Gene flow and introgression are pervasive forces shaping the evolution of bacterial species

Abstract

Background Although originally thought to evolve clonally, studies have revealed that most bacteria exchange DNA. However, it remains unclear to what extent gene flow shapes the evolution of bacterial genomes and maintains the cohesion of species. Results Here, we analyze the patterns of gene flow within and between >2600 bacterial species. Our results show that fewer than 10% of bacterial species are truly clonal, indicating that purely asexual species are rare in nature. We further demonstrate that the taxonomic criterion of ~95% genome sequence identity routinely used to define bacterial species does not accurately represent a level of divergence that imposes an effective barrier to gene flow across bacterial species. Interruption of gene flow can occur at various sequence identities across lineages, generally from 90 to 98% genome identity. This likely explains why a ~95% genome sequence identity threshold has empirically been judged as a good approximation to define bacterial species. Our results support a universal mechanism where the availability of identical genomic DNA segments required to initiate homologous recombination is the primary determinant of gene flow and species boundaries in bacteria. We show that these barriers of gene flow remain porous since many distinct species maintain some level of gene flow, similar to introgression in sexual organisms. Conclusions Overall, bacterial evolution and speciation are likely shaped by similar forces driving the evolution of sexual organisms. Our findings support a model where the interruption of gene flow—although not necessarily the initial cause of speciation—leads to the establishment of permanent and irreversible species borders.

Introgression impacts the evolution of bacteria, but species borders are rarely fuzzy

“…Gene flow is pervasive between closely related genomes of most species and rarely occurs between genomes showing more than 2 to 10% nucleotide divergence 12 . This restriction is thought to reflect the mechanistic constraints of the homologous recombination machinery, which requires the presence of stretches of identical nucleotides shared between the recipient strand and the incoming strand 31 .…”

“…Average of % of introgressed core genes among species across genera Genus similar principles as in the Biological Species Concept (i.e., BSC-species) 12 . Therefore, the levels of introgression estimated above may be inflated by the inaccurate identification of species borders (i.e., if two ANI-species may in fact represent a single BSC-species).…”

“…This restriction is thought to reflect the mechanistic constraints of the homologous recombination machinery, which requires the presence of stretches of identical nucleotides shared between the recipient strand and the incoming strand 31 . However, gene flow can occasionally occur between more distantly related genomes 12,22,24,32,33 . Such patterns were clearly detailed in a study comparing Campylobacter coli and Campylobacter jejuni , where a substantial portion (∼20%) of the genome of these two species appears to be engaging in gene flow, while the rest of the genome is substantially diverged (∼85% sequence identity) 33 .…”

“…Because bacteria are asexual organisms, they do not easily adhere to the species concepts developed for sexual organisms, i.e., the Biological Species Concept (BSC) and related definitions 4,5 . However, a growing body of evidence is supporting the idea that the vast majority of bacteria do engage in gene flow and that the BSC may be applicable to these organisms [6][7][8][9][10][11][12] . Through diverse routes and vessels, bacterial cells are capable of exchanging genetic material and the transferred DNA may be related enough to sequences of the recipient genome to be swapped through homologous recombination.…”

“…In contrast, HGT can lead to the gain of new genes previously absent in the recipient genome and can occur between more distantly related-or unrelated-sequences [13][14][15] . For the purpose of species definition, we and others have focused primarily on the patterns of gene flow (i.e., homologous recombination) as a force maintaining the genetic cohesiveness of bacterial species 8,10,12,16,17 . However, gene flow can also have the opposite effect: blurring species boundaries.Earlier studies relying on multi-locus sequence typing (MLST) first observed clear discrepancies across sequence markers while attempting to classify and type bacterial strains of several lineages [18][19][20][21][22][23] .…”