Eurotiomycetes

Dactylospora parasitica, copyright Jason Hollinger.

Belongs within: Ascomycota.
Contains: Pyrenulales, Chaetothyriales, Verrucariaceae, Eurotiomycetidae.

Black yeasts, black lichens and rotting wood: the Chaetothyriomycetidae
Published 25 November 2014

There is no denying that the advent of molecular phylogenetic analysis has been a boon for fungal systematics. It has allowed a much greater resolution of relationships than was previously possible (especially for comparisons between asexually- and sexually-reproducing fungi), and has even lead to the identification of a number of major lineages that probably could have never been recognised from morphological data alone. One such lineage is the Chaetothyriomycetidae, whose members vary from lichens on tropical tree trunks, to saprobes living in the deep sea, to pathogens in the brains of humans.

Pyrenula cruenta, copyright Gary Perlmutter.

The Chaetothyriomycetidae (or Chaetothyriomycetes in many older references: the botanical code goes rather all out in the rather irritating practice of changing the endings of names to indicate arbitrary taxonomic ranks) has been divided by Gueidan et al. (2014) into four major lineages. Two of these, the Pyrenulales and Verrucariaceae, are mostly comprised of lichens. Lichenised fungi in the Pyrenulales associate with green algae of the family Trentopohliaceae (which, despite being ‘green algae’, are generally orange in colour), and are most commonly found on tree bark in tropical forests. Only one lichenised genus, Strigula, is also found growing on leaves; non-lichenised Pyrenulales are found on bark, leaves or wood (Geiser et al. 2006).

Verrucaria maura on coastal rocks, copyright A. J. Silverside.

The Verrucariaceae, in contrast, associate with different symbiotic algae, and prefer to grow on rocks. Lichens of this family are often blackish; their hyphae are darkened by a melanin-like compound which allows them to tolerate quite exposed conditions. Certain species are particularly prominent around the marine shoreline. Gueidan et al. (2014) also identified a small as-yet-unnamed lineage close to Verrucariaceae including rock-dwelling and moss-associated non-lichenised fungi, but support for this grouping requires further testing.

Another somewhat novel lineage identified by Gueidan et al. (2014) was the Celotheliaceae. The type genus, Celothelium, is a lichenised fungus that associates with the alga Trentepohlia in the manner of Pyrenulaceae. Other members of the Celotheliaceae, however, are quite different in ecology, being mostly pathogens of woody plants. Phaeomoniella chlamydospora is a causative agent of grapevine trunk disease, resulting in conditions such as esca, and the rather ominously named ‘black goo decline’ (so-called because the stems become filled with ‘black goo’, as the xylem vessels become clogged with fungal hyphae). Dolabra nepheliae causes canker in lychee and rambutan trees. These pathogenic taxa are commonly largely anamorphic (that is, they produce asexual reproductive structures).

Culture of black yeast Exophiala dermatitidis, from here.

The last and most diverse lineage (so far as we know, anyway) is the Chaetothyriales. Like the Verrucariaceae, the Chaetothyriales have melanised hyphae and often grow on exposed substrates such as rocks. Indeed, molecular analyses have supported a closer relationship between Verrucariaceae and Chaetothyriales than the other major lineages. However, members of the Chaetothyriales are not lichenised. Many are saprobic; others, such as the Chaetothyriaceae, grow on plant leaves but in many cases it is unclear whether they are saprobic or parasitic. The mostly saprobic family Herpotrichiellaceae also includes a number of asexually-reproducing forms that grow as yeasts and are opportunistic pathogens, including in humans. Infections by black yeasts (Exophiala) are most commonly cutaneous and relatively superficial, but they can also cause severe and life-threatening infections of deeper organ systems. These infections are most common in patients with pre-existing conditions affecting the immune system, but at least one species, E. dermatitidis, has been recorded causing fatal brain infections in otherwise healthy individuals.

And I referred at the beginning of this post to the deep sea? Well, the Chaetothyriomycetidae samples from there are, I believe, yet to be described. It is possible that this diverse group of fungi still has surprises for us.

Eurotiomycetes: small but significant fungi
Published 27 February 2021

Mention the word ‘fungi’ and most people’s thoughts will probably go to images of mushrooms or toadstools. A few may conjure up pictures of lichens. Nevertheless, the great majority of fungal species are microscopic and likely to pass unremarked by most observers. That does not, however, mean that they are of no consequence. Today’s post involves one major group that, for all their visual insignificance, include some of the most significant fungal species for modern human society: the Eurotiomycetes.

