Symbiotic Human Gut Bacteria with Variable Metabolic Priorities for Host Mucosal Glycans

ABSTRACT Many symbiotic gut bacteria possess the ability to degrade multiple polysaccharides, thereby providing nutritional advantages to their hosts. Like microorganisms adapted to other complex nutrient environments, gut symbionts give different metabolic priorities to substrates present in mixtur...

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Autores principales:	Nicholas A. Pudlo, Karthik Urs, Supriya Suresh Kumar, J. Bruce German, David A. Mills, Eric C. Martens
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2015
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/33918e25a38b475b9339fefd485c2f0b
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spelling	oai:doaj.org-article:33918e25a38b475b9339fefd485c2f0b2021-11-15T15:41:24ZSymbiotic Human Gut Bacteria with Variable Metabolic Priorities for Host Mucosal Glycans10.1128/mBio.01282-152150-7511https://doaj.org/article/33918e25a38b475b9339fefd485c2f0b2015-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01282-15https://doaj.org/toc/2150-7511ABSTRACT Many symbiotic gut bacteria possess the ability to degrade multiple polysaccharides, thereby providing nutritional advantages to their hosts. Like microorganisms adapted to other complex nutrient environments, gut symbionts give different metabolic priorities to substrates present in mixtures. We investigated the responses of Bacteroides thetaiotaomicron, a common human intestinal bacterium that metabolizes more than a dozen different polysaccharides, including the O-linked glycans that are abundant in secreted mucin. Experiments in which mucin glycans were presented simultaneously with other carbohydrates show that degradation of these host carbohydrates is consistently repressed in the presence of alternative substrates, even by B. thetaiotaomicron previously acclimated to growth in pure mucin glycans. Experiments with media containing systematically varied carbohydrate cues and genetic mutants reveal that transcriptional repression of genes involved in mucin glycan metabolism is imposed by simple sugars and, in one example that was tested, is mediated through a small intergenic region in a transcript-autonomous fashion. Repression of mucin glycan-responsive gene clusters in two other human gut bacteria, Bacteroides massiliensis and Bacteroides fragilis, exhibited variable and sometimes reciprocal responses compared to those of B. thetaiotaomicron, revealing that these symbionts vary in their preference for mucin glycans and that these differences occur at the level of controlling individual gene clusters. Our results reveal that sensing and metabolic triaging of glycans are complex processes that vary among species, underscoring the idea that these phenomena are likely to be hidden drivers of microbiota community dynamics and may dictate which microorganisms preferentially commit to various niches in a constantly changing nutritional environment. IMPORTANCE Human intestinal microorganisms impact many aspects of health and disease, including digestion and the propensity to develop disorders such as inflammation and colon cancer. Complex carbohydrates are a major component of the intestinal habitat, and numerous species have evolved and refined strategies to compete for these coveted nutrients. Our findings reveal that individual bacteria exhibit different preferences for carbohydrates emanating from host diet and mucosal secretions and that some of these prioritization strategies are opposite to one another. Thus, we reveal new aspects of how individual bacteria, some with otherwise similar metabolic potential, partition to “preferred niches” in the complex gut ecosystem, which has important and immediate implications for understanding and predicting the behavioral dynamics of this community.Nicholas A. PudloKarthik UrsSupriya Suresh KumarJ. Bruce GermanDavid A. MillsEric C. MartensAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 6 (2015)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Nicholas A. Pudlo Karthik Urs Supriya Suresh Kumar J. Bruce German David A. Mills Eric C. Martens Symbiotic Human Gut Bacteria with Variable Metabolic Priorities for Host Mucosal Glycans
description	ABSTRACT Many symbiotic gut bacteria possess the ability to degrade multiple polysaccharides, thereby providing nutritional advantages to their hosts. Like microorganisms adapted to other complex nutrient environments, gut symbionts give different metabolic priorities to substrates present in mixtures. We investigated the responses of Bacteroides thetaiotaomicron, a common human intestinal bacterium that metabolizes more than a dozen different polysaccharides, including the O-linked glycans that are abundant in secreted mucin. Experiments in which mucin glycans were presented simultaneously with other carbohydrates show that degradation of these host carbohydrates is consistently repressed in the presence of alternative substrates, even by B. thetaiotaomicron previously acclimated to growth in pure mucin glycans. Experiments with media containing systematically varied carbohydrate cues and genetic mutants reveal that transcriptional repression of genes involved in mucin glycan metabolism is imposed by simple sugars and, in one example that was tested, is mediated through a small intergenic region in a transcript-autonomous fashion. Repression of mucin glycan-responsive gene clusters in two other human gut bacteria, Bacteroides massiliensis and Bacteroides fragilis, exhibited variable and sometimes reciprocal responses compared to those of B. thetaiotaomicron, revealing that these symbionts vary in their preference for mucin glycans and that these differences occur at the level of controlling individual gene clusters. Our results reveal that sensing and metabolic triaging of glycans are complex processes that vary among species, underscoring the idea that these phenomena are likely to be hidden drivers of microbiota community dynamics and may dictate which microorganisms preferentially commit to various niches in a constantly changing nutritional environment. IMPORTANCE Human intestinal microorganisms impact many aspects of health and disease, including digestion and the propensity to develop disorders such as inflammation and colon cancer. Complex carbohydrates are a major component of the intestinal habitat, and numerous species have evolved and refined strategies to compete for these coveted nutrients. Our findings reveal that individual bacteria exhibit different preferences for carbohydrates emanating from host diet and mucosal secretions and that some of these prioritization strategies are opposite to one another. Thus, we reveal new aspects of how individual bacteria, some with otherwise similar metabolic potential, partition to “preferred niches” in the complex gut ecosystem, which has important and immediate implications for understanding and predicting the behavioral dynamics of this community.
format	article
author	Nicholas A. Pudlo Karthik Urs Supriya Suresh Kumar J. Bruce German David A. Mills Eric C. Martens
author_facet	Nicholas A. Pudlo Karthik Urs Supriya Suresh Kumar J. Bruce German David A. Mills Eric C. Martens
author_sort	Nicholas A. Pudlo
title	Symbiotic Human Gut Bacteria with Variable Metabolic Priorities for Host Mucosal Glycans
title_short	Symbiotic Human Gut Bacteria with Variable Metabolic Priorities for Host Mucosal Glycans
title_full	Symbiotic Human Gut Bacteria with Variable Metabolic Priorities for Host Mucosal Glycans
title_fullStr	Symbiotic Human Gut Bacteria with Variable Metabolic Priorities for Host Mucosal Glycans
title_full_unstemmed	Symbiotic Human Gut Bacteria with Variable Metabolic Priorities for Host Mucosal Glycans
title_sort	symbiotic human gut bacteria with variable metabolic priorities for host mucosal glycans
publisher	American Society for Microbiology
publishDate	2015
url	https://doaj.org/article/33918e25a38b475b9339fefd485c2f0b
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Symbiotic Human Gut Bacteria with Variable Metabolic Priorities for Host Mucosal Glycans

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