Fungal Systematics: Is a New Age to Some Fungal Taxonomists, the Changes Were Seismic11

Home , Archaeorhizomycetes, Eurotium herbariorum, Penicillium camemberti, Volutella (fungus)

Nature Reviews Microbiology | AOP, published online 3 January 2013; doi:10.1038/nrmicro2942 PERSPECTIVES

Nomenclature for Algae, Fungi, and Plants ESSAY (ICN). To many scientists, these may seem like overdue, common-sense measures, but Fungal systematics: is a new age to some fungal taxonomists, the changes were seismic11. of enlightenment at hand? In the long run, a unitary nomenclature system for pleomorphic fungi, along with the other changes, will promote effective David S. Hibbett and John W. Taylor communication. In the short term, however, Abstract | Fungal taxonomists pursue a seemingly impossible quest: to discover the abandonment of dual nomenclature will require mycologists to work together and give names to all of the world’s mushrooms, moulds and yeasts. Taxonomists to resolve the correct names for large num‑ have a reputation for being traditionalists, but as we outline here, the community bers of fungi, including many economically has recently embraced the modernization of its nomenclatural rules by discarding important pathogens and industrial organ‑ the requirement for Latin descriptions, endorsing electronic publication and isms. Here, we consider the opportunities ending the dual system of nomenclature, which used different names for the sexual and challenges posed by the repeal of dual nomenclature and the parallels and con‑ and asexual phases of pleomorphic species. The next, and more difficult, step will trasts between nomenclatural practices for be to develop community standards for sequence-based classification. fungi and prokaryotes. We also explore the options for fungal taxonomy based on Taxonomists create the language of bio‑ efforts to classify taxa that are discovered environmental sequences and ask whether diversity, enabling communication about through metagenomics5. sequence-based taxonomy can be reconciled different organisms among basic and In the lead‑up to the last IBC in July with the ICN. applied scientists, educators, students and 2011, a vocal and well-organized group of the general public. This essential work is mycologists launched a ‘One fungus, one One name, one fungus particularly challenging in hyperdiverse name’ campaign aimed at ending the system The dual nomenclature system for pleomor‑ and morphologically cryptic groups, such of dual nomenclature. The movement culmi‑ phic fungal species arose in the nineteenth as the kingdom Fungi. Roughly 100,000 nated in the publication of ‘The Amsterdam century, influenced by the use of sexual species of fungi are accepted in the current declaration on fungal nomenclature’ (by morphology in the Linnaean classification taxonomy1, but more than 400,000 fun‑ 88 co-authors from 26 countries)4, which of plants12,13. Despite the fact that is illogi‑ gal species names — including numerous suggested that if dual nomenclature were cal to assign multiple names to one species, synonyms — are recorded in the literature, retained in the botanical code, it might be the dual nomenclature system persisted, and it is likely that millions of new species2 necessary to create a separate MycoCode for in part because the morphology of sexual still await description. Thus, the challenge the kingdom Fungi6. Independently, some reproductive structures was assumed to be for modern fungal taxonomy is to weed out mycologists had already begun to publish superior to that of asexual forms for infer‑ redundant published names while accelerat‑ new fungal names that ignored reproductive ring the evolutionary relationships of fungi14. ing the naming of newly discovered species. morphology, putting sexual and asexual spe‑ However, sexual characteristics lost their To regulate the naming of fungi, mycologists cies in the same genus and thus deliberately pre-eminence for classifying fungi in the adhere to the International Code of Botanical disregarding the code7–9. Facing nomenclatu‑ late 1980s, when PCR made DNA variation Nomenclature3. The code provides stability ral disobedience and the threat of secession, accessible to systematic mycologists. More to a potentially chaotic discipline, but it is the Nomenclature Section of the 2011 IBC than 20 years later, the dual nomenclature updated only once every 7 years and only voted to abolish the dual system of fungal system was finally abolished. at meetings of the Nomenclature Section nomenclature10,11. At the same time, and in As is always the case, the hard work during the International Botanical Congress response to pressure from other activists, begins after the revolution. For mycologists, (IBC), which makes the code slow to adapt the Nomenclature Section also voted to this means choosing names for thousands of to modern practices in systematics. The eliminate Latin descriptions (English will pleomorphic fungal species. Some choices fungal elements of the code that have been now suffice), to allow the publication of will be difficult. For example, the anamor‑ criticized as archaic include the dual system new names in online-only journals (previ‑ phic genus Penicillium (with teleomorphic of nomenclature4, which creates different ously, print was required) and to require genera Eupenicillium and Talaromyces) names for the anamorphs (asexual forms) registration of new fungal names in a pub‑ contains fungi as important as Penicillium and teleomorphs (sexual forms) of the same lically accessible database such as Index rubens (the original source of penicillin), species (FIG. 1), and the requirement for Fungorum or MycoBank10. Finally, the code Penicillium marneffei (the causative agent physical type specimens, which complicates itself was renamed the International Code of of an AIDS-defining disease in Thailand),

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time, the goal was to begin working through the myriad options for the classification of pleomorphic fungi in light of the new rules. Similar meetings and workshops on the taxonomy of the genus Fusarium, the order Hypocreales and other groups were held in association with meetings of the Mycological Society of Japan (May 2012), the Mycological Society of America (July 2012) and the Mycological Society of China (August, 2012).

