The bacterial species dilemma and the genomic-phylogenetic species concept

Abstract

The number of species of Bacteria and Archaea (ca 5000) is surprisingly small considering their early evolution, genetic diversity and residence in all ecosystems. The bacterial species definition accounts in part for the small number of named species. The primary procedures required to identify new species of Bacteria and Archaea are DNA-DNA hybridization and phenotypic characterization. Recently, 16S rRNA gene sequencing and phylogenetic analysis have been applied to bacterial taxonomy. Although 16S phylogeny is arguably excellent for classification of Bacteria and Archaea from the Domain level down to the family or genus, it lacks resolution below that level. Newer approaches, including multilocus sequence analysis, and genome sequence and microarray analyses, promise to provide necessary information to better understand bacterial speciation. Indeed, recent data using these approaches, while meagre, support the view that speciation processes may occur at the subspecies level within ecological niches (ecovars) and owing to biogeography (geovars). A major dilemma for bacterial taxonomists is how to incorporate this new information into the present hierarchical system for classification of Bacteria and Archaea without causing undesirable confusion and contention. This author proposes the genomic-phylogenetic species concept (GPSC) for the taxonomy of prokaryotes. The aim is twofold. First, the GPSC would provide a conceptual and testable framework for bacterial taxonomy. Second, the GPSC would replace the burdensome requirement for DNA hybridization presently needed to describe new species. Furthermore, the GPSC is consistent with the present treatment at higher taxonomic levels.

Figure 1

A phase photomicrograph showing a strain of the mammalian oral bacterium, Simonsiella. Note the filamentous cells and dorsal–ventral asymmetry. Cell diameter is about 2 μm.

Figure 2

A 16S rDNA tree of Simonsiella strains from four different mammalian species, human, sheep, cat and dog. Note that the four strains from each animal host form clades and there is a pattern typical of coevolution illustrated with the evolution of the animal hosts. See text for details on the phylogeny. Courtesy of Brian Hedlund.