Sulfation of Arabinogalactan Proteins Confers Privileged Nutrient Status to <named-content content-type="genus-species">Bacteroides plebeius</named-content>

ABSTRACT The human gut microbiota (HGM) contributes to the physiology and health of its host. The health benefits provided by dietary manipulation of the HGM require knowledge of how glycans, the major nutrients available to this ecosystem, are metabolized. Arabinogalactan proteins (AGPs) are a ubiq...

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Autores principales:	Jose Munoz-Munoz, Didier Ndeh, Pedro Fernandez-Julia, Gemma Walton, Bernard Henrissat, Harry J. Gilbert
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	Bacteroides human microbiota arabinogalactan glycan-degrading enzymes microbial ecology privileged nutrient Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/d4cbf81e8ac14385a892f1109659a480
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spelling	oai:doaj.org-article:d4cbf81e8ac14385a892f1109659a4802021-11-10T18:37:51ZSulfation of Arabinogalactan Proteins Confers Privileged Nutrient Status to <named-content content-type="genus-species">Bacteroides plebeius</named-content>10.1128/mBio.01368-212150-7511https://doaj.org/article/d4cbf81e8ac14385a892f1109659a4802021-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01368-21https://doaj.org/toc/2150-7511ABSTRACT The human gut microbiota (HGM) contributes to the physiology and health of its host. The health benefits provided by dietary manipulation of the HGM require knowledge of how glycans, the major nutrients available to this ecosystem, are metabolized. Arabinogalactan proteins (AGPs) are a ubiquitous feature of plant polysaccharides available to the HGM. Although the galactan backbone and galactooligosaccharide side chains of AGPs are conserved, the decorations of these structures are highly variable. Here, we tested the hypothesis that these variations in arabinogalactan decoration provide a selection mechanism for specific Bacteroides species within the HGM. The data showed that only a single bacterium, B. plebeius, grew on red wine AGP (Wi-AGP) and seaweed AGP (SW-AGP) in mono- or mixed culture. Wi-AGP thus acts as a privileged nutrient for a Bacteroides species within the HGM that utilizes marine and terrestrial plant glycans. The B. plebeius polysaccharide utilization loci (PULs) upregulated by AGPs encoded a polysaccharide lyase, located in the enzyme family GH145, which hydrolyzed Rha-Glc linkages in Wi-AGP. Further analysis of GH145 identified an enzyme with two active sites that displayed glycoside hydrolase and lyase activities, respectively, which conferred substrate flexibility for different AGPs. The AGP-degrading apparatus of B. plebeius also contained a sulfatase, BpS1_8, active on SW-AGP and Wi-AGP, which played a pivotal role in the utilization of these glycans by the bacterium. BpS1_8 enabled other Bacteroides species to access the sulfated AGPs, providing a route to introducing privileged nutrient utilization into probiotic and commensal organisms that could improve human health. IMPORTANCE Dietary manipulation of the HGM requires knowledge of how glycans available to this ecosystem are metabolized. The variable structures that decorate the core component of plant AGPs may influence their utilization by specific organisms within the HGM. Here, we evaluated the ability of Bacteroides species to utilize a marine and terrestrial AGP. The data showed that a single bacterium, B. plebeius, grew on Wi-AGP and SW-AGP in mono- or mixed culture. Wi-AGP is thus a privileged nutrient for a Bacteroides species that utilizes marine and terrestrial plant glycans. A key component of the AGP-degrading apparatus of B. plebeius is a sulfatase that conferred the ability of the bacterium to utilize these glycans. The enzyme enabled other Bacteroides species to access the sulfated AGPs, providing a route to introducing privileged nutrient utilization into probiotic and commensal organisms that could improve human health.Jose Munoz-MunozDidier NdehPedro Fernandez-JuliaGemma WaltonBernard HenrissatHarry J. GilbertAmerican Society for MicrobiologyarticleBacteroideshuman microbiotaarabinogalactanglycan-degrading enzymesmicrobial ecologyprivileged nutrientMicrobiologyQR1-502ENmBio, Vol 12, Iss 4 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Bacteroides human microbiota arabinogalactan glycan-degrading enzymes microbial ecology privileged nutrient Microbiology QR1-502
