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Title: Polysaccharide utilization loci in Bacteroides determine population fitness and community-level interactions

Journal Article · · Cell Host & Microbe

Polysaccharide utilization loci (PULs) are co-regulated bacterial genes that sense nutrients and enable glycan digestion. Human gut microbiome members, notably Bacteroides, contain numerous PULs that enable glycan utilization and shape ecological dynamics. To investigate the role of PULs on fitness and inter-species interactions, we develop a CRISPR-based genome editing tool to study 23 PULs in Bacteroides uniformis (BU). BU PULs show distinct glycan-degrading functions and transcriptional coordination that enables the population to adapt upon loss of other PULs. Exploiting a BU mutant barcoding strategy, we demonstrate that in vitro fitness and BU colonization in the murine gut are enhanced by deletion of specific PULs and modulated by glycan availability. PULs mediate glycan-dependent interactions with butyrate producers that depend on the degradation mechanism and glycan utilization ability of the butyrate producer. Thus, PULs determine community dynamics and butyrate production and provide a selective advantage or disadvantage depending on the nutritional landscape.

Research Organization:
University of Wisconsin, Madison, WI (United States)
Sponsoring Organization:
USDOE Office of Science (SC); National Institutes of Health (NIH); National Institute of Biomedical Imaging and Bioengineering; Multi University Research Initiative (MURI)
Grant/Contract Number:
FC02-07ER64494
OSTI ID:
1976962
Journal Information:
Cell Host & Microbe, Journal Name: Cell Host & Microbe Journal Issue: 2 Vol. 30; ISSN 1931-3128
Publisher:
ElsevierCopyright Statement
Country of Publication:
United States
Language:
English

References (93)