Developmental stages of Aspergillus glaucus, with cleistothecia as figs 21–23, from Raper & Fennel (1965).

The class Eurotiomycetes has been recognised in recent years as including a diverse assemblage of fungi, associated with a wide range of morphologies and habitats, that are united as a clade by molecular analyses. Réblová et al. (2017) recognised five subclasses within the Eurotiomycetes of which the two largest (or at least the most studied) are the Eurotiomycetidae and the Chaetothyriomycetidae. The Eurotiomycetidae are, for the greater part, saprobes. They were largely recognised as a distinctive group even before the advent of molecular phylogenetic analysis owing to the production by sexually reproducing forms of a distinctive type of fruiting body, the cleistothecium. In cleistothecia, the fruiting body is completely enclosed with no openings to faciliatate the release of spores, which only escape when the fruiting body itself breaks down. Cleistothecia are most commonly produced by fungi that grow in enclosed locations such as underground (the Eurotiomycetidae are not the only group of fungi to produce cleistothecia though they are one of the most diverse). Within the cleistothecium, spores develop within globular asci with a single wall that breaks down shortly after maturity (Geiser et al. 2015).

Penicillium expansum on rotting pear, copyright H. J. Larsen.

For many people, though, the most familiar members of the Eurotiomycetidae are likely to be asexually reproducing forms. This is the clade containing the moulds of the genera Aspergillus and Penicillium. Even before a species of the latter achieved fame as the shource of the first known antibiotic, penicillin, members of these genera had a great impact on human lives. Species of Penicillium are the moulds used in the production of cheeses such as Roquefort and camembert. Species of Aspergillus are used to ferment soy beans and rice in the production of comestibles such as soy sauce and sake. On the flip side, a number of species of Eurotiomycetidae act as pathogens of mammals including humans, causing conditions such as respiratory illnesses or tinea, with the former being of particular concern in immunocompromised individuals. Eurotiomycetid moulds may also cause problems for food storage and the like, particularly as many species are capable of growing under remarkably hot and/or dry conditions. Some Aspergillus moulds produce dangerous toxins, capable of causing acute poisioning or cancer development.

Verrucaria maura, copyright Richard Droker.

The Chaetothyriomycetidae are less clearly defined morphologically than the Eurotiomycetidae but fruiting bodies are mostly produced as perithecia: flask-shaped structures with an apical pore through which spores are released. The asci within the perithecium usually possess a double wall. Like many eurotiomycetids, chaetothyriomycetids have a tendency to be associated with habitats where water availability is a concern such as in very dry and/or saline environments. A number of chaetothyriomycetid species form lichens. One genus, Verrucaria, is often found as a thin black lichen growing on rocks along the seashore. Some species grow within the cavities of myrmecophytes, plants that form mutualistic associations with ants (the plant provides food and/or accomodation for the ants and the ants help keep the plant clear of grazers or sap-suckers). The fungi are cultivated by the ants that use them for food.

The other three subclasses of the Eurotiomycetes are less well known and recognised as containing a single order each. The Sclerococcales were first recognised as such by Réblová et al. (2017) via molecular analysis. Fruiting bodies, where known, are apothecia (open bowls) bearing single-walled asci. Representatives are known from marine and terrestrial habitats, growing on wood or lichens, and some have been isolated from within the digestive tracts of bark beetles. The Coryneliaceae, living as parasites on podocarps, have been considered as morphologically intermediate between chaetothyriomycetids and eurotiomycetids. Molecular analysis positions them as sister to the latter (Wood et al. 2016). Finally, the Mycocaliciales live as parasites or commensals of other fungi, particularly lichens.

There are other representatives of the Eurotiomycetes that I haven’t even had the time to gloss over, such as endophytes and ectomycorrhizal truffles. You may not know they’re there but that doesn’t mean they don’t mean anything to you.

