverse olive (3D5/E8), flat, velvety with granular centre, margin undulate and with abundant submerged mycelium. Mycelium superficial and immersed, composed of septate, branched, 2.5–5 μm wide, subhyaline to pale brown, smooth to slightly roughened, thin-walled hyphae. Conidiophores erect, straight, cylindrical, non-nodulose, septate, simple or branched, up to 130 μm long, 2.5–4 μm wide, pale brown, smooth or sparingly verrucose with darkened and refractive scars. Conidiogenous cells terminal or intercalary, cylindrical, geniculate, 7–36 × 2–4 μm, with up to five apical loci of 1.5–2 μm diam, thickened and refractive. Ramoconidia aseptate, subcylindrical to cylindrical, 11–36 × 2–3 μm, pale brown, smooth-walled. Conidia forming branched chains with up to three conidia in the terminal unbranched part, pale brown, sparingly verrucose, with protuberant, somewhat darkened and refractive conidial hila; small terminal conidia aseptate, oval, 5–6.5 × 2–3.5 μm (av. (± SD) 5.9 (± 0.4) × 2.8 (± 0.4)); intercalary conidia aseptate, ellipsoidal to almost cylindrical with attenuated ends, 7–13 × 2.5–3 μm (av. (± SD) 10.6 (± 2.5) × 2.6 (± 0.2)); secondary ramoconidia 0–1-septate, ellipsoidal, 8.5–18 × 2–3 μm (av. (± SD) 14.3 (± 3.3) × 2.6 (± 0.5)).
Cardinal temperature for growth — Optimum 20–25 °C, maximum 30 °C, minimum 15 °C.
Specimen examined. USA, California, from animal bronchoalveolar lavage fluid, Mar. 2009, D.A. Sutton (holotype CBS H-22379, culture ex-type CBS 140690 = UTHSC DI-13-225 = FMR 13338).
Notes — Cladosporium alboflavescens is morphologically similar to C. pini-ponderosae and C. verrucocladosporioides (Schubert et al. 2009, Bensch et al. 2010). However, the new species differs mainly by its pale coloured vegetative structures, and its yellow to pale olive colonies on OA and PDA vs olivaceous grey in the two latter species. The phylogenetically closely related species C. iranicum (Bensch et al. 2010) also shows similar micro-morphological characteristics to C. alboflavescens, but it differs in forming longer conidial chains with up to 10 conidia in the terminal unbranched part and often showing subrostrate intercalary conidia, while conidial chains of the novel species are much shorter and intercalary conidia ellipsoidal to cylindrical being also genetically well differentiated (99.8 %, 87.9 % and 90.1 % sequence similarity for ITS, tef1 and actA, respectively).
Cladosporium angulosum Sandoval-Denis, Deanna A. Sutton & Guarro, sp. nov. — MycoBank MB815333; Fig. 3
Etymology. From Latin angulosus ‘full of corners’, referring to the shape of the conidiophore.
Colonies on OA reaching 52–55 mm after 14 d at 25 °C, olive brown (4E3/F8), flat, velvety to granular, with regular margin; reverse olive brown (4E3/F8) to black. On PDA attaining 50–56 mm diam after 14 d at 25 °C, olive brown (4F4/F8), with a raised or umbonate centre and radially folded towards the periphery, velvety to dusty or granular, with regular margin; reverse dark green (30F8) to black. On SNA reaching 37–40 mm after 14 d at 25 °C, olive brown (4D4/F6), flat, velvety, with lobulated margin; reverse olive brown (4D4/F6) to black. Mycelium superficial and immersed, composed of septate, branched, 1.5–3 μm wide, pale olivaceous brown, with smooth and thin-walled hyphae. Conidiophores erect, cylindrical, non-nodulose, septate, septa darkened, branched, frequently branching near the base in a 90° angle, up to 150 μm long, 3–4 μm wide, pale brown, smooth and thin-walled. Conidiogenous cells terminal or intercalary, cylindrical, 8–46 × 2–3.5 μm, bearing up to four conidiogenous loci of 1–1.5 μm diam, darkened and refringent. Ramoconidia aseptate, subcylindrical, straight, 24.5–46 × 2–3.5 μm, pale brown, finely roughened, with scars protuberant, thickened and darkened. Conidia forming long branched chains with up to 14 conidia in the terminal unbranched part, pale olivaceous brown, smooth and thin-walled, with protuberant conidial hila, not darkened; small terminal conidia aseptate, obovate to nearly cylindrical, 3.5–4.5 × 2–2.5 μm (av. (± SD) 4.1 (± 0.3) × 2.3 (± 0.3)); intercalary conidia aseptate, ellipsoidal, 4–6 × 2–3 μm (av. (± SD) 5.3 (± 0.6) × 2.4 (± 0.4)); secondary ramoconidia 0–1-septate, usually constricted at septum, subcylindrical, 8–17 × 2.5–3 μm (av. (± SD) 12.2 (± 2.6) × 2.8 (± 0.3)).
Cardinal temperature for growth — Optimum 25 °C, maximum 35 °C, minimum 15 °C.
Specimen examined. USA, Texas, from human bronchoalveolar lavage fluid, Sept. 2008, D.A. Sutton (holotype CBS H-22380, culture ex-type CBS 140692 = UTHSC DI-13-235 = FMR 13348).
