Host ecology regulates interspecies recombination in bacteria of the genus Campylobacter.

Evangelos Mourkas,Martin Cj Maiden,Jessica K Calland,Håkan Johansson,Zilia Y Muñoz-Ramirez,Ben Pascoe,Patrik Ellström,Leonardos Mageiros,Sion C Bayliss,Santiago Sandoval-Motta,Samuel K Sheppard,Keith A Jolley,Grant Futcher,Matthew D Hitchings,Koji Yahara,Javier Torres,Guillaume Méric,Jonas Waldenström

doi:10.7554/elife.73552

Abstract

Horizontal gene transfer (HGT) can allow traits that have evolved in one bacterial species to transfer to another. This has potential to rapidly promote new adaptive trajectories such as zoonotic transfer or antimicrobial resistance. However, for this to occur requires gaps to align in barriers to recombination within a given time frame. Chief among these barriers is the physical separation of species with distinct ecologies in separate niches. Within the genus Campylobacter, there are species with divergent ecologies, from rarely isolated single-host specialists to multihost generalist species that are among the most common global causes of human bacterial gastroenteritis. Here, by characterizing these contrasting ecologies, we can quantify HGT among sympatric and allopatric species in natural populations. Analyzing recipient and donor population ancestry among genomes from 30 Campylobacter species, we show that cohabitation in the same host can lead to a six-fold increase in HGT between species. This accounts for up to 30% of all SNPs within a given species and identifies highly recombinogenic genes with functions including host adaptation and antimicrobial resistance. As described in some animal and plant species, ecological factors are a major evolutionary force for speciation in bacteria and changes to the host landscape can promote partial convergence of distinct species through HGT.

Highlights

It is well established that bacteria do not conform to a strict clonal model of reproduction but engage in regular horizontal gene transfer (HGT) [1]
91 Second, because at least 12 species have been identified as human pathogens [29] and C. jejuni and C. coli among the most common global causes of bacterial gastroenteritis [30], large numbers of isolate genomes have been sequenced from potential reservoir hosts as part of public health source tracking programs [31, 32]
Consistent with previous studies, certain species are principally associated with a 300 specific host niche

Summary

Introduction

It is well established that bacteria do not conform to a strict clonal model of reproduction but engage in regular horizontal gene transfer (HGT) [1]. By identifying recombining species pairs within the same and different hosts we can describe interactions where co-localization enhances gene flow, quantify the impact of ecological barriers in these populations and distinguish highly recombinogenic genes that are found in multiple genetic backgrounds. Further evidence of introgression came from pairwise ANI comparison of genus-wide core genes, in all isolates of the 15 major Campylobacter species, to the C. jejuni genome (Figure 3–figure supplement 4b). There was increased recombination in genomes sampled from cattle between C. jejuni CC61 (donor; C. jejuni) and C. fetus and C. hyointestinalis (recipients) with 71.75% of all within-host recombining SNPs from all 10 comparisons detected in these two pairs (Figure 4c–figure supplement 2–3, Supplementary File 4). By considering genes that overcome barriers to interspecies recombination and establish in multiple new genetic backgrounds, it may be possible to infer important phenotypes that allow bacteria to adapt to different hosts and environments

295 Discussion

943 Supplementary

Findings

945 Supplementary