Systematics of Eurotiomycetes
<==Eurotiomycetes [Plectomycetes]AS12
    |  i. s.: Pseudoamauroascus australiensisPA-W02
    |         Calyptrozyma Boekhout & Spaay 1995EB03O, KC01
    |           `--C. arxiiSL02
    |         Sclerococcum Fr. 1819KC01 [incl. Spilomium Nyl. 1858KC01; SclerococcalesAB19, Sclerococcomycetidae]
    |           `--S. parmeliaeE98
    |--Mycocaliciaceae [Mycocaliciales, Mycocaliciomycetidae]LS01
    |    |--Phaeocalicium Schmidt 1970KC01
    |    |--Stenocybe Nyl. ex Körb. 1855KC01
    |    |    `--S. septataKC01
    |    |--Mycocalicium Vain. 1890SH05, KC01 [incl. Sphinctrinella Nádv. 1942KC01]
    |    |    |--M. albonigrumSH05
    |    |    |--M. polyporaeumHM17
    |    |    `--M. victoriaeSH05
    |    `--Chaenothecopsis Vain. 1927 (see below for synonymy)KC01
    |         |  i. s.: C. savonicaLS01
    |         |--C. montanaHM17
    |         `--+--C. sitchensisHM17
    |            `--SphinctrinaceaeKC01
    |                 |--Pyrgidium Nylander 1867 [=Pyrgidiomyces Cif. & Tomas. 1953]KC01
    |                 `--Sphinctrina Fr. 1825HM17, KC01 [incl. Phacotiella Vain. 1927KC01]
    |                      `--S. turbinataLS01
    `--+--Dactylospora Körb. 1855SS09, KC01 (see below for synonymy)
       |    |--D. haliotrephaSS09
       |    |--D. heimerliiKC01
       |    |--D. mangroveiSS09
       |    `--D. parasiticaE98
       `--+--Chaetothyriomycetidae [Chaetothyriomycetes]JKW03
          |    |  i. s.: Rhynchostoma Karst. 1870KC01 [incl. Arthropycnis Constant. 1992KC01; RhynchostomataceaeEB03O]
          |    |--PyrenulalesLK04
          |    `--+--ChaetothyrialesSS09
          |       `--Verrucariales [Verrucomycetidae]EB03O
          |            |  i. s.: Pocsia Vězda 1975KC01
          |            |--VerrucariaceaeJK06
          |            `--AdelococcaceaeEB03O
          |                 |--Adelococcus Theiss. & Syd. 1918KC01
          |                 `--Sagediopsis (Sacc.) Vain. 1921KC01
          `--+--EurotiomycetidaeAB19
             `--Coryneliaceae [Coryneliales, Coryneliomycetidae]SS09
                  |--Bicornispora Checa, Barrasa et al. 1996EB03O, KC01
                  |--Corynelia Ach. 1823 [incl. Alboffia Speg. 1899, Endohormidium Auersw. & Rabenh. 1869]KC01
                  |--Coryneliopsis Butin 1972KC01
                  |--Coryneliospora Fitzp. 1942KC01
                  |--Fitzpatrickella Benny, Samuelson & Kimbr. 1985KC01
                  |--Lagenulopsis Fitzp. 1942KC01
                  |--Tripospora Sacc. 1886 [=Tripocorynelia Kuntze 1898]KC01
                  `--Caliciopsis Peck 1880 (see below for synonymy)KC01
                       |--C. orientalisHM17
                       `--C. pineaSS09

Caliciopsis Peck 1880 [incl. Capnodiella (Sacc.) Sacc. 1905, Hypsotheca Ellis & Everh. 1885, Lagenula Arnaud 1930 nec Lour. 1790 nec de Montfort 1808 (ICZN), Sorica Giesenh. 1904]KC01

Chaenothecopsis Vain. 1927 [incl. Asterophoma Hawksw. 1981, Catenomycopsis Tibell & Constant 1991, Chaenotheciella Räsänen 1943, Pseudocalicium Marchand 1896, Strongyleuma Vain. 1927]KC01

Dactylospora Körb. 1855SS09, KC01 [incl. Abrothallomyces Cif. & Tomas. 1953KC01, Kymadiscus Kohlm. & Kohlm. 1971KC01, Mycolecidia Karst. 1888KC01, Mycolecis Clem. 1909KC01, Paruephaedria Zukal 1891KC01, Pseudokarschia Velen. 1934KC01; Dactylosporaceae]

*Type species of generic name indicated

References

[AB19] Adl, S. M., D. Bass, C. E. Lane, J. Lukeš, C. L. Schoch, A. Smirnov, S. Agatha, C. Berney, M. W. Brown, F. Burki, P. Cárdenas, I. Čepička, L. Chistyakova, J. del Campo, M. Dunthorn, B. Edvardsen, Y. Eglit, L. Guillou, V. Hampl, A. A. Heiss, M. Hoppenrath, T. Y. James, A. Karnkowska, S. Karpov, E. Kim, M. Kolisko, A. Kudryavtsev, D. J. G. Lahr, E. Lara, L. Le Gall, D. H. Lynn, D. G. Mann, R. Massana, E. A. D. Mitchell, C. Morrow, J. S. Park, J. W. Pawlowski, M. J. Powell, D. J. Richter, S. Rueckert, L. Shadwick, S. Shimano, F. W. Spiegel, G. Torruella, N. Youssef, V. Zlatogursky & Q. Zhang. 2019. Revisions to the classification, nomenclature, and diversity of eukaryotes. Journal of Eukaryotic Microbiology 66: 4–119.

