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and Penicillium camemberti and Penicilliumroqueforti (used to make Camembert andBrie, and Roquefort cheeses, respectively).However, Penicillium spp., as traditionallydelimited, are paraphyletic as well as pleo-morphic, so these well-known speciescannot all remain in this historic genus15.
Under the revised code, any of the exist-ing valid names for a species can be selectedas its correct name, with preference given tothe oldest name. However, this libertarian
view is tempered by two additional revi-sions, both involving review by the GeneralCommittee (GC) of the ICN, which isempowered to vote on proposals to conserveor reject names of fungal taxa, as well as tomodify the ICN itself 3. First, in situations inwhich both the anamorph and teleomorphnames for the same taxon are widely used— for example, Fusarium (anamorph) andGibberella (teleomorph) at the genus level— the teleomorph name can be chosen with-out approval of the GC, but selection of theanamorph name, even if it is the older name,requires approval. Apparently, it is hard for
systematists to abandon the primacy of sex-ual characteristics. Second, the GC has theauthority to approve lists of names, whichpresumably will be generated by committeesof mycologists with expertise in particulartaxonomic groups. However, mycologistshave retained the right to appeal any deci-sion about names through the establishedprocess of conservation of names.
No one has had a chance to choose aname for a pleomorphic fungal speciesunder the new code, which only cameinto effect on 1 January 2013, but the
nomenclatural changes mentioned aboveillustrate what might lie ahead. Anotherexample is the work of Gräfenhan et al.9 on the taxonomy of the anamorphic genusFusarium, one of the largest genera of fungi,containing nearly 1,500 species, subspecies,
varieties and formae speciales. Fusarium spp. include important plant and animalpathogens and mycotoxin producers andhave been linked to as many as seven tele-omorph genera. On the basis of sequenceanalyses for RNA polymerase II and ATPcitrate lyase genes, Gräfenhan et al.9 identi-fied 15 clades with Fusarium-like asexualforms and gave six of them names based onanamorphs, although five of these six haveknown teleomorphic forms. The reclassifica-tion of Fusarium by Gräfenhan et al. is basedon robust phylogenies and would be nomen-claturally valid under the forthcoming ICN.Nevertheless, name changes in the genusFusarium sensu lato might confuse andinconvenience user communities and regula-tory bodies in agriculture and medicine, andit remains to be seen how these constituencies
will react to the new taxonomy.The complex nomenclatural history of
many groups of pleomorphic fungi, coupledwith phylogenetic uncertainty and the some-times passionate opinions of stakeholders,presents a very challenging taxonomic prob-lem. The code provides guidance, but manydecisions about names cannot be reducedto ‘legal’ algorithms. As a follow-up to the‘One fungus, one name’ movement that ledto the repeal of dual nomenclature, a ‘Onefungus, which name?’ conference was heldin Amsterdam in April 2012 (REF. 16). This
time, the goal was to begin working throughthe myriad options for the classificationof pleomorphic fungi in light of the newrules. Similar meetings and workshops onthe taxonomy of the genus Fusarium, theorder Hypocreales and other groups wereheld in association with meetings of theMycological Society of Japan (May 2012),the Mycological Society of America (July2012) and the Mycological Society of China(August, 2012).
Classification of environmental sequences
Now that dual nomenclature has beenabolished, the next major challenge forfungal taxonomy is to develop strategiesfor classifying environmental sequences(FIG. 2). Nobody knows how many unnamedspecies have already been detected throughmetagenomic studies (and this fact aloneindicates the need for a centralized database
of species that are based on environmentalsequences), but as early as 2007 the numberof clusters of closely related rRNA genesbeing discovered with Sanger chemistryapproached the number of species beingdescribed from specimens5, and the rateof molecular species discovery has surelyincreased with the application of next-generation sequencing in metagenomics.
