Episode 69: Background to bacterial taxonomy

Bacterial taxonomy: history, naming rules and genomes

Andrew Page and Nabil-Fareed Alikhan discuss the background to bacterial taxonomy with Phil Hugenholtz, Iain Sutcliffe and Mark Pallen. Prompted by debate over changes to bacterial phyla, the panel distinguishes classification from naming rules and examines how genomes could simplify species descriptions. They also disagree over the usefulness of the term prokaryotes and discuss why culture requirements create difficulties for naming organisms discovered through metagenomics.

Listen to Episode 69: Background to bacterial taxonomy on SoundCloud

In this episode

From Linnaeus to evolutionary classification

Mark Pallen separates two achievements of Linnaeus: arranging organisms into nested groups and establishing binomial names, illustrated by Homo sapiens and Escherichia coli. Darwin subsequently supplied an evolutionary explanation for those groups: common descent. Classification should therefore reflect genealogy, rather than simply collect organisms with similar appearances or habits.

Pallen describes Hennig’s later emphasis on branches of the evolutionary tree rather than grades of complexity. Fish illustrate the distinction: a classification containing all fish would also have to include humans and other terrestrial vertebrates. He then credits Carl Woese with bringing molecular approaches into bacterial classification, initially through RNA fragments and later sequence-based comparisons. Mycoplasmas appearing as a small branch within the Gram-positive group illustrate how molecular evidence can challenge classifications based on conspicuous traits.

Is prokaryotes still a useful term?

Pallen argues that grouping bacteria and archaea as prokaryotes conflicts with phylogenetic classification because eukaryotes are closer to archaea than to bacteria. He objects particularly when teaching materials use prokaryotes while actually describing mechanisms specific to bacteria, citing questions about DNA and RNA replication that he challenged as an external examiner.

Iain Sutcliffe accepts the historical baggage but sees value in a vernacular term for organisms without nuclei. Another panellist similarly distinguishes convenient shorthand for bacteria and archaea from inaccurate use meaning bacteria alone. Sutcliffe says his formal writing increasingly uses archaea and bacteria, while arguing that the ICSP has more pressing questions than changing its name.

Naming rules are not a compulsory taxonomy

Sutcliffe explains that the International Committee on Systematics of Prokaryotes, or ICSP, primarily oversees the International Code of Nomenclature of Prokaryotes, or ICNP. It also helps oversee the journal of record for nomenclature. These responsibilities do not mean that the committee dictates a single classification: the code protects freedom of taxonomic thought.

His example is Rhodococcus: GTDB can treat it as one genus while he considers that it should be divided into several genera. The distinction is between classification decisions and rules for assigning names. Under the code described here, valid naming requires cultured organisms deposited in culture collections—a substantial limitation for organisms recovered through metagenomics.

Replacing the species-description assembly line

Asked how taxonomy can catch up with genomics, Sutcliffe argues that genomes contain the information needed for robust classification. Drawing on editorial work between 2009 and 2019 involving more than 800 bacterial species descriptions, he criticises repetitive papers built around checklists of biochemical and phenotypic tests.

He describes a one-colony, one-species, one-paper workflow: find an isolate with a sufficiently different 16S rRNA sequence, perform a battery of tests, and write a six-page description. Each paper then requires an editor and two reviewers. His objection is not to studying organisms, but to the human effort spent producing routine descriptions whose individual findings are often unremarkable. He sees changing publication expectations as central to modernisation.

A shorter route to describing cultured species

Pallen distinguishes the code’s requirements from conventions imposed by editors and reviewers. In work on the chicken gut microbiome, his group wanted to name uncultured organisms alongside 30 cultured organisms. They used terse descriptions identifying the type strain and setting a 95% ANI boundary for membership of the species.

Those descriptions passed peer review, but culture deposition and its validation remained a separate obstacle: more than a year after sending strains to collections, the process was still being completed. Pallen argues that taxonomists can satisfy requirements for descriptions, circumscription and name derivations without reproducing every traditional test or lengthy linguistic explanation.

Diagnosis, genomes and horizontal gene transfer

Sutcliffe points to a paper advocating a return to Linnaeus’s focus on diagnosis rather than description, using DNA characters in formal species naming. For him, genomic evidence can establish a taxon’s position and distinctiveness while the accompanying naming description remains brief.

Pallen recalls clinical colleagues dismissing genomically distinct Acinetobacter species because they could not distinguish them in the laboratory. He argues for genomic classification, but qualifies what that means: horizontal gene transfer makes it important to use a suitable subset of genes rather than treat every gene as an equivalent evolutionary signal. His lorry analogy separates the cab from its cargo. Phil Hugenholtz closes positively, seeing current disagreements as growing pains towards a fuller account of microbial diversity.

