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The Invisible Dimension of Fungal Diversity David Hibbett Science 351, 1150 (2016); DOI: 10.1126/Science.Aae0380

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The Invisible Dimension of Fungal Diversity David Hibbett Science 351, 1150 (2016); DOI: 10.1126/Science.Aae0380 INSIGHTS | PERSPECTIVES begin enforcing proper use of AIS. Simply observation technologies outweigh costs of MICROBIOLOGY having an AIS unit aboard a vessel, but renegotiating the boundaries of industrial failing to use it properly, can no longer be privacy. Recognizing these values, the ma- viewed as legal compliance. As noncompli- rine shipping industry has almost univer- The invisible ance becomes better controlled, we also sally adopted AIS, as well as supplemental encourage that AIS data be more widely data-sharing systems. considered as admissible evidence in mari- Reforms under way to begin managing the dimension time judicial proceedings. ocean at vastly larger and ecologically mean- Evidence suggests that it is possible to ingful scales will only matter if we can see equip all commercial fi shing vessels in the and act on what is happening in these spaces. of fungal world with AIS and enforce its use. About Transparency is an extremely important part 75% of EU fi shing vessels complied with 2014 of this process. Parallel closed-access track- diversity AIS mandates within months (9). We esti- ing systems can and should be linked to AIS mated that 71% of large fi shing vessels (>24 to improve our view of vessel activity, but Can microbial taxa be m) worldwide use AIS, and we observed a closed-access systems allow only part of the 17% increase in global AIS coverage for fi sh- picture to be seen by few actors and, conse- defi ned from environmental ing vessels during 2014 (4). Closing remain- quently, have more limited value to science molecular sequences? ing gaps among users resistant to compliance and transboundary biodiversity manage- will be dif cult but critically important. ment. Unfortunately, current lack of legisla- By David Hibbett Widespread implementation of publicly tive support for AIS has stunted this system accessible AIS would ef ectively bring an into a service that best observes vessels that axonomy plays a central role in un- end to the era of marine anonymity. There don’t mind being seen. Although the policy derstanding the diversity of life, is growing awareness in marine and ter- shifts we call for require brave revisioning of translating the products of biological restrial sectors that benefi ts for human the primacy of privacy on the oceans, failure exploration and discovery—specimens and environmental safety derived from to close loopholes will continue to foster ille- and observations—into systems of gal activities that steal income and biodiver- names that capture the relationships sity from developing nations, promote social Tbetween species. Taxonomic names facilitate injustice at sea, and undermine ef orts to co- communication among scientists and the PIPA operatively manage the sustained vitality of public and provide conceptual handles for EEZ our shared marine resources. ■ complex phylogenetic hypotheses. However, on March 14, 2016 Fishing days taxonomy can be challenging, particularly REFERENCES AND NOTES for fungi and other microorganisms, which 1.0 8.0 >_ 15.0 1. D. J. McCauley, Nature 515, 29 (2014). 2. United Nations General Assembly, “Oceans and the law of are morphologically simple and extremely A the sea: Development of an international legally binding di verse (1). Molecular environmental surveys 0° instrument under the United Nations Convention on the have revealed previously unknown branches Law of the Sea on the conservation and sustainable use of marine biological diversity of areas beyond national of the fungal tree of life (2–5) and illuminated jurisdiction” (A/69/922, 2015). biogeographic patterns across all groups of 3. C. Pala, Tracking f shy behavior, from space. The Atlantic fungi (6, 7). Yet the products of this research Downloaded from (16 November 2014). are not being translated into formal species 4. Materials, methods, and data used in this paper are avail- able as supplementary materials on Science Online. names, in part because of the very rules de- 5°S 5. International Maritime Organization (IMO), International signed to facilitate taxonomy. Convention for the Safety of Life at Sea (SOLAS) (1184 Two recently recognized groups of fungi, UNTS 3, 2002). 6. D. J. McCauley et al., Science 347, 1255641 (2015). Archaeorhizomycetes and Cryptomycota, il- 7. J. Lubchenco, K. Grorud-Colvert, Science. 350, 382 (2015). lustrate the magnitude of ongoing molecu- 8. Convention on Biological Diversity, Decision X/2, The lar species discovery. Archaeorhizomycetes 175°W 170°W Strategic Plan for Biodiversity 2011–2020 and the Aichi Biodiversity Targets (Nagoya, Japan, 2010). are root-associated soil fungi that have B 9. F. Natale, M. Gibin, A. Alessandrini, M. Vespe, A. Paulrud, been found in more than 100 independent 0° PLOS ONE 10, e0130746 (2015). studies. When Menkis et al. (3) pooled envi- 10. B. B. Collette et al., Science. 333, 291 (2011). 11. N. K. Dulvy et al., Aquat. Conserv. Mar. Freshw. Ecosyst. 