Notes — The clade representative of C. angulosum includes several strains previously identified as C. perangustum, a species accepted with a considerable morphological and genetic diversity by Bensch et al. (2010, 2012, 2015). However, it shows a sufficient genetic distance (ITS, 100 %; tef1, 77 %; actA, 85.4 % similarity) with respect to the ex-type strain of C. perangustum to be considered a distinct species. Morphologically, C. angulosum can be mainly differentiated from C. perangustum by its conidiophores, which are usually branched forming a 90° angle, while those of the latter are only occasionally branched. In addition, the new species produces smaller secondary ramoconidia and intercalary conidia (up to 17 μm and 6 μm long, respectively, vs 6–30(–34) μm and 4–16(–19) μm long, respectively, in C. perangustum) (Bensch et al. 2012). Another closely related species is C. xantochromaticum, but it is genetically well differentiated from C. angulosum (99.1 %, 81.1 % and 90.8 % similarity for ITS, tef1 and actA, respectively), and morphologically it has longer conidiogenous cells (up to 32 μm long vs 27 μm long in C. angulosum), smaller ramoconidia (up to 39 μm long vs 46 μm long in C. angulosum) and does not grow at 35 °C.
Cladosporium anthropophilum Sandoval-Denis, Gené & Wiederhold, sp. nov. — MycoBank MB815334, Fig. 4
Etymology. From the Greek ánthrōpos (áνθρωποζ) ‘human’ and philos (íλοζ) ‘fondness’, referring to the source of the ex-type, human clinical samples.
Colonies on OA attaining 27–32 mm diam after 14 d at 25 °C, olive to olive brown (3F2/4F8), flat, dusty or granular, aerial mycelium scarce, with fimbriate margin; reverse olive brown (4F8) to black, without diffusible pigment. On PDA attaining 17–39 mm diam after 14 d at 25 °C, grey-green to deep green (28D7/D8), flat or folded, velvety to dusty or granular, aerial mycelium scarce, sometimes showing cottony to floccose white to grey cushions, with a regular margin; reverse dark green (28F8) to black. On SNA reaching 23–26 mm after 14 d at 25 °C, olive to olive brown (3F2/4F8), flat, dusty to cottony, aerial mycelium abundant, often with irregular to arachnoid margins; reverse olive to olive brown (3F2/4F8). Mycelium superficial and immersed, composed of septate, branched, 2–3 μm wide, subhyaline to pale green, smooth and thick-walled, anastomosing hyphae. Conidiophores erect, cylindrical, non-nodulose, geniculate, septate, usually branched, up to 550 μm long, 2–5 μm wide, pale green-brown, slightly roughened to verruculose toward the base, with a thickened and refractive wall. Conidiogenous cells terminal and intercalary, cylindrical or subcylindrical, 15–54 × 3–5 μm, often with a swollen apex, bearing 3–8(–10), protuberant, subdenticulate, 1–2.5 μm diam, thickened and somewhat darkened conidiogenous loci. Ramoconidia aseptate, cylindrical, 20–42 × 2–5 μm, pale green, smooth, with conidial scars protuberant, thickened and darkened. Conidia forming short branched chains with up to four conidia in the terminal unbranched part of the chain, aseptate, smooth or finely roughened, reticulate under SEM; small terminal conidia oval to ellipsoidal, 3.5–9 × 2–3 μm (av. (± SD) 5.6 (± 1.2) × 2.5 (± 0.4)), subhyaline; intercalary conidia limoniform to ellipsoidal, 4.5–11 × 2–3 μm (av. (± SD) 6.9 (± 1.8) × 2.7 (± 0.3)), light green-brown; secondary ramoconidia 0–1-septate, ellipsoidal to subcylindrical, usually attenuated at the centre, 7–28 × 2–5 μm (av. (± SD) 13.7 (± 4.8) × 3.4 (± 0.6)).
Cardinal temperature for growth — Optimum 25 °C, maximum 35 °C, minimum 5 °C.
Specimens examined. USA, Minnesota, from human bronchoalveolar lavage fluid, Sept. 2012, D.A. Sutton (holotype CBS H-22381, culture ex-type CBS 140685 = UTHSC DI-13-269 = FMR 13382); from human bronchoalveolar lavage fluid, Sept. 2012, D.A. Sutton, UTHSC DI-13-168 = FMR 13293; California, from a hand, Oct. 2010, D.A. Sutton, UTHSC DI-13-179 = FMR 13304; Florida, from human bronchoalveolar lavage fluid, Jan. 2007, D.A. Sutton, UTHSC DI-13-271 = FMR 13384; from human bronchoalveolar lavage fluid, Mar. 2007, D.A. Sutton, UTHSC DI-13-246 = FMR 13359; from an animal abscess, Jan. 2012, D.A. Sutton, UTHSC DI-13-178 = FMR 13303; Massachusetts, from human bronchoalveolar lavage fluid, Mar. 2012, D.A. Sutton, UTHSC DI-13-169 = FMR 13294; Texas, from human cerebrospinal fluid, Mar. 2009, D.A. Sutton, UTHSC DI-13-207 = FMR 13320; from human bronchoalveolar lavage fluid, Jan. 2009, D.A. Sutton, UTHSC DI-13-226 = FMR 13339; from human foot skin, May 2008, D.A. Sutton, UTHSC DI-13-228 = FMR 13341; from human pleural fluid, Apr. 2008, D.A. Sutton, UTHSC DI-13-244 = FMR 13357.