Highlights

00:00:47 — The hosts introduce the panel and the debate over changes to bacterial phyla.
00:01:51 — Pallen traces classification and naming from Linnaeus through evolutionary and molecular approaches.
00:08:33 — Why Pallen objects to prokaryotes as a phylogenetic grouping.
00:09:45 — Sutcliffe explains the historical terminology and defends its vernacular usefulness.
00:12:57 — Culture requirements, the ICSP’s responsibilities and freedom of taxonomic thought.
00:17:02 — Sutcliffe makes the case for genomics and against repetitive phenotypic checklists.
00:19:30 — Pallen distinguishes written rules from publishing conventions, using chicken gut species descriptions.
00:22:09 — Diagnosis rather than lengthy description as a basis for naming species.
00:23:30 — Genomically defined species and the complication of horizontal gene transfer.
00:24:52 — Hugenholtz explains why he sees an encouraging future for microbial taxonomy.

In their own words

There’s no official taxonomy, there’s no official approach to taxonomy.

— Mark Pallen, 00:19:30

Who is talking

Andrew Page (host)
Nabil-Fareed Alikhan (host)
Lee Katz (host)
Phil Hugenholtz (guest, Australian Centre for Ecogenomics, University of Queensland)
Iain Sutcliffe (guest, Northumbria University)
Mark Pallen (guest, University of East Anglia; Quadram Institute)

Tools and resources mentioned

GTDB, NCBI, ANI, cladistics.

Questions this episode answers

What is the difference between bacterial taxonomy and nomenclature?

The panel distinguishes classification decisions from rules governing names. Sutcliffe explains that the nomenclatural code protects freedom of taxonomic thought, so it does not impose one compulsory classification.

Why do some microbiologists avoid the term prokaryotes?

Pallen argues that it groups bacteria and archaea despite eukaryotes being closer to archaea, and can encourage inaccurate generalisations about bacterial biology. Sutcliffe still considers it useful as vernacular shorthand for organisms without nuclei.

Do bacterial species descriptions require long lists of biochemical tests?

Pallen argues that many such expectations are publishing conventions rather than explicit code requirements. He describes accepted chicken gut species descriptions based on a type strain and a 95% ANI boundary.

Why are uncultured organisms difficult to name under the code discussed?

Sutcliffe explains that valid naming under the ICNP described in this episode requires organisms to be cultured and deposited in culture collections. That requirement excludes many organisms found through metagenomics.

This page was written from a machine transcript of the episode and checked against it. Listen to the episode for the whole conversation.

Show notes

There has been a lot of discussion about bacterial taxonomy recently announced regarding phyla, and this revealed a lot of misconceptions around taxonomy in general. Today we discuss the background to bacterial taxonomy with: Professor Phil Hugenholtz, Professor Iain Sutcliffe and Professor Mark Pallen.

Selective bibliography as pdf: https:// github.com/MicroBinfie/MicroBinfie.github.io/raw/45db8eb57d73217644907 3065dbdacc88a288fe9/assets/Taxonomy_Selective_bibliography.pdf

Selective bibliography

Linnaeus and classification

https://en.wikipedia.org/wiki/10th_edition_of_Systema_Naturae
W. T. Stearn The Background of Linnaeus’s Contributions to the Nomenclature and Methods of Systematic Biology Systematic Zoology, 8 (1), Mar., 1959), pp. 4-22 http://www.jstor.org/stable/2411603
Daniel F. Austin. The Nuance and Wit of Carolus Linnaeus The Palmetto 13(4), 1993 https://www.fnps.org/assets/pdf/palmetto/v13i4p8austin.pdf

Darwin and evolution

http://darwin-online.org.uk/Variorum/Introduction.html
Kevin Padian Charles Darwin’s Views of Classification in Theory and Practice Syst. Biol. 48(2):352–364, 1999 https://doi.org/10.1080/106351599260337

Hennig and cladistics

http://aracnologia.macn.gov.ar/st/biblio/Hennig%201966%20Phylogenetic%20Systematics.pdf
Hennig, Willi (1975), “‘Cladistic analysis or cladistic classification?’: a reply to Ernst Mayr” (PDF), Systematic Zoology, 24 (2): 244–256, https://doi.org/10.2307/2412765
Chi-Chun Ho, Susanna K. P. Lau, Patrick C. Y. Woo. Romance of the three domains: how cladistics transformed the classification of cellular organisms Protein Cell 2013, 4(9): 664–676 https://doi.org/10.1007/s13238-013-3050-9

Woese, sequences and domains

Woese CR. Bacterial evolution. Microbiol Rev. 1987 Jun;51(2):221-71. https://doi.org/10.1128/mr.51.2.221-271.1987
Problems with “procaryote”. Pace NR. J Bacteriol. 2009 Apr;191(7):2008-10; discussion 2011. https://doi.org/10.1128/JB.01224-08

