Taxonomy of Rhizobiaceae revisited: proposal of a new framework for genus delimitation

The alphaproteobacterial family Rhizobiaceae is highly diverse, with 168 species with validly published names classified into 17 genera with validly published names. Most named genera in this family are delineated based on genomic relatedness and phylogenetic relationships, but some historically named genera show inconsistent distribution and phylogenetic breadth. The most problematic is Rhizobium, which is notorious for being highly paraphyletic, as most newly described species in the family are assigned to this genus without consideration of their proximity to existing genera, or the need to create novel genera. Moreover, many Rhizobiaceae genera lack synapomorphic traits that would give them biological and ecological significance. We propose a common framework for genus delimitation within the family Rhizobiaceae, wherein genera are defined as monophyletic groups in a core-genome gene phylogeny, that are separated from related species using a pairwise core-proteome average amino acid identity (cpAAI) threshold of approximately 86%. We further propose that additional genomic or phenotypic evidence can justify division of species into separate genera even if they share greater than 86% cpAAI. Applying this framework, we propose to reclassify Rhizobium rhizosphaerae and Rhizobium oryzae into Xaviernesmea gen. nov. Data is also provided to support the formation of Peteryoungia aggregata comb. nov., Endobacterium yantingense comb. nov., Neorhizobium petrolearium comb. nov., Pararhizobium arenae comb. nov., Pseudorhizobium tarimense comb. nov. and Mycoplana azooxidifex comb. nov. Lastly, we present arguments that the unification of the genera Ensifer and Sinorhizobium in Opinion 84 of the Judicial Commission is no longer justified by current genomic and phenotypic data. Despite pairwise cpAAI values for all Ensifer species and all Sinorhizobium species being >86%, additional genomic and phenotypic data suggest that they significantly differ in their biology and ecology. We therefore propose emended descriptions of Ensifer and Sinorhizobium, which we argue should be considered as separate genera.