Inference of convergent gene acquisition among Pseudomonas syringae strains isolated from watermelon, cantaloupe, and squash

Eric A. Newberry, Mohamed Ebrahim, Sujan Timilsina, Nevena Zlatković, Aleksa Obradović, Carolee Theresa Bull, Erica M. Goss, Jose C. Huguet-Tapia, Mathews L. Paret, Jeffrey B. Jones, Neha Potnis

Research output: Contribution to journalArticle

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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.

Original languageEnglish (US)
Article number270
JournalFrontiers in Microbiology
Volume10
Issue numberFEB
DOIs
StatePublished - Jan 1 2019

Fingerprint

Cucumis melo
Citrullus
Pseudomonas syringae
Cucurbita
Genome
Genes
Horizontal Gene Transfer
Homologous Recombination
Bacterial Secretion Systems
Virulence
Serbia
Plant Diseases
Multilocus Sequence Typing
Nucleic Acid Databases
Virulence Factors
Italy
Genetic Recombination
France
Disease Outbreaks
China

All Science Journal Classification (ASJC) codes

  • Microbiology
  • Microbiology (medical)

Cite this

Newberry, Eric A. ; Ebrahim, Mohamed ; Timilsina, Sujan ; Zlatković, Nevena ; Obradović, Aleksa ; Bull, Carolee Theresa ; Goss, Erica M. ; Huguet-Tapia, Jose C. ; Paret, Mathews L. ; Jones, Jeffrey B. ; Potnis, Neha. / Inference of convergent gene acquisition among Pseudomonas syringae strains isolated from watermelon, cantaloupe, and squash. In: Frontiers in Microbiology. 2019 ; Vol. 10, No. FEB.
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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.",
author = "Newberry, {Eric A.} and Mohamed Ebrahim and Sujan Timilsina and Nevena Zlatković and Aleksa Obradović and Bull, {Carolee Theresa} and Goss, {Erica M.} and Huguet-Tapia, {Jose C.} and Paret, {Mathews L.} and Jones, {Jeffrey B.} and Neha Potnis",
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Newberry, EA, Ebrahim, M, Timilsina, S, Zlatković, N, Obradović, A, Bull, CT, Goss, EM, Huguet-Tapia, JC, Paret, ML, Jones, JB & Potnis, N 2019, 'Inference of convergent gene acquisition among Pseudomonas syringae strains isolated from watermelon, cantaloupe, and squash' Frontiers in Microbiology, vol. 10, no. FEB, 270. https://doi.org/10.3389/fmicb.2019.00270

Inference of convergent gene acquisition among Pseudomonas syringae strains isolated from watermelon, cantaloupe, and squash. / Newberry, Eric A.; Ebrahim, Mohamed; Timilsina, Sujan; Zlatković, Nevena; Obradović, Aleksa; Bull, Carolee Theresa; Goss, Erica M.; Huguet-Tapia, Jose C.; Paret, Mathews L.; Jones, Jeffrey B.; Potnis, Neha.

In: Frontiers in Microbiology, Vol. 10, No. FEB, 270, 01.01.2019.

Research output: Contribution to journalArticle

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T1 - Inference of convergent gene acquisition among Pseudomonas syringae strains isolated from watermelon, cantaloupe, and squash

AU - Newberry, Eric A.

AU - Ebrahim, Mohamed

AU - Timilsina, Sujan

AU - Zlatković, Nevena

AU - Obradović, Aleksa

AU - Bull, Carolee Theresa

AU - Goss, Erica M.

AU - Huguet-Tapia, Jose C.

AU - Paret, Mathews L.

AU - Jones, Jeffrey B.

AU - Potnis, Neha

PY - 2019/1/1

Y1 - 2019/1/1

N2 - 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.

AB - 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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