Notes — Cladosporium anthropophilum is probably a common saprobic fungus, as determined by the number of isolates evaluated, and can also represent a clinically relevant fungus, being the second most prevalent species identified in a set of clinical isolates from the USA after C. halotolerans (Sandoval-Denis et al. 2015). The new taxon is morphologically similar to C. cladosporioides and C. pseudocladosporioides, but phylogenetically distant. Although the three species are difficult to separate morphologically, C. anthropophilum mainly differs by its longer (up to 550 μm) conidiophores and oval to ellipsoidal terminal conidia (3.5–9 μm long) showing a fine reticulation under SEM. The conidiophores of C. cladosporioides and C. pseudocladosporioides are 10–250 μm and 15–155 μm long, respectively, and their terminal conidia are subglobose to limoniform ((3–)4–8(–11) μm long) and with a irregularly reticulate or striped wall in the former, and obovoid to ellipsoidal (3–5.5 μm long) and smooth-walled or almost so in the latter species (De Vries 1952, Bensch et al. 2012). Cladosporium anthropophilum also resembles C. tenuissimum, a species previously described as human opportunistic pathogen (De Hoog et al. 2011). However both are genetically well differentiated (99.3 %, 87.7 % and 89.9 % similarity for ITS, tef1 and actA, respectively) and, morphologically, C. anthropophilum shows longer terminal conidia (3.5–9 μm long (av. (± SD) 5.6 (± 1.2)) vs (2–)2.5–5(–6) μm long (av. (± SD) 3.7 ± 1.0)) in C. tenuissimum) and shorter intercalary conidia (4.5–11 μm long (av. (± SD) 6.9 (± 1.8)) vs 4–12(–17) μm long (av. (± SD) 8.1 (± 2.7)) in C. tenuissimum) (Bensch et al. 2012).
Cladosporium crousii Sandoval-Denis, Cano & Guarro, sp. nov. — MycoBank MB815341; Fig. 5
Etymology. In honour of Pedro W. Crous for his extensive work on Cladosporium.
Colonies on OA attaining 47–50 mm diam after 14 d at 25 °C, olive to dark green (3F8/30F8), flat, velvety to granular, aerial mycelium scarce, margin fimbriate and with abundant submerged mycelia; reverse olive to dark green (3F8/30F8) to black, without diffusible pigment. On PDA attaining 73–77 mm diam after 14 d at 25 °C, olive brown (4E3/E6), radially folded, velvety or granular with floccose centre and regular margin; reverse at first dark brown (7F8) turning black. On SNA reaching 39–41 mm after 14 d at 25 °C, olive brown (4D5/F8), flat, velvety with floccose centre, margin fimbriate and with abundant submerged mycelium; reverse black. Mycelium superficial and immersed, composed of septate, branched, 2.5–3.5 μm wide, subhyaline hyphae, with slightly roughened walls. Conidiophores erect, cylindrical, septate, usually unbranched or sparingly branched, up to 230 μm long, 2–3.5 μm wide, pale green-brown, smooth-walled. Conidiogenous cells terminal and intercalary, cylindrical, sometimes geniculate toward the apex, 11–23 × 2.5–4 μm, bearing 1–4 conidiogenous loci of 1.5–2 μm diam, protuberant, black and refringent. Ramoconidia 0–1-septate, subcylindrical to cylindrical, 19–39 × 2–3 μm, pale brown, smooth. Conidia forming long branched chains with up to seven conidia in the terminal unbranched part of the chain, subhyaline, smooth, with protuberant, thickened and darkened conidial hila; small terminal conidia aseptate, ellipsoidal to subcylindrical, with a central constriction, 7–9 × 2–2.5 μm (av. (± SD) 7.8 (± 0.7) × 2.2 (± 0.2)); intercalary conidia aseptate, ellipsoidal to cylindrical, slightly curved, aseptate, 9–10 × 2–3 μm (av. (± SD) 9.5 (± 0.5) × 2.3 (± 0.4)); secondary ramoconidia 0–1-septate, cylindrical, 9.5–24 × 2.5–3.5 μm (av. (± SD) 15.7 (± 4.4) × 2.8 (± 0.3)).
Cardinal temperature for growth — Optimum 25 °C, maximum 30 °C, minimum 15 °C.
Specimen examined. USA, South Carolina, from human bronchoalveolar lavage fluid, May 2008, D.A. Sutton (holotype CBS H-22385, culture ex-type CBS 140686 = UTSHC DI-13-247 = FMR 13360).
Notes — Cladosporium crousii is closely related to C. gamsianum, but morphologically they are clearly differentiated. The first species is characterised by longer (up to 230 μm long) and pale coloured conidiophores with unthickened walls, and longer ellipsoidal terminal conidia (7–9 μm long). In contrast, C. gamsianum exhibits dark brown and thick-walled conidiophores of 10–146 μm long, and obovoid terminal conidia of 3–6 μm long (Bensch et al. 2010).
Cladosporium flavovirens Sandoval-Denis, Gené & Guarro, sp. nov. — MycoBank MB814508; Fig. 6
Etymology. From Latin flavus ‘yellow’ and virens ‘green’, referring to the colony colour on OA.
Colonies on OA attaining 53–55 mm diam after 14 d at 25 °C, olive yellow to olive (2D8/3F8) with olive grey to olive (2F2/E2) patches, flat, velvety to floccose, margin fimbriate and with abundant submerged mycelium; reverse olive yellow to olive (2D8/3F8) to black, without diffusible pigment. On PDA attaining 63–65 mm diam after 14 d at 25 °C, obverse and reverse green-grey to dark green (30F2/F8), flat or umbonate and radially folded, velvety, with regular margin. On SNA reaching from 30–32 mm after 14 d at 25 °C, olive to olive brown (2E8/3E8), flat, velvety to granular, margin slightly irregular and with abundant submerged mycelium; reverse olive yellow (2D8) to black. Mycelium superficial and immersed composed of septate, branched, 2–3 μm wide, subhyaline to pale green-brown, rough- and thick-walled hyphae, with abundant anastomoses. Conidiophores erect, cylindrical, sometimes geniculate, non-nodulose, septate, simple or branched, up to 170 μm long, 4–5 μm wide, medium green-brown, slightly roughened to verruculose, with thick and refractive walls. Conidiogenous cells terminal or intercalary, subcylindrical or cylindrical, 15–54 × 3–5 μm, bearing up to four conidiogenous loci of 1–2 μm diam, darkened and refringent. Ramoconidia 0–1-septate, subcylindrical to cylindrical, often geniculate, 27–75 × 3–4 μm, smooth or finely verruculose. Conidia forming branched chains with up to five conidia in the terminal unbranched part, pale green-brown, smooth- and thick-walled, with protuberant and darkened conidial hila; small terminal conidia aseptate, obovoidal to short ellipsoidal, 5–7 × 2.5–3 μm (av. (± SD) 5.9 (± 0.6) × 2.9 (± 0.2)); intercalary conidia aseptate, ellipsoidal, 7–10 × 3–3.5 μm (av. (± SD) 8.3 (± 0.9) × 3.2 (± 0.2)); secondary ramoconidia 0–2-septate, ellipsoidal to cylindrical, 9–30 × 3.5–4 μm (av. (± SD) 16.2 (± 6.7) × 3.8 (± 0.3)).