Classification of environmental sequences Now that dual nomenclature has been abolished, the next major challenge for fungal taxonomy is to develop strategies Figure 1 | Two names, one fungus. Eurotium herbariorum is a pleomorphic fungus that has a sexual Nature Reviews | Microbiology for classifying environmental sequences phase, reproducing by ascospores (the teleomorphic form; left), as well as a conidium-producing (FIG. 2). Nobody knows how many unnamed asexual phase (the anamorphic form; right) that has been named Aspergillus glaucus. Images courtesy species have already been detected through of Paul F. Cannon, Royal Botanical Gardens, Kew, London, UK, and the Centre for Agricultural metagenomic studies (and this fact alone Bioscience International (CABI). indicates the need for a centralized database of species that are based on environmental sequences), but as early as 2007 the number and Penicillium camemberti and Penicillium nomenclatural changes mentioned above of clusters of closely related rRNA genes roqueforti (used to make Camembert and illustrate what might lie ahead. Another being discovered with Sanger chemistry Brie, and Roquefort cheeses, respectively). example is the work of Gräfenhan et al.9 approached the number of species being However, Penicillium spp., as traditionally on the taxonomy of the anamorphic genus described from specimens5, and the rate delimited, are paraphyletic as well as pleo‑ Fusarium, one of the largest genera of fungi, of molecular species discovery has surely morphic, so these well-known species containing nearly 1,500 species, subspecies, increased with the application of next- cannot all remain in this historic genus15. varieties and formae speciales. Fusarium generation sequencing in metagenomics. Under the revised code, any of the exist‑ spp. include important plant and animal Environmental studies have revealed ing valid names for a species can be selected pathogens and mycotoxin producers and not only individual species, but also as its correct name, with preference given to have been linked to as many as seven tele‑ major clades of fungi, such as the class the oldest name. However, this libertarian omorph genera. On the basis of sequence Archaeorhizomycetes17, containing a view is tempered by two additional revi‑ analyses for RNA polymerase II and ATP diverse group of soil-inhabiting fungi from sions, both involving review by the General citrate lyase genes, Gräfenhan et al.9 identi‑ the phylum Ascomycota. Sequences of Committee (GC) of the ICN, which is fied 15 clades with Fusarium-like asexual Archaeorhizomycetes members have been empowered to vote on proposals to conserve forms and gave six of them names based on reported in more than 50 independent stud‑ or reject names of fungal taxa, as well as to anamorphs, although five of these six have ies, and they can be grouped into more than modify the ICN itself 3. First, in situations in known teleomorphic forms. The reclassifica‑ 100 species-level entities17. Nevertheless, which both the anamorph and teleomorph tion of Fusarium by Gräfenhan et al. is based only one species, Archaeorhizomyces names for the same taxon are widely used on robust phylogenies and would be nomen‑ finlayi, has been formally described, based — for example, Fusarium (anamorph) and claturally valid under the forthcoming ICN. on a culture that was obtained from coni‑ Gibberella (teleomorph) at the genus level Nevertheless, name changes in the genus fer roots. A similar example is provided — the teleomorph name can be chosen with‑ Fusarium sensu lato might confuse and by the phylum Rozellomycota18 (also out approval of the GC, but selection of the inconvenience user communities and regula‑ known as Cryptomycota19), a large clade anamorph name, even if it is the older name, tory bodies in agriculture and medicine, and of aquatic and soil-inhabiting fungi that is requires approval. Apparently, it is hard for it remains to be seen how these constituencies known almost entirely from environmen‑ systematists to abandon the primacy of sex‑ will react to the new taxonomy. tal sequences. The phylum Rozellomycota ual characteristics. Second, the GC has the The complex nomenclatural history of has been shown to contain the previously authority to approve lists of names, which many groups of pleomorphic fungi, coupled described chytrid genus Rozella19, but most presumably will be generated by committees with phylogenetic uncertainty and the some‑ of the diversity of this phylum is in groups of mycologists with expertise in particular times passionate opinions of stakeholders, that are known only from environmental taxonomic groups. However, mycologists presents a very challenging taxonomic prob‑ sequences and have not been named. These have retained the right to appeal any deci‑ lem. The code provides guidance, but many examples, and many others from fungal sion about names through the established decisions about names cannot be reduced molecular ecology, illustrate the profound process of conservation of names. to ‘legal’ algorithms. As a follow‑up to the disconnect that now exists between formal No one has had a chance to choose a ‘One fungus, one name’ movement that led taxonomy and species discovery through name for a pleomorphic fungal species to the repeal of dual nomenclature, a ‘One environmental sequences. Barriers to the under the new code, which only came fungus, which name?’ conference was held naming of such species include a perceived into effect on 1 January 2013, but the in Amsterdam in April 2012 (REF. 16). This conflict with the code, and errors and

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Uncultured fungus clone unisequences#37-3808_2763 ITS2, PS Uncultured fungus clone MOTU_2635_GVUGVSB04J56R4 18S rRNA gene, PS, ITS Uncultured fungus clone MOTU_3006_GVUGV5B04JIHT 18S rRNA gene Uncultured fungus clone MOTU_1888_GVUGV5B04JJTLJ 18S rRNA gene Uncultured fungus clone MOTU_2993_GOKCVYYY06HH12J 18S rRNA gene, PS, ITS Uncultured fungus clone MOTU_2930_GOKCVYYY06G7201 18S rRNA gene, PS, ITS Fibulobasidium murrhardtense strain CB59109 18S rRNA gene Uncultured fungus clone MOTU_141_GOKCVYYY06G5FYL 18S rRNA gene, PS, ITS Uncultured Tremellales clone LTSP_EUKA_P4L03 18S rRNA gene, PS, ITS Uncultured fungus clone MOTU_601_GOK Uncultured basidiomycete ITS Uncultured fungus clone unisequence#65-3936_0554 ITS2, PS Fungi 3 leaves Uncultured fungus clone unisequence Uncultured Tremellales clone LTSP_EUKA Trichosporonales sp. LM559 18S rRNA gene Uncultured fungus clone unisequences #65-3574_00447, ITS2, PS Uncultured fungus clone MOTU_4349_GOKCVYYY06GR7WA 18S rRNA gene, PS, ITS2 Uncultured fungus clone unisequences#69-3466_2373 ITS2, PS Uncultured fungus clone MOTU_43 Uncultured fungus clone F66N0BQ02H1NX5 18S rRNA gene Uncultured fungus clone LT5P_EUKA_P5H04 18S rRNA gene, 18S–25/28S rRNA gene Uncultured fungus clone MOTU_1778_GVUGB5B04IF01X 18S rRNA gene, PS Uncultured fungus clone MOTU_4043_GVUGB5B04JK5N2 18S rRNA gene, PS, ITS2 Uncultured fungus clone MOTU_2412 Uncultured Agaricomycotina clone 6_g19 18S rRNA gene Uncultured fungus clone MOTU_3797_GOKCVYYY06HBZ1X 18S rRNA gene, PS, ITS2 Uncultured Rhodotorula IT51, 5.8S rRNA, ITS2 and partial 28S rRNA, clone MNIB2FAST_K1 Uncultured Tremellales clone 5_D20 18S rRNA, ITS1, 5.8S rRNA gene, ITS1 Uncultured fungus clone U_QM_090130_127_1A_plate1g12.b1 18S rRNA gene, PS, ITS1 Uncultured fungus clone OTU_1445_1GW5CJXV07HXDTO 18S rRNA gene Uncultured fungus clone MOTU_3163_GYUGV5B0412KQP 18S rRNA gene, PS, ITS1 Uncultured fungus clone MOTU_533_GOKCVYYY06GU3JA18S rRNA gene, PS, ITS1 Uncultured fungus clone U_QM_090130_240_B_plate1a12.b1 18S rRNA gene, PS, ITS1 Uncultured fungus clone OTU_403_GW5CJXV07IOX5A 18S rRNA gene Uncultured fungus clone singleton_70-3063_2201 18S rRNA gene, PS, ITS gi|22497358|gb|FJ761130.1| uncultured fungus clone singleton_70-3063_2201 18S rRNA gene

Figure 2 | Unnamed diversity. A demonstration of the problem posed distance tree tool, only two of the 35 most closely related sequences were by unnamed fungi that are known only from environmental DNA from cultured organisms (green boxes),Nature and onlyReviews one | Microbiologywas named sequences. When a new environmental sequence (the bottom-most opera- (Fibulobasidium murrhardtense). Without names, the information content tional taxonomic unit, gi|22497358; blue box) was used in a BLAST search of this tree leaves much to be desired. ITS, internal transcribed spacer; of the GenBank database and the result displayed using the BLAST PS, partial sequence. incomplete taxon sampling in reference the publication of P. cryptodigmaticus pro‑ is, generate well-documented reference sequence databases. vides a model for environmental molecular sequences21 — and is already being pur‑ The perceived incompatibility of the biologists who would like to formalize sued through the fungal bar-coding initia‑ code with sequence-based taxonomy is a their discoveries through code-compliant tive22 and the creation of custom-curated consequence of the requirement for type taxonomic names. databases of well-documented reference specimens. However, the code places no Errors and incomplete taxonomic sequences, such as the RefSeq collection restrictions on the form of type specimens, sampling in sequence databases, such as within GenBank, and the UNITE database which need not be complete or representa‑ GenBank, present a psychological barrier for mycorrhizal fungi23. tive; all that is required of a type specimen to naming environmental sequences; if is that it should be a physical specimen. an environmental