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A Genetically Adaptable Strategy for Ribose Scavenging in a Human Gut Symbiont Plays a Diet-Dependent Role in Colon Colonization

54 Pages Posted: 20 Mar 2019 Sneak Peek Status: Review Complete

See all articles by Robert W. P. Glowacki

Robert W. P. Glowacki

University of Michigan at Ann Arbor - Department of Microbiology and Immunology

Nicholas A. Pudlo

University of Michigan at Ann Arbor - Department of Microbiology and Immunology

Yunus Tuncil

Purdue University - Department of Food Science; Purdue University - Whistler Center for Carbohydrate Research

Ana S. Luis

University of Michigan at Ann Arbor - Department of Microbiology and Immunology

Anton I. Terekhov

Purdue University - Department of Food Science; Purdue University - Whistler Center for Carbohydrate Research

Bruce R. Hamaker

Purdue University - Department of Food Science; Purdue University - Whistler Center for Carbohydrate Research

Eric C. Martens

University of Michigan at Ann Arbor - Department of Microbiology and Immunology

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Abstract

Efficient nutrient acquisition in the competitive human gut is essential for microbial persistence. While polysaccharides have been well-studied nutrients for the gut microbiome, other resources such as co-factors and nucleic acids have been less examined. We describe a series of ribose utilization systems (RUSs) that are broadly represented in Bacteroidetes and appear to have diversified to allow access to ribose from a variety of substrates. One Bacteroides thetaiotaomicron RUS variant is critical for competitive gut colonization in a diet-specific fashion. Using molecular genetics, we probed the nature of the ribose source underlying this dietspecific phenotype, revealing that hydrolytic functions in RUS (e.g., to cleave ribonucleosides) are present but dispensable. Instead, ribokinases that are activated in vivo and participate in cellular ribose-phosphate metabolism are essential. Our results underscore the extensive mechanisms that gut symbionts have evolved to access nutrients and how metabolic context determines the impact of these functions in vivo

Keywords: symbiosis, mutualist, microbiome, nutrient acquisition, Bacteroides

Suggested Citation

Glowacki, Robert W. P. and Pudlo, Nicholas A. and Tuncil, Yunus and Luis, Ana S. and Terekhov, Anton I. and Hamaker, Bruce R. and Martens, Eric C., A Genetically Adaptable Strategy for Ribose Scavenging in a Human Gut Symbiont Plays a Diet-Dependent Role in Colon Colonization (March 19, 2019). Available at SSRN: https://ssrn.com/abstract=3354892 or http://dx.doi.org/10.2139/ssrn.3354892
This is a paper under consideration at Cell Press and has not been peer-reviewed.

Robert W. P. Glowacki (Contact Author)

University of Michigan at Ann Arbor - Department of Microbiology and Immunology

Ann Arbor, MI 48109
United States

Nicholas A. Pudlo

University of Michigan at Ann Arbor - Department of Microbiology and Immunology

Ann Arbor, MI 48109
United States

Yunus Tuncil

Purdue University - Department of Food Science

West Lafayette, IN 47907
United States

Purdue University - Whistler Center for Carbohydrate Research

West Lafayette, IN 47907
United States

Ana S. Luis

University of Michigan at Ann Arbor - Department of Microbiology and Immunology

Ann Arbor, MI 48109
United States

Anton I. Terekhov

Purdue University - Department of Food Science

West Lafayette, IN 47907
United States

Purdue University - Whistler Center for Carbohydrate Research

West Lafayette, IN 47907
United States

Bruce R. Hamaker

Purdue University - Department of Food Science

West Lafayette, IN 47907
United States

Purdue University - Whistler Center for Carbohydrate Research

West Lafayette, IN 47907
United States

Eric C. Martens

University of Michigan at Ann Arbor - Department of Microbiology and Immunology ( email )

Ann Arbor, MI 48109
United States

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