Cardinal temperature for growth — Optimum 25 °C, maximum 35 °C, minimum 15 °C.
Specimen examined. USA, Florida, from human toenail, Nov. 2006, D.A. Sutton (holotype CBS H-22326, culture ex-type CBS 140462 = UTHSC DI-13-273 = FMR 13386).
Notes — Cladosporium flavovirens is morphologically and phylogenetically related to C. flabelliforme. However, the new species is genetically well differentiated (99.8 %, 80.9 % and 81.8 % sequence similarity for ITS, tef1 and actA, respectively) and produces somewhat longer secondary ramoconidia (up to 30 μm) which are often septate, in contrast to the aseptate secondary ramoconidia of C. flabelliforme which are up to 27 μm long (Bensch et al. 2012).
Cladosporium floccosum Sandoval-Denis, Cano & Guarro, sp. nov. — MycoBank MB814509; Fig. 7
Etymology. From Latin floccosus ‘spotted with small tufts’, referring to the macroscopic characteristics of the colony.
Colonies on OA reaching 24–27 mm after 14 d at 25 °C, grey-beige to olive brown (4C1/F4), slightly umbonate and radially folded, velvety to dusty with regular margins; reverse olive brown (4D4/F4), without diffusible pigments. On PDA attaining 47–50 mm diam after 14 d at 25 °C, grey-green to dark green (30E5/F7), flat to umbonate and slightly folded, velvety with white cottony centre and regular margin; reverse olive brown (4D8/E8) with black patches. On SNA reaching 15–20 mm after 14 d at 25 °C, olive brown (4D2/F4), flat, velvety to floccose with abundant grey aerial mycelium, margin lobate and fimbriate with abundant submerged mycelium; reverse olive brown to dull green (4E4/30E4). Mycelium superficial and immersed composed of septate, branched, 1.5–4.5 μm wide, subhyaline to pale brown, verruculose and thin-walled hyphae. Conidiophores erect, flexuous, subcylindrical, distinctly geniculate, septate, mostly unbranched, up to 100 μm long, 4–5 μm wide, pale to medium olivaceous brown, smooth to slightly roughened, with thickened, darkened and refractive walls. Conidiogenous cells terminal, cylindrical, nodulose, 16–24 × 3–5 μm, smooth and thick-walled, bearing up to three conspicuous, refractive, slightly darkened conidiogenous loci of 1.5–2.5 μm diam. Ramoconidia not observed. Conidia forming unbranched chains with up to three conidia, pale brown, echinulate, with protuberant and darkened conidial hila; small terminal conidia 0–1-septate, sometimes slightly constricted at septa, obovoidal to ovoidal, 8–12.5 × 6–8.5 μm (av. (± SD) 10.7 (± 1.8) × 6.8 (± 0.9)); intercalary conidia 0–1-septate, ellipsoidal, 12–15 × 6–8.5 μm (av. (± SD) 13.7 (± 1.0) × 7.5 (± 0.8)); secondary ramoconidia not observed.
Cardinal temperature for growth — Optimum 25 °C, maximum 30 °C, minimum 15 °C.
Specimen examined. USA, Minnesota, from human ethmoid sinus, Sept. 2010, D.A. Sutton (holotype CBS H-22327, culture ex-type CBS 140463 = UTHSC DI-13-212 = FMR 13325).
Notes — Cladosporium floccosum is morphologically similar to C. sinuosum, which is also its closest phylogenetic relative; both species have distinctly geniculate conidiophores and do not form ramoconidia. However, C. floccosum has considerably smaller (up to 100 μm long) and rarely branched conidiophores and slightly shorter terminal conidia (up to 12.5 μm long) respect to those of C. sinuosum, which has conidiophores up to 380 μm long and terminal conidia up to 15 μm long (Schubert et al. 2007, Bensch et al. 2015).
Cladosporium subcinereum Sandoval-Denis, Deanna A. Sutton & Gené, sp. nov. — MycoBank MB814511; Fig. 8
Etymology. From Latin subcinereus ‘somewhat grey’, referring to the colony colour.
