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Modulation of bacterial multicellularity via spatio-specific polysaccharide secretion

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  • Salim T Islam
  • Israel Vergara Alvarez
  • Fares Saïdi
  • Annick Guiseppi
  • Evgeny Vinogradov
  • Gaurav Sharma
  • Leon Espinosa
  • Castrese Morrone
  • Gael Brasseur
  • Jean-François Guillemot
  • Anaïs Benarouche
  • Jean-Luc Bridot
  • Gokulakrishnan Ravicoularamin
  • Alain Cagna
  • Charles Gauthier
  • Mitchell Singer
  • Henri-Pierre Fierobe
  • Tâm Mignot
  • Emilia M F Mauriello

Abstract

The development of multicellularity is a key evolutionary transition allowing for differentiation of physiological functions across a cell population that confers survival benefits; among unicellular bacteria, this can lead to complex developmental behaviors and the formation of higher-order community structures. Herein, we demonstrate that in the social δ-proteobacterium Myxococcus xanthus, the secretion of a novel biosurfactant polysaccharide (BPS) is spatially modulated within communities, mediating swarm migration as well as the formation of multicellular swarm biofilms and fruiting bodies. BPS is a type IV pilus (T4P)-inhibited acidic polymer built of randomly acetylated β-linked tetrasaccharide repeats. Both BPS and exopolysaccharide (EPS) are produced by dedicated Wzx/Wzy-dependent polysaccharide-assembly pathways distinct from that responsible for spore-coat assembly. While EPS is preferentially produced at the lower-density swarm periphery, BPS production is favored in the higher-density swarm interior; this is consistent with the former being known to stimulate T4P retraction needed for community expansion and a function for the latter in promoting initial cell dispersal. Together, these data reveal the central role of secreted polysaccharides in the intricate behaviors coordinating bacterial multicellularity.A study of the social bacterium Myxococcus xanthus reveals that the bacteria preferentially secrete specific polysaccharides within distinct zones of a swarm to facilitate spreading across a surface.

Suggested Citation

  • Salim T Islam & Israel Vergara Alvarez & Fares Saïdi & Annick Guiseppi & Evgeny Vinogradov & Gaurav Sharma & Leon Espinosa & Castrese Morrone & Gael Brasseur & Jean-François Guillemot & Anaïs Benarouc, 2020. "Modulation of bacterial multicellularity via spatio-specific polysaccharide secretion," PLOS Biology, Public Library of Science, vol. 18(6), pages 1-31, June.
    • Handle: RePEc:plo:pbio00:3000728
    DOI: 10.1371/journal.pbio.3000728
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    References listed on IDEAS

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    1. Laura M. Faure & Jean-Bernard Fiche & Leon Espinosa & Adrien Ducret & Vivek Anantharaman & Jennifer Luciano & Sébastien Lhospice & Salim T. Islam & Julie Tréguier & Mélanie Sotes & Erkin Kuru & Michae, 2016. "The mechanism of force transmission at bacterial focal adhesion complexes," Nature, Nature, vol. 539(7630), pages 530-535, November.
    2. Changjiang Dong & Konstantinos Beis & Jutta Nesper & Anne L. Brunkan-LaMontagne & Bradley R. Clarke & Chris Whitfield & James H. Naismith, 2006. "Wza the translocon for E. coli capsular polysaccharides defines a new class of membrane protein," Nature, Nature, vol. 444(7116), pages 226-229, November.
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