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The Marine Bacterium Shewanella woodyi Produces C8-HSL to Regulate Bioluminescence

  • Environmental Microbiology
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Abstract

Quorum sensing (QS), a cell-to-cell communication system involved in the synchronization of bacterial behavior in a cell-density-dependent manner has been shown to control phenotypes such as luminescence, virulence, and biofilm formation. The marine strain, Shewanella woodyi MS32 has been identified as a luminous bacterium. Very little information is known on this bacterium, in particular if its luminescence and biofilm formation are controlled by QS. In this study, we have demonstrated that S. woodyi MS32 emits luminescence in planktonic and sessile conditions. The putative QS regulatory genes homologous to luxI and luxR identified in the S. woodyi MS32 genome, named swoI and swoR, are divergently transcribed and are not genetically linked to the lux operon in contrast with its closest parent Shewanella hanedai and with Aliivibrio fischeri. Interestingly, the phylogenetic analysis based on the SwoI and SwoR sequences shows that a separate horizontal gene transfer (HGT) occurred for the regulatory genes and for the lux operon. Functional analyses demonstrate that the swoI and swoR mutants were non-luminescent. Expression of lux genes was impaired in the QS regulatory mutants. N-octanoyl-L-homoserine lactone (C8-HSL) identified using liquid chromatography mass spectrometry in the wild-type strain (but not in ΔswoI) can induce S. woodyi luminescence. No significant difference has been detected between the wild-type and mutants on adhesion and biofilm formation in the conditions tested. Therefore, we have demonstrated that the luxCDABEG genes of S. woodyi MS32 are involved in luminescence emission and that the swoR/swoI genes, originated from a separate HGT, regulate luminescence through C8-HSL production.

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Acknowledgements

We thank J.A. Gralnick from the BioTechnology Institute and Department of Plant and Microbial Biology, University of Minnesota-Twin Cities for kindly providing the Shewanella strain and the pSMV3 and pBBR1MCS-2 plasmids. We thank Yoan Ferandin for the advisory help in the qPCR. We thank P. Poupin from the Laboratory of Microbial Biodiversity and Biotechnology of the Sorbonne Universities and CNRS for his help in the construction of the complementation plasmids. We also thank anonymous reviewers for their commentaries and suggestions.

Funding

Mahmoud Hayek is the beneficiary of the Lebanese grants from the Association of Specialization and Scientific Guidance (ASSG). This research was also partly funded by the EMBRC network.

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  1. Laboratoire MAPIEM, EA4323, Université de Toulon, Avenue de l’université, BP 20132, 83957, La Garde Cedex, France

    Mahmoud Hayek, Claudine Baraquet, Yves Blache & Maëlle Molmeret

  2. Sorbonne Universités, CNRS, Laboratoire de Biodiversité et Biotechnologies Microbiennes (LBBM), Observatoire Océanologique, Banyuls-sur-Mer, France

    Raphaël Lami

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Hayek, M., Baraquet, C., Lami, R. et al. The Marine Bacterium Shewanella woodyi Produces C8-HSL to Regulate Bioluminescence. Microb Ecol 79, 865–881 (2020). https://doi.org/10.1007/s00248-019-01454-z

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