sequence has no match Lessons from prokaryotic taxonomy In principle, an aliquot of DNA extracted in GenBank, it could still represent a Many of the taxonomic challenges faced from an environmental sample, or a por‑ described but unsequenced species. Faced by mycologists parallel those faced by tion of the substrate from which the DNA with such uncertainty, fungal taxonomists researchers studying prokaryotes, but the was isolated, can serve as a legitimate type might be reluctant to describe new species nomenclatural practices adopted by the two specimen. To prove this point, Kirk et al.20 based on environmental sequences. They groups are often divergent. For example, recently described a new species of rumen should not be; current estimates of the the expanded power of the GC to rule on chytrid, Piromyces cryptodigmaticus, based actual diversity in the kingdom Fungi range the legitimacy of choices among existing on sequence data, and typified it with a from as few as 500,000 species to millions names under the forthcoming ICN might sample from the fermenter from which the of species2, suggesting that most unmatched worry some mycologists, who could fear DNA was extracted. The new taxon name environmental sequences probably do rep‑ a loss of taxonomic freedom, but the new was validly published, even though the resent new species5. Even if some environ system for fungi might seem familiar to fungus was never directly observed. In the mental species prove to be redundant, prokaryote taxonomists, who have long future, if purely sequence-based taxonomy taxonomists are accustomed to resolving used a Judicial Commission to accept or is incorporated into the code, it may be pos‑ synonymy based on the principle of priority. reject newly proposed names24,25. Another sible to forego the deposition of physical Finally, the solution to the GenBank prob‑ key difference between the nomenclatural type materials altogether. In the meantime, lem is conceptually straightforward — that codes for prokaryotes26 and fungi3 is that

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the prokaryotic code specifies the technical the reason why the number of new spe‑ community effort will be needed to develop means to recognize new species, and all new cies described per year is about twice as the broadly accepted protocols required for species are recorded in the International many for fungi as it is for prokaryotes5,32. a mass movement towards sequence-based Journal of Systematic and Evolutionary The ICN will increase the centralization of taxonomy. Microbiology, whereas the ICN specifies no taxonomic authority for fungi, although the At least one difficult issue appears to particular technique for the recognition of basic criteria for fungal species recognition have been resolved: the internal transcribed fungal species, which can be published in will remain unrestricted. It is important spacer (ITS) region of the nuclear rRNA diverse venues. Under the ICN, acceptance that as the new rules of the ICN are imple‑ gene has been proposed as the fungal bar‑ of fungal species is left to the mycology mented, the GC acts with restraint and code locus22 and is being used for sequence- community; new names are picked up by does nothing to impede progress in fungal based species delimitation in environmental other mycologists and appear in the litera‑ species description. surveys for many groups of fungi. However, ture, or they are simply ignored. The highly Mycologists can also learn from the expe‑ other key issues remain problematic. Longer regulated system for prokaryotes promotes rience of bacterial and archaeal researchers reads that provide sequences for the ITS and uniformity in the species recognition cri with regard to the classification of environ‑ the phylogenetically tractable large subu‑ teria and preserves the stability of names, mental sequences. The requirement for a nit (LSU) rRNA cannot be obtained until but it can also limit the rate of species living type culture for describing bacterial there are improvements in next-generation description. By contrast, the laissez-faire or archaeal species26 is comparable to the sequencing. The gold standard for species system for fungi results in non-uniform spe‑ requirement for a physical type specimen for delimitation in fungi is the genealogical cies recognition criteria (for example, many naming fungal species. To enable the naming concordance method, which uses multiple new species descriptions lack supporting of bacteria that lack cultures but are known genetic loci to assess the limits of recombina‑ molecular data5), extensive synonymy, an by “more than a mere sequence” (REF. 33), tion36. Such approaches are not applicable ongoing challenge in compiling new names Murray and Schleifer34 suggested that the in