Environmental studies have revealednot only individual species, but alsomajor clades of fungi, such as the classArchaeorhizomycetes17, containing adiverse group of soil-inhabiting fungi fromthe phylum Ascomycota. Sequences ofArchaeorhizomycetes members have beenreported in more than 50 independent stud-ies, and they can be grouped into more than100 species-level entities17. Nevertheless,only one species, Archaeorhizomyces finlayi, has been formally described, basedon a culture that was obtained from coni-fer roots. A similar example is providedby the phylum Rozellomycota18 (alsoknown as Cryptomycota19), a large cladeof aquatic and soil-inhabiting fungi that isknown almost entirely from environmen-
tal sequences. The phylum Rozellomycotahas been shown to contain the previouslydescribed chytrid genus Rozella19, but mostof the diversity of this phylum is in groupsthat are known only from environmentalsequences and have not been named. Theseexamples, and many others from fungalmolecular ecology, illustrate the profounddisconnect that now exists between formaltaxonomy and species discovery throughenvironmental sequences. Barriers to thenaming of such species include a perceivedconflict with the code, and errors and
Figure 1 | Two names, one fungus. Eurotium herbariorum is a pleomorphic fungus that has a sexual
phase, reproducing by ascospores (the teleomorphic form; left), as well as a conidium-producing
asexual phase (the anamorphic form; right) that has been named Aspergillus glaucus. Images courtesy
of Paul F. Cannon, Royal Botanical Gardens, Kew, London, UK, and the Centre for Agricultural
Bioscience International (CABI).
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incomplete taxon sampling in referencesequence databases.
The perceived incompatibility of thecode with sequence-based taxonomy is aconsequence of the requirement for typespecimens. However, the code places norestrictions on the form of type specimens,which need not be complete or representa-tive; all that is required of a type specimenis that it should be a physical specimen.In principle, an aliquot of DNA extractedfrom an environmental sample, or a por-tion of the substrate from which the DNA
was isolated, can serve as a legitimate typespecimen. To prove this point, Kirk et al.20 recently described a new species of rumenchytrid, Piromyces cryptodigmaticus, basedon sequence data, and typified it with asample from the fermenter from which theDNA was extracted. The new taxon namewas validly published, even though thefungus was never directly observed. In thefuture, if purely sequence-based taxonomyis incorporated into the code, it may be pos-sible to forego the deposition of physicaltype materials altogether. In the meantime,
the publication of P. cryptodigmaticus pro- vides a model for environmental molecularbiologists who would like to formalizetheir discoveries through code-complianttaxonomic names.
Errors and incomplete taxonomicsampling in sequence databases, such asGenBank , present a psychological barrierto naming environmental sequences; ifan environmental sequence has no matchin GenBank, it could still represent adescribed but unsequenced species. Facedwith such uncertainty, fungal taxonomists
might be reluctant to describe new speciesbased on environmental sequences. Theyshould not be; current estimates of theactual diversity in the kingdom Fungi rangefrom as few as 500,000 species to millionsof species2, suggesting that most unmatchedenvironmental sequences probably do rep-resent new species5. Even if some environ-mental species prove to be redundant,taxonomists are accustomed to resolvingsynonymy based on the principle of priority . Finally, the solution to the GenBank prob-lem is conceptually straightforward — that
is, generate well-documented referencesequences21 — and is already being pur-sued through the fungal bar-coding initia-tive22 and the creation of custom-curateddatabases of well-documented referencesequences, such as the RefSeq collectionwithin GenBank, and the UNITE databasefor mycorrhizal fungi23.
