Intestinal IgA Regulates Expression of a Fructan Polysaccharide Utilization Locus in Colonizing Gut Commensal <named-content content-type="genus-species">Bacteroides thetaiotaomicron</named-content>

ABSTRACT Gut-derived immunoglobulin A (IgA) is the most abundant antibody secreted in the gut that shapes gut microbiota composition and functionality. However, most of the microbial antigens targeted by gut IgA remain unknown, and the functional effects of IgA targeting these antigens are currently...

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Autores principales:	Payal Joglekar, Hua Ding, Pablo Canales-Herrerias, Pankaj Jay Pasricha, Justin L. Sonnenburg, Daniel A. Peterson
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Bacteroides thetaiotaomicron immunoglobulin A diet fructan microbiota Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/bd8e93cbce1f4eb3ba499b83fc751a32
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spelling	oai:doaj.org-article:bd8e93cbce1f4eb3ba499b83fc751a322021-11-15T15:54:45ZIntestinal IgA Regulates Expression of a Fructan Polysaccharide Utilization Locus in Colonizing Gut Commensal <named-content content-type="genus-species">Bacteroides thetaiotaomicron</named-content>10.1128/mBio.02324-192150-7511https://doaj.org/article/bd8e93cbce1f4eb3ba499b83fc751a322019-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02324-19https://doaj.org/toc/2150-7511ABSTRACT Gut-derived immunoglobulin A (IgA) is the most abundant antibody secreted in the gut that shapes gut microbiota composition and functionality. However, most of the microbial antigens targeted by gut IgA remain unknown, and the functional effects of IgA targeting these antigens are currently understudied. This study provides a framework for identifying and characterizing gut microbiota antigens targeted by gut IgA. We developed a small intestinal ex vivo culture assay to harvest lamina propria IgA from gnotobiotic mice, with the aim of identifying antigenic targets in a model human gut commensal, Bacteroides thetaiotaomicron VPI-5482. Colonization by B. thetaiotaomicron induced a microbe-specific IgA response that was reactive against diverse antigens, including capsular polysaccharides, lipopolysaccharides, and proteins. IgA against microbial protein antigens targeted membrane and secreted proteins with diverse functionalities, including an IgA specific against proteins of the polysaccharide utilization locus (PUL) that are necessary for utilization of fructan, which is an important dietary polysaccharide. Further analyses demonstrated that the presence of dietary fructan increased the production of fructan PUL-specific IgA, which then downregulated the expression of fructan PUL in B. thetaiotaomicron, both in vivo and in vitro. Since the expression of fructan PUL has been associated with the ability of B. thetaiotaomicron to colonize the gut in the presence of dietary fructans, our work suggests a novel role for gut IgA in regulating microbial colonization by modulating their metabolism. IMPORTANCE Given the significant impact that gut microbes have on our health, it is essential to identify key host and environmental factors that shape this diverse community. While many studies have highlighted the impact of diet on gut microbiota, little is known about how the host regulates this critical diet-microbiota interaction. In our present study, we discovered that gut IgA targeted a protein complex involved in the utilization of an important dietary polysaccharide: fructan. While the presence of dietary fructans was previously thought to allow unrestricted growth of fructan-utilizing bacteria, our work shows that gut IgA, by targeting proteins responsible for fructan utilization, provides the host with tools that can restrict the microbial utilization of such polysaccharides, thereby controlling their growth.Payal JoglekarHua DingPablo Canales-HerreriasPankaj Jay PasrichaJustin L. SonnenburgDaniel A. PetersonAmerican Society for MicrobiologyarticleBacteroides thetaiotaomicronimmunoglobulin AdietfructanmicrobiotaMicrobiologyQR1-502ENmBio, Vol 10, Iss 6 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Bacteroides thetaiotaomicron immunoglobulin A diet fructan microbiota Microbiology QR1-502
spellingShingle	Bacteroides thetaiotaomicron immunoglobulin A diet fructan microbiota Microbiology QR1-502 Payal Joglekar Hua Ding Pablo Canales-Herrerias Pankaj Jay Pasricha Justin L. Sonnenburg Daniel A. Peterson Intestinal IgA Regulates Expression of a Fructan Polysaccharide Utilization Locus in Colonizing Gut Commensal <named-content content-type="genus-species">Bacteroides thetaiotaomicron</named-content>
