Modulation of bacterial multicellularity via spatio-specific polysaccharide secretion

• Published in: PLoS biology Vol. 18; no. 6; p. e3000728
• Main Authors: Islam, Salim T., Vergara Alvarez, Israel, Saïdi, Fares, Guiseppi, Annick, Vinogradov, Evgeny, Sharma, Gaurav, Espinosa, Leon, Morrone, Castrese, Brasseur, Gael, Guillemot, Jean-François, Benarouche, Anaïs, Bridot, Jean-Luc, Ravicoularamin, Gokulakrishnan, Cagna, Alain, Gauthier, Charles, Singer, Mitchell, Fierobe, Henri-Pierre, Mignot, Tâm, Mauriello, Emilia M. F.
• Format: Journal Article
• Language: English
• Published: San Francisco Public Library of Science 09.06.2020; Public Library of Science (PLoS)
• Subjects: Antigens; Assembly; Bacteria; Biofilms; Biology and Life Sciences; Biosynthesis; Biotechnology; Cell survival; Density; Dispersal; Exopolysaccharides; Extracellular matrix; Fruit bodies; Funding; Gram-positive bacteria; Life Sciences; Medicine and Health Sciences; Motility; Physical Sciences; Physiology; Polymers; Polysaccharides; Proteins; Saccharides; Secretion; Software; Spore coats; Supervision; Canada; Israel; California; France; United States > US; Quebec Canada; Statistical data; Polysaccharides; Pathogen motility; Protein domains; Emulsions; Exopolysaccharides; Polymers; Monosaccharides
• ISSN: 1545-7885; 1544-9173; 1545-7885
• DOI: 10.1371/journal.pbio.3000728

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.