Fungal Systematics: Is a New Age of Enlightenment at Hand?

Home , Aspergillus glaucus, Cosmospora, Eurotium herbariorum, Penicillium camemberti, Species description, Volutella (fungus)

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),

NATURE REVIEWS | MICROBIOLOGY VOLUME 11 | FEBRUARY 2013 | 129

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

130 | FEBRUARY 2013 | VOLUME 11 www.nature.com/reviews/micro

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 specimen. To prove this point, Kirk et al.20 based on environmental sequences. They two groups are often divergent. For exam‑ recently described a new species of rumen should not be; current estimates of the ple, the expanded power of the GC to rule chytrid, Piromyces cryptodigmaticus, based actual diversity in the kingdom Fungi range on the legitimacy of choices among exist‑ on sequence data, and typified it with a from as few as 500,000 species to millions ing names under the forthcoming ICN sample from the fermenter from which the of species2, suggesting that most unmatched might worry some mycologists, who could DNA was extracted. The new taxon name environmental sequences probably do rep‑ fear a loss of taxonomic freedom, but the was validly published, even though the resent new species5. Even if some environ new system for fungi might seem familiar fungus was never directly observed. In the mental species prove to be redundant, to 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 nomenclatu‑ type materials altogether. In the meantime, lem is conceptually straightforward — that ral codes for prokaryotes26 and fungi3 is