description	ABSTRACT Gut-derived immunoglobulin A (IgA) is the most abundant antibody secreted in the gut that shapes gut microbiota composition and functionality. However, most of the microbial antigens targeted by gut IgA remain unknown, and the functional effects of IgA targeting these antigens are currently understudied. This study provides a framework for identifying and characterizing gut microbiota antigens targeted by gut IgA. We developed a small intestinal ex vivo culture assay to harvest lamina propria IgA from gnotobiotic mice, with the aim of identifying antigenic targets in a model human gut commensal, Bacteroides thetaiotaomicron VPI-5482. Colonization by B. thetaiotaomicron induced a microbe-specific IgA response that was reactive against diverse antigens, including capsular polysaccharides, lipopolysaccharides, and proteins. IgA against microbial protein antigens targeted membrane and secreted proteins with diverse functionalities, including an IgA specific against proteins of the polysaccharide utilization locus (PUL) that are necessary for utilization of fructan, which is an important dietary polysaccharide. Further analyses demonstrated that the presence of dietary fructan increased the production of fructan PUL-specific IgA, which then downregulated the expression of fructan PUL in B. thetaiotaomicron, both in vivo and in vitro. Since the expression of fructan PUL has been associated with the ability of B. thetaiotaomicron to colonize the gut in the presence of dietary fructans, our work suggests a novel role for gut IgA in regulating microbial colonization by modulating their metabolism. IMPORTANCE Given the significant impact that gut microbes have on our health, it is essential to identify key host and environmental factors that shape this diverse community. While many studies have highlighted the impact of diet on gut microbiota, little is known about how the host regulates this critical diet-microbiota interaction. In our present study, we discovered that gut IgA targeted a protein complex involved in the utilization of an important dietary polysaccharide: fructan. While the presence of dietary fructans was previously thought to allow unrestricted growth of fructan-utilizing bacteria, our work shows that gut IgA, by targeting proteins responsible for fructan utilization, provides the host with tools that can restrict the microbial utilization of such polysaccharides, thereby controlling their growth.
format	article
author	Payal Joglekar Hua Ding Pablo Canales-Herrerias Pankaj Jay Pasricha Justin L. Sonnenburg Daniel A. Peterson
author_facet	Payal Joglekar Hua Ding Pablo Canales-Herrerias Pankaj Jay Pasricha Justin L. Sonnenburg Daniel A. Peterson
author_sort	Payal Joglekar
title	Intestinal IgA Regulates Expression of a Fructan Polysaccharide Utilization Locus in Colonizing Gut Commensal <named-content content-type="genus-species">Bacteroides thetaiotaomicron</named-content>
title_short	Intestinal IgA Regulates Expression of a Fructan Polysaccharide Utilization Locus in Colonizing Gut Commensal <named-content content-type="genus-species">Bacteroides thetaiotaomicron</named-content>
title_full	Intestinal IgA Regulates Expression of a Fructan Polysaccharide Utilization Locus in Colonizing Gut Commensal <named-content content-type="genus-species">Bacteroides thetaiotaomicron</named-content>
title_fullStr	Intestinal IgA Regulates Expression of a Fructan Polysaccharide Utilization Locus in Colonizing Gut Commensal <named-content content-type="genus-species">Bacteroides thetaiotaomicron</named-content>
title_full_unstemmed	Intestinal IgA Regulates Expression of a Fructan Polysaccharide Utilization Locus in Colonizing Gut Commensal <named-content content-type="genus-species">Bacteroides thetaiotaomicron</named-content>
title_sort	intestinal iga regulates expression of a fructan polysaccharide utilization locus in colonizing gut commensal <named-content content-type="genus-species">bacteroides thetaiotaomicron</named-content>
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/bd8e93cbce1f4eb3ba499b83fc751a32
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Intestinal IgA Regulates Expression of a Fructan Polysaccharide Utilization Locus in Colonizing Gut Commensal <named-content content-type="genus-species">Bacteroides thetaiotaomicron</named-content>

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