The evolution of ecological facilitation within mixed-species biofilms in the mouse gastrointestinal tract.

Xiaoxi B Lin,Wei Wu,Jens Walter,Liz A Cody,Jukka Corander,Jun Wang,Sarah C L Knowles,Robert Schmaltz,Theodore Grenier,Laima Baltrūnaitė,Stephanie Tollenaar,Paul Stothard,John F Baines,Guergana Tasseva,Amanda E Ramer-Tait,Tuo Wang

doi:10.1038/s41396-018-0211-0

Abstract

The eco-evolutionary interactions among members of the vertebrate gut microbiota that ultimately result in host-specific communities are poorly understood. Here we show that Lactobacillus reuteri coexists with speciesthat belong tothe Lactobacillus johnsonii cluster (L. johnsonii, L. gasseri, and L taiwanensis) in a taxonomically wide range of rodents, suggesting cohabitation over evolutionary times. The two dominant Lactobacillus species found in wild mice establish a commensalistic relationship in gastric biofilms when introduced together into germ-free mice in which L. reuteri facilitates colonization of L. taiwanensis. Genomic analysis revealed allopatric diversification in strains of both species that originated from geographically separated locations (Scotland and France). Allopatry of the strains resulted in reduced formation of mixed biofilms in vitro, indicating that interspecies interactions in gastric Lactobacillus-biofilms are the result of an adaptive evolutionary process that occurred in a biogeographical context. In summary, these findings suggest that members within the vertebrate gut microbiota can evolve inter-dependencies through ecological facilitation, which could represent one mechanism by which host-specific bacterial communities assemble across vertebrate species andan explanation for their spatial and biogeographic patterns.

Highlights

Our research has provided clear evidence for a persistent and specific evolution of L. reuteri with rodent hosts and the mechanisms by which host specificity is established, nothing is yet known about how this species evolves in the context of the bacterial communities in which it exists in nature
The cultivable Lactobacillus population was dominated by L. reuteri and species related to L. johnsonii (L. johnsonii-like), such as L. rodentium [23] and species that cannot be differentiated from L. johnsonii based on 16S rRNA sequences, e.g., L. taiwanensis and L. gasseri [24]
Neither L. johnsonii nor L. reuteri was isolated from shrews (Fig. 1a and Table 1), which are small mammals belonging to the order Eulipotyphla, suggesting the important role of host phylogeny in these symbiont relationships

Summary

Introduction

We have established the species Lactobacillus reuteri as a model to study the evolution of a gut symbiont and the consequences of its symbiosis with the vertebrate host [9]. This species can be divided into several phylogenetic clades that correlate with host origin [10] and whose genome content reflects niche characteristics in respective hosts [11]. Our research has provided clear evidence for a persistent and specific evolution of L. reuteri with rodent hosts and the mechanisms by which host specificity is established, nothing is yet known about how this species evolves in the context of the bacterial communities in which it exists in nature

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