The Evolution of Host Specialization in the Vertebrate Gut Symbiont Lactobacillus reuteri

Abstract

Recent research has provided mechanistic insight into the important contributions of the gut microbiota to vertebrate biology, but questions remain about the evolutionary processes that have shaped this symbiosis. In the present study, we showed in experiments with gnotobiotic mice that the evolution of Lactobacillus reuteri with rodents resulted in the emergence of host specialization. To identify genomic events marking adaptations to the murine host, we compared the genome of the rodent isolate L. reuteri 100-23 with that of the human isolate L. reuteri F275, and we identified hundreds of genes that were specific to each strain. In order to differentiate true host-specific genome content from strain-level differences, comparative genome hybridizations were performed to query 57 L. reuteri strains originating from six different vertebrate hosts in combination with genome sequence comparisons of nine strains encompassing five phylogenetic lineages of the species. This approach revealed that rodent strains, although showing a high degree of genomic plasticity, possessed a specific genome inventory that was rare or absent in strains from other vertebrate hosts. The distinct genome content of L. reuteri lineages reflected the niche characteristics in the gastrointestinal tracts of their respective hosts, and inactivation of seven out of eight representative rodent-specific genes in L. reuteri 100-23 resulted in impaired ecological performance in the gut of mice. The comparative genomic analyses suggested fundamentally different trends of genome evolution in rodent and human L. reuteri populations, with the former possessing a large and adaptable pan-genome while the latter being subjected to a process of reductive evolution. In conclusion, this study provided experimental evidence and a molecular basis for the evolution of host specificity in a vertebrate gut symbiont, and it identified genomic events that have shaped this process.

The inconstant gut microbiota of Drosophila species revealed by 16S rRNA gene analysis

“…In this respect, Drosophila appears to parallel mammals, for which no phylogenetic pattern in the composition of the gut microbiota has been found (Ley et al, 2008a;Muegge et al, 2011). Our results differ from the evidence for congruence between host phylogeny and gut microbiota composition obtained, for example, for bacterial community composition in laboratory cultures of jewel wasps Nasonia (Brucker and Bordenstein, 2012), and wild populations of both great apes/humans and termites (Hongoh et al, 2005); and the genotypes of one bacterial species, Lactobacillus reuteri, in studies that included inbred lab mice and rats (Oh et al, 2010;Frese et al, 2011). An important issue for future work is the ecological factors that dictate the variation in the congruence of host-microbiota phylogenies across different animal groups.…”

Induction of farnesoid X receptor signaling in germ-free mice colonized with a human microbiota

“…of the donor sample is more preserved when transferred to a recipient of the same species. Previous studies have shown that bacterial species (e.g., Lactobacillus reuteri) can have subpopulations with strong host specificity and a gene content reflecting the niche characteristics for the specific hosts (29). This phenomenon might explain why Clostridiales from human feces colonize mice in lower abundance than Clostridiales with mouse origin.…”

Microbial Reprogramming Inhibits Western Diet-Associated Obesity

“…However, in separate epidemiological studies, the presence of L. reuteri in human guts has been associated with obesity [48][49]. Whether this discrepancy reflects the wide genomic variation of L. reuteri strains or differences [50] in hostmicrobial interactions warrants further investigation. A healthprotective role for L. reuteri in host metabolism, as displayed in the present study, offers mutually beneficial gut symbiont-host relationship and co-evolution [51].…”