Colonies on OA reaching 29–32 mm after 14 d at 25 °C, yellow-grey to olive grey (3B2/E2), flat, velvety to cottony, with regular margin, abundant crystalline exudates occasionally present; reverse yellow-grey to olive grey (3B2/E2) to black. On PDA attaining 34–37 mm diam after 14 d at 25 °C, yellow-grey to olive (3B2/F8), flat to radially folded, velvety to floccose, with regular margin; reverse dark green (30F8) to black. On SNA reaching 14–16 mm after 14 d at 25 °C, obverse and reverse white to olive (3A1/E3), flat, velvety to cottony, with regular margin. Mycelium superficial and immersed, composed of branched, septate, 2–5 μm wide, subhyaline hyphae with smooth or minutely verruculose and unthickened walls. Conidiophores erect, flexuous, geniculate and nodulose, septate, simple or branched, up to 140 μm long, 4–6 μm wide, pale to medium-brown, smooth to verruculose and thick-walled. Conidiogenous cells terminal, subcylindrical, nodulose, geniculate, 16–38 × 4–6 μm, thick-walled, bearing up to three conidiogenous loci of 2–3 μm diam, protuberant, darkened and refractive. Ramoconidia rarely formed, 0–2 septate, cylindrical, nodulose, 19–59 × 3–6 μm, pale brown, finely roughened. Conidia in branched chains, with up to three conidia in the terminal unbranched part, pale brown, echinulate, muricate to pustulate under SEM and thick-walled, with protuberant and not darkened conidial hila; small terminal conidia 0–1-septate, globose to subglobose, 5–7 × 4.5–6.5 μm (av. (± SD) 5.6 (± 0.7) × 5.3 (± 0.6)); intercalary conidia 0–1-septate, subglobose, obovoidal to ellipsoidal, 6–10 × 5–6.5 μm (av. (± SD) 8.9 (± 1.4) × 5.9 (± 0.6)); secondary ramoconidia 0–2-septate, sometimes constricted at septum, ellipsoidal to subcylindrical, often inflated at the apex, 8–27 × 4–7 μm (av. (± SD) 16.3 (± 5.6) × 5.0 (± 0.8)).
Cardinal temperature for growth — Optimum 25 °C, maximum 30 °C, minimum 15 °C.
Specimen examined. USA, Montana, from human sputum, Sept. 2007, D.A. Sutton (holotype CBS H-22329, culture ex-type CBS 140465 = UTHSC DI-13-257 = FMR 13370).
Notes — This species is phylogenetically related to C. angustiherbarum and C. variabile. However, C. angustiherbarum produces shorter and narrower conidiophores (up to 60 μm long and 4 μm wide) and does not form ramoconidia, while C. variabile produces multiseptate ramoconidia and long chains of broadly ellipsoidal conidia with a fine granulate ornamentation under SEM (De Vries 1952, Bensch et al. 2012). In C. subcinereum the ramoconidia are rarely formed and when present they are 0–2-septate, and its conidia are subglobose, obovoidal to ellipsoidal, exhibiting a much prominent muricate to pustulate ornamentation under SEM. Cladosporium herbaroides and C. herbarum are also morphologically similar to C. subcinereum, but they can be mainly differentiated by having larger/longer conidia (3–33 × (2–)3–6(–7) μm and 10–26(–35) × 2–3.5 μm respect to the two types of conidia described in C. herbaroides, and 4–10 × 3–5(–6) μm in C. herbarum) (Schubert et al. 2007, Bensch et al. 2012).
Cladosporium succulentum Sandoval-Denis, Deanna A. Sutton & Cano, sp. nov. — MycoBank MB814512; Fig. 9
Etymology. From Latin succo ‘juice’ and ulentum ‘full of’, referring to the abundant production of exudates on PDA.
Colonies on OA reaching 23–25 mm after 14 d at 25 °C, dark green (30F3/F8), flat, granular to floccose, with fimbriate margin; reverse olive to dark green (3F8/30F4) turning black. On PDA attaining 28–35 mm diam after 14 d at 25 °C, olive brown (4F4/F8), flat, velvety to granular, with regular margin, producing abundant dark green exudates after 20–25 d; reverse black-blue (20F8) to black. On SNA reaching 27–32 mm after 14 d at 25 °C, obverse and reverse olive to olive brown (3E8/4E8), flat, downy to granular, with regular margin. Mycelium superficial and immersed, composed of septate, branched, 1.5–3.5 μm wide, subhyaline, smooth- and thin-walled hyphae. Conidiophores erect, straight or flexuous, septate, highly branched, up to 190 μm long, 2.5–4 μm wide, subhyaline, pale green-brown, smooth to finely roughened and thin-walled. Conidiogenous cells terminal and intercalary, cylindrical, 13–30 × 2–4 μm, thin-walled, bearing 2–6 conidiogenous loci of 1–2.5 μm diam, darkened and refractive. Ramoconidia 0–1-septate, cylindrical to subcylindrical, flexuous, 20–36 × 2–4 μm, pale green-brown, smooth to finely roughened. Conidia in branched chains, with up to six conidia in the terminal unbranched part, aseptate, pale green-brown, smooth- and thin-walled, with protuberant and darkened conidial hila; small terminal conidia oval to short clavate, 3–4 × 2–3 μm (av. (± SD) 3.6 (± 0.4) × 2.2 (± 0.4)), aseptate, with conspicuous and darkened conidial scars; intercalary conidia ovoid to limoniform, 4–6 × 2–3 μm (av. (± SD) 5.1 (± 0.6) × 2.3 (± 0.4)), with protuberant and not darkened conidial scars; secondary ramoconidia ellipsoidal to subcylindrical, 5–10 × 2–4.5 μm (av. (± SD) 8.2 (± 1.5) × 2.5 (± 0.4)).
Cardinal temperature for growth — Optimum 25 °C, maximum 35 °C, minimum 15 °C.
Specimen examined. USA, Florida, from a dolphin bronchus, July 2007, D.A. Sutton (holotype CBS H-22330, culture ex-type CBS 140466 = UTHSC DI-13-262 = FMR 13375).