A β-mannan utilization locus in Bacteroides ovatus involves a GH36 α-galactosidase active on galactomannans journal June 2016
Laboratory Maintenance and Cultivation of Bacteroides Species journal May 2008
Specificity of Polysaccharide Use in Intestinal Bacteroides Species Determines Diet-Induced Microbiota Alterations journal June 2010
Cpf1 Is a Single RNA-Guided Endonuclease of a Class 2 CRISPR-Cas System journal October 2015
From Dietary Fiber to Host Physiology: Short-Chain Fatty Acids as Key Bacterial Metabolites journal June 2016
A Dietary Fiber-Deprived Gut Microbiota Degrades the Colonic Mucus Barrier and Enhances Pathogen Susceptibility journal November 2016
Tunable Expression Tools Enable Single-Cell Strain Distinction in the Gut Microbiome journal April 2017
Engineered Regulatory Systems Modulate Gene Expression of Human Commensals in the Gut journal April 2017
Extensive Unexplored Human Microbiome Diversity Revealed by Over 150,000 Genomes from Metagenomes Spanning Age, Geography, and Lifestyle journal January 2019
Programming a Human Commensal Bacterium, Bacteroides thetaiotaomicron, to Sense and Respond to Stimuli in the Murine Gut Microbiota journal July 2015
Mucosal Glycan Foraging Enhances Fitness and Transmission of a Saccharolytic Human Gut Bacterial Symbiont journal November 2008
Eating For Two: How Metabolism Establishes Interspecies Interactions in the Gut journal October 2011
Modulation of a Circulating Uremic Solute via Rational Genetic Manipulation of the Gut Microbiota journal December 2016
The Impact of Dietary Fiber on Gut Microbiota in Host Health and Disease journal June 2018
Adaptive Evolution within Gut Microbiomes of Healthy People journal May 2019
Distinct Polysaccharide Utilization Profiles of Human Intestinal Prevotella copri Isolates journal November 2019
An Ecological Network of Polysaccharide Utilization among Human Intestinal Symbionts journal January 2014
Development of a novel plasmid vector pTIO-1 adapted for electrotransformation of Porphyromonas gingivalis journal October 2014
Starch Catabolism by a Prominent Human Gut Symbiont Is Directed by the Recognition of Amylose Helices journal July 2008
A human gut microbial gene catalogue established by metagenomic sequencing journal March 2010
A discrete genetic locus confers xyloglucan metabolism in select human gut Bacteroidetes journal January 2014
Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism journal January 2015
The evolution of cooperation within the gut microbiota journal April 2016
Complex pectin metabolism by gut bacteria reveals novel catalytic functions journal March 2017
Glycan complexity dictates microbial resource allocation in the large intestine journal June 2015
Fast and sensitive protein alignment using DIAMOND journal November 2014
An insider's perspective: Bacteroides as a window into the microbiome journal April 2017
The Phyre2 web portal for protein modeling, prediction and analysis journal May 2015
How glycan metabolism shapes the human gut microbiota journal April 2012
The abundance and variety of carbohydrate-active enzymes in the human gut microbiota journal June 2013
Molecular basis of an agarose metabolic pathway acquired by a human intestinal symbiont journal March 2018
Bacteroidetes use thousands of enzyme combinations to break down glycans journal May 2019
Metabolism of multiple glycosaminoglycans by Bacteroides thetaiotaomicron is orchestrated by a versatile core genetic locus journal January 2020
Design of synthetic human gut microbiome assembly and butyrate production journal May 2021
Dietary pectic glycans are degraded by coordinated enzyme pathways in human colonic Bacteroides journal December 2017
A surface endogalactanase in Bacteroides thetaiotaomicron confers keystone status for arabinogalactan degradation journal October 2018
Complex N-glycan breakdown by gut Bacteroides involves an extensive enzymatic apparatus encoded by multiple co-regulated genetic loci journal June 2019
Gut microbiota in human metabolic health and disease journal September 2020
A new genomic blueprint of the human gut microbiota journal February 2019
SignalP 5.0 improves signal peptide predictions using deep neural networks journal February 2019
A unified catalog of 204,938 reference genomes from the human gut microbiome journal July 2020
A mitochondrial-like aconitase in the bacterium Bacteroides fragilis : Implications for the evolution of the mitochondrial Krebs cycle journal March 2002
Characterizing a model human gut microbiota composed of members of its two dominant bacterial phyla journal March 2009
Extensive personal human gut microbiota culture collections characterized and manipulated in gnotobiotic mice journal March 2011
One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products journal May 2000
Gnotobiotic mouse model of phage-bacterial host dynamics in the human gut journal November 2013
Coordinate Regulation of Glycan Degradation and Polysaccharide Capsule Biosynthesis by a Prominent Human Gut Symbiont journal July 2009
Dissecting the in Vivo Metabolic Potential of Two Human Gut Acetogens journal May 2010
