The role of recombination, niche‐specific gene pools and flexible genomes in the ecological speciation of bacteria

Abstract

Bacteria diversify into genetic clusters analogous to those observed in sexual eukaryotes, but the definition of bacterial species is an ongoing problem. Recent work has focused on adaptation to distinct ecological niches as the main driver of clustering, but there remains debate about the role of recombination in that process. One view is that homologous recombination occurs too rarely for gene flow to constrain divergent selection. Another view is that homologous recombination is frequent enough in many bacterial populations that barriers to gene flow are needed to permit divergence. Niche‐specific gene pools have been proposed as a general mechanism to limit gene flow. We use theoretical models to evaluate additional hypotheses that evolving genetic architecture, specifically the effect sizes of genes and gene gain and loss, can limit gene flow between diverging populations. Our model predicts that (a) in the presence of gene flow and recombination, ecological divergence is concentrated in few loci of large effect and (b) high rates of gene flow plus recombination promote gene loss and favor the evolution of niche‐specific genes. The results show that changing genetic architecture and gene loss can facilitate ecological divergence, even without niche‐specific gene pools. We discuss these results in the context of recent studies of sympatric divergence in microbes.

A drift‐barrier model drives the genomic landscape of a structured bacterial population

“…For instance, in ISL2, two COGs shared by all subpopulations and subject to strong selective constraints (means d N /d S < 0.19) were related to phosphonate utilization, which could suggest adaptation to low‐phosphate environments (Feingersch et al., 2012). Recently, Schmutzer and Barraclough (2019) suggested that, in the presence of gene fluxes among diverging populations, the concentration of locally adapted genes in a reduced number of loci could be favoured, as it would (a) reduce the negative impact of insertions along the genome of horizontally transferred genes; and (b) increase the relative efficacy of selection on a few “mega” loci compared to many dispersed loci of reduced effect. Thus, ISL1, ISL2 and ISL2.1 might concentrate “flexible” genes that are essential for all these clades.…”

Speciation across the Tree of Life

“…Much literature on bacterial speciation has addressed how barriers to recombination could drive bacterial speciation (e.g. Fraser et al ., 2007; Polz et al ., 2013; Schmutzer & Barraclough, 2019). Most importantly, recombination seems to decrease in frequency with greater genetic divergence between individuals (e.g.…”

“…Vulic, Lenski & Radman, 1999). Simulations suggest that reduced recombination may be important in those clades with relatively high recombination rates (Schmutzer & Barraclough, 2019). However, this mechanism may not apply to prokaryotic lineages that have little or no homologous recombination, including archaeans and many bacterial species (e.g.…”

Exploring the mobilome and resistome of Enterococcus faecium in a One Health context across two continents

“…Cohan & Perry hypothesized that periodic selective sweeps reduce genetic variation between the genomes of organisms specialized to certain ecological niches, increasing the differences between these ecotypes and the rest of the named species [69]. However, other authors emphasize the role of recombination in bacterial divergence which allows for gene-specific sweeps [70].…”