[AS12] Adl, S. M., A. G. B. Simpson, C. E. Lane, J. Lukeš, D. Bass, S. S. Bowser, M. W. Brown, F. Burki, M. Dunthorn, V. Hampl, A. Heiss, M. Hoppenrath, E. Lara, E. Le Gall, D. H. Lynn, H. McManus, E. A. D. Mitchell, S. E. Mozley-Stanridge, L. W. Parfrey, J. Pawlowski, S. Rueckert, L. Shadwick, C. L. Schoch, A. Smirnov & F. W. Spiegel. 2012. The revised classification of eukaryotes. Journal of Eukaryotic Microbiology 59 (5): 429–493.

[EB03] Eriksson, O. E., H. O. Barah, R. S. Currah, K. Hansen, C. P. Kurtzman, G. Rambold & T. Laessøe (eds.) 2003. Outline of Ascomycota—2003. Myconet 9: 1–89.

Geiser, D. M., C. Gueidan, J. Miadlikowska, F. Lutzoni, F. Kauff, V. Hofstetter, E. Fraker, C. L. Schoch, L. Tibell, W. A. Untereiner & A. Aptroot. 2006. Eurotiomycetes: Eurotiomycetidae and Chaetothyriomycetidae. Mycologia 98 (6): 1053–1064.

Geiser, D. M., K. F. LoBuglio & C. Gueidan. 2015. Pezizomycotina: Eurotiomycetes. In: D. J. McLaughlin, & J. W. Spatafora (eds) The Mycota 2nd ed. vol. 7. Systematics and Evolution part B pp. 121–141. Springer-Verlag: Berlin.

Gueidan, C., A. Aptroot, M. E. da Silva Cáceres, H. Badali & S. Stenroos. 2014. A reappraisal of orders and families within the subclass Chaetothyriomycetidae (Eurotiomycetes, Ascomycota). Mycol. Progress 13: 1027–1039.

[HM17] Hongsanan, S., S. S. N. Maharachchikumbura, K. D. Hyde, M. C. Samarakoon, R. Jeewon, Q. Zhao, A. M. Al-Sadi & A. H. Bahkali. 2017. An updated phylogeny of Sordariomycetes based on phylogenetic and molecular clock evidence. Fungal Diversity 84: 25–41.

[JKW03] Jacobs, K., T. Kirisits & M. J. Wingfield. 2003. Taxonomic re-evaluation of three related species of Graphium, based on morphology, ecology and phylogeny. Mycologia 95 (4): 714–727.

[JK06] James, T. Y., F. Kauff, C. L. Schoch, P. B. Matheny, V. Hofstetter, C. J. Cox, G. Celio, C. Gueidan, E. Fraker, J. Miadlikowska, H. T. Lumbsch, A. Rauhut, V. Reeb, A. E. Arnold, A. Amtoft, J. E. Stajich, K. Hosaka, G.-H. Sung, D. Johnson, B. O’Rourke, M. Crockett, M. Binder, J. M. Curtis, J. C. Slot, Z. Wang, A. W. Wilson, A. Schüßler, J. E. Longcore, K. O’Donnell, S. Mozley-Standridge, D. Porter, P. M. Letcher, M. J. Powell, J. W. Taylor, M. M. White, G. W. Griffith, D. R. Davies, R. A. Humber, J. B. Morton, J. Sugiyama, A. Y. Rossman, J. D. Rogers, D. H. Pfister, D. Hewitt, K. Hansen, S. Hambleton, R. A. Shoemaker, J. Kohlmeyer, B. Volkmann-Kohlmeyer, R. A. Spotts, M. Serdani, P. W. Crous, K. W. Hughes, K. Matsuura, E. Langer, G. Langer, W. A. Untereiner, R. Lücking, B. Büdel, D. M. Geiser, A. Aptroot, P. Diederich, I. Schmitt, M. Schultz, R. Yahr, D. S. Hibbett, F. Lutzoni, D. J. McLaughlin, J. W. Spatafora & R. Vilgalys. 2006. Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443: 818–822.

