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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| creator | 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 Roberts, Roland G |
| description | 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. |
| doi_str_mv | 10.1371/journal.pbio.3000728 |
| format | Article |
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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. 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F</au><au>Roberts, Roland G</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Modulation of bacterial multicellularity via spatio-specific polysaccharide secretion</atitle><jtitle>PLoS biology</jtitle><date>2020-06-09</date><risdate>2020</risdate><volume>18</volume><issue>6</issue><spage>e3000728</spage><epage>e3000728</epage><pages>e3000728-e3000728</pages><issn>1545-7885</issn><issn>1544-9173</issn><eissn>1545-7885</eissn><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. 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| recordid | cdi_plos_journals_2424465645 |
| source | PubMed (Medline); DOAJ Directory of Open Access Journals; Free E-Journal (出版社公開部分のみ）; PLoS - Public Library of Sciencem (Open Access) |
| subjects | Analysis Antigens Assembly Bacteria Bacterial cell walls Biofilms Biology and Life Sciences Biosynthesis Biotechnology Cell survival Control Density Dispersal Exopolysaccharides Extracellular matrix Fruit bodies Funding Gram-positive bacteria Life Sciences Medicine and Health Sciences Microbial polysaccharides Microorganisms Motility Physical Sciences Physiological aspects Physiology Polymers Polysaccharides Proteins Saccharides Secretion Software Spore coats Supervision |
| title | Modulation of bacterial multicellularity via spatio-specific polysaccharide secretion |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-01T06%3A56%3A16IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Modulation%20of%20bacterial%20multicellularity%20via%20spatio-specific%20polysaccharide%20secretion&rft.jtitle=PLoS%20biology&rft.au=Islam,%20Salim%20T&rft.date=2020-06-09&rft.volume=18&rft.issue=6&rft.spage=e3000728&rft.epage=e3000728&rft.pages=e3000728-e3000728&rft.issn=1545-7885&rft.eissn=1545-7885&rft_id=info:doi/10.1371/journal.pbio.3000728&rft_dat=%3Cgale_plos_%3EA632939188%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2424465645&rft_id=info:pmid/32516311&rft_galeid=A632939188&rft_doaj_id=oai_doaj_org_article_1c485093bfaf4b719b33284bbf6aaf58&rfr_iscdi=true |