biostudies-literatureIslam STNatural Sciences and Engineering Research Council of CanadaInstitut national de la recherche scientifiqueConsejo Nacional de Ciencia y TecnologíaAix-Marseille UniversitéAgence Nationale de la RechercheBanting Research FoundationCentre National de la Recherche ScientifiquePROTEOCanadian Institutes of Health ResearchCIHRNational Science Foundatione3000728https://www.ebi.ac.uk/biostudies/studies/S-EPMC7310880biostudies-literatureUnknown18(6)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.PLoS biologyModulation of bacterial multicellularity via spatio-specific polysaccharide secretion.PMC7310880AMIDEXANR-14-CE11‐0023‐01IOS1354622018-1400RGPIN-2016-06637ANR-15-CE13-0006 BACTOCOMPASS321028Espinosa LIslam STVergara Alvarez IFierobe HPSaidi FSharma GMorrone CBrasseur GGauthier CMignot TMauriello EMFSinger MBenarouche AGuiseppi AGuillemot JFCagna ABridot JLVinogradov ERavicoularamin GfalseModulation of bacterial multicellularity via spatio-specific polysaccharide secretion.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.2020-01-01T00:00:00Z2020 Jun2024-11-08T21:53:25.773Z2020-07-01T07:04:45ZS-EPMC73108803251631110.1371/journal.pbio.3000728