Notes — Cladosporium succulentum is morphologically similar but genetically distant to C. halotolerans (98.4 %, 66.5 % and 79.8 % sequence similarity for ITS, tef1 and actA, respectively) and C. sphaerospermum (97.5 %, 72.7 % and 83.8 % sequence similarity for ITS, tef1 and actA, respectively). The latter two species can be differentiated from C. succulentum by having a maximum growth temperature at 30 °C (Zalar et al. 2007, Bensch et al. 2012) (35 °C in C. succulentum), and in the length and number of septa of their ramoconidia. In C. halotolerans and C. sphaerospermum these are 15–37 μm and (11.5–)20.5–40(–48) μm long, respectively, and they have up to five septa (Zalar et al. 2007, Bensch et al. 2012), while in C. succulentum the ramoconidia are 20–36 μm long with 0–1 septa. The phylogenetically closest species to C. succulentum are C. fusiforme and C. velox (sequence similarities less than 99.8 %, 80.7 % and 86.6 % for ITS, tef1 and actA, respectively), but the new species can be differentiated by the abundant production of ramoconidia and by its oval to short clavate terminal conidia. Ramoconidia in C. fusiforme and C. velox are rarely formed and their terminal conidia are obovoid to fusiform in the first species and globose to ovoid in the latter one (Zalar et al. 2007).
Cladosporium tuberosum Sandoval-Denis, Cano & Wiederhold, sp. nov. — MycoBank MB815339; Fig. 10
Etymology. From Latin tūberōsus ‘lumpy’ (full of protuberances), because of the nodulose shape of its conidiophores.
Colonies on OA reaching 23–26 mm after 14 d at 25 °C, olive brown (4D5/F7), flat, velvety to floccose, margin regular and with abundant submerged mycelium; reverse olive brown (4D5/F7) to black. On PDA attaining 44–50 mm diam after 14 d at 25 °C, dull green to dark green (30E4/F7), flat and radially folded, velvety to dusty, margin regular and white; reverse olive brown (4E8) to black. On SNA reaching 13–20 mm after 14 d at 25 °C, olive brown (4E4/F4), flat, velvety with cottony patches, margin irregular and with abundant submerged mycelium; reverse olive brown (4E4/F4) to black. Mycelium superficial and immersed, composed of septate, branched, 3–4.5 μm wide, subhyaline, smooth and thin-walled hyphae. Conidiophores erect, flexuous, cylindrical-oblong, nodulose, or bent once or several times being geniculate, laterally swollen, septate, unbranched or rarely laterally branched, up to 390 μm long, 5–6 μm wide, pale brown to olivaceous brown, smooth- and thick-walled. Conidiogenous cells terminal or intercalary, cylindrical or subnodulose, 15–38 × 4–5.5 μm, proliferating sympodially, forming lateral shoulders, bearing 1–2 conidiogenous loci at each shoulder, loci protuberant, 2–2.5 μm diam, darkened and refringent. Ramoconidia not observed. Conidia in branched chains, with up to three conidia in the terminal part, 0–1-septate, green-brown to yellow-brown, verrucose to echinulate and thick-walled with protuberant and darkened conidial hila; small terminal conidia oval, obovate or short ellipsoidal, 8–14 × 7–9 μm (av. (± SD) 13.1 (± 0.7) × 8.0 (± 0.8)); intercalary conidia ellipsoidal to limoniform, 11–16 × 7–10 μm (av. (± SD) 13.9 (± 1.7) × 8.5 (± 0.9)); secondary ramoconidia ellipsoidal to subcylindrical, 14–18 × 6–10 μm (av. (± SD) 16.1 (± 1.2) × 7.1 (± 1.3)).
Cardinal temperature for growth — Optimum 25 °C, maximum 30 °C, minimum 5 °C.
Specimens examined. USA, Florida, from human nasal biopsy, Dec. 2009, D.A. Sutton (holotype CBS H-22387, culture ex-type CBS 140693 = UTHSC DI-13-217 = FMR 13330); Washington, from human foot, Oct. 2009, D.A. Sutton, UTHSC DI-13-219 = FMR 13332.
Notes — This species is represented by two isolates of human clinical origin which cluster in a lineage clearly differentiated and together with C. basiinflatum group in a position basal to the remaining species of the C. herbarum complex (Fig. 1). Despite this basal position, it shows the typical morphological features of the species of the complex. Cladosporium tuberosum morphologically resembles C. sinuosum in the production of short conidial chains and the absence of ramoconidia (Schubert et al. 2007). However, in C. tuberosum the conidiophores are not as geniculate as in C. sinuosum and the conidia are always grouped forming short chains, while the conidia in C. sinuosum are often solitary although short chains can be also present (Bensch et al. 2015). In addition, C. tuberosum exhibits a faster growth rate on PDA, forming colonies almost black at the obverse rather than the olivaceous grey to pale olivaceous grey colonies of C. sinuosum (Bensch et al. 2015).
Cladosporium xantochromaticum Sandoval-Denis, Gené & Cano, sp. nov. — MycoBank MB815340; Fig. 11
Etymology. From Greek xanthós (ξανθóζ) ‘yellow’ and khrôma (χρμα) ‘colour’, referring to the production of a yellow diffusible pigment on PDA.