environmental data sets, which usually (although the new requirement for name prefix Candidatus be used, indicating that use single loci amplified from pooled DNAs. registration will solve this problem) and the name is provisional. This recommen‑ Moreover, in order to carry out species frequent changes in species-level classifica‑ dation has been appended to the bacterial delimitation in environmental samples, the tions. At the same time, the fungal system code25, but fewer than 400 bacteria and consequences of intragenomic heterogeneity promotes rapid taxonomic updates to reflect archaea have been described as Candidatus in multicopy rRNA genes, as well as error new discoveries and advances in phylogenetic species35. If mycologists wish to adopt a new owing to gene tree versus species tree con‑ reconstruction. category similar to Candidatus to accommo‑ flict, will have to be determined empirically Changes in fungal species classifica‑ date the huge numbers of species discovered in relation to multigene data sets. The names tions often occur when evidence for through environmental sequences, as has of species known only from environmental genetic diversity is discovered within been suggested5, they will need to find ways sequences might require a new taxonomic morphological taxa. For example, it to facilitate high-throughput taxonomy, category comparable to the Candidatus might have surprised readers to learn that almost certainly involving automated status for bacteria and archaea5, or an iden‑ Alexander Fleming’s Penicillium species, work flows. tifying suffix (for example, ENAS (environ‑ Penicillium chrysogenum, is now known as mental nucleic acid sequence) or eMOTU P. rubens27, but the change was necessitated The future of fungal taxonomy (environmental molecular operational when phylogenetic and population genet‑ Twenty-five years after the first descrip‑ taxonomic unit))6. The reality of sequenc‑ ics data showed that the P. chrysogenum of tion of PCR, species-level fungal taxonomy ing errors might prevent naming until the old harboured several genetically isolated is finally catching up with the molecular same sequence is found a second time and species28. Older mycologists may grumble revolution. Change has come slowly and by a different research group. Finally, myco‑ about having to learn a new name, but the has been prompted by the actions of radi‑ logical databases such as MycoBank must new classification reflects the current state cals, who flouted and subverted the code prepare for a massive influx of new species, of knowledge, and new students will not by naming taxa based on anamorphs7,8 or especially if automated work flows are devel‑ be bothered by the change. By contrast, the environmental sequences20. Such individual oped to describe fungi from environmental archaeon Sulfolobus islandicus was shown acts of rebellion illuminate the way forward, nucleic acid sequences. Given the rate of to comprise several genetically isolated but ultimately fungal taxonomy is a group species discovery, mycologists do not have species according to population genetics enterprise that can succeed only with the another 25 years to ponder the problem. techniques, which showed genetic isolation support and participation of the broad David S. Hibbett is at The Biology Department, 29 by distance and also evidence of ecologi‑ community of mycologists. Proponents Clark University, Worcester, Massachusetts 01610, USA. 30 cal speciation , but these species were left of unitary taxonomy worked effectively John W. Taylor is at The Department of Plant and unnamed, in part because the now passé as a community to repeal dual nomencla‑ Microbial Biology, University of California, technique of DNA–DNA hybridization ture and are now organizing themselves Berkeley, California 94720, USA. would have been required for formal spe‑ to resolve the correct names of scores of Correspondence to D.S.H. cies descriptions24. Admittedly, there are pleomorphic fungal species. Supporters of e-mail: [email protected] huge challenges in determining species sequence-based taxonomy have not been doi:10.1038/nrmicro2942 limits in bacteria and archaea, particularly so unified, however. The publication of Published online 3 January 2013 in the face of extensive horizontal gene P. cryptodigmaticus demonstrates that it is 1. Kirk, P. et al. (eds) Dictionary of the Fungi 10th edn transfer31. Nonetheless, the differences ‘legally’ possible, under the code, to describe (CABI, 2008). 2. Bass, D. & Richards, T. A. Three reasons to re‑evaluate in nomenclatural practices for bacteria new species based on sequences (as long as a fungal diversity “on Earth and in the ocean”. Fungal and archaea versus fungi may be part of nominal type is deposited somewhere), but Biol. Rev. 25, 159–164 (2011).

