The Evolution of the Genus Bacteroides in the House Mouse Species Complex

The mammalian intestinal tract harbors a complex community of microorganisms that share an ancient evolutionary history and establish mutually beneficial relationships with their hosts. Despite inter-individual variation in gut microbial community composition, the major bacterial phyla remain conserved over the time of mammalian evolution. However, much less is known about evolutionary processes in the mammalian gut. Bacteroides are dominant intestinal bacteria and linked to many health-related traits of the host. Despite the importance of this genus, only a few species are well studied. Thus, there is still a lack of information regarding the patterns of within-species diversity across different host species, which could be linked to potential local adaption to different host environments. Using the house mouse species complex as a model, I first aimed to identify potential signatures of differentiation in Bacteroides abundance according to host subspecies. By performing a geographical survey of Mus musculus musculus and M. m. domesticus gut microbiota using 16S rRNA gene sequencing, I found host subspecies to play minor role in gut community structure compared to the impact of geography. Nevertheless, indicator species analysis of the Bacteroides genus identified consistent host subspecies-Bacteroides associations across different geographic locations. Next, I aimed to characterize candidate Bacteroides taxa [strain level amplicon sequence variants (ASVs)] and identify the differences in their genomes that might contribute to bacterial adaptation to the different mouse subspecies. For this, a combination of culturing and genomic analysis methods was used, which yielded fully sequenced genomes of 146 Bacteroides isolates. Taxonomic classification indicates that two potentially new Bacteroides species were isolated, along with B. acidifaciens, B. caecimuris and B. sartorii strains. Furthermore, a perfect match between a candidate indicator Bacteroides ASV, which strongly associates to M. m. musculus, and both unclassified isolates was detected, suggesting the involvement of this potentially new Bacteroides species in the intriguing host-microbe association. Finally, I aimed to identify contact-independent antagonistic interactions between gut-associated Bacteroides strains among these two house mouse subspecies. I found some Bacteroides isolates to engage in antagonistic interactions, and the observed inhibitory interactions seem to occur mostly between isolates belonging to different Bacteroides species (inter-species antagonism) and to different mouse populations than between strains isolated from different host subspecies. In conclusion, the present work is the first study systematically investigating gut-associated Bacteroides among two house mouse subspecies. Strong host-Bacteroides associations were identified to be consistent across different geographic locations. Whole genome sequencing of the isolated strains sheds light on the Bacteroides pan genome in terms of protein content and functions. Moreover, this is the first study identifying antagonistic interactions among mouse-associated B. acidifaciens, B. caecimuris and B. sartorii strains isolated from two host subspecies.


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