Capsular Polysaccharide Cross-Regulation Modulates <named-content content-type="genus-species">Bacteroides thetaiotaomicron</named-content> Biofilm Formation

ABSTRACT Bacteroides thetaiotaomicron is one of the most abundant gut symbiont species, whose contribution to host health through its ability to degrade dietary polysaccharides and mature the immune system is under intense scrutiny. In contrast, adhesion and biofilm formation, which are potentially...

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Autores principales:	Nathalie Béchon, Jovana Mihajlovic, Sol Vendrell-Fernández, Florian Chain, Philippe Langella, Christophe Beloin, Jean-Marc Ghigo
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	capsule Bacteroides thetaiotaomicron biofilm Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/a7dc8b6cb51f444cadd51dd2a08a80e5
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spelling	oai:doaj.org-article:a7dc8b6cb51f444cadd51dd2a08a80e52021-11-15T15:56:46ZCapsular Polysaccharide Cross-Regulation Modulates <named-content content-type="genus-species">Bacteroides thetaiotaomicron</named-content> Biofilm Formation10.1128/mBio.00729-202150-7511https://doaj.org/article/a7dc8b6cb51f444cadd51dd2a08a80e52020-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00729-20https://doaj.org/toc/2150-7511ABSTRACT Bacteroides thetaiotaomicron is one of the most abundant gut symbiont species, whose contribution to host health through its ability to degrade dietary polysaccharides and mature the immune system is under intense scrutiny. In contrast, adhesion and biofilm formation, which are potentially involved in gut colonization and microbiota structure and stability, have hardly been investigated in this intestinal bacterium. To uncover B. thetaiotaomicron biofilm-related functions, we performed a transposon mutagenesis in the poorly biofilm-forming reference strain VPI-5482 and showed that capsule 4, one of the eight B. thetaiotaomicron capsules, hinders biofilm formation. We then showed that the production of capsules 1, 2, 3, 5, and 6 also inhibits biofilm formation and that decreased capsulation of the population correlated with increased biofilm formation, suggesting that capsules could be masking adhesive surface structures. In contrast, we showed that capsule 8 displayed intrinsic adhesive properties. Finally, we demonstrated that BT2934, the wzx homolog of the B. thetaiotaomicron glycosylation locus, competes with capsule production and impacts its adhesion capacity. This study therefore establishes B. thetaiotaomicron capsule regulation as a major determinant of B. thetaiotaomicron biofilm formation, providing new insights into how modulation of different B. thetaiotaomicron surface structures affects in vitro biofilm formation. IMPORTANCE The human gut harbors a complex bacterial community that plays important roles in host health and disease, including nutrient acquisition, maturation of the immune system, and resistance to infections. The capacity to adhere to surfaces and form communities called biofilms is believed to be important for niche colonization and maintenance of gut bacteria. However, little is known about the adhesion capacity of most gut bacteria. In this study, we investigated biofilm formation in Bacteroides thetaiotaomicron, one of the most abundant bacteria of the normal mammalian intestine. We identified that B. thetaiotaomicron capsules, a group of eight surface-exposed polysaccharidic layers mediating important interactions with the gut environment, are also major determinants of biofilm formation that mask or unmask adhesion factors. Studying how B. thetaiotaomicron regulates its adhesion properties will allow us to better understand the physiology and specific properties of this important gut symbiont within anaerobic biofilms.Nathalie BéchonJovana MihajlovicSol Vendrell-FernándezFlorian ChainPhilippe LangellaChristophe BeloinJean-Marc GhigoAmerican Society for MicrobiologyarticlecapsuleBacteroides thetaiotaomicronbiofilmMicrobiologyQR1-502ENmBio, Vol 11, Iss 3 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	capsule Bacteroides thetaiotaomicron biofilm Microbiology QR1-502
spellingShingle	capsule Bacteroides thetaiotaomicron biofilm Microbiology QR1-502 Nathalie Béchon Jovana Mihajlovic Sol Vendrell-Fernández Florian Chain Philippe Langella Christophe Beloin Jean-Marc Ghigo Capsular Polysaccharide Cross-Regulation Modulates <named-content content-type="genus-species">Bacteroides thetaiotaomicron</named-content> Biofilm Formation