NATURE REVIEWS | MICROBIOLOGY VOLUME 11 | FEBRUARY 2013 | 131

that the prokaryotic code specifies the and archaea versus fungi may be part of the code, to describe new species based technical means to recognize new spe‑ the reason why the number of new spe‑ on sequences (as long as a nominal type cies, and all new species are recorded in cies described per year is about twice as is deposited somewhere), but commu‑ the International Journal of Systematic and many for fungi as it is for prokaryotes5,32. nity effort will be needed to develop the Evolutionary Microbiology, whereas the The ICN will increase the centralization of broadly accepted protocols required for a ICN specifies no particular technique for taxonomic authority for fungi, although the mass movement towards sequence-based the recognition of fungal species, which basic criteria for fungal species recognition taxonomy. can be published in diverse venues. Under will remain unrestricted. It is important At least one difficult issue appears to the ICN, acceptance of fungal species is left that as the new rules of the ICN are imple‑ have been resolved: the internal transcribed to the mycology community; new names mented, the GC acts with restraint and spacer (ITS) region of the nuclear rRNA are picked up by other mycologists and does nothing to impede progress in fungal gene has been proposed as the fungal bar‑ appear in the literature, or they are simply species description. code locus22 and is being used for sequence- ignored. The highly regulated system for Mycologists can also learn from the based species delimitation in environmental prokaryotes promotes uniformity in the experience of bacterial and archaeal surveys for many groups of fungi. However, species recognition criteria and preserves researchers with regard to the classifica‑ other key issues remain problematic. Longer the stability of names, but it can also limit tion of environmental sequences. The reads that provide sequences for the ITS the rate of species description. By contrast, requirement for a living type culture for and the phylogenetically tractable large the laissez-faire system for fungi results in describing bacterial or archaeal species26 subunit (LSU) rRNA cannot be obtained non-uniform species recognition criteria is comparable to the requirement for a until there are improvements in next- (for example, many new species descrip‑ physical type specimen for naming fungal generation sequencing. The gold standard tions lack supporting molecular data5), species. To enable the naming of bacteria for species delimitation in fungi is the extensive synonymy, an ongoing challenge that lack cultures but are known by “more genealogical concordance method, which in compiling new names (although the than a mere sequence” (REF. 33), Murray uses multiple genetic loci to assess the limits new requirement for name registration and Schleifer34 suggested that the prefix of recombination36. Such approaches are will solve this problem) and frequent Candidatus be used, indicating that the not applicable in environmental data sets, changes in species-level classifications. At name is provisional. This recommendation which usually use single loci amplified from the same time, the fungal system promotes has been appended to the bacterial code25, pooled DNAs. Moreover, in order to carry rapid taxonomic updates to reflect new but fewer than 400 bacteria and archaea out species delimitation in environmental discoveries and advances in phylogenetic have been described as Candidatus spe‑ samples, the consequences of intragenomic reconstruction. cies35. If mycologists wish to adopt a new heterogeneity in multicopy rRNA genes, Changes in fungal species classifica‑ category similar to Candidatus to accom‑ as well as error owing to gene tree versus tions often occur when evidence for modate the huge numbers of species dis‑ species tree conflict, will have to be deter‑ genetic diversity is discovered within covered through environmental sequences, mined empirically in relation to multigene morphological taxa. For example, it as has been suggested5, they will need to data sets. The names of species known might have surprised readers to learn that find ways to facilitate high-throughput tax‑ only from environmental sequences might Alexander Fleming’s Penicillium species, onomy, almost certainly involving require a new taxonomic category compa‑ Penicillium chrysogenum, is now known as automated work flows. rable to the Candidatus status for bacteria P. rubens27, but the change was necessitated and archaea5, or an identifying suffix (for when phylogenetic and population genet‑ The future of fungal taxonomy example, ENAS (environmental nucleic ics data showed that the P. chrysogenum of Twenty-five years after the first descrip‑ acid sequence) or eMOTU (environmental old harboured several genetically isolated tion of PCR, species-level fungal taxonomy molecular operational taxonomic unit))6. species28. Older mycologists may grumble is finally catching up with the molecular The reality of sequencing errors might about having to learn a new name, but the revolution. Change has come slowly and prevent naming until the same sequence new classification reflects the current state has been prompted by the actions of radi‑ is found a second time and by a different of knowledge, and new students will not cals, who flouted and subverted the code research group. Finally, mycological data‑ be bothered by the change. By contrast, the by naming taxa based on anamorphs7,8 bases such as MycoBank must prepare for archaeon Sulfolobus islandicus was shown or environmental sequences20. Such indi‑ a massive influx of new species, especially to comprise several genetically isolated vidual acts of rebellion illuminate the way if automated work flows are developed to species according to population genetics forward, but ultimately fungal taxonomy describe fungi from environmental nucleic techniques, which showed genetic isolation is a group enterprise that can succeed acid sequences. Given the rate of species by distance29 and also evidence of ecologi‑ only with the support and participation discovery, mycologists do not have another cal speciation30, but these species were left of the broad community of mycologists. 25 years to ponder the problem. unnamed, in part because the now passé Proponents of unitary taxonomy worked David S. Hibbett is at The Biology Department, technique of DNA–DNA hybridization effectively as a community to repeal dual Clark University, Worcester, Massachusetts 01610, USA. would have been required for formal spe‑ nomenclature and are now organizing John W. Taylor is at The Department of Plant and 24 cies descriptions . Admittedly, there are themselves to resolve the correct names Microbial Biology, University of California, huge challenges in determining species of scores of pleomorphic fungal species. Berkeley, California 94720, USA. limits in bacteria and archaea, particularly Supporters of sequence-based taxonomy Correspondence to D.S.H. in the face of extensive horizontal gene have not been so unified, however. The e-mail: [email protected] 31 transfer . Nonetheless, the differences publication of P. cryptodigmaticus dem‑ doi:10.1038/nrmicro2963 in nomenclatural practices for bacteria onstrates that it is ‘legally’ possible, under Published online 3 January 2013

