Genetic Variation of the SusC/SusD Homologs from a Polysaccharide Utilization Locus Underlies Divergent Fructan Specificities and Functional Adaptation in <italic toggle="yes">Bacteroides thetaiotaomicron</italic> Strains

ABSTRACT Genomic differences between gut-resident bacterial strains likely underlie significant interindividual variation in microbiome function. Traditional methods of determining community composition, such as 16S rRNA gene amplicon sequencing, fail to capture this functional diversity. Metagenomi...

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Autores principales:	Payal Joglekar, Erica D. Sonnenburg, Steven K. Higginbottom, Kristen A. Earle, Carl Morland, Sarah Shapiro-Ward, David N. Bolam, Justin L. Sonnenburg
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Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	Bacteroides microbiome polysaccharide utilization locus Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/e02fbe6683e9432eaef60450c3075033
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spelling	oai:doaj.org-article:e02fbe6683e9432eaef60450c30750332021-11-15T15:24:22ZGenetic Variation of the SusC/SusD Homologs from a Polysaccharide Utilization Locus Underlies Divergent Fructan Specificities and Functional Adaptation in <italic toggle="yes">Bacteroides thetaiotaomicron</italic> Strains10.1128/mSphereDirect.00185-182379-5042https://doaj.org/article/e02fbe6683e9432eaef60450c30750332018-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphereDirect.00185-18https://doaj.org/toc/2379-5042ABSTRACT Genomic differences between gut-resident bacterial strains likely underlie significant interindividual variation in microbiome function. Traditional methods of determining community composition, such as 16S rRNA gene amplicon sequencing, fail to capture this functional diversity. Metagenomic approaches are a significant step forward in identifying strain-level sequence variants; however, given the current paucity of biochemical information, they too are limited to mainly low-resolution and incomplete functional predictions. Using genomic, biochemical, and molecular approaches, we identified differences in the fructan utilization profiles of two closely related Bacteroides thetaiotaomicron strains. B. thetaiotaomicron 8736 (Bt-8736) contains a fructan polysaccharide utilization locus (PUL) with a divergent susC/susD homolog gene pair that enables it to utilize inulin, differentiating this strain from other characterized Bt strains. Transfer of the distinct pair of susC/susD genes from Bt-8736 into the noninulin using type strain B. thetaiotaomicron VPI-5482 resulted in inulin use by the recipient strain, Bt(8736-2). The presence of the divergent susC/susD gene pair alone enabled the hybrid Bt(8736-2) strain to outcompete the wild-type strain in vivo in mice fed an inulin diet. Further, we discovered that the susC/susD homolog gene pair facilitated import of inulin into the periplasm without surface predigestion by an endo-acting enzyme, possibly due to the short average chain length of inulin compared to many other polysaccharides. Our data builds upon recent reports of dietary polysaccharide utilization mechanisms found in members of the Bacteroides genus and demonstrates how the acquisition of two genes can alter the functionality and success of a strain within the gut. IMPORTANCE Dietary polysaccharides play a dominant role in shaping the composition and functionality of our gut microbiota. Dietary interventions using these microbiota-accessible carbohydrates (MACs) serve as a promising tool for manipulating the gut microbial community. However, our current gap in knowledge regarding microbial metabolic pathways that are involved in the degradation of these MACs has made the design of rational interventions difficult. The issue is further complicated by the diversity of pathways observed for the utilization of similar MACs, even in closely related microbial strains. Our current work focuses on divergent fructan utilization pathways in two closely related B. thetaiotaomicron strains and provides an integrated approach to characterize the molecular basis for strain-level functional differences.Payal JoglekarErica D. SonnenburgSteven K. HigginbottomKristen A. EarleCarl MorlandSarah Shapiro-WardDavid N. BolamJustin L. SonnenburgAmerican Society for MicrobiologyarticleBacteroidesmicrobiomepolysaccharide utilization locusMicrobiologyQR1-502ENmSphere, Vol 3, Iss 3 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	Bacteroides microbiome polysaccharide utilization locus Microbiology QR1-502
spellingShingle	Bacteroides microbiome polysaccharide utilization locus Microbiology QR1-502 Payal Joglekar Erica D. Sonnenburg Steven K. Higginbottom Kristen A. Earle Carl Morland Sarah Shapiro-Ward David N. Bolam Justin L. Sonnenburg Genetic Variation of the SusC/SusD Homologs from a Polysaccharide Utilization Locus Underlies Divergent Fructan Specificities and Functional Adaptation in <italic toggle="yes">Bacteroides thetaiotaomicron</italic> Strains
