Origins and Evolution of Novel Bacteroides in Captive Apes

Abstract

Bacterial strains evolve in response to the gut environment of their hosts, with genomic changes that influence their interactions with hosts as well as with other members of the gut community. Great apes in captivity have acquired strains of Bacteroides xylanisolvens, which are common within gut microbiome of humans but not typically found other apes, thereby enabling characterization of strain evolution following colonization. Here, we isolate, sequence and reconstruct the history of gene gain and loss events in numerous captive-ape-associated strains since their divergence from their closest human-associated strains. We show that multiple captive-ape-associated B. xylanisolvens lineages have independently acquired gene complexes that encode functions related to host mucin metabolism. Our results support the finding of high genome fluidity in Bacteroides, in that several strains, in moving from humans to captive apes, have rapidly gained large genomic regions that augment metabolic properties not previously present in their relatives. Significance statementChronicling the changes that occur in bacterial genomes after a host-switch event is normally difficult due to age of most bacteria-host associations, which renders uncertainties about the bacterial ancestor (and ancestral genome) prior to colonization of the new host. However, the gut microbiomes of great apes in captivity contain bacterial strains that are unique to humans, allowing fine-scale assessment and reconstruction of the genomic changes that follow colonization. By sequencing and comparing closely related strains of Bacteroides that are restricted both to human and to captive great apes, we found that multiple bacterial lineages convergently acquired sets of genes involved in the metabolism of dietary polysaccharides. These results show that over relatively short timescales, the incorporation of strains into microbiomes involves large-scale genomic events that correspond to characteristics of the new host environment.