Recombination Does Not Hinder Formation or Detection of Ecological Species of Synechococcus Inhabiting a Hot Spring Cyanobacterial Mat

Abstract

Recent studies of bacterial speciation have claimed to support the biological species concept—that reduced recombination is required for bacterial populations to diverge into species. This conclusion has been reached from the discovery that ecologically distinct clades show lower rates of recombination than that which occurs among closest relatives. However, these previous studies did not attempt to determine whether the more-rapidly recombining close relatives within the clades studied may also have diversified ecologically, without benefit of sexual isolation. Here we have measured the impact of recombination on ecological diversification within and between two ecologically distinct clades (A and B') of Synechococcus in a hot spring microbial mat in Yellowstone National Park, using a cultivation-free, multi-locus approach. Bacterial artificial chromosome (BAC) libraries were constructed from mat samples collected at 60°C and 65°C. Analysis of multiple linked loci near Synechococcus 16S rRNA genes showed little evidence of recombination between the A and B' lineages, but a record of recombination was apparent within each lineage. Recombination and mutation rates within each lineage were of similar magnitude, but recombination had a somewhat greater impact on sequence diversity than mutation, as also seen in many other bacteria and archaea. Despite recombination within the A and B' lineages, there was evidence of ecological diversification within each lineage. The algorithm Ecotype Simulation identified sequence clusters consistent with ecologically distinct populations (ecotypes), and several hypothesized ecotypes were distinct in their habitat associations and in their adaptations to different microenvironments. We conclude that sexual isolation is more likely to follow ecological divergence than to precede it. Thus, an ecology-based model of speciation appears more appropriate than the biological species concept for bacterial and archaeal diversification.

Transmission in the Origins of Bacterial Diversity, From Ecotypes to Phyla

“…They concluded that the higher rates of recombination within the clades prevented ecological diversification. However, these studies did not actually attempt to determine whether the more rapidly recombining close relatives within the clades may have diversified ecologically, without the benefit of sexual isolation (44). My colleagues and I recently investigated, in hot spring Synechococcus, the possibility of ecological diversification among extremely close relatives that were not sexually isolated, and we found that the highest rates of recombination within clades did not prevent their ecological diversification (44).…”

“…However, these studies did not actually attempt to determine whether the more rapidly recombining close relatives within the clades may have diversified ecologically, without the benefit of sexual isolation (44). My colleagues and I recently investigated, in hot spring Synechococcus, the possibility of ecological diversification among extremely close relatives that were not sexually isolated, and we found that the highest rates of recombination within clades did not prevent their ecological diversification (44). Where it has been investigated in bacteria, an absence of sexual isolation has not precluded ecological diversification among closest relatives (45).…”

Genomic Inference of Recombination-Mediated Evolution in Xanthomonas euvesicatoria and X. perforans

“…One view is that genetic exchange rarely hinders genetic divergence in bacterial populations (56). Rather, recombination fosters the acquisition of novel genes and operons that aid in adaptation, thereby promoting divergence (5,57). A competing hypothesis suggests that recombination is a cohesive force that prevents bacterial diversification and maintains lineages by homogenizing populations (57,58).…”

“…H omologous and nonhomologous recombination are major drivers of evolution in bacterial populations (1)(2)(3)(4)(5). Horizontal gene transfer (HGT; also called nonhomologous recombination or lateral gene transfer) occurs between and within species (6).…”

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

“…It is also consistent with observed reductions of HR between ecologically distinct species (Polz et al ). Melendrez et al () also found that gene‐specific selective sweeps occur within ecologically divergent species of Synechococcus , but in rebuttal of this hypothesis, they argued that separate gene pools were a consequence of ecological divergence rather than a cause. In theory, strong enough selection against recombinant genotypes could permit divergence even without niche‐specific gene flow at the outset (Bürger, ; Gavrilets, ).…”