A complex LuxR–LuxI type quorum sensing network in a roseobacterial marine sponge symbiont activates flagellar motility and inhibits biofilm formation

Authors

  • Jindong Zan,

    1. Institute of Marine and Environmental Technology, University of Maryland Center for Environmental Science, 701 E Pratt St., Baltimore, MD 21202, USA.
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    • These authors contributed equally to this work.

  • Elisha M. Cicirelli,

    1. Department of Biology, 1001 E. 3rd St., Jordan Hall 142, Indiana University, Bloomington, IN 47405, USA.
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    • These authors contributed equally to this work.

    • Present addresses: Bio-Amber Inc., Minneapolis, MN, USA;

  • Naglaa M. Mohamed,

    1. Institute of Marine and Environmental Technology, University of Maryland Center for Environmental Science, 701 E Pratt St., Baltimore, MD 21202, USA.
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  • Hiruy Sibhatu,

    1. Department of Pharmacology, School of Medicine, University of Colorado Denver, 12801 East 17th Avenue, Aurora, CO 80045-0511, USA.
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    • Department of Pharmacology, University of California, San Diego, CA, USA;

  • Stephanie Kroll,

    1. Department of Biology, 1001 E. 3rd St., Jordan Hall 142, Indiana University, Bloomington, IN 47405, USA.
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    • Cayman Chemical Co., Ann Arbor, MI, USA;

  • Okhee Choi,

    1. Department of Biology, 1001 E. 3rd St., Jordan Hall 142, Indiana University, Bloomington, IN 47405, USA.
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    • Gyeongsang National University, Jinju, Korea.

  • Charis L. Uhlson,

    1. Department of Pharmacology, School of Medicine, University of Colorado Denver, 12801 East 17th Avenue, Aurora, CO 80045-0511, USA.
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  • Christina L. Wysoczynski,

    1. Department of Pharmacology, School of Medicine, University of Colorado Denver, 12801 East 17th Avenue, Aurora, CO 80045-0511, USA.
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  • Robert C. Murphy,

    1. Department of Pharmacology, School of Medicine, University of Colorado Denver, 12801 East 17th Avenue, Aurora, CO 80045-0511, USA.
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  • Mair E. A. Churchill,

    1. Department of Pharmacology, School of Medicine, University of Colorado Denver, 12801 East 17th Avenue, Aurora, CO 80045-0511, USA.
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  • Russell T. Hill,

    1. Institute of Marine and Environmental Technology, University of Maryland Center for Environmental Science, 701 E Pratt St., Baltimore, MD 21202, USA.
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  • Clay Fuqua

    Corresponding author
    1. Department of Biology, 1001 E. 3rd St., Jordan Hall 142, Indiana University, Bloomington, IN 47405, USA.
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Summary

Bacteria isolated from marine sponges, including the Silicibacter–Ruegeria (SR) subgroup of the Roseobacter clade, produce N-acylhomoserine lactone (AHL) quorum sensing signal molecules. This study is the first detailed analysis of AHL quorum sensing in sponge-associated bacteria, specifically Ruegeria sp. KLH11, from the sponge Mycale laxissima. Two pairs of luxR and luxI homologues and one solo luxI homologue were identified and designated ssaRI, ssbRI and sscI (sponge-associated symbiont locus A, B and C, luxR or luxI homologue). SsaI produced predominantly long-chain 3-oxo-AHLs and both SsbI and SscI specified 3-OH-AHLs. Addition of exogenous AHLs to KLH11 increased the expression of ssaI but not ssaR, ssbI or ssbR, and genetic analyses revealed a complex interconnected arrangement between SsaRI and SsbRI systems. Interestingly, flagellar motility was abolished in the ssaI and ssaR mutants, with the flagellar biosynthesis genes under strict SsaRI control, and active motility only at high culture density. Conversely, ssaI and ssaR mutants formed more robust biofilms than wild-type KLH11. AHLs and the ssaI transcript were detected in M. laxissima extracts, suggesting that AHL signalling contributes to the decision between motility and sessility and that it may also facilitate acclimation to different environments that include the sponge host.

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