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Science depends on nomenclature, but nomenclature is not science - Nature Reviews Microbiology
Science depends on nomenclature, but nomenclature is not science Download PDF Comment . Published: 10 January 2022 . Science depends on nomenclature, but nomenclature is not science . Karen G. Lloyd ? ORCID: orcid.org/0000-0003-0914-6375 1 & . Guillaume Tahon ? ORCID: orcid.org/0000-0001-7020-4162 2 ? . Nature Reviews Microbiology ( 2022 ) Cite this article 726 Accesses 29 Altmetric Metrics details Subjects . Archaea . Bacteria . Taxonomy . The International Committee on Systematics of Prokaryotes (ICSP) has recently altered long-standing phylum names and given no guidance for taxonomy of uncultured or imperfectly cultured archaea and bacteria, disrupting progress towards a universal system of microbial taxonomy. Inclusion of new members into ICSP may help it to keep up to date.

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Download PDF Official names of bacteria and archaea are determined by the International Committee on Systematics of Prokaryotes (ICSP), comprised of 26 scientists representing major international microbial societies, with no membership from South or Central America or most of Africa or Asia. Recently, ICSP reversed its long-standing policy of not assigning phylum names, disrupting commonly used names 1 . This decision should be viewed in the context of the fact that ICSP has not assumed responsibility for naming bacteria and archaea that are not readily cultured. Here, we describe the way ICSP naming works currently, how it fails some of the demands of modern microbiology, and how recent name changes make it worse. We then propose solutions. To have a name officially recognized by the ICSP, a microorganism must be in axenic culture or, in rare cases, a defined co-culture, and be capable of being maintained in two freely shared culture collections. Its name must follow ICSP’s strict nomenclature rules. Nomenclature is a system of names for organisms and classification is a model of the evolutionary relationships among organisms. Taxonomy incorporates both. Classification should reflect an organisms’ evolutionary history, which can be tested empirically. Nomenclature should reflect classification, but nomenclature itself cannot be refuted by experiment. The ICSP relies on strict nomenclature rules and experts in microbial subgroups to ensure that nomenclature is stable and follows a polyphasic classification combining phenotype and genotype. If all bacteria and archaea on Earth were amenable to unfussy, axenic growth on human timescales under common laboratory conditions, then the method currently used by ICSP would be the best way to organize them into properly named taxa. However, since the 1990s, DNA from environmental samples has shown that most microbial diversity has never been cultured. This ‘microbial dark matter’ dominates most environments and is central to Earth’s microbiome 2 . Many of these organisms could be obligate syntrophs that may never yield to axenic culture, such as ANME-1, Lokiarchaeota, and the members of the candidate phyla radiation. Others are fastidious and/or slow-growing, such as SAR11, Saccharibacteria (also called TM7), and Atribacteria, so decades of research is needed before strains can be added to culture collections. Uncultured microorganisms need to be named while they are undergoing the rich research enabled by metagenomics, metatranscriptomics, metaproteomics, meta-metabolomics, single-cell genomics and activity, geochemical inference and in situ functional assays. Researchers whose governments restrict sharing through the Nagoya Protocol often cannot meet ICSP requirements 3 . Others cannot overcome the slow and expensive naming process to bring all their existing cultures to be published officially, leaving thousands of cultures languishing in obscurity. In nature, bacteria and archaea almost never grow axenically or with unlimited resources, so the ICSP requirements clearly deviate from natural conditions under which most of life evolved. Perhaps facile, axenic culture on human timescales should not be the only metric by which a microorganism is deemed worthy of a name. Out of necessity, researchers have been publishing names for difficult-to-culture