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Activation of Vibrio cholerae quorum sensing promotes survival of an arthropod host

Nature Microbiology volume 3, pages 243–252 (2018)Cite this article

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Abstract

Vibrio cholerae colonizes the human terminal ileum to cause cholera, and the arthropod intestine and exoskeleton to persist in the aquatic environment. Attachment to these surfaces is regulated by the bacterial quorum-sensing signal transduction cascade, which allows bacteria to assess the density of microbial neighbours. Intestinal colonization with V. cholerae results in expenditure of host lipid stores in the model arthropod Drosophila melanogaster. Here we report that activation of quorum sensing in the Drosophila intestine retards this process by repressing V. cholerae succinate uptake. Increased host access to intestinal succinate mitigates infection-induced lipid wasting to extend survival of V. cholerae-infected flies. Therefore, quorum sensing promotes a more favourable interaction between V. cholerae and an arthropod host by reducing the nutritional burden of intestinal colonization.

In a process known as quorum sensing, bacteria produce small molecules termed autoinducers that accumulate in the environment as a function of cell density. Upon reaching a particular concentration threshold, these autoinducers alter collective bacterial gene transcription in a fashion that is hypothesized to be adaptive. Quorum sensing may thus allow a bacterium to respond to environmental conditions as a multicellular rather than unicellular organism. Behaviours that benefit from coordinated multicellular action include utilization of available nutrients1,2, surface attachment or biofilm formation3,4,5, natural competence6,7,8, and regulation of virulence and symbiosis strategies9,10. Quorum sensing by the human diarrhoeal pathogen Vibrio cholerae modulates all of these1,5,11,12.

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Fig. 1: V. cholerae high-cell-density quorum-sensing-dependent signalling is activated in the Drosophila intestine and promotes host survival of infection.
Fig. 2: V. cholerae quorum sensing promotes host survival independent of biofilm formation.
Fig. 3: V. cholerae quorum sensing and succinate supplementation prevent host lipolysis.
Fig. 4: Dilp6 knockdown inhibits host infection-induced lipolysis and prolongs host survival.

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Acknowledgements

Microscopy was performed at the Microscopy Resources on the North Quad (MicRoN) core facility at Harvard Medical School. This work was supported by National Institutes of Health grants R21 AI109436 (P.I.W.) and R01 AI097405 (J.G.M.). Many stocks obtained from the Bloomington Drosophila Stock Center (NIH P40OD018537) and the Vienna Drosophila Resource Centre were used in this study. This work was partially supported by NIH grants 5P30CA006516 (J.M.A.) and 5P01CA120964 (J.M.A.). The authors thank S. Breitkopf and M. Yuan for help with mass spectrometry experiments, and R. Taylor for sharing strain C6706 with us. This skilled and generous scientist has left a great mark on the field and a void in our hearts.

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Author notes

  1. Layla Kamareddine and Adam C.N. Wong contributed equally to this work.

Authors and Affiliations

  1. Division of Infectious Diseases, Boston Children’s Hospital, Harvard Medical School, Boston, MA, USA

    Layla Kamareddine, Adam C. N. Wong, Audrey S. Vanhove, Saiyu Hang, Alexandra E. Purdy, Katharine Kierek-Pearson & Paula I. Watnick

  2. Department of Entomology and Nematology, University of Florida, Gainesville, FL, USA

    Adam C. N. Wong

  3. University of Massachusetts Medical School, Worcester, MA, USA

    Saiyu Hang

  4. Department of Biology, AC #2237, Amherst College, Amherst, MA, USA

    Alexandra E. Purdy

  5. Division of Signal Transduction/Mass Spectrometry Core, Beth Israel Deaconess Medical Center, Boston, MA, USA

    John M. Asara

  6. Department of Medicine, Harvard Medical School, Boston, MA, USA

    John M. Asara

  7. Emerging Pathogens Institute University of Florida, Gainesville, FL, USA

    Afsar Ali & J. Glenn Morris Jr

  8. Department of Environmental & Global Health, School of Public Health and Health Profession, University of Florida, Gainesville, FL, USA

    Afsar Ali

  9. Department of Microbiology and Immunobiology, Harvard Medical Schoolm, Boston, MA, USA

    Paula I. Watnick

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Contributions

L.K., A.C.N.W., A.S.V., S.H., J.M.A. and P.I.W. designed the experiments. L.K., A.C.N.W., A.S.V., S.H. and J.M.A. performed the experiments. K.K.-P., A.E.P., A.A. and J.G.M. contributed critical reagents. L.K., A.C.N.W., A.S.V., S.H., J.M.A. and P.I.W. analysed the data. P.I.W. wrote the manuscript. All authors reviewed, edited and approved the manuscript.

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Correspondence to Paula I. Watnick.

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Supplementary Information

Supplementary Figures 1–9.

Life Sciences Reporting Summary

Supplementary Table 1

Normalized levels of polar metabolites in LB broth and the spent supernatants of parental strain CH494 and corresponding ΔhapR and ΔhapRΔvpsA mutants.

Supplementary Table 2

Significantly different metabolites in the spent supernatants of the parental strain CH494 and corresponding ΔhapR and ΔhapRΔvpsA mutants calculated by a one-way ANOVA with FDR 0.05.

Supplementary Table 3

Strains and plasmids.

Supplementary Table 4

Primers used in this study.

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Kamareddine, L., Wong, A.C.N., Vanhove, A.S. et al. Activation of Vibrio cholerae quorum sensing promotes survival of an arthropod host. Nat Microbiol 3, 243–252 (2018). https://doi.org/10.1038/s41564-017-0065-7

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