Recombination of ecologically and evolutionarily significant loci maintains genetic cohesion in the Pseudomonas syringae species complex

Abstract

BackgroundPseudomonas syringae is a highly diverse bacterial species complex capable of causing a wide range of serious diseases on numerous agronomically important crops. We examine the evolutionary relationships of 391 agricultural and environmental strains using whole-genome sequencing and evolutionary genomic analyses.ResultsWe describe the phylogenetic distribution of all 77,728 orthologous gene families in the pan-genome, reconstruct the core genome phylogeny using the 2410 core genes, hierarchically cluster the accessory genome, identify the diversity and distribution of type III secretion systems and their effectors, predict ecologically and evolutionary relevant loci, and establish the molecular evolutionary processes operating on gene families. Phylogenetic and recombination analyses reveals that the species complex is subdivided into primary and secondary phylogroups, with the former primarily comprised of agricultural isolates, including all of the well-studied P. syringae strains. In contrast, the secondary phylogroups include numerous environmental isolates. These phylogroups also have levels of genetic diversity typically found among distinct species. An analysis of rates of recombination within and between phylogroups revealed a higher rate of recombination within primary phylogroups than between primary and secondary phylogroups. We also find that “ecologically significant” virulence-associated loci and “evolutionarily significant” loci under positive selection are over-represented among loci that undergo inter-phylogroup genetic exchange.ConclusionsWhile inter-phylogroup recombination occurs relatively rarely, it is an important force maintaining the genetic cohesion of the species complex, particularly among primary phylogroup strains. This level of genetic cohesion, and the shared plant-associated niche, argues for considering the primary phylogroups as a single biological species.Electronic supplementary materialThe online version of this article (10.1186/s13059-018-1606-y) contains supplementary material, which is available to authorized users.

Arabidopsis thaliana and Pseudomonas Pathogens Exhibit Stable Associations over Evolutionary Timescales

“…Only one gene for an effector homolog was broadly conserved across OTU5, avrE . It was shared with other P. syringae type isolates ( Dillion et al., 2017 ), but found rarely outside this group. avrE encodes an effector that leads to increased humidity of the extracellular environment inside the plant, the apoplast ( Xin et al., 2016 ).…”

Recently emerged and diverse lineages of Xanthomonas perforans have independently evolved through plasmid acquisition and homologous recombination originating from multiple Xanthomonas species

“…In the absence of barriers such as adaptive incompatibility, related bacterial lineages are expected to display evidence of admixture in their evolutionary history when they inhabit overlapping environmental niches (4). Therefore, patterns of recombination are hypothesized to reflect a corresponding microbial ecology and maintain the cohesion of various bacterial species as monophyletic groups (5). In contrast to many genera of plant-pathogenic bacteria including Pseudomonas , Ralstonia , and Burkholderia , among others which are abundant in multiple environments including water and soil, the life history of Xanthomonas spp.…”

A complete genome sequence for Pseudomonas syringae pv. pisi PP1 highlights the importance of multiple modes of horizontal gene transfer during phytopathogen evolution

“…Recent years and many draft genomes have provided a much needed comparative genomic framework for understanding phytopathogen evolution(Baltrus et al ., ; Dillon et al ., ). Such studies have clearly demonstrated that rapid evolution of bacterial phytopathogens relies heavily on recombination and horizontal gene transfer of virulence factors.…”

“…Pseudomonas syringae phylogroup 2 strains can be isolated as pathogens from a range of different host plants, are found relatively often during sampling of host plants in the absence of disease as well as from other environmental sources and overall harbour a reduced set of type III effectors compared to other P. syringae phylogroups (Baltrus et al ., , ; Dillon et al ., ). This lack of effectors is correlated with the presence of phytotoxins such as syringolin, syringomycin and syringopeptin, which are conserved widely throughout this phylogroup (Dillon et al ., ). Correlations between phytotoxin acquisition and effector loss have sparked the idea that phytotoxins could be carrying out virulence functions that render effectors useless, either through phenotypic redundancy during infection or through alterations in ecological mechanisms of virulence (Baltrus et al ., ; Hockett et al ., ).…”