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DNA-uptake pili of Vibrio cholerae are required for chitin colonization and capable of kin recognition via sequence-specific self-interaction

Nature Microbiology volume 4, pages 1545–1557 (2019)Cite this article

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Abstract

How bacteria colonize surfaces and how they distinguish the individuals around them are fundamental biological questions. Type IV pili are a widespread and multipurpose class of cell surface polymers. Here we directly visualize the DNA-uptake pilus of Vibrio cholerae, which is produced specifically during growth on its natural habitat—chitinous surfaces. As predicted, these pili are highly dynamic and retract before DNA uptake during competence for natural transformation. Interestingly, DNA-uptake pili can also self-interact to mediate auto-aggregation. This capability is conserved in disease-causing pandemic strains, which typically encode the same major pilin subunit, PilA. Unexpectedly, however, we discovered that extensive strain-to-strain variability in PilA (present in environmental isolates) creates a set of highly specific interactions, enabling cells producing pili composed of different PilA subunits to distinguish between one another. We go on to show that DNA-uptake pili bind to chitinous surfaces and are required for chitin colonization under flow, and that pili capable of self-interaction connect cells on chitin within dense pili networks. Our results suggest a model whereby DNA-uptake pili function to promote inter-bacterial interactions during surface colonization. Moreover, they provide evidence that type IV pili could offer a simple and potentially widespread mechanism for bacterial kin recognition.

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Fig. 1: Direct observation of dynamic DNA-uptake pili.
Fig. 2: Competent cells auto-aggregate in the absence of pilus retraction.
Fig. 3: A1552 PilA is sufficient for aggregation in a non-pandemic strain.
Fig. 4: PilA variability governs auto-aggregation and enables kin-recognition.
Fig. 5: The unusual tail of ATCC25872/V52 PilA inhibits aggregation.
Fig. 6: DNA-uptake pili form networks on chitin surfaces.

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Data availability

The data that support the findings of this study are available from the corresponding authors upon request.

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Acknowledgements

The authors thank members of the Blokesch laboratory for scientific discussions and I. Mateus-Gonzalez for assistance with bioinformatics analyses. The authors also thank A. Boehm, S. Pukatzki, J. Mekalanos, J. Reidl and members of the Institut National de Recherche Biomédicale of the Democratic Republic of the Congo for providing V. cholerae strains and V. Pelicic for advice on pheS-mediated counter-selection. Work on this issue was supported by a Marie Skłodowska-Curie Individual Fellowship (703340, CMDNAUP) to D.W.A. and by EPFL intramural funding and an ERC Starting (309064-VIR4ENV) and Consolidator (724630-CholeraIndex) Grant from the European Research Council to M.B. M.B. is a Howard Hughes Medical Institute (HHMI) International Research Scholar (grant no. 55008726).

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  1. Laboratory of Molecular Microbiology, Global Health Institute, School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne (EPFL), Lausanne, Switzerland

    David. W. Adams, Sandrine Stutzmann, Candice Stoudmann & Melanie Blokesch

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Contributions

Conception, design and analysis were carried out by D.W.A. and M.B. D.W.A., S.S., C.S. and M.B. performed the research. D.W.A and M.B. wrote the manuscript.

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Correspondence to David. W. Adams or Melanie Blokesch.

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Supplementary information

Supplementary Information

Supplementary Table 1, Supplementary References, Supplementary Figs. 1–21, Supplementary Video legends.

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Supplementary File 1

Details of the 647 V. cholerae genomes used for bioinformatic analyses.

Supplementary File 2

DNA sequences of pilA and the deduced amino acid sequences of the proteins they encode from a collection of 22 environmental and clinical V. cholerae strains.

Supplementary Video 1

DNA-uptake pili exhibit rapid assembly dynamics.

Supplementary Video 2

Additional examples of dynamic DNA-uptake pili.

Supplementary Video 3

High time-resolution imaging of pilus extension and retraction.

Supplementary Video 4

Retraction of an unusually long pilus.

Supplementary Video 5

Pilus retraction followed by DNA-uptake.

Supplementary Video 6

Cells lacking pilT produce multiple static pili.

Supplementary Video 7

Additional examples of static pili in retraction deficient cells.

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Adams, D.W., Stutzmann, S., Stoudmann, C. et al. DNA-uptake pili of Vibrio cholerae are required for chitin colonization and capable of kin recognition via sequence-specific self-interaction. Nat Microbiol 4, 1545–1557 (2019). https://doi.org/10.1038/s41564-019-0479-5

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