Lessons from prokaryotic taxonomy
Many of the taxonomic challenges facedby mycologists parallel those faced byresearchers studying prokaryotes, but the
nomenclatural practices adopted by thetwo groups are often divergent. For exam-ple, the expanded power of the GC to ruleon the legitimacy of choices among exist-ing names under the forthcoming ICNmight worry some mycologists, who couldfear a loss of taxonomic freedom, but thenew system for fungi might seem familiarto prokaryote taxonomists, who have longused a Judicial Commission to accept orreject newly proposed names24,25. Anotherkey difference between the nomenclatu-ral codes for prokaryotes26 and fungi3 is
Uncultured fungus clone unisequences#37-3808_2763 ITS2, PS
Uncultured Agaricomycotina clone 6_g19 18S rRNA gene
Uncultured fungus clone MOTU_4043_GVUGB5B04JK5N2 18S rRNA gene, PS, ITS2
Uncultured fungus clone MOTU_1778_GVUGB5B04IF01X 18S rRNA gene, PSUncultured fungus clone LT5P_EUKA_P5H04 18S rRNA gene, 18S–25/28S rRNA gene
Uncultured fungus clone F66N0BQ02H1NX5 18S rRNA geneUncultured fungus clone MOTU_43
Uncultured fungus clone unisequences#69-3466_2373 ITS2, PSUncultured fungus clone MOTU_4349_GOKCVYYY06GR7WA 18S rRNA gene, PS, ITS2
Uncultured fungus clone unisequences #65-3574_00447, ITS2, PS
Trichosporonales sp. LM559 18S rRNA geneUncultured Tremellales clone LTSP_EUKA
Uncultured fungus clone unisequenceFungi 3 leaves
Uncultured fungus clone unisequence#65-3936_0554 ITS2, PSUncultured basidiomycete ITS
Uncultured fungus clone MOTU_601_GOK
Uncultured Tremellales clone LTSP_EUKA_P4L03 18S rRNA gene, PS, ITSUncultured fungus clone MOTU_141_GOKCVYYY06G5FYL 18S rRNA gene, PS, ITS
Fibulobasidium murrhardtense strain CB59109 18S rRNA gene
Uncultured fungus clone MOTU_2930_GOKCVYYY06G7201 18S rRNA gene, PS, ITSUncultured fungus clone MOTU_2993_GOKCVYYY06HH12J 18S rRNA gene, PS, ITS
Uncultured fungus clone MOTU_1888_GVUGV5B04JJTLJ 18S rRNA gene
Uncultured fungus clone MOTU_3006_GVUGV5B04JIHT 18S rRNA geneUncultured fungus clone MOTU_2635_GVUGVSB04J56R4 18S rRNA gene, PS, ITS
gi|22497358|gb|FJ761130.1| uncultured fungus clone singleton_70-3063_2201 18S rRNA gene
Uncultured fungus clone singleton_70-3063_2201 18S rRNA gene, PS, ITSUncultured fungus clone OTU_403_GW5CJXV07IOX5A 18S rRNA gene
Uncultured fungus clone U_QM_090130_240_B_plate1a12.b1 18S rRNA gene, PS, ITS1
Uncultured fungus clone OTU_1445_1GW5CJXV07HXDTO 18S rRNA geneUncultured fungus clone U_QM_090130_127_1A_plate1g12.b1 18S rRNA gene, PS, ITS1
Uncultured fungus clone MOTU_3163_GYUGV5B0412KQP 18S rRNA gene, PS, ITS1Uncultured fungus clone MOTU_533_GOKCVYYY06GU3JA18S rRNA gene, PS, ITS1
Uncultured Tremellales clone 5_D20 18S rRNA, ITS1, 5.8S rRNA gene, ITS1
Uncultured Rhodotorula IT51, 5.8S rRNA, ITS2 and partial 28S rRNA, clone MNIB2FAST_K1
Uncultured fungus clone MOTU_3797_GOKCVYYY06HBZ1X 18S rRNA gene, PS, ITS2
Uncultured fungus clone MOTU_2412
Figure 2 | Unnamed diversity. A demonstration of the problem posed
by unnamed fungi that are known only from environmental DNA
sequences. When a new environmental sequence (the bottom-most opera-
tional taxonomic unit, gi|22497358; blue box) was used in a BLAST search
of the GenBank database and the result displayed using the BLAST
distance tree tool, only two of the 35 most closely related sequences were
from cultured organisms (green boxes), and only one was named
(Fibulobasidium murrhardtense). Without names, the information content
of this tree leaves much to be desired. ITS, internal transcribed spacer;
PS, partial sequence.
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that the prokaryotic code specifies thetechnical means to recognize new spe-cies, and all new species are recorded inthe International Journal of Systematic andEvolutionary Microbiology , whereas theICN specifies no particular technique forthe recognition of fungal species, whichcan be published in diverse venues. Underthe ICN, acceptance of fungal species is leftto the mycology community; new namesare picked up by other mycologists andappear in the literature, or they are simplyignored. The highly regulated system forprokaryotes promotes uniformity in thespecies recognition criteria and preservesthe stability of names, but it can also limitthe rate of species description. By contrast,the laissez-faire system for fungi results innon-uniform species recognition criteria(for example, many new species descrip-tions lack supporting molecular data5),
extensive synonymy, an ongoing challengein compiling new names (although thenew requirement for name registrationwill solve this problem) and frequentchanges in species-level classifications. Atthe same time, the fungal system promotesrapid taxonomic updates to reflect newdiscoveries and advances in phylogeneticreconstruction.
