Modulation of bacterial multicellularity via spatio-specific polysaccharide secretion

• DOI: 10.1371/journal.pbio.3000728
• Publication Date: 2020-06-09T17:54:19Z
• Authors: Salim T. Islam; Israel Vergara Al...; Fares Saïdi; Annick Guiseppi; Evgeny Vinogradov; Gaurav Sharma; Leon Espinosa; Castrese Morrone; Gael Brasseur; Jean-François Gui...; Anaïs Benarouche; Jean-Luc Bridot; Gokulakrishnan Ra...; Alain Cagna; Charles Gauthier; Mitchell Singer; Henri-Pierre Fierobe; Tâm Mignot; Emilia M. F. Maur...
• Keywords: 0301 basic medicine; 570; Exopolysaccharides; Myxococcus xanthus; Polymers; QH301-705.5; [SDV]Life Sciences [q-bio]; Proton Magnetic Resonance Spectroscopy; protein domains; polysaccharides; Protein domains; statistical data; -; emulsions; Medical and Health Sciences; Surface-Active Agents; 03 medical and health sciences; Polysaccharides; Pathogen motility; Biology (General); Carbon-13 Magnetic Resonance Spectroscopy; polymers; Agricultural and Veterinary Sciences; exopolysaccharides; Monosaccharides; pathogen motility; Cell Membrane; Polysaccharides, Bacterial; Bacterial; 500; Acetylation; Biological Sciences; Statistical data; Biosynthetic Pathways; [SDV] Life Sciences [q-bio]; monosaccharides; Multigene Family; Emulsions; Developmental Biology; Research Article

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.