description	ABSTRACT Genomic differences between gut-resident bacterial strains likely underlie significant interindividual variation in microbiome function. Traditional methods of determining community composition, such as 16S rRNA gene amplicon sequencing, fail to capture this functional diversity. Metagenomic approaches are a significant step forward in identifying strain-level sequence variants; however, given the current paucity of biochemical information, they too are limited to mainly low-resolution and incomplete functional predictions. Using genomic, biochemical, and molecular approaches, we identified differences in the fructan utilization profiles of two closely related Bacteroides thetaiotaomicron strains. B. thetaiotaomicron 8736 (Bt-8736) contains a fructan polysaccharide utilization locus (PUL) with a divergent susC/susD homolog gene pair that enables it to utilize inulin, differentiating this strain from other characterized Bt strains. Transfer of the distinct pair of susC/susD genes from Bt-8736 into the noninulin using type strain B. thetaiotaomicron VPI-5482 resulted in inulin use by the recipient strain, Bt(8736-2). The presence of the divergent susC/susD gene pair alone enabled the hybrid Bt(8736-2) strain to outcompete the wild-type strain in vivo in mice fed an inulin diet. Further, we discovered that the susC/susD homolog gene pair facilitated import of inulin into the periplasm without surface predigestion by an endo-acting enzyme, possibly due to the short average chain length of inulin compared to many other polysaccharides. Our data builds upon recent reports of dietary polysaccharide utilization mechanisms found in members of the Bacteroides genus and demonstrates how the acquisition of two genes can alter the functionality and success of a strain within the gut. IMPORTANCE Dietary polysaccharides play a dominant role in shaping the composition and functionality of our gut microbiota. Dietary interventions using these microbiota-accessible carbohydrates (MACs) serve as a promising tool for manipulating the gut microbial community. However, our current gap in knowledge regarding microbial metabolic pathways that are involved in the degradation of these MACs has made the design of rational interventions difficult. The issue is further complicated by the diversity of pathways observed for the utilization of similar MACs, even in closely related microbial strains. Our current work focuses on divergent fructan utilization pathways in two closely related B. thetaiotaomicron strains and provides an integrated approach to characterize the molecular basis for strain-level functional differences.
format	article
author	Payal Joglekar Erica D. Sonnenburg Steven K. Higginbottom Kristen A. Earle Carl Morland Sarah Shapiro-Ward David N. Bolam Justin L. Sonnenburg
author_facet	Payal Joglekar Erica D. Sonnenburg Steven K. Higginbottom Kristen A. Earle Carl Morland Sarah Shapiro-Ward David N. Bolam Justin L. Sonnenburg
author_sort	Payal Joglekar
title	Genetic Variation of the SusC/SusD Homologs from a Polysaccharide Utilization Locus Underlies Divergent Fructan Specificities and Functional Adaptation in <italic toggle="yes">Bacteroides thetaiotaomicron</italic> Strains
title_short	Genetic Variation of the SusC/SusD Homologs from a Polysaccharide Utilization Locus Underlies Divergent Fructan Specificities and Functional Adaptation in <italic toggle="yes">Bacteroides thetaiotaomicron</italic> Strains
title_full	Genetic Variation of the SusC/SusD Homologs from a Polysaccharide Utilization Locus Underlies Divergent Fructan Specificities and Functional Adaptation in <italic toggle="yes">Bacteroides thetaiotaomicron</italic> Strains
title_fullStr	Genetic Variation of the SusC/SusD Homologs from a Polysaccharide Utilization Locus Underlies Divergent Fructan Specificities and Functional Adaptation in <italic toggle="yes">Bacteroides thetaiotaomicron</italic> Strains
title_full_unstemmed	Genetic Variation of the SusC/SusD Homologs from a Polysaccharide Utilization Locus Underlies Divergent Fructan Specificities and Functional Adaptation in <italic toggle="yes">Bacteroides thetaiotaomicron</italic> Strains
title_sort	genetic variation of the susc/susd homologs from a polysaccharide utilization locus underlies divergent fructan specificities and functional adaptation in <italic toggle="yes">bacteroides thetaiotaomicron</italic> strains
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/e02fbe6683e9432eaef60450c3075033
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Genetic Variation of the SusC/SusD Homologs from a Polysaccharide Utilization Locus Underlies Divergent Fructan Specificities and Functional Adaptation in <italic toggle="yes">Bacteroides thetaiotaomicron</italic> Strains

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