Recombination and the Species Structure of the Genus Bacteroides

Bacteroides play prominent roles in maintaining gut homeostasis through the fermentation of dietary carbohydrates, the production of metabolites, and the regulation of host immune response. The genus Bacteroides comprises several dozen named species, several of which serve as a nexus of gene exchange in gut microbiomes, especially in humans. Because gene exchange will blur the historically defined species boundaries, we assessed the patterns and extent of recombination for nearly 2,000 fully sequenced Bacteroides genomes representing 36 named species, and redefined species boundaries based on their capacity to exchange genes. We recognized numerous incongruences between traditional classification schemes, those based on nucleotide sequence identity thresholds, and species defined by gene flow. Almost all named species of sufficient sample size for analysis included genomes that failed to recombine with other genomes that were historically assigned to the same species. Such misclassifications occurred even for cases in which sequence identities surpassed the thresholds regularly used to define species. Conversely, we detected instances in which species previously considered distinct were found to recombine extensively--the most striking of which supported unification of B. kribbi, B. koreensis, and B. ovatus (which freely recombines with B. xylanisolvens). Among the broadly distributed populations of B. fragilis, we detected elevated levels of recombination among human-derived strains, although this result is confounded by geographic and sampling biases. Our findings emphasize the utility of a universal species concept based on gene flow, not only for refining bacterial classifications but also for understanding the variation within and across gut microbiomes. IMPORTANCE STATEMENTBacteroides is a diverse genus comprising some of the most pervasive taxa in the mammalian gut microbiome, with several species playing key roles in the maintenance of gut ecosystem stability. The propensity for Bacteroides to exchange genes, both within and among species, has eluded efforts to understand its diversity and to delineate species boundaries, both by traditional classification schemes as well as methods that rely on genomic sequence identity. To circumvent these obstacles and to circumscribe species in a manner that can be uniformly applied across lifeforms, we analyzed all complete genomes assigned to Bacteroides and reclassified them based on their capacity for gene flow, uncovering numerous inconsistencies with both recent and historical classifications. Our approach offers a biologically grounded alternative to the use of sequence identity thresholds, offering a better understanding of the diversity and relationships among genomes within the genus Bacteroides at large.