Galactomannan Catabolism Conferred by a Polysaccharide Utilization Locus of Bacteroides ovatus : ENZYME SYNERGY AND CRYSTAL STRUCTURE OF A β-MANNANASE journal November 2016
Complex Glycan Catabolism by the Human Gut Microbiota: The Bacteroidetes Sus-like Paradigm journal June 2009
Contribution of acetate to butyrate formation by human faecal bacteria journal June 2004
PSLpred: prediction of subcellular localization of bacterial proteins journal February 2005
PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes journal May 2010
PEAR: a fast and accurate Illumina Paired-End reAd mergeR journal October 2013
featureCounts: an efficient general purpose program for assigning sequence reads to genomic features journal November 2013
Heavy-tailed prior distributions for sequence count data: removing the noise and preserving large differences journal November 2018
GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database journal November 2019
PULDB: the expanded database of Polysaccharide Utilization Loci journal October 2017
dbCAN2: a meta server for automated carbohydrate-active enzyme annotation journal May 2018
Structural dissection of a complex Bacteroides ovatus gene locus conferring xyloglucan metabolism in the human gut journal July 2016
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes journal May 2015
Glycan Foraging in Vivo by an Intestine-Adapted Bacterial Symbiont journal March 2005
Adaptation of Syntenic Xyloglucan Utilization Loci of Human Gut Bacteroidetes to Polysaccharide Side Chain Diversity journal August 2019
Reduced Dietary Intake of Carbohydrates by Obese Subjects Results in Decreased Concentrations of Butyrate and Butyrate-Producing Bacteria in Feces journal December 2006
Characterization of the Primary Starch Utilization Operon in the Obligate Anaerobe Bacteroides fragilis : Regulation by Carbon Source and Oxygen journal July 2006
Physiological Characterization of SusG, an Outer Membrane Protein Essential for Starch Utilization byBacteroides thetaiotaomicron journal December 1999
Characterization of a Bacteroides Mobilizable Transposon, NBU2, Which Carries a Functional Lincomycin Resistance Gene journal June 2000
Characterization of Four Outer Membrane Proteins Involved in Binding Starch to the Cell Surface ofBacteroides thetaiotaomicron journal October 2000
Location and characterization of genes involved in binding of starch to the surface of Bacteroides thetaiotaomicron. journal September 1992
Synergy between Cell Surface Glycosidases and Glycan-Binding Proteins Dictates the Utilization of Specific Beta(1,3)-Glucans by Human Gut Bacteroides journal April 2020
Reciprocal Prioritization to Dietary Glycans by Gut Bacteria in a Competitive Environment Promotes Stable Coexistence journal October 2017
Multiple Signals Govern Utilization of a Polysaccharide in the Gut Bacterium Bacteroides thetaiotaomicron journal October 2016
Streamlined Genetic Manipulation of Diverse Bacteroides and Parabacteroides Isolates from the Human Gut Microbiota journal August 2019
Molecular Dissection of Xyloglucan Recognition in a Prominent Human Gut Symbiont journal April 2016
Intestinal IgA Regulates Expression of a Fructan Polysaccharide Utilization Locus in Colonizing Gut Commensal Bacteroides thetaiotaomicron journal November 2019
The Critical Roles of Polysaccharides in Gut Microbial Ecology and Physiology journal September 2017
Prodigal: prokaryotic gene recognition and translation initiation site identification journal March 2010
Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes journal June 2002
Xylan degradation by the human gut Bacteroides xylanisolvens XB1AT involves two distinct gene clusters that are linked at the transcriptional level journal May 2016
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 journal December 2014
The healthy human microbiome journal April 2016
Recognition and Degradation of Plant Cell Wall Polysaccharides by Two Human Gut Symbionts journal December 2011
Population Diversification in a Yeast Metabolic Program Promotes Anticipation of Environmental Shifts journal January 2015
Complex Carbohydrate Utilization by the Healthy Human Microbiome journal June 2012
CELLO2GO: A Web Server for Protein subCELlular LOcalization Prediction with Functional Gene Ontology Annotation journal June 2014
Deciphering microbial interactions in synthetic human gut microbiome communities journal June 2018
An Adaptive Metropolis Algorithm journal April 2001
The Glycolytic Versatility of Bacteroides uniformis CECT 7771 and Its Genome Response to Oligo and Polysaccharides journal August 2017
Bacteroides thetaiotaomicron Starch Utilization Promotes Quercetin Degradation and Butyrate Production by Eubacterium ramulus journal May 2019
Metabolism of Glycosphingolipids and Their Role in the Pathophysiology of Lysosomal Storage Disorders journal September 2020
Degradation of Marine Algae-Derived Carbohydrates by Bacteroidetes Isolated from Human Gut Microbiota journal March 2017
Bacteroides thetaiotaomicron Fosters the Growth of Butyrate-Producing Anaerostipes caccae in the Presence of Lactose and Total Human Milk Carbohydrates journal October 2020
Polysaccharide utilization loci in Bacteroides determine population fitness and community-level interactions dataset January 2021