Bacterial Species Concepts

by

Frederick M. Cohan

• LAST MODIFIED: 24 October 2024
• DOI: 10.1093/obo/9780199941728-0156

Introduction

To classify bacteria at the species level, systematists may choose between concepts based in theory versus the theory-free definitions used in the practice and tradition of systematics. Theory-based approaches aim to demarcate species as groups that hold certain species-like, dynamic properties. Following Ernst Mayr, many zoologists have attempted to demarcate their species as cohesive lineages—that is, species are classified so that populations of the same species are hindered from diverging owing to recombination between them. Some bacterial systematists have argued for extending recombination-based demarcation to bacterial species. However, both theoretical and experimental evidence argue that recombination is unlikely to hinder either the splitting of bacterial species or their further divergence, owing to the low frequency of recombination in bacteria, although this conclusion is not universally accepted. Among alternative, dynamic properties ascribed to bacterial species is that each species is ecologically distinct and irreversibly separate from other species; moreover, each species is cohesive in that some force constrains diversification within a species. In the rarely recombining bacteria, this force of cohesion may be natural selection favoring novel adaptive mutations within an ecologically homogeneous group (an ecotype). The cohesive, species-like ecotypes may be recognized as sequence clusters, and many such ecotypes may fit within the more broadly defined species recognized by the traditions of bacterial systematics. Alternatively, a “speciation spectrum” model argues that, depending on the bacterial group, either selection or genetic exchange may be more important in the cohesion of species—here, lineages may be classified by their ability to coexist as a result of some combination of ecological divergence and sexual isolation. Most bacterial systematists defer to theory-free traditions on the quantity of diversity that should be included within a species. As the criteria for discovering and characterizing bacterial taxa have shifted from phenotypes to various sequence and whole-genome characters, systematists have aimed to recalibrate the threshold of divergence within species with one aim—that species should appear as clusters with clear phenotypic and molecular gaps between them. Recent developments suggest that theory-based and tradition-based systematics may be able to reach a rapprochement, in that the traditional species recognized by most systematists as well as the theory-based ecotypes may both be subject to a kind of cohesion. Molecular characterizations of bacterial diversity have shown that systematists will never come close to describing all bacterial species unless radical changes are made in how species can be classified. To characterize and classify all bacterial diversity at all taxonomic levels, from infraspecific ecotypes to species to phyla, systematists will need to streamline classification using genome-based methods.

Overview of Bacterial Species Concepts

Rosselló-Móra and Amann 2015 argues for a theory-free demarcation, whereby species are classified as clusters based on their phenotypic, molecular, and genomic characteristics. The article also contends that the dynamic features of species should be less important for classification than clustering patterns. With the aim of conveniently classifying species to yield clusters, many works by systematists have adopted theory-free, universal, molecular thresholds of divergence for classification from species to phyla, and Parks, et al. 2020 develops a new method utilizing relative evolutionary distance (RED). On the other hand, works by microbial population biologists have focused on defining bacterial species as cohesive units. Bobay 2020 argues for species demarcation according to patterns of genetic exchange and sexual isolation. Cohan 2021 argues for defining species-like ecotypes as lineages of ecologically homogeneous organisms that are subject to cohesion by recurring natural selection events. Shapiro and Polz 2015 argues for discovery of species-like lineages that are ecologically distinct and/or sexually isolated groups that can coexist in the same habitat; it argues for a “speciation spectrum,” where selection and genetic exchange can differ in their effects on species cohesion across bacteria. A similar approach is taken in Achtman and Wagner 2008, in declaring that a species should be a metapopulation lineage that evolves separately from others and has a unique adaptive zone, but the authors are agnostic in not specifying the dynamics underlying divergence within and between species. Doolittle and Zhaxybayeva 2009 argues that, owing to the ubiquity of horizontal genetic transfer of adaptive genes in bacteria, it is pointless to try to find cohesive groups. Cohan 2016 provides an overview of all these approaches to species concepts.