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Stud. prokaryote strains for taxonomic purposes. Int. The authors thank their colleagues and members of their labo‑ Mycol. 68, 79–113 (2011). J. Syst. Evol. Microbiol. 60, 249–266 (2010). ratories for discussions on the principles of fungal taxonomy, 10. Norvell, L. L. Fungal nomenclature. 1. Melbourne 25. De Vos, P., Trüper, H. G. & Tindall, B. J. Judicial and the International Mycological Association and the approves a new Code. Mycotaxon 116, 481–490 Commission of the International Committee on Centraalbureau voor Schimmelcultures for hosting meetings (2011). Systematics of Prokaryotes; Xth International (IUMS) addressing the revolution in fungal nomenclature. Research in 11. Hawksworth, D. A new dawn for the naming of fungi: Congress of Bacteriology and Applied Microbiology; the authors’ laboratories is supported by the Open Tree of Life impacts of decisions made in Melbourne in July 2011 Minutes of the meetings, 28, 29 and 31 July and Project (http://opentreeoflife.org/), the US National Science on the future publication and regulation of fungal 1 August 2002, Paris, France. Int. J. Syst. Evol. Foundation (grant DEB-1208719 to D.S.H.), the US National names. IMA Fungus 2, 155–162 (2011). Microbiol. 55, 525–532 (2005). Institutes of Health (grant U54-AI65359 to J.T.W.) and the 12. Weresub, L. K. & Pirozynski, K. A. in The Whole 26. Lapage, S. et al. (eds) International Code Of Energy Biosciences Institute (grant EBI 001J09 to J.W.T.). Fungus: The Sexual-Asexual Synthesis (ed. Kendrick, B.) Nomenclature Of Bacteria. (American Society for 17–30 (National Museum of Natural Sciences and Microbiology, 1992). Competing interests statement National Museums of Canada, 1979). 27. Houbraken, J., Frisvad, J. C. & Samson, R. A. Fleming’s The authors declare no competing financial interests. 13. Tulasne, L.‑R. & Tulasne, C. Selecta Fungorum penicillin producing strain is not Penicillium chrysogenum Carpologia. Vol. 1 (Imperial Typographer, 1861). but P. rubens. IMA Fungus 2, 87–95 (2011). 14. Kendrick, B. (ed.) The Whole Fungus: The Sexual- 28. Henk, D. A. et al. Speciation despite globally FURTHER INFORMATION Asexual Synthesis. (National Museum of Natural overlapping distributions in Penicillium chrysogenum: David S. Hibbett’s homepage: http://www.clarku.edu/ Sciences and National Museums of Canada, 1979). the population genetics of Alexander Fleming’s lucky faculty/dhibbett/ 15. Houbraken, J. & Samson, R. A. Phylogeny of fungus. Mol. Ecol. 20, 4288–4301 (2011). John W. Taylor’s homepage: http://taylorlab.berkeley.edu/ Penicillium and the segregation of Trichocomaceae 29. Whitaker, R. J., Grogan, D. W. & Taylor, J. W. GenBank: http://www.ncbi.nlm.nih.gov/genbank/ into three families. Stud. Mycol. 70, 1–51 (2011). Geographic barriers isolate endemic populations of IndexFungorum: http://www.indexfungorum.org/ 16. Hawksworth, D. L. & Taylor, J. W. One fungus = which hyperthermophilic archaea. Science 301, 976–978 MycoBank: http://www.mycobank.org/ name? IMA Fungus 3, 10–14 (2012). (2003). RefSeq: http://www.ncbi.nlm.nih.gov/RefSeq/ 17. Rosling, A. et al. Archaeorhizomycetes: unearthing an 30. Cadillo-Quiroz, H. et al. Patterns of gene flow define UNITE: http://unite.ut.ee/ ancient class of ubiquitous soil fungi. Science 333, species of thermophilic Archaea. PLoS Biol. 10, ALL LINKS ARE ACTIVE IN THE ONLINE PDF 876–879 (2011). e1001265 (2012).

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