Modulation 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 communi...

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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	Analysis Antigens Assembly Bacteria Bacterial cell walls Biofilms Biology and Life Sciences Biosynthesis Biotechnology Cell survival Control Density Dispersal emulsions Exopolysaccharides Extracellular matrix Fruit bodies Funding Gram-positive bacteria Life Sciences Medicine and Health Sciences Microbial polysaccharides Microorganisms monosaccharides Motility pathogen motility Physical Sciences Physiological aspects Physiology Polymers Polysaccharides protein domains Proteins Saccharides Secretion Software Spore coats statistical data Supervision Canada Israel California France United States > US Quebec Canada Statistical data Polysaccharides Pathogen motility Protein domains Emulsions Exopolysaccharides Polymers Monosaccharides
Online Access	Get full text
ISSN	1545-7885 1544-9173 1545-7885
DOI	10.1371/journal.pbio.3000728

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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. NRC publication: Yes
AbstractList	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. 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. 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.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. The development of multicellularity is a key evolutionary transition allowing for differentiation of physiological functions across a cell population that confers survival benefits; among uni-cellular bacteria, this can lead to complex developmental behaviors and the formation of higher-order community structures. Herein, we demonstrate that in the social δ-proteobac-terium 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. 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 [delta]-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 [beta]-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.
Audience	Academic
Author	Espinosa, Leon Morrone, Castrese Islam, Salim T Guillemot, Jean-François Benarouche, Anaïs Cagna, Alain Fierobe, Henri-Pierre Guiseppi, Annick Vinogradov, Evgeny Vergara Alvarez, Israel Sharma, Gaurav Gauthier, Charles Saïdi, Fares Mignot, Tâm Bridot, Jean-Luc Ravicoularamin, Gokulakrishnan Brasseur, Gael Mauriello, Emilia M. F Singer, Mitchell
AuthorAffiliation	6 Institute of Bioinformatics and Applied Biotechnology, Electronic City, Bengaluru, Karnataka, India 3 Laboratoire de Chimie Bactérienne, CNRS–Université Aix-Marseille UMR, Institut de Microbiologie de la Méditerranée, Marseille, France 2 PROTEO, the Quebec Network for Research on Protein Function, Engineering, and Applications, Université Laval, Québec, Québec, Canada Universitat zu Koln, GERMANY 1 Armand Frappier Health & Biotechnology Research Centre, Institut National de la Recherche Scientifique, Université du Québec, Institut Pasteur International Network, Laval, Québec, Canada 5 Department of Microbiology and Molecular Genetics, University of California–Davis, Davis, California, United States of America 7 CNRS–Institut de Microbiologie de la Méditerranée, Marseille, France 8 Teclis Scientific, Civrieux d’Azergue, France 4 Human Health Therapeutics Portfolio, National Research Council of Canada, Ottawa, Ontario, Canada
AuthorAffiliation_xml	– name: 8 Teclis Scientific, Civrieux d’Azergue, France – name: 6 Institute of Bioinformatics and Applied Biotechnology, Electronic City, Bengaluru, Karnataka, India – name: 4 Human Health Therapeutics Portfolio, National Research Council of Canada, Ottawa, Ontario, Canada – name: 2 PROTEO, the Quebec Network for Research on Protein Function, Engineering, and Applications, Université Laval, Québec, Québec, Canada – name: 5 Department of Microbiology and Molecular Genetics, University of California–Davis, Davis, California, United States of America – name: 3 Laboratoire de Chimie Bactérienne, CNRS–Université Aix-Marseille UMR, Institut de Microbiologie de la Méditerranée, Marseille, France – name: 7 CNRS–Institut de Microbiologie de la Méditerranée, Marseille, France – name: Universitat zu Koln, GERMANY – name: 1 Armand Frappier Health & Biotechnology Research Centre, Institut National de la Recherche Scientifique, Université du Québec, Institut Pasteur International Network, Laval, Québec, Canada
Author_xml	– sequence: 1 fullname: Islam, Salim T – sequence: 2 fullname: Vergara Alvarez, Israel – sequence: 3 fullname: Saïdi, Fares – sequence: 4 fullname: Guiseppi, Annick – sequence: 5 fullname: Vinogradov, Evgeny – sequence: 6 fullname: Sharma, Gaurav – sequence: 7 fullname: Espinosa, Leon – sequence: 8 fullname: Morrone, Castrese – sequence: 9 fullname: Brasseur, Gael – sequence: 10 fullname: Guillemot, Jean-François – sequence: 11 fullname: Benarouche, Anaïs – sequence: 12 fullname: Bridot, Jean-Luc – sequence: 13 fullname: Ravicoularamin, Gokulakrishnan – sequence: 14 fullname: Cagna, Alain – sequence: 15 fullname: Gauthier, Charles – sequence: 16 fullname: Singer, Mitchell – sequence: 17 fullname: Fierobe, Henri-Pierre – sequence: 18 fullname: Mignot, Tâm – sequence: 19 fullname: Mauriello, Emilia M. F
BackLink	https://amu.hal.science/hal-02880850$$DView record in HAL
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Keywords	Statistical data Polysaccharides Pathogen motility Protein domains Emulsions Exopolysaccharides Polymers Monosaccharides
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SubjectTerms	Analysis Antigens Assembly Bacteria Bacterial cell walls Biofilms Biology and Life Sciences Biosynthesis Biotechnology Cell survival Control Density Dispersal emulsions Exopolysaccharides Extracellular matrix Fruit bodies Funding Gram-positive bacteria Life Sciences Medicine and Health Sciences Microbial polysaccharides Microorganisms monosaccharides Motility pathogen motility Physical Sciences Physiological aspects Physiology Polymers Polysaccharides protein domains Proteins Saccharides Secretion Software Spore coats statistical data Supervision
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Title	Modulation of bacterial multicellularity via spatio-specific polysaccharide secretion
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