[KC01] Kirk, P. M., P. F. Cannon, J. C. David & J. A. Stalpers. 2001. Ainsworth & Bisby’s Dictionary of the Fungi 9th ed. CAB International: Wallingford (UK).

[LS01] Lumbsch, H. T., I. Schmitt, H. Döring & M. Wedin. 2001. Molecular systematics supports the recognition of an additional order of Ascomycota: the Agyriales. Mycological Research 105 (1): 16–23.

[LK04] Lutzoni, F., F. Kauff, C. J. Cox, D. McLaughlin, G. Celio, B. Dentinger, M. Padamsee, D. Hibbett, T. Y. James, E. Baloch, M. Grube, V. Reeb, V. Hofstetter, C. Schoch, A. E. Arnold, J. Miadlikowska, J. Spatafora, D. Johnson, S. Hambleton, M. Crockett, R. Shoemaker, G.-H. Sung, R. Lücking, T. Lumbsch, K. O’Donnell, M. Binder, P. Diederich, D. Ertz, C. Gueidan, K. Hansen, R. C. Harris, K. Hosaka, Y.-W. Lim, B. Matheny, H. Nishida, D. Pfister, J. Rogers, A. Rossman, I. Schmitt, H. Sipman, J. Stone, J. Sugiyama, R. Yahr & R. Vilgalys. 2004. Assembling the fungal tree of life: progress, classification, and evolution of subcellular traits. American Journal of Botany 91 (10): 1446–1480.

[PA-W02] Pang, K.-L., M. A. Abdel-Wahab, S. Sivichai, H. M. El-Sharouney & E. B. G. Jones. 2002. Jahnulales (Dothideomycetes, Ascomycota): a new order of lignicolous freshwater ascomycetes. Mycological Research 106 (9): 1031–1042.

Réblová, M., W. A. Untereiner, V. Štěpánek & W. Gams. 2017. Disentangling Phialophora section Catenulatae: disposition of taxa with pigmented conidiophores and recognition of a new subclass, Sclerococcomycetidae (Eurotiomycetes). Mycological Progress 16: 27–46.

[SS09] Schoch, C. L., G.-H. Sung, F. López-Giráldez, J. P. Townsend, J. Miadlikowska, V. Hofstetter, B. Robbertse, P. B. Matheny, F. Kauff, Z. Wang, C. Gueidan, R. M. Andrie, K. Trippe, L. M. Ciufetti, A. Wynns, E. Fraker, B. P. Hodkinson, G. Bonito, J. Z. Groenewald, M. Arzanlou, G. S. de Hoog, P. W. Crous, D. Hewitt, D. H. Pfister, K. Peterson, M. Gryzenhout, M. J. Wingfield, A. Aptroot, S.-O. Suh, M. Blackwell, D. M. Hillis, G. W. Griffith, L. A. Castlebury, A. Y. Rossman, H. T. Lumbsch, R. Lücking, B. Büdel, A. Rauhut, P. Diederich, D. Ertz, D. M. Geiser, K. Hosaka, P. Inderbitzin, J. Kohlmeyer, B. Volkmann-Kohlmeyer, L. Mostert, K. O’Donnell, H. Sipman, J. D. Rogers, R. A. Shoemaker, J. Sugiyama, R. C. Summerbell, W. Untereiner, P. R. Johnston, S. Stenroos, A. Zuccaro, P. S. Dyer, P. D. Crittenden, M. S. Cole, K. Hansen, J. M. Trappe, R. Yahr, F. Lutzoni & J. W. Spatafora. 2009. The Ascomycota tree of life: a phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits. Systematic Biology 58 (2): 224–239.

[SL02] Schweigkofler, W., K. Lopandic, O. Molnár & H. Prillinger. 2002. Analysis of phylogenetic relationships among Ascomycota with yeast phases using ribosomal DNA sequences and cell wall sugars. Organisms Diversity & Evolution 2: 1–17.

[SH05] Selbmann, L., G. S. de Hoog, A. Mazzaglia, E. I. Friedman & S. Onofri. 2005. Fungi at the edge of life: cryptoendolithic black fungi from Antarctic desert. Studies in Mycology 51: 1–32.

Wood, A. R., U. Damm, E. J. van der Linde, J. Z. Groenewald, R. Cheewangkoon & P. W. Crous. 2016. Finding the missing link: resolving the Coryneliomycetidae within Eurotiomycetes. Persoonia 37: 37–56.

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