Colonies on OA reaching 40–50 mm after 14 d at 25 °C, obverse and reverse olive brown to grey-green (4F8/30E7), flat, granular, radiate, margin regular and with abundant submerged mycelium; diffusible pigment absent. On PDA attaining 60–67 mm diam after 14 d at 25 °C, olive brown (4E8/F8), flat or folded at centre, dusty or granular, velvety toward the periphery, margin regular, white to yellow, and with abundant submerged mycelium; reverse black, with a light yellow to grey-yellow (2A5/B5) diffusible pigment. On SNA reaching 35–37 mm after 14 d at 25 °C, olive brown (4E5/E8), flat, velvety to granular, radiate, margin regular and with abundant submerged mycelium; reverse olive brown (4E5/E8) to black, without diffusible pigment. Mycelium superficial and immersed, composed of septate, branched, 1.5–3 μm wide, pale brown, smooth and thin-walled hyphae. Conidiophores erect, flexuous, cylindrical, non-nodulose, septate, simple or branched typically immediately before a septum, up to 210 μm long, 2–4 μm wide, pale brown, smooth and thin-walled. Conidiogenous cells terminal, cylindrical, sometimes geniculate, 12–32 × 3–4 μm, bearing up to three conidiogenous loci of 1–1.5 μm diam, darkened and refringent. Ramoconidia aseptate, subcylindrical to cylindrical, 18–36 × 2–3.5 μm, pale brown, smooth or finely roughened. Conidia forming branched chains, with up to four conidia in the terminal unbranched part, pale green-brown, smooth- and thin-walled, with protuberant, not darkened conidial hila; small terminal conidia aseptate, obovate to short ellipsoidal 4–5 × 2–2.5 μm (av. (± SD) 4.3 (± 0.3) × 2.2 (± 0.2)); intercalary conidia aseptate, ellipsoidal to limoniform, 5–7 × 2.5–3.5 μm (av. (± SD) 5.8 (± 0.6) × 2.6 (± 0.3)); secondary ramoconidia 0–1-septate, subcylindrical, sometimes slightly constricted at the centre, 10–28 × 3–4 μm (av. (± SD) 15.7 (± 5.2) × 3.3 (± 0.4)).
Cardinal temperature for growth — Optimum 20 °C, maximum 30 °C, minimum 5 °C.
Specimen examined. USA, Texas, from human bronchoalveolar lavage fluid, Sept. 2010, D.A. Sutton (holotype CBS H-22388, culture ex-type CBS 140691 = UTHSC DI-13-211 = FMR 13324).
Notes — This species belongs to the C. cladosporioides species complex and clusters with C. angulosum and C. perangustum, forming a basal lineage characterised by narrow conidia and slightly roughened conidiophores and conidia. Bensch et al. (2012) considered C. perangustum a species with considerable genetic variability but morphologically uniform. The new species, however, is genetically (99.1 %, 75 % and 89.1 % sequence similarity for ITS, tef1 and actA, respectively) and phenotypically well differentiated from C. perangustum. Cladosporium xantochromaticum has smaller ramoconidia (18–36 × 2–3.5 μm) and smooth-walled conidiophores, while in C. perangustum the ramoconidia are 25–45 × 2.5–3(–4.5) μm and the conidiophores are more or less rough-walled especially towards the base, asperulate-verruculose, and smooth to almost so at the apex (Bensch et al. 2010).
DISCUSSION
The genus Cladosporium has been extensively reviewed in recent years in efforts to clarify the phylogeny and taxonomic structure of its species and allied fungi, and has resulted in a modern redefinition of the genus (Crous et al. 2007a, b, Schubert et al. 2007, Zalar et al. 2007, Bensch et al. 2010, 2012, 2015). However, until recently, no attempt had been made to study the impact of these new approaches in the diversity of Cladosporium species of clinical interest.
In a previous study, we demonstrated that the species diversity of Cladosporium associated to clinical samples was underestimated (Sandoval-Denis et al. 2015). Furthermore, we found that species traditionally considered clinically relevant, identified by phenotypic criteria alone, were among the least represented. In fact, several morphologically similar sibling species were found to be more prevalent, including putative new taxa (De Hoog et al. 2011, Sandoval-Denis et al. 2015). Those previously undescribed lineages are characterised here using both molecular and phenotypic criteria and resulting in the proposal of 10 new Cladosporium species. Sampling for this study was limited to isolates from the USA, and a wider sampling area is expected to provide a more precise reflection of the real distribution of these new species around the world.
The new species proposed here have been mostly isolated from human respiratory samples, which might be explained by the fact that Cladosporium conidia are easily dispersed by air (David 1997). However, the clinical relevance of the species of this genus, at least to produce invasive disease, has been questioned by their inability to grow at 37 °C (De Hoog et al. 2011, Sandoval-Denis et al. 2015), which was also confirmed with the new species. Nevertheless, despite the large number of species involved in this study, some of them were represented by numerous isolates, such as C. anthropophilum, which could be linked to a certain degree of specialisation towards colonisation of the human respiratory tract.
Within a given species complex, the different species of Cladosporium are often difficult to identify from morphological characters alone. However, some key differential features have been identified and have been detailed in a series of monographic papers (Schubert et al. 2007, Zalar et al. 2007, Bensch et al. 2012). We have followed the criteria from those papers in order to distinguish potentially new species from their closest phylogenetic and morphological relatives. As is usual in this genus, no sexual morphs were observed in any of them. In fact, sexual structures have been observed in vitro in only eight accepted species of Cladosporium (Bensch et al. 2012). Among the species described here, the most relevant differential morphological traits were the presence of ramoconidia, the length, complexity and ornamentation of the conidiophores, intercalary and terminal conidia. However, given the overlapping of these features, and the need for standardisation using special culture media and scanning electron microscopy procedures, the use of a molecular approach should be mandatory for correct identification of the species in this complex fungal group. With these studies, we have considerably expanded the list of Cladosporium species as potential human opportunistic fungi, which makes their identification difficult given their high morphological similarity (De Hoog et al. 2015). That said, distinguishing morphologically similar species of Cladosporium seems not to be as relevant from a clinical perspective because the in vitro antifungal response does not differ considerably between species of the same species complex (Sandoval-Denis et al. 2015). In contrast, in vitro antifungal susceptibilities do differ between species complexes, with the C. sphaerospermum complex showing higher inhibitory concentrations against amphotericin B, azoles and caspofungin (Sandoval-Denis et al. 2015).
