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Phenotypic and genomic diversification in complex carbohydrate degrading human gut bacteria

Nicholas A. Pudlo, Karthik Urs, Ryan Crawford, Ali Pirani, Todd Atherly, Roberto Jimenez, Nicolas Terrapon, Bernard Henrissat, Daniel Peterson, Cherie Ziemer, Evan Snitkin, Eric C. Martens
doi: https://doi.org/10.1101/2021.07.15.452266
Nicholas A. Pudlo
1Department of Microbiology and Immunology, University of Michigan Medical School, Ann Arbor, MI 48109
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Karthik Urs
1Department of Microbiology and Immunology, University of Michigan Medical School, Ann Arbor, MI 48109
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Ryan Crawford
2Department of Computational Medicine and Bioinformatics, University of Michigan Medical School, Ann Arbor, MI 48109
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Ali Pirani
1Department of Microbiology and Immunology, University of Michigan Medical School, Ann Arbor, MI 48109
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Todd Atherly
3Iowa State University, Dept. of Animal Science, Ames, IA
4United States Department of Agriculture Agricultural Research Station, Ames, IA
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Roberto Jimenez
5University of Nebraska, Department of Food Sciences, Lincoln, NE
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Nicolas Terrapon
6Aix Marseille Univ, CNRS, UMR7257 AFMB, Marseille, France
7INRAE, USC1408 AFMB, Marseille, France
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Bernard Henrissat
6Aix Marseille Univ, CNRS, UMR7257 AFMB, Marseille, France
7INRAE, USC1408 AFMB, Marseille, France
8Department of Biological Sciences, King Abdulaziz University, Jeddah, Saudi Arabia
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Daniel Peterson
5University of Nebraska, Department of Food Sciences, Lincoln, NE
9Johns Hopkins University, Department of Pathology, Baltimore, MD
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Cherie Ziemer
3Iowa State University, Dept. of Animal Science, Ames, IA
4United States Department of Agriculture Agricultural Research Station, Ames, IA
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Evan Snitkin
1Department of Microbiology and Immunology, University of Michigan Medical School, Ann Arbor, MI 48109
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Eric C. Martens
1Department of Microbiology and Immunology, University of Michigan Medical School, Ann Arbor, MI 48109
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  • For correspondence: emartens@umich.edu
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Abstract

Symbiotic bacteria are responsible for the majority of complex carbohydrate digestion in the human colon. Since the identities and amounts of dietary polysaccharides directly impact the gut microbiota, determining which microorganisms consume specific nutrients is central to defining the relationship between diet and gut microbial ecology. Using a custom phenotyping array, we determined carbohydrate utilization profiles for 354 members of the Bacteroidetes, a dominant saccharolytic phylum. There was wide variation in the numbers and types of substrates degraded by individual bacteria, but phenotype-based clustering grouped members of the same species indicating that each species performs characteristic roles. The ability to utilize dietary polysaccharides and endogenous mucin glycans was negatively correlated, suggesting exclusion between these niches. By analyzing related Bacteroides ovatus/xylanisolvens strains that vary in their ability to utilize mucin glycans, we addressed whether gene clusters that confer this complex, multi-locus trait are being gained or lost in individual strains. Pangenome reconstruction of these strains revealed a remarkably mosaic architecture in which genes involved in polysaccharide metabolism are highly variable and bioinformatics data provide evidence of interspecies gene transfer that might explain this genomic heterogeneity. Global transcriptomic analyses suggest that the ability to utilize mucin has been lost in some lineages of B. ovatus and B. xylanisolvens, which still harbor residual gene clusters that are involved in mucin utilization by strains that still actively express this phenotype. Our data provide insight into the breadth and complexity of carbohydrate metabolism in the microbiome and the underlying genomic events that shape these behaviors.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC 4.0 International license.
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Phenotypic and genomic diversification in complex carbohydrate degrading human gut bacteria
Nicholas A. Pudlo, Karthik Urs, Ryan Crawford, Ali Pirani, Todd Atherly, Roberto Jimenez, Nicolas Terrapon, Bernard Henrissat, Daniel Peterson, Cherie Ziemer, Evan Snitkin, Eric C. Martens
bioRxiv 2021.07.15.452266; doi: https://doi.org/10.1101/2021.07.15.452266
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Phenotypic and genomic diversification in complex carbohydrate degrading human gut bacteria
Nicholas A. Pudlo, Karthik Urs, Ryan Crawford, Ali Pirani, Todd Atherly, Roberto Jimenez, Nicolas Terrapon, Bernard Henrissat, Daniel Peterson, Cherie Ziemer, Evan Snitkin, Eric C. Martens
bioRxiv 2021.07.15.452266; doi: https://doi.org/10.1101/2021.07.15.452266

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