132 | FEBRUARY 2013 | VOLUME 11 www.nature.com/reviews/micro

1. Kirk, P. et al. (eds) Dictionary of the Fungi 10th edn 29. Whitaker, R. J., Grogan, D. W. & Taylor, J. W. Acknowledgments (CABI, 2008). Geographic barriers isolate endemic populations of The authors thank their colleagues and members of their labo‑ 2. Bass, D. & Richards, T. A. Three reasons to re‑evaluate hyperthermophilic archaea. Science 301, 976–978 ratories for discussions on the principles of fungal taxonomy, fungal diversity “on Earth and in the ocean”. Fungal (2003). and the International Mycological Association and the Biol. Rev. 25, 159–164 (2011). 30. Cadillo-Quiroz, H. et al. Patterns of gene flow define Centraalbureau voor Schimmelcultures for hosting meetings 3. McNeill, J. et al. (eds) International Code of Botanical species of thermophilic Archaea. PLoS Biol. 10, addressing the revolution in fungal nomenclature. Research in Nomenclature (Vienna Code) (Gantner, 2006). e1001265 (2012). the authors’ laboratories is supported by the Open Tree of Life 4. Hawksworth, D. L. et al. The Amsterdam declaration on 31. Gevers, D. et al. Re‑evaluating prokaryotic species. Project (http://opentreeoflife.org/), the US National Science fungal nomenclature. IMA Fungus 2, 105–112 (2011). Nature Rev. Microbiol. 3, 733–739 (2005). Foundation (grant DEB-1208719 to D.S.H.), the US National 5. Hibbett, D. S. et al. Progress in molecular and 32. Rainey, F. A. & Oren, A. in Methods in Microbiology. Institutes of Health (grant U54-AI65359 to J.T.W.) and the morphological taxon discovery in Fungi and options Vol. 38 (eds Rainey, F. & Oren, A.) 1–5 (Academic, Energy Biosciences Institute (grant EBI 001J09 to J.W.T.). for formal classification of environmental sequences. 2011). Fungal Biol. Rev. 25, 38–47 (2011). 33. Murray, R. G. E. & Stackebrandt, E. Taxonomic note: Competing interests statement 6. Taylor, J. W. One fungus = one name: DNA and fungal implementation of the provisional status Candidatus The authors declare no competing financial interests. nomenclature twenty years after PCR. IMA Fungus 2, for incompletely described procaryotes. Int. J. Syst. 113–120 (2011). Bacteriol. 45, 186–187 (1995). 7. Houbraken, J., Frisvad, J. C. & Samson, R. A. 34. Murray, R. G. E. & Schleifer, K. H. Taxonomic notes: a FURTHER INFORMATION Taxonomy of Penicillium citrinum and related species. proposal for recording the properties of putative taxa David S. Hibbett’s homepage: http://www.clarku.edu/ Fungal Divers. 44, 117–133 (2010). of procaryotes. Int. J. Syst. Bacteriol. 44, 174–176 faculty/dhibbett/ 8. Crous, P. W. et al. Phylogenetic lineages in the (1994). John W. Taylor’s homepage: http://taylorlab.berkeley.edu/ Botryosphaeriaceae. Stud. Mycol. 55, 235–253 35. Euzéby, J. P. Some names included in the category GenBank: http://www.ncbi.nlm.nih.gov/genbank/ (2006). Candidatus. List of Prokaryotic Names with Standing IndexFungorum: http://www.indexfungorum.org/ 9. Gräfenhan, T., Schroers, H.‑J., Nirenberg, H. I. & in Nomenclature [online], http://www.bacterio.cict.fr/ MycoBank: http://www.mycobank.org/ Seifert, K. A. An overview of the taxonomy, phylogeny, candidatus.html (2012). RefSeq: http://www.ncbi.nlm.nih.gov/RefSeq/ and typification of nectriaceous fungi in Cosmospora, 36. Taylor, J. et al. Phylogenetic species recognition and UNITE: http://unite.ut.ee/ Acremonium, Fusarium, Stilbella, and Volutella. Stud. species concepts in fungi. Fungal Genet. Biol. 31, ALL LINKS ARE ACTIVE IN THE ONLINE PDF Mycol. 68, 79–113 (2011). 21–32 (2000). 10. Norvell, L. L. Fungal nomenclature. 1. Melbourne approves a new Code. Mycotaxon 116, 481–490 (2011). 11. Hawksworth, D. A new dawn for the naming of fungi: impacts of decisions made in Melbourne in July 2011 on the future publication and regulation of fungal ESSAY names. IMA Fungus 2, 155–162 (2011). 12. Weresub, L. K. & Pirozynski, K. A. in The Whole Fungus: The Sexual-Asexual Synthesis (ed. Kendrick, B.) 17–30 (National Museum of Natural Sciences and The changing face of pathogen National Museums of Canada, 1979). 13. Tulasne, L.‑R. & Tulasne, C. Selecta Fungorum Carpologia. Vol. 1 (Imperial Typographer, 1861). 14. Kendrick, B. (ed.) The Whole Fungus: The Sexual- discovery and surveillance Asexual Synthesis. (National Museum of Natural Sciences and National Museums of Canada, 1979). 15. Houbraken, J. & Samson, R. A. Phylogeny of W. Ian Lipkin Penicillium and the segregation of Trichocomaceae into three families. Stud. Mycol. 