Our phylogenetic studies agree with previous revisions of the genus (Schubert et al. 2007, Zalar et al. 2007, Bensch et al. 2012). The most phylogenetic informative markers were actA and tef1, while ITS sequences were usually identical for species of the same complex as previously reported by Bensch et al. (2010). Although most of the taxa in the present study are consistently separated in terms of their genetic and morphological differences, a high genetic variability was observed in the clades representing the new species C. anthropophilum and C. tuberosum, as well in clades representing well-known species, i.e. C. allicinum, C. perangustum, C. pseudocladosporioides, C. sinuosum and C. tenuissimum. This might indicate an ongoing process of active divergence and speciation as it has been described for other fungi, which demands further study (Gao et al. 2015).
Several studies have shown a higher number of species in the C. cladosporioides complex (Bensch et al. 2010, 2012, 2015) and our results agree with them. Of the taxa that were newly described here, six species belonged to the C. cladosporioides complex, whereas only three and one, belonged to the C. herbarum and C. sphaerospermum species complexes, respectively. The C. cladosporioides complex is phylogenetically well defined and includes a large group of species characterised by unbranched or branched, almost cylindrical conidiophores, bearing ovoid to ellipsoidal intercalary and terminal conidia, smooth or rarely showing a fine ornamentation (Bensch et al. 2012). Although most of the known species of this complex do not tolerate high temperatures, our results showed that in the C. cladosporioides complex at least three of the new species (C. angulosum, C. anthropophilum and C. flavovirens), as well as several isolates identified as C. pseudocladosporioides are able to grow at 35 °C, which might explain their relatively high rate of isolation from homoeothermic hosts.
The C. herbarum species complex is also phylogenetically and morphologically well defined and contains a less diverse group of species characterized by nodulose conidiophores, bearing distinctly ornamented, globose to subglobose terminal conidia (Schubert et al. 2007). It is interesting that none of the new species of this complex were able to grow at temperatures higher than 30 °C. In contrast, the only new species described in the C. sphaerospermum complex was able to growth and sporulate, although poorly, at 35 °C. The members of the C. sphaerospermum species complex are morphologically homogeneous, characterised by conidiophores that are usually branched and lacking nodose inflations, producing both smooth-walled and ornamented conidia (Zalar et al. 2007). Most species currently included in this group exhibit a high degree of osmotic tolerance, but are unable to grow at temperatures exceeding 30 °C (Zalar et al. 2007, Bensch et al. 2012). However, it has been suggested previously that this complex does not represent a monophyletic group, but most likely represents various species complexes instead (Bensch et al. 2012). This was also suggested by our phylogenetic results which revealed that the species currently included in the C. sphaerospermum complex consistently grouped together as a polyphyletic arrangement in both combined and individual analyses, forming at least five different lineages with high statistical support and important genetic differences. The new species C. succulentum grouped in a lineage with C. aciculare, C. fusiforme, C. longissimum, C. sphaerospermum and C. velox. However, as previously described, there are no phenotypic differences to discriminate among these closely related taxa that would warrant the establishment of additional species complexes to accommodate these lineages (Zalar et al. 2007, Bensch et al. 2015).
In this study, the analysis of isolates from human and animal clinical specimens has allowed us to considerably increase the known diversity of species for the genus, expanding substantially the spectrum of species of potential clinical interest. Further studies are needed to fully understand the ecology and importance of these new species in the aetiology of infections in warm-blooded hosts.
Acknowledgments
This study was supported by the Spanish Ministerio de Economía y Competitividad, grants CGL 2011-27185 and CGL2013-43789-P.
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Nucleotide Sequences (Showing 590 of 590)
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- (1 citation) ENA - HM148128
- (1 citation) ENA - HM148490
- (1 citation) ENA - HM148491
- (1 citation) ENA - HM148370
- (1 citation) ENA - HM148371
- (1 citation) ENA - HM148372
- (1 citation) ENA - HM148130
- (1 citation) ENA - HM148494
- (1 citation) ENA - HM148131
- (1 citation) ENA - HM148373
- (1 citation) ENA - EF101388
- (1 citation) ENA - HM148239
- (1 citation) ENA - JN906989
- (1 citation) ENA - HM148118
- (1 citation) ENA - JN906988
- (1 citation) ENA - EF101385
- (1 citation) ENA - HM148119
- (1 citation) ENA - JN906987
- (1 citation) ENA - JN906986
- (1 citation) ENA - JN906985
- (1 citation) ENA - JN906984
- (1 citation) ENA - JN906983
- (1 citation) ENA - JN906982
- (1 citation) ENA - HM148110
- (1 citation) ENA - JN906981
- (1 citation) ENA - JN906980
- (1 citation) ENA - HM148111
- (1 citation) ENA - HM148354
- (1 citation) ENA - HM148112
- (1 citation) ENA - HM148355
- (1 citation) ENA - HM148476
- (1 citation) ENA - HM148235
- (1 citation) ENA - HM148356
- (1 citation) ENA - HM148236
- (1 citation) ENA - HM148599
- (1 citation) ENA - HM148115
- (1 citation) ENA - HM148238
- (1 citation) ENA - HM148359
- (1 citation) ENA - HM148117
- (1 citation) ENA - HM148481
- (1 citation) ENA - HM148482
- (1 citation) ENA - HM148240
- (1 citation) ENA - HM148361
- (1 citation) ENA - HM148241
- (1 citation) ENA - HM148362
- (1 citation) ENA - HM148120
- (1 citation) ENA - JN906979
Show less
RefSeq - NCBI Reference Sequence Database
- (1 citation) RefSeq - NR_121315
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