18, ronmental sequences of ribosomal internal 459 (2008). transcribed spacer (ITS) genes, they found 12. C. M. Brooks et al., Stan. Envtl. LJ. 33, 289 (2013). 50 lineages of Archaeorhizomycetes contain- 13. E. Druel, K. M. Gjerde, Mar. Policy 49, 90 (2014). 14. L. B. Crowder et al., Science 313, 617 (2006). ing at least two independent sequences with SCIENCE 15. S. Flothmann et al., Science 328, 1235 (2010). 97% similarity, a standard cutof for recog- 5°S nizing OTUs (operational taxonomic units, ACKNOWLEDGMENTS often equated with species). They also found We thank the Alfred P. Sloan Foundation, the Beniof Ocean Initiative, and NSERC for support; K. Gjerde, F. Joyce, P. 95 unique sequences (singletons). Thus, as DeSalles, A. Guerra, and B. S. Mitchell for comments/advice; many as 145 species of Archaeorhizomyce- CARY/ N. BY ADAPTED , 175°W 170°W and ORBCOMM and the Western and Central Pacif c Fisheries tes have been discovered. But only two have ET AL. Commission for data access. The views expressed in this article been formally named, Archaeorhizomyces Observing marine protected areas from space. are those of the authors only and do not necessarily ref ect the Summary of long-line and purse seine f shing as views of any af liated institution or company. fi n l a y i and A. borealis, based on the only measured using S-AIS data in PIPA during the 6 months live cultures obtained so far (see the fi gure). before (A) and 6 months after (B) it was closed to SUPPLEMENTARY MATERIALS www.sciencemag.org/content/351/6278/1148/suppl/DC1 commercial f shing by the Kiribati government on 1 Jan Biology Department, Clark University, Worcester, MA 01610, 2015 (4). 10.1126/science.aad5686 USA. E-mail: [email protected] MCCAULEY ILLUSTRATION: 1150 11 MARCH 2016 • VOL 351 ISSUE 6278 sciencemag.org SCIENCE Published by AAAS A. borealis A. fnlayi KEY Unnamed environmental OTUs Named species Outgroup Taphrinomycotina Unique singletons Visible and invisible diversity of Archaeorhizomycetes. Phylogenetic analysis of environmental DNA sequences resolves 50 species-level groups of Archaeorhizomycetes (3), but only two have been formally named. The existence of 95 unique singleton sequences suggests that there is much unsampled diversity. Archaeorhizomycetes is the most diverse class in the Taphrinomycotina, which include well-known plant pathogens and the model f ssion yeast. Tree topology from (3); micrographs by A. Rosling. The aptly named Cryptomycota have also similarity cutof . In other words, this study precedented resources for taxonomists, who been detected repeatedly in molecular stud- detected ~30,000 OTUs that could be new could use the new data to describe new spe- ies of soil, freshwater, and marine habitats (4, species—about 15 times the number of new cies or enhance existing descriptions with ex- 5). Phylogenetic analyses suggest that Cryp- fungal species descriptions published in panded geographic ranges and new insights tomycota make up an ancient clade of fungi. journals and recorded in nomenclatural da- into ecological roles. Cryptomycota cells have been visualized in tabases in the same year (1). Unfortunately, the rules that govern bio- environmental samples with fl uorescent tags, Environmental sequences have trans- logical nomenclature prohibit formal nam- but these observations are not linked to cul- formed understanding of the fungal tree ing of fungi and other microbial taxa based tures or specimens (4). Lazarus and James of life, from its deepest roots to its fi nest on environmental sequences. Physical type analyzed 109 environmental sequences of branches. Why are these discoveries not be- specimens are required by the botanical and Cryptomycota and resolved 12 strongly sup- ing formalized in taxonomic names? zoological codes of nomenclature, which col- ported groups (5). However, they could only First, there are legitimate scientifi c con- lectively determine conditions for valid publi- assign three sequences to a formally named cerns over the nature of evidence required cation of names of fungi and protists, and the taxon, the genus Rozella, which includes en- to delimit species. Mycologists have selected bacteriological code requires type cultures. doparasites of protists and other fungi. ITS as the of cial barcode locus (9), but in Classical taxonomy is thus cut of , by its own Molecular ecological studies have investi- some groups multiple species may have nomenclatural rules, from the major modes gated fungal distributions on global (7) and identical ITS sequences, whereas in other of discovery for microbial organisms. Work- local (8) scales. In one recent global survey, groups there may be multiple forms of ITS in ing models for purely sequence-based de- Davison et al. (6) analyzed the distribution a single genome. Single-cell genomics could limitation of fungal taxa do exist (3, 6, 10, 11), of arbuscular mycorrhizal fungi, which form provide multiple genes from individuals in but do not yet confer nomenclatural validity. symbioses with about 80% of plants, but environmental samples, but these technically Community standards for sequence-based do not produce mushrooms and cannot be demanding approaches are not yet widely ap- taxon defi nition and revision of the codes of grown in pure culture.
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