Changes in fungal species classifica-tions often occur when evidence forgenetic diversity is discovered withinmorphological taxa. For example, itmight have surprised readers to learn thatAlexander Fleming’s Penicillium species,Penicillium chrysogenum, is now known asP. rubens27, but the change was necessitatedwhen phylogenetic and population genet-ics data showed that the P. chrysogenum ofold harboured several genetically isolatedspecies28. Older mycologists may grumbleabout having to learn a new name, but thenew classification reflects the current stateof knowledge, and new students will notbe bothered by the change. By contrast, thearchaeon Sulfolobus islandicus was shownto comprise several genetically isolated
species according to population geneticstechniques, which showed genetic isolationby distance29 and also evidence of ecologi-cal speciation30, but these species were leftunnamed, in part because the now passétechnique of DNA–DNA hybridizationwould have been required for formal spe-cies descriptions24. Admittedly, there arehuge challenges in determining specieslimits in bacteria and archaea, particularlyin the face of extensive horizontal genetransfer31. Nonetheless, the differencesin nomenclatural practices for bacteria
and archaea versus fungi may be part ofthe reason why the number of new spe-cies described per year is about twice asmany for fungi as it is for prokaryotes5,32.The ICN will increase the centralization oftaxonomic authority for fungi, although thebasic criteria for fungal species recognitionwill remain unrestricted. It is importantthat as the new rules of the ICN are imple-mented, the GC acts with restraint anddoes nothing to impede progress in fungalspecies description.
Mycologists can also learn from theexperience of bacterial and archaealresearchers with regard to the classifica-tion of environmental sequences. Therequirement for a living type culture fordescribing bacterial or archaeal species26 is comparable to the requirement for aphysical type specimen for naming fungalspecies. To enable the naming of bacteria
that lack cultures but are known by “morethan a mere sequence” (REF. 33), Murrayand Schleifer34 suggested that the prefixCandidatus be used, indicating that thename is provisional. This recommendationhas been appended to the bacterial code25,but fewer than 400 bacteria and archaeahave been described as Candidatus spe-cies35. If mycologists wish to adopt a newcategory similar to Candidatus to accom-modate the huge numbers of species dis-covered through environmental sequences,as has been suggested5, they will need tofind ways to facilitate high-throughput tax-onomy, almost certainly involvingautomated work flows.
The future of fungal taxonomy
Twenty-five years after the first descrip-tion of PCR, species-level fungal taxonomyis finally catching up with the molecularrevolution. Change has come slowly andhas been prompted by the actions of radi-cals, who flouted and subverted the codeby naming taxa based on anamorphs7,8 or environmental sequences20. Such indi-
vidual acts of rebel lion illuminate the way
forward, but ultimately fungal taxonomyis a group enterprise that can succeedonly with the support and participationof the broad community of mycologists.Proponents of unitary taxonomy workedeffectively as a community to repeal dualnomenclature and are now organizingthemselves to resolve the correct namesof scores of pleomorphic fungal species.Supporters of sequence-based taxonomyhave not been so unified, however. Thepublication of P. cryptodigmaticus dem-onstrates that it is ‘legally’ possible, under
the code, to describe new species basedon sequences (as long as a nominal typeis deposited somewhere), but commu-nity effort will be needed to develop thebroadly accepted protocols required for amass movement towards sequence-basedtaxonomy.
At least one difficult issue appears tohave been resolved: the internal transcribedspacer (ITS) region of the nuclear rRNAgene has been proposed as the fungal bar-code locus22 and is being used for sequence-based species delimitation in environmentalsurveys for many groups of fungi. However,other key issues remain problematic. Longerreads that provide sequences for the ITSand the phylogenetically tractable largesubunit (LSU) rRNA cannot be obtaineduntil there are improvements in next-generation sequencing. The gold standardfor species delimitation in fungi is the
genealogical concordance method, whichuses multiple genetic loci to assess the limitsof recombination36. Such approaches arenot applicable in environmental data sets,which usually use single loci amplified frompooled DNAs. Moreover, in order to carryout species delimitation in environmentalsamples, the consequences of intragenomicheterogeneity in multicopy rRNA genes,as well as error owing to gene tree versusspecies tree conflict, will have to be deter-mined empirically in relation to multigenedata sets. The names of species knownonly from environmental sequences mightrequire a new taxonomic category compa-rable to the Candidatus status for bacteriaand archaea5, or an identifying suffix (forexample, ENAS (environmental nucleicacid sequence) or eMOTU (environmentalmolecular operational taxonomic unit))6.The reality of sequencing errors mightprevent naming until the same sequenceis found a second time and by a differentresearch group. Finally, mycological data-bases such as MycoBank must prepare fora massive influx of new species, especiallyif automated work flows are developed to
describe fungi from environmental nucleicacid sequences. Given the rate of speciesdiscovery, mycologists do not have another25 years to ponder the problem.