spellingShingle	Bacteroides human microbiota arabinogalactan glycan-degrading enzymes microbial ecology privileged nutrient Microbiology QR1-502 Jose Munoz-Munoz Didier Ndeh Pedro Fernandez-Julia Gemma Walton Bernard Henrissat Harry J. Gilbert Sulfation of Arabinogalactan Proteins Confers Privileged Nutrient Status to <named-content content-type="genus-species">Bacteroides plebeius</named-content>
description	ABSTRACT The human gut microbiota (HGM) contributes to the physiology and health of its host. The health benefits provided by dietary manipulation of the HGM require knowledge of how glycans, the major nutrients available to this ecosystem, are metabolized. Arabinogalactan proteins (AGPs) are a ubiquitous feature of plant polysaccharides available to the HGM. Although the galactan backbone and galactooligosaccharide side chains of AGPs are conserved, the decorations of these structures are highly variable. Here, we tested the hypothesis that these variations in arabinogalactan decoration provide a selection mechanism for specific Bacteroides species within the HGM. The data showed that only a single bacterium, B. plebeius, grew on red wine AGP (Wi-AGP) and seaweed AGP (SW-AGP) in mono- or mixed culture. Wi-AGP thus acts as a privileged nutrient for a Bacteroides species within the HGM that utilizes marine and terrestrial plant glycans. The B. plebeius polysaccharide utilization loci (PULs) upregulated by AGPs encoded a polysaccharide lyase, located in the enzyme family GH145, which hydrolyzed Rha-Glc linkages in Wi-AGP. Further analysis of GH145 identified an enzyme with two active sites that displayed glycoside hydrolase and lyase activities, respectively, which conferred substrate flexibility for different AGPs. The AGP-degrading apparatus of B. plebeius also contained a sulfatase, BpS1_8, active on SW-AGP and Wi-AGP, which played a pivotal role in the utilization of these glycans by the bacterium. BpS1_8 enabled other Bacteroides species to access the sulfated AGPs, providing a route to introducing privileged nutrient utilization into probiotic and commensal organisms that could improve human health. IMPORTANCE Dietary manipulation of the HGM requires knowledge of how glycans available to this ecosystem are metabolized. The variable structures that decorate the core component of plant AGPs may influence their utilization by specific organisms within the HGM. Here, we evaluated the ability of Bacteroides species to utilize a marine and terrestrial AGP. The data showed that a single bacterium, B. plebeius, grew on Wi-AGP and SW-AGP in mono- or mixed culture. Wi-AGP is thus a privileged nutrient for a Bacteroides species that utilizes marine and terrestrial plant glycans. A key component of the AGP-degrading apparatus of B. plebeius is a sulfatase that conferred the ability of the bacterium to utilize these glycans. The enzyme enabled other Bacteroides species to access the sulfated AGPs, providing a route to introducing privileged nutrient utilization into probiotic and commensal organisms that could improve human health.
format	article
author	Jose Munoz-Munoz Didier Ndeh Pedro Fernandez-Julia Gemma Walton Bernard Henrissat Harry J. Gilbert
author_facet	Jose Munoz-Munoz Didier Ndeh Pedro Fernandez-Julia Gemma Walton Bernard Henrissat Harry J. Gilbert
author_sort	Jose Munoz-Munoz
title	Sulfation of Arabinogalactan Proteins Confers Privileged Nutrient Status to <named-content content-type="genus-species">Bacteroides plebeius</named-content>
title_short	Sulfation of Arabinogalactan Proteins Confers Privileged Nutrient Status to <named-content content-type="genus-species">Bacteroides plebeius</named-content>
title_full	Sulfation of Arabinogalactan Proteins Confers Privileged Nutrient Status to <named-content content-type="genus-species">Bacteroides plebeius</named-content>
title_fullStr	Sulfation of Arabinogalactan Proteins Confers Privileged Nutrient Status to <named-content content-type="genus-species">Bacteroides plebeius</named-content>
title_full_unstemmed	Sulfation of Arabinogalactan Proteins Confers Privileged Nutrient Status to <named-content content-type="genus-species">Bacteroides plebeius</named-content>
title_sort	sulfation of arabinogalactan proteins confers privileged nutrient status to <named-content content-type="genus-species">bacteroides plebeius</named-content>
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/d4cbf81e8ac14385a892f1109659a480
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Sulfation of Arabinogalactan Proteins Confers Privileged Nutrient Status to <named-content content-type="genus-species">Bacteroides plebeius</named-content>

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