Diversification of the gut symbiont Lactobacillus reuteri as a result of host-driven evolution

Abstract

The vertebrate digestive tract, including that of humans, is the habitat to trillions of bacteria that are of significant importance to host biology and health. Although these communities are often postulated to have coevolved with their hosts, evidence is lacking, yet critical for our understanding of microbial symbiosis in vertebrates. To gain insight into the evolution of a gut symbiont, we have characterized the population genetic structure and phylogeny of Lactobacillus reuteri strains isolated from six different host species (human, mouse, rat, pig, chicken and turkey) using Amplified-Fragment Length Polymorphism (AFLP) and Multi-Locus Sequence Analysis (MLSA). The results revealed considerable genetic heterogeneity within the L. reuteri population and distinct monophyletic clades reflecting host origin but not provenance. The evolutionary patterns detected indicate a long-term association of L. reuteri lineages with particular vertebrate species and hostdriven diversification. Results from a competition experiment in a gnotobiotic mouse model revealed that rodent isolates showed elevated ecological performance, indicating that evolution of L. reuteri lineages was adaptive. These findings provide evidence that some vertebrate gut microbes are not promiscuous, but have diversified into host-adapted lineages by a long-term evolutionary process, allowing the development of a highly specialized symbiosis.

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.…”

Host-microbial symbiosis in the vertebrate gastrointestinal tract and the Lactobacillus reuteri paradigm

“…However, the population structure also indicates that evolution was not specific to the host genus, because isolates from rodents (mice and rats) and poultry (chickens and turkeys) form joint clades. This suggests that L. reuteri lineages evolved with groups of related vertebrates and occasional horizontal transfer between these hosts (68). The population genetic analysis indicates that L. reuteri employs a markedly different lifestyle and adaptive strategy than commensal E. coli.…”

“…Host specialization is indeed reflected by the phenotypic characteristics of strains. Several experiments in animals showed that indigenous strains of L. reuteri outperform exogenous strains when competing in the gastrointestinal tract (63,(68)(69)(70)(71). Furthermore, the ability of L. reuteri strains to adhere to epithelia and epithelial cells in the proximal gut is to a large degree host-specific (53,54,72).…”

“…Sticking Together: Evolution of L. reuteri with Its Host To gain insight into the evolution of L. reuteri, we have recently characterized the population genetic structure and phylogeny of strains isolated from six different hosts (human, mouse, rat, pig, chicken, and turkey) from global geographic locations (68). Although the 16S rRNA genes of the isolates used in the study were >99% identical, there was considerable genetic heterogeneity within the L. reuteri population that could be resolved by amplified fragment length polymorphism and MLSA.…”

Evaluation of bifidobacterial adhesion to acidic sugar chains of porcine colonic mucins

“…31) On the other hand, the adhesion properties of probiotic bacteria to mucus are thought to be more dependent on the strain than on the host. 32,33) Our results showed no clear correlation between the host of origin of the bifidobacteria and the origin of the mucin.…”