David S. Hibbett is at The Biology Department,
Clark University, Worcester, Massachusetts 01610, USA.
John W. Taylor is at The Department of Plant and
Microbial Biology, University of California,
Berkeley, California 94720, USA.
Correspondence to D.S.H.
e-mail: [email protected]
doi:10.1038/nrmicro2963
Published online 3 January 2013
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AcknowledgmentsThe authors thank their colleagues and members of their labo-
ratories for discussions on the principles of fungal taxonomy,
and the International Mycological Association and the
Centraalbureau voor Schimmelcultures for hosting meetings
addressing the revolution in fungal nomenclature. Research in
the authors’ laboratories is supported by the Open Tree of Life
Project (http://opentreeoflife.org/), the US National Science
Foundation (grant DEB-1208719 to D.S.H.), the US National
Institutes of Health (grant U54-AI65359 to J.T.W.) and the
Energy Biosciences Institute (grant EBI 001J09 to J.W.T.).
Competing interests statementThe authors declare no competing financial interests.
FURTHER INFORMATIONDavid S. Hibbett’s homepage: http://www.clarku.edu/
faculty/dhibbett/
John W. Taylor’s homepage:http://taylorlab.berkeley.edu/
GenBank: http://www.ncbi.nlm.nih.gov/genbank/
IndexFungorum:http://www.indexfungorum.org/
MycoBank: http://www.mycobank.org/
RefSeq: http://www.ncbi.nlm.nih.gov/RefSeq/
UNITE: http://unite.ut.ee/
ALL LINKS ARE ACTIVE IN THE ONLINE PDF
When the H1N1 influenza virus struck in
1918, little was known about how infectiousdiseases emerge or their routes of transmis-sion. Indeed, even the identification of thecausative agent as a virus (that is, capableof passing through a filter) rather than thebacterium Haemophilus influenzae (cham-pioned by some leading microbiologistsat the time) was in dispute until late in thecourse of the pandemic1. The 1918 virus hadan estimated case fatality rate of 10–20%,spread to six continents, infected ~500 mil-lion people and killed approximately 3% ofthe world’s population2,3. The severe acute
respiratory syndrome (SARS) coronavirus
pandemic of 2002–2003, the first pandemicof the twenty-first century, had a case fatalityrate of near 10%, but infected far fewer people(8,096) than the H1N1 influenza virus ofthe 1918 pandemic4. Transmissibility, as esti-mated by R
0 (the basic reproduction number;
that is, the number of cases generatedthrough contact with one infected individ-ual) was similar for the influenza pandemicof 1918 (R
0 = 2–3)5 and the SARS pandemic of
2003 (R 0 = 2–5)6,7. However, the global
response to SARS was facilitated by advancesin epidemiology and microbiology that
ESSAY
The changing face of pathogendiscovery and surveillance
W. Ian Lipkin
Abstract | The pace of pathogen discovery is rapidly accelerating. This reflects
not only factors that enable the appearance and globalization of new microbial
infections, but also improvements in methods for ascertaining the cause of
a new disease. Innovative molecular diagnostic platforms, investments in
pathogen surveillance (in wildlife, domestic animals and humans) and the advent
of social media tools that mine the World Wide Web for clues indicating the
occurrence of infectious-disease outbreaks are all proving to be invaluable for
the early recognition of threats to public health. In addition, models of microbial
pathogenesis are becoming more complex, providing insights into the mechanisms
by which microorganisms can contribute to chronic illnesses like cancer, peptic
ulcer disease and mental illness. Here, I review the factors that contribute to
infectious-disease emergence, as well as strategies for addressing the challenges
of pathogen surveillance and discovery.
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NATURE REVIEWS | MICROBIOLOGY VOLUME 11 | FEBRUARY 2013 | 133
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