bacteria and archaea over the past 30 years. The problem with this approach is exactly what ICSP was initiated to prevent: confusion from overlapping and inexact naming systems using non-standard nomenclature. For example, Lokiarchaeota were renamed from Marine Benthic Group B (MBG-B) and Deep-Sea Archaeal Group (DSAG). They are now members of the Asgard super-phylum and their nearly pure enrichment is ‘ Candidatus Prometheoarchaeum syntrophicum’ 4 . Bathyarchaeota were renamed from Miscellaneous Crenarchaeal Group (MCG) and Marine Benthic Group C, with parallel nomenclature for sub-groupings therein 5 . Many modern microbiologists carry out large DNA surveys, often using the 16S rRNA gene to determine microbial identities. Therefore, the Silva database has largely replaced ICSP for both nomenclature and classification as Silva adopts informal names and offers easily downloadable files for automated classification of 16S rRNA gene sequences. Many scientists also use metagenome-assembled genomes (MAGs) to assess microbial communities. The simplest way to classify MAGs is to use the Genome Taxonomy Database Toolkit (GTDB-Tk). However, unlike Silva, the GTDB-Tk is not simply a database reflecting nomenclature from the peer-reviewed literature. It departs from polyphasic taxonomy that combines physiological, morphological and genomic phylogenies. Instead, it uses a new metric called the relative evolutionary divergence (RED) to determine thresholds for taxonomic ranks 6 . The Silva database has incorporated many GTDB taxonomies into release version 138, but did not include newer GTDB taxonomies for the 138.1 release. Problems have arisen from reducing the complexities of taxonomy to genome-only metrics. For example, some members of the validly named genus Geobacter were reassigned Citrifermentans , even though no Geobacter culture has been shown to ferment citrate and GTDB purports to not rename validly named strains 7 . GTDB has since altered the name, but Citrifermentans remains on the List of Prokaryotic Names with Standing in Nomenclature (LPSN). Input from physiological experts could have prevented this. The GTDB taxonomic reclassifications have been widespread and frequent. For example, ‘ Candidatus Odinarchaeota’ was first classified under class Lokiarchaeia, order LCB-4, subsequently under the order Odinarchaeales, and most recently was transferred to the class Lokiarchaeia A. Environmental microbiologists recently proposed a roadmap for incorporating genomes as type material into ICSP, resulting in a unified taxonomy 8 . However, ICSP rejected a similar proposal, largely because pure cultures plus genomes make better type material than genomes alone. Although undoubtedly true, we cannot simply wish for tidy cultures but must adapt to the messy reality of the microbial world. The heavy influence of employees of large culture collections on this ICSP decision may be a financial conflict of interest, as the decision could affect the number of strains deposited. On one hand, we have ICSP, which is in danger of becoming obsolete by refusing to accept genomic type material. A separate code, SeqCode, is already under development. On the other hand, we have GTDB, which goes to the opposite extreme by using a new genome-only taxonomic metric that has not yet been fully accepted by the community. There appears to be some merging of the two, as the originator of the GTDB, Phil Hugenholtz, has recently become a member of ICSP. It is in this climate of confusion that ICSP voted recently to decide phylum names 1 . Historically, the scientific community has agreed upon phylum names such as Proteobacteria, Actinobacteria, Firmicutes and Thaumarchaeota by common usage. However, since November 2015, ICSP has proposed to change these historic and widely used names three times. First, the suffix -aeota was introduced for phylum names (for example, Proteobacteria became Alphaproteobacteraeota) 9 . Soon after, the suffix was changed to -ota, because -aeota was ‘somewhat awkward’ (for example, Alphaproteobacteraeota became Alphaproteobacterota) 10 . Most recently, ICSP has changed the abovementioned phylum names to Pseudomonadota, Actinomycetota, Bacillota and Nitrososphaerota 1 . Such frequent changes impede scientific progress and give the impression that the ICSP does not consider