Inference of Convergent Gene Acquisition Among Pseudomonas syringae Strains Isolated From Watermelon, Cantaloupe, and Squash

Abstract

Pseudomonas syringae sensu stricto (phylogroup 2; referred to as P. syringae ) consists of an environmentally ubiquitous bacterial population associated with diseases of numerous plant species. Recent studies using multilocus sequence analysis have indicated the clonal expansion of several P. syringae lineages, located in phylogroups 2a and 2b, in association with outbreaks of bacterial spot disease of watermelon, cantaloupe, and squash in the United States. To investigate the evolutionary processes that led to the emergence of these epidemic lineages, we sequenced the genomes of six P. syringae strains that were isolated from cucurbits grown in the United States, Europe, and China over a period of more than a decade, as well as eight strains that were isolated from watermelon and squash grown in six different Florida counties during the 2013 and 2014 seasons. These data were subjected to comparative analyses along with 42 previously sequenced genomes of P. syringae stains collected from diverse plant species and environments available from GenBank. Maximum likelihood reconstruction of the P. syringae core genome revealed the presence of a hybrid phylogenetic group, comprised of cucurbit strains collected in Florida, Italy, Serbia, and France, which emerged through genome-wide homologous recombination between phylogroups 2a and 2b. Functional analysis of the recombinant core genome showed that pathways involved in the ATP-dependent transport and metabolism of amino acids, bacterial motility, and secretion systems were enriched for recombination. A survey of described virulence factors indicated the convergent acquisition of several accessory type 3 secreted effectors (T3SEs) among phylogenetically distinct lineages through integrative and conjugative element and plasmid loci. Finally, pathogenicity assays on watermelon and squash showed qualitative differences in virulence between strains of the same clonal lineage, which correlated with T3SEs acquired through various mechanisms of horizontal gene transfer (HGT). This study provides novel insights into the interplay of homologous recombination and HGT toward pathogen emergence and highlights the dynamic nature of P. syringae sensu lato genomes.

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“…Biological diversity within an ST (two strains of X. fastidiosa subsp. multiplex ST7 were shown to have different host ranges under experimental conditions) was recently demonstrated on X. fastidiosa (Nunney et al, 2019) and this is generally observed for other bacterial pathogens (Jaureguy et al, 2008;Nicolas-Chanoine et al, 2014;Newberry et al, 2019). In addition, generation of novel strains with specific host range has been evidenced for X. fastidiosa (Nunney et al, 2014b).…”

Cherry picking by pseudomonads: After a century of research on canker, genomics provides insights into the evolution of pathogenicity towards stone fruits

“…It forms a REG with HopC1 in P. syringae pv. tomato DC3000 during Arabidopsis infection (Wei et al, 2007), indicating a similar role in virulence, and is often clustered with this effector physically on the genome (Baltrus et al, 2012;Newberry et al, 2019). Although the four highlighted effectors appear to have important roles in virulence, further functional characterization is required to support the in silico predictions.…”

“…A host specificity study on cucurbits showed remarkable variation in the virulence of phylogroup 2 strains on two different host species (Newberry et al, 2019), which was postulated to be due to differences in effector repertoires. Another study by Rezaei and Taghavi (2014)…”

“…For example, the hopH1 gene is within 10 kb of other effector genes such as hopF4 in Psm R2 (on a putative integrative conjugative element, ICE) and a disrupted copy of the hopAW1 gene in Pss (Hulin et al, 2018a). Interestingly, Newberry et al (2019)…”

“…syringae that infect a common host and identified genomic signatures of host specificity Newberry et al (2019). used pangenomic analysis of curcubit strains across phylogroup 2, and hypothesized that the T3Es HopC1, HopH1, and HopAR1 may serve as negative pathogenicity factors in cucurbits, whilst HopZ5 may be important for pathogenicity due to its convergent gain across two clades of phylogroup 2.…”