A genus definition for Bacteria and Archaea based on genome relatedness and taxonomic affiliation.

Abstract

Genus assignment is fundamental in the characterization of microbes, yet there is currently no unambiguous way to demarcate genera solely using standard genomic relatedness indices. Here, we propose an approach to demarcate genera that relies on the combined use of the average nucleotide identity, genome alignment fraction, and the distinction between type species and non-type species. More than 750 genomes representing type strains of species from 10 different phyla, and 19 different taxonomic orders/families in Gram-positive/negative, bacterial and archaeal lineages were tested. Overall, all 19 analyzed taxa conserved significant genomic differences between members of a genus and type species of other genera in the same taxonomic family. Bacillus, Flavobacterium, Hydrogenovibrio, Lactococcus, Methanosarcina, Thiomicrorhabdus, Thiomicrospira, Shewanella, and Vibrio are discussed in detail. Less than 1% of the type strains analyzed need reclassification, highlighting that the adoption of the 16S rRNA gene as a taxonomic marker has provided consistency to the classification of microorganisms in recent decades. One exception to this is the genus Bacillus with 61% of type strains needing reclassification, including the human pathogens B. cereus and B. anthracis. The results provide a first line of evidence that the combination of genomic indices provides appropriate resolution to effectively demarcate genera within the current taxonomic framework that is based on the 16S rRNA gene. We also identify the emergence of natural breakpoints at the genome level that can further help in the circumscription of genera. Altogether, these results show that a distinct difference between distant relatives and close relatives at the genome level (i.e., genomic coherence) is an emergent property of genera in Bacteria and Archaea.