70, 1–51 (2011). 16. Hawksworth, D. L. & Taylor, J. W. One fungus = which Abstract | The pace of pathogen discovery is rapidly accelerating. This reflects name? IMA Fungus 3, 10–14 (2012). not only factors that enable the appearance and globalization of new microbial 17. Rosling, A. et al. Archaeorhizomycetes: unearthing an ancient class of ubiquitous soil fungi. Science 333, infections, but also improvements in methods for ascertaining the cause of 876–879 (2011). 18. James, T. Y. & Berbee, M. L. No jacket required – new a new disease. Innovative molecular diagnostic platforms, investments in fungal lineage defies dress code: recently described zoosporic fungi lack a cell wall during trophic phase. pathogen surveillance (in wildlife, domestic animals and humans) and the advent Bioessays 34, 94–102 (2012). 19. Jones, M. D. et al. Discovery of novel intermediate of social media tools that mine the World Wide Web for clues indicating the forms redefines the fungal tree of life. Nature 474, occurrence of infectious-disease outbreaks are all proving to be invaluable for 200–203 (2011). 20. Kirk, P. M. Index Fungorum no. 2. Index Fungorum the early recognition of threats to public health. In addition, models of microbial [online] http://www.indexfungorum.org/Publications/ Index%20Fungorum%20no.2.pdf (2012). pathogenesis are becoming more complex, providing insights into the mechanisms 21. Bidartondo, M. I. Preserving accuracy in GenBank. Science 319, 1616 (2008). by which microorganisms can contribute to chronic illnesses like cancer, peptic 22. Schoch, C. L. et al. Nuclear ribosomal internal ulcer disease and mental illness. Here, I review the factors that contribute to transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc. Natl Acad. Sci. USA infectious-disease emergence, as well as strategies for addressing the challenges 109, 6241–6246 (2012). 23. Abarenkov, K. et al. The UNITE database for molecular of pathogen surveillance and discovery. identification of fungi – recent updates and future perspectives. New Phytol. 186, 281–285 (2010). 24. Tindall, B. J., Rossello-Mora, R., Busse, H. J., Ludwig, W. & Kampfer, P. Notes on the characterization of When the H1N1 influenza virus struck in respiratory syndrome (SARS) coronavirus prokaryote strains for taxonomic purposes. Int. 1918, little was known about how infectious pandemic of 2002–2003, the first pandemic J. Syst. Evol. Microbiol. 60, 249–266 (2010). 25. De Vos, P., Trüper, H. G. & Tindall, B. J. Judicial diseases emerge or their routes of transmis‑ of the twenty-first century, had a case fatality Commission of the International Committee on sion. Indeed, even the identification of the rate of near 10%, but infected far fewer people Systematics of Prokaryotes; Xth International (IUMS) Congress of Bacteriology and Applied Microbiology; causative agent as a virus (that is, capable (8,096) than the H1N1 influenza virus of Minutes of the meetings, 28, 29 and 31 July and of passing through a filter) rather than the the 1918 pandemic4. Transmissibility, as esti‑ 1 August 2002, Paris, France. Int. J. Syst. Evol. Microbiol. 55, 525–532 (2005). bacterium Haemophilus influenzae (cham‑ mated by R0 (the basic reproduction number; 26. Lapage, S. et al. (eds) International Code Of pioned by some leading microbiologists that is, the number of cases generated Nomenclature Of Bacteria. (American Society for Microbiology, 1992). at the time) was in dispute until late in the through contact with one infected individ‑ 27. Houbraken, J., Frisvad, J. C. & Samson, R. A. Fleming’s course of the pandemic1. The 1918 virus had ual) was similar for the influenza pandemic penicillin producing strain is not Penicillium chrysogenum 5 but P. rubens. IMA Fungus 2, 87–95 (2011). an estimated case fatality rate of 10–20%, of 1918 (R0 = 2–3) and the SARS pandemic of 28. Henk, D. A. et al. Speciation despite globally 6,7 spread to six continents, infected ~500 mil‑ 2003 (R0 = 2–5) . However, the global overlapping distributions in Penicillium chrysogenum: the population genetics of Alexander Fleming’s lucky lion people and killed approximately 3% of response to SARS was facilitated by advances fungus. Mol. Ecol. 20, 4288–4301 (2011). the world’s population2,3. The severe acute in epidemiology and microbiology that

NATURE REVIEWS | MICROBIOLOGY VOLUME 11 | FEBRUARY 2013 | 133