impacts on the global microbiological community before implementing them. The decision to change phylum names was not driven by data-backed reclassification. It is simply for the purpose of nomenclature, which has little underlying empiricism. Historical phylum names have meaning and purpose, as they have been used for decades to describe some of the most important bacteria and archaea for medicine, bioremediation, agriculture and Earth systems. Because nomenclature is not science, ICSP should have kept these useful names to aid research efforts, rather than disrupt scientific progress to adhere to nomenclature rules. The ideal solution for naming both phyla and untamed bacteria and archaea would be for ICSP to take input from the broader community of microbiologists affected by their decisions, including more input from those who regularly work with genomic type material and those who are restricted by the Nagoya Protocol and/or financial limitations. They should also loosen their strict nomenclature rules to reflect the fact that consistency and stability are often more important than using proper Latin and Greek, especially in cases in which emergent names have filled a long-standing gap left by ICSP. In the meantime, microbiologists can mitigate the damage by citing all the names for a particular clade, if feasible. In this way, we can bridge the gap until we achieve a stable system of taxonomy that includes all microorganisms, not just those that are well behaved. References . 1. Oren, A. & Garrity, G. M. Valid publication of the names of forty-two phyla of prokaryotes. Int. J. Syst. Evol. Microbiol. 71 , 005056 (2021). Google Scholar ? 2. Lloyd, K. G., Steen, A. D., Ladau, J., Yin, J. & Crosby, L. Phylogenetically novel uncultured microbial cells dominate Earth microbiomes. mSystems 3 , e00055-18 (2018). CAS ? Article ? Google Scholar ? 3. Rahi, P. Regulating access can restrict participation in reporting new species and taxa. Nat. Microbiol. 6 , 1469–1470 (2021). CAS ? Article ? Google Scholar ? 4. Imachi, H. et al. Isolation of an archaeon at the prokaryote–eukaryote interface. Nature 577 , 519–525 (2020). CAS ? Article ? Google Scholar ? 5. Meng, J. et al. Genetic and functional properties of uncultivated MCG archaea assessed by metagenome and gene expression analyses. ISME J. 8 , 650–659 (2014). CAS ? Article ? Google Scholar ? 6. Parks, D. H. et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat. Biotechnol. 36 , 996–1004 (2018). CAS ? Article ? Google Scholar ? 7. Sanford, R. A., Lloyd, K. G., Konstantinidis, K. T. & L?ffler, F. E. Microbial taxonomy run amok. Trends Microbiol. 29 , 394–404 (2021). CAS ? Article ? Google Scholar ? 8. Murray, A. E. et al. Roadmap for naming uncultivated Archaea and Bacteria. Nat. Microbiol. 5 , 987–994 (2020). CAS ? Article ? Google Scholar ? 9. Oren, A. et al. Proposal to include the rank of phylum in the International Code of Nomenclature of Prokaryotes. Int. J. Syst. Evol. Microbiol. 65 , 4284–4287 (2015). CAS ? Article ? Google Scholar ? 10. Whitman, W. B. et al. Proposal of the suffix -ota to denote phyla. Addendum to ‘proposal to include the rank of phylum in the International Code of Nomenclature of Prokaryotes’. Int. J. Syst. Evol. Microbiol. 68 , 967–969 (2018). Article ? Google Scholar ? Download references Author information . Affiliations . Microbiology Department, University of Tennessee, Knoxville, TN, USA Karen G. Lloyd Department of Agrotechnology and Food Sciences, University of Wageningen, Wageningen, Netherlands Guillaume Tahon Authors Karen G. Lloyd View author publications You can also search for this author in PubMed ? Google Scholar Guillaume Tahon View author publications You can also search for this author in PubMed ? Google Scholar Corresponding author . Correspondence to Karen G. Lloyd . Ethics declarations . Competing interests . The authors declare no competing interests. Rights and permissions . Reprints and Permissions About this article . Cite this article . Lloyd, K.G., Tahon, G. Science depends on nomenclature, but nomenclature is not science. Nat Rev Microbiol (2022). https://doi.org/10.1038/s41579-022-00684-2 Download citation Published : 10 January 2022 DOI : https://doi.org/10.1038/s41579-022-00684-2 Share this article . 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