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Convergent gain and loss of genomic islands drive lifestyle changes in plant-associated Pseudomonas

The ISME Journal (2019) | Download Citation

Abstract

Host-associated bacteria can have both beneficial and detrimental effects on host health. While some of the molecular mechanisms that determine these outcomes are known, little is known about the evolutionary histories of pathogenic or mutualistic lifestyles. Using the model plant Arabidopsis, we found that closely related strains within the Pseudomonas fluorescens species complex promote plant growth and occasionally cause disease. To elucidate the genetic basis of the transition between commensalism and pathogenesis, we developed a computational pipeline and identified genomic islands that correlate with outcomes for plant health. One island containing genes for lipopeptide biosynthesis and quorum-sensing is required for pathogenesis. Conservation of the quorum-sensing machinery in this island allows pathogenic strains to eavesdrop on quorum signals in the environment and coordinate pathogenic behavior. We found that genomic loci associated with both pathogenic and commensal lifestyles were convergently gained and lost in multiple lineages through homologous recombination, possibly constituting an early step in the differentiation of pathogenic and commensal lifestyles. Collectively this work provides novel insights into the evolution of commensal and pathogenic lifestyles within a single clade of host-associated bacteria.

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Acknowledgements

We thank Dr. Clay Fuqua for providing the Chromobacterium violaceum CV026 biosensor strain, Dr. Teresa de Kievit and Dr. Ricardo Oliva for providing Pseudomonas isolates, and Dr. Adam Steinbrenner and Dr. Justin Meyer for critical reading of the manuscript. RAM is a Simons Foundation Fellow of the Life Sciences Research Foundation. This work was also supported by an NSERC Discovery Grant (NSERC-RGPIN-2016-04121), Canada Foundation for Innovation, and Canada Research Chair grants awarded to CHH, and an NSERC USRA to SSH. The computational research was carried out with support provided by WestGrid and Compute Canada. RAM and CHH designed research and discussed results. RAM and SSH performed experiments. RAM wrote code and performed all bioinformatics analyses. RAM wrote the manuscript with input from CHH and SSH.

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    • Ryan A. Melnyk

    Present address: Department of Plant Biology, University of California, Davis, Davis, CA, USA

Affiliations

  1. Department of Microbiology and Immunology, The University of British Columbia, Vancouver, BC, Canada

    • Ryan A. Melnyk
    • , Sarzana S. Hossain
    •  & Cara H. Haney

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The authors declare that they have no conflict of interest.

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Correspondence to Cara H. Haney.

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https://doi.org/10.1038/s41396-019-0372-5