Hugenholtz and GTDB

Novel division level bacterial diversity in a Yellowstone hot spring. Hugenholtz P, Pitulle C, Hershberger KL, Pace NR. J Bacteriol. 1998 Jan;180(2):366-76. https://doi.org/10.1128/JB.180.2.366-376.1998
A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Parks DH, Chuvochina M, Waite DW, Rinke C, Skarshewski A, Chaumeil PA, Hugenholtz P.Nat Biotechnol. 2018 Nov;36(10):996-1004. https://doi.org/10.1038/nbt.4229
Genome Taxonomy Database: https://gtdb.ecogenomic.org/
GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database. Chaumeil PA, Mussig AJ, Hugenholtz P, Parks DH.Bioinformatics. 2019 Nov 15;36(6):1925-7. https://doi.org/10.1093/bioinformatics/btz848
A complete domain-to-species taxonomy for Bacteria and Archaea. Parks DH, Chuvochina M, Chaumeil PA, Rinke C, Mussig AJ, Hugenholtz P.Nat Biotechnol. 2020 Sep;38(9):1079-1086. https://doi.org/10.1038/s41587-020-0501-8
GTDB: an ongoing census of bacterial and archaeal diversity through a phylogenetically consistent, rank normalized and complete genome-based taxonomy. Parks DH, Chuvochina M, Rinke C, Mussig AJ, Chaumeil PA, Hugenholtz P.Nucleic Acids Res. 2021 Sep 14:gkab776. https://doi.org/10.1093/nar/gkab776
Reclassification of Shigella species as later heterotypic synonyms of Escherichia coli in the Genome Taxonomy DatabaseDonovan H. Parks, Maria Chuvochina, Peter R. Reeves, Scott A. Beatson, Philip Hugenholtz https://doi.org/10.1101/2021.09.22.461432

Sutcliffe and modernizing bacterial taxonomy

Challenging the anthropocentric emphasis on phenotypic testing in prokaryotic species descriptions: rip it up and start again. Sutcliffe IC. Front Genet. 2015 Jun 17;6:218. https://doi.org/10.3389/fgene.2015.00218
Roadmap for naming uncultivated Archaea and Bacteria. Murray AE, Freudenstein J, Gribaldo S, Hatzenpichler R, Hugenholtz P, Kämpfer P, Konstantinidis KT, Lane CE, Papke RT, Parks DH, Rossello-Mora R, Stott MB, Sutcliffe IC, Thrash JC, Venter SN, Whitman WB, Acinas SG, Amann RI, Anantharaman K, Armengaud J, Baker BJ, Barco RA, Bode HB, Boyd ES, Brady CL, Carini P, Chain PSG, Colman DR, DeAngelis KM, de Los Rios MA, Estrada-de Los Santos P, Dunlap CA, Eisen JA, Emerson D, Ettema TJG, Eveillard D, Girguis PR, Hentschel U, Hollibaugh JT, Hug LA, Inskeep WP, Ivanova EP, Klenk HP, Li WJ, Lloyd KG, Löffler FE, Makhalanyane TP, Moser DP, Nunoura T, Palmer M, Parro V, Pedrós-Alió C, Probst AJ, Smits THM, Steen AD, Steenkamp ET, Spang A, Stewart FJ, Tiedje JM, Vandamme P, Wagner M, Wang FP, Yarza P, Hedlund BP, Reysenbach AL.Nat Microbiol. 2020 Aug;5(8):987-994. https://doi.org/10.1038/s41564-020-0733-x
Addressing the sublime scale of the microbial world: reconciling an appreciation of microbial diversity with the need to describe species. Sutcliffe IC, Rosselló-Móra R, Trujillo ME.New Microbes New Infect. 2021 Aug 13;43:100931. https://doi.org/10.1016/j.nmni.2021.100931
Out with the old and in with the new: time to rethink twentieth century chemotaxonomic practices in bacterial taxonomy. Vandamme P, Sutcliffe I.Int J Syst Evol Microbiol. 2021 Nov;71(11).https://doi.org/10.1099/ijsem.0.005127

Pallen and modernizing bacterial nomenclature

Extensive microbial diversity within the chicken gut microbiome revealed by metagenomics and culture.Gilroy R, Ravi A, Getino M, Pursley I, Horton DL, Alikhan NF, Baker D, Gharbi K, Hall N, Watson M, Adriaenssens EM, Foster-Nyarko E, Jarju S, Secka A, Antonio M, Oren A, Chaudhuri RR, La Ragione R, Hildebrand F, Pallen MJ. PeerJ. 2021 Apr 6;9:e10941. https://10.7717/peerj.10941
Bacterial nomenclature in the era of genomics M. J. Pallen New Microbe and New Infect 2021; 44: 100942 https://doi.org/10.1016/j.nmni.2021.100942
The Next Million Names for Archaea and Bacteria. Pallen MJ, Telatin A, Oren A. Trends Microbiol. 2021 Apr;29(4):289-298. https://doi.org/10.1016/j.tim.2020.10.009
Naming the Unnamed: Over 45,000 Candidatus Names for Unnamed Archaea and Bacteria in the Genome Taxonomy Database M Pallen, NF Alikhan. Preprints. https://doi.org/10.20944/preprints202111.0557.v1