PerspectiveMicrobiology

The invisible dimension of fungal diversity

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Science  11 Mar 2016:
Vol. 351, Issue 6278, pp. 1150-1151
DOI: 10.1126/science.aae0380

Taxonomy plays a central role in understanding the diversity of life, translating the products of biological exploration and discovery—specimens and observations—into systems of names that capture the relationships between species. Taxonomic names facilitate communication among scientists and the public and provide conceptual handles for complex phylogenetic hypotheses. However, taxonomy can be challenging, particularly for fungi and other microorganisms, which are morphologically simple and extremely diverse (1). Molecular environmental surveys have revealed previously unknown branches of the fungal tree of life (25) and illuminated biogeographic patterns across all groups of fungi (6, 7). Yet the products of this research are not being translated into formal species names, in part because of the very rules designed to facilitate taxonomy.

Two recently recognized groups of fungi, Archaeorhizomycetes and Cryptomycota, illustrate the magnitude of ongoing molecular species discovery. Archaeorhizomycetes are root-associated soil fungi that have been found in more than 100 independent studies. When Menkis et al. (3) pooled environmental sequences of ribosomal internal transcribed spacer (ITS) genes, they found 50 lineages of Archaeorhizomycetes containing at least two independent sequences with 97% similarity, a standard cutoff for recognizing OTUs (operational taxonomic units, often equated with species). They also found 95 unique sequences (singletons). Thus, as many as 145 species of Archaeorhizomycetes have been discovered. But only two have been formally named, Archaeorhizomyces finlayi and A. borealis, based on the only live cultures obtained so far (see the figure).

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 fission yeast. Tree topology from (3); micrographs by A. Rosling.

ILLUSTRATION: K. SUTLIFF/SCIENCE

The aptly named Cryptomycota have also been detected repeatedly in molecular studies of soil, freshwater, and marine habitats (4, 5). Phylogenetic analyses suggest that Cryptomycota make up an ancient clade of fungi. Cryptomycota cells have been visualized in environmental samples with fluorescent tags, but these observations are not linked to cultures or specimens (4). Lazarus and James analyzed 109 environmental sequences of Cryptomycota and resolved 12 strongly supported groups (5). However, they could only assign three sequences to a formally named taxon, the genus Rozella, which includes endoparasites of protists and other fungi.

Molecular ecological studies have investigated fungal distributions on global (7) and local (8) scales. In one recent global survey, Davison et al. (6) analyzed the distribution of arbuscular mycorrhizal fungi, which form symbioses with about 80% of plants, but do not produce mushrooms and cannot be grown in pure culture. Using 18S ribosomal RNA gene sequences, the authors detected 246 OTUs, of which 93% occurred on multiple continents and 34% on six continents. This level of endemism is surprisingly low for fungi that do not produce airborne spores (6). However, the results provide limited information about distributions of known taxa, because only 41 of the OTUs (17%) include sequences from named species.

In the largest study of fungal diversity to date, Tedersoo et al. (7) analyzed 1.4 million ITS sequences from 365 sites worldwide and recovered ~45,000 OTUs represented by at least two sequences, with a further ~36,000 singletons. Only about one-third of the nonsingleton OTUs matched any sequences in public databases at the 97% similarity cutoff. In other words, this study detected ~30,000 OTUs that could be new species—about 15 times the number of new fungal species descriptions published in journals and recorded in nomenclatural databases in the same year (1).

Environmental sequences have transformed understanding of the fungal tree of life, from its deepest roots to its finest branches. Why are these discoveries not being formalized in taxonomic names?

First, there are legitimate scientific concerns over the nature of evidence required to delimit species. Mycologists have selected ITS as the official barcode locus (9), but in some groups multiple species may have identical ITS sequences, whereas in other groups there may be multiple forms of ITS in a single genome. Single-cell genomics could provide multiple genes from individuals in environmental samples, but these technically demanding approaches are not yet widely applied in fungal ecology. Until they are, most studies will rely on single markers such as ITS, which can never reveal the patterns of gene flow that provide clues to the limits of reproductively isolated lineages.

Second, species names are no longer needed to test ecological or evolutionary hypotheses. Ecologists once relied on taxonomic resources to identify the species whose interactions they sought to explain; today, they use automated pipelines to cluster OTUs without reference to keys, vouchers, and monographs (10). Ecologists and evolutionary biologists do not need to undertake the tedious work of identification and formal taxon description to address the problems that motivate them. On the other hand, molecular ecological studies are providing unprecedented resources for taxonomists, who could use the new data to describe new species or enhance existing descriptions with expanded geographic ranges and new insights into ecological roles.

Unfortunately, the rules that govern biological nomenclature prohibit formal naming of fungi and other microbial taxa based on environmental sequences. Physical type specimens are required by the botanical and zoological codes of nomenclature, which collectively determine conditions for valid publication of names of fungi and protists, and the bacteriological code requires type cultures. Classical taxonomy is thus cut off, by its own nomenclatural rules, from the major modes of discovery for microbial organisms. Working models for purely sequence-based delimitation of fungal taxa do exist (3, 6, 10, 11), but do not yet confer nomenclatural validity. Community standards for sequence-based taxon definition and revision of the codes of nomenclature are needed to make the products of molecular environmental surveys visible to scientific and lay communities.

References and Notes

  1. Centre for Agriculture and Biosciences International, Species Fungorum; www.speciesfungorum.org.
  2. Acknowledgments: I thank T. James, P. Kirk, M. Öpik, J. Davison, and A. Rosling for images and comments.

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