• Achtman, M., and M. Wagner. 2008. Microbial diversity and the genetic nature of microbial species. Nature Reviews Microbiology 6.6: 431–440.

  DOI: 10.1038/nrmicro1872

  The authors’ concept of bacterial species derives from Simpson’s Evolutionary Species Concept: a species is a metapopulation lineage that evolves separately from others and has its own ecological niche. The concept does not include a set of cohesion mechanisms, and the approach does not suggest how to demarcate species in practice.

• Bobay, L. -M. 2020. The prokaryotic species concept and challenges. In The pangenome: Diversity, dynamics and evolution of genomes. Edited by H. Tettelin and D. Medini, 21–49. Cham, Switzerland: Springer International Publishing.

  DOI: 10.1007/978-3-030-38281-0_2

  Bobay previously analyzed the recombination rates within and between bacterial species, and found that recombination rates are much greater within than between species. Here he argues that recombination acts as a force of cohesion within species, and he calls for a conception of species based on recombination rates.

• Cohan, F. M. 2016. Bacterial species concepts. In Encyclopedia of evolutionary biology. Vol. 1. Edited by R. M. Kliman, 119–129. Amsterdam: Academic Press. 1.

  This overview argues for a need to recognize infraspecific, ecologically distinct “ecotype” lineages. Illustrates the dynamics of bacterial speciation with figures.

• Cohan, F. M. 2021. Genomes reveal the cohesiveness of bacterial species taxa and provide a path towards describing all of bacterial diversity. In Trends in the systematics of bacteria and fungi. Edited by P. Bridge, D. Smith, and E. Stackebrandt, 282–300. Wallingford, UK: CAB International.

  Outlines the ecotype model of bacterial species and speciation, where periodic selection recurrently purges the diversity, genome-wide, within ecologically homogeneous ecotypes. Evolution of sexual isolation is argued to have a minimal role in the origin of species, owing to the rarity of recombination.

• Doolittle, W. F., and O. Zhaxybayeva. 2009. On the origin of prokaryotic species. Genome Research 19.5: 744–756.

  DOI: 10.1101/gr.086645.108

  Expresses pessimism toward the prospect of a universal species concept for all prokaryotes. Argues rates of horizontal genetic transfer can be so high that the set of organisms that are ecologically homogeneous may be as small as one bacterium and its daughter.

• Parks, D. H., M. Chuvochina, P. -A. Chaumeil, C. Rinke, A. J. Mussig, and P. Hugenholtz. 2020. A complete domain-to-species taxonomy for bacteria and archaea. Nature Biotechnology 38.9: 1079–1086.

  DOI: 10.1038/s41587-020-0539-7

  Systematists have for decades found divergence thresholds for species demarcation that yield species as clusters. This paper presents an automated approach that demarcates all species by an infraspecific Average Nucleotide Identity at around 95 percent or greater, yielding species as clusters of genome sequence similarity.

• Rosselló-Móra, R., and R. Amann. 2015. Past and future species definitions for bacteria and archaea. Systematic and Applied Microbiology 38.4: 209–216.

  DOI: 10.1016/j.syapm.2015.02.001

  Reviews the species concept that the authors have espoused for decades and that has been followed by most practicing systematists. Argues here that a species should be a monophyletic lineage that is genomically and phenotypically coherent, such that species members share physiological and ideally ecological properties.

• Shapiro, B. J., and M. F. Polz. 2015. Microbial speciation. Cold Spring Harbor Perspectives in Biology 7.10: a018143–a018143.

  DOI: 10.1101/cshperspect.a018143

  Aims to classify closely related, species-like lineages that coexist owing to ecological differences. These lineages show cohesion within them but not between them, owing to both periodic selection and recombination. The disparities among bacteria in ecology, population sizes, and recombination yield a “speciation spectrum” across the bacteria.