description	ABSTRACT Bacteroides thetaiotaomicron is one of the most abundant gut symbiont species, whose contribution to host health through its ability to degrade dietary polysaccharides and mature the immune system is under intense scrutiny. In contrast, adhesion and biofilm formation, which are potentially involved in gut colonization and microbiota structure and stability, have hardly been investigated in this intestinal bacterium. To uncover B. thetaiotaomicron biofilm-related functions, we performed a transposon mutagenesis in the poorly biofilm-forming reference strain VPI-5482 and showed that capsule 4, one of the eight B. thetaiotaomicron capsules, hinders biofilm formation. We then showed that the production of capsules 1, 2, 3, 5, and 6 also inhibits biofilm formation and that decreased capsulation of the population correlated with increased biofilm formation, suggesting that capsules could be masking adhesive surface structures. In contrast, we showed that capsule 8 displayed intrinsic adhesive properties. Finally, we demonstrated that BT2934, the wzx homolog of the B. thetaiotaomicron glycosylation locus, competes with capsule production and impacts its adhesion capacity. This study therefore establishes B. thetaiotaomicron capsule regulation as a major determinant of B. thetaiotaomicron biofilm formation, providing new insights into how modulation of different B. thetaiotaomicron surface structures affects in vitro biofilm formation. IMPORTANCE The human gut harbors a complex bacterial community that plays important roles in host health and disease, including nutrient acquisition, maturation of the immune system, and resistance to infections. The capacity to adhere to surfaces and form communities called biofilms is believed to be important for niche colonization and maintenance of gut bacteria. However, little is known about the adhesion capacity of most gut bacteria. In this study, we investigated biofilm formation in Bacteroides thetaiotaomicron, one of the most abundant bacteria of the normal mammalian intestine. We identified that B. thetaiotaomicron capsules, a group of eight surface-exposed polysaccharidic layers mediating important interactions with the gut environment, are also major determinants of biofilm formation that mask or unmask adhesion factors. Studying how B. thetaiotaomicron regulates its adhesion properties will allow us to better understand the physiology and specific properties of this important gut symbiont within anaerobic biofilms.
format	article
author	Nathalie Béchon Jovana Mihajlovic Sol Vendrell-Fernández Florian Chain Philippe Langella Christophe Beloin Jean-Marc Ghigo
author_facet	Nathalie Béchon Jovana Mihajlovic Sol Vendrell-Fernández Florian Chain Philippe Langella Christophe Beloin Jean-Marc Ghigo
author_sort	Nathalie Béchon
title	Capsular Polysaccharide Cross-Regulation Modulates <named-content content-type="genus-species">Bacteroides thetaiotaomicron</named-content> Biofilm Formation
title_short	Capsular Polysaccharide Cross-Regulation Modulates <named-content content-type="genus-species">Bacteroides thetaiotaomicron</named-content> Biofilm Formation
title_full	Capsular Polysaccharide Cross-Regulation Modulates <named-content content-type="genus-species">Bacteroides thetaiotaomicron</named-content> Biofilm Formation
title_fullStr	Capsular Polysaccharide Cross-Regulation Modulates <named-content content-type="genus-species">Bacteroides thetaiotaomicron</named-content> Biofilm Formation
title_full_unstemmed	Capsular Polysaccharide Cross-Regulation Modulates <named-content content-type="genus-species">Bacteroides thetaiotaomicron</named-content> Biofilm Formation
title_sort	capsular polysaccharide cross-regulation modulates <named-content content-type="genus-species">bacteroides thetaiotaomicron</named-content> biofilm formation
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/a7dc8b6cb51f444cadd51dd2a08a80e5
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Capsular Polysaccharide Cross-Regulation Modulates <named-content content-type="genus-species">Bacteroides thetaiotaomicron</named-content> Biofilm Formation

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