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Food Microbiology | Spotlight

A Human Gut Commensal Ferments Cranberry Carbohydrates To Produce Formate

Ezgi Özcan, Jiadong Sun, David C. Rowley, David A. Sela
Christopher A. Elkins, Editor
Ezgi Özcan
aDepartment of Food Science, University of Massachusetts, Amherst, Massachusetts, USA
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Jiadong Sun
bCollege of Pharmacy, University of Rhode Island, Kingston, Rhode Island, USA
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David C. Rowley
bCollege of Pharmacy, University of Rhode Island, Kingston, Rhode Island, USA
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David A. Sela
aDepartment of Food Science, University of Massachusetts, Amherst, Massachusetts, USA
cCenter for Microbiome Research, University of Massachusetts Medical School, Worcester, Massachusetts, USA
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Christopher A. Elkins
FDA Center for Food Safety and Applied Nutrition
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DOI: 10.1128/AEM.01097-17
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ABSTRACT

Commensal bifidobacteria colonize the human gastrointestinal tract and catabolize glycans that are impervious to host digestion. Accordingly, Bifidobacterium longum typically secretes acetate and lactate as fermentative end products. This study tested the hypothesis that B. longum utilizes cranberry-derived xyloglucans in a strain-dependent manner. Interestingly, the B. longum strain that efficiently utilizes cranberry xyloglucans secretes 2.0 to 2.5 mol of acetate-lactate. The 1.5 acetate:lactate ratio theoretical yield obtained in hexose fermentations shifts during xyloglucan metabolism. Accordingly, this metabolic shift is characterized by increased acetate and formate production at the expense of lactate. α-l-Arabinofuranosidase, an arabinan endo-1,5-α-l-arabinosidase, and a β-xylosidase with a carbohydrate substrate-binding protein and carbohydrate ABC transporter membrane proteins are upregulated (>2-fold change), which suggests carbon flux through this catabolic pathway. Finally, syntrophic interactions occurred with strains that utilize carbohydrate products derived from initial degradation from heterologous bacteria.

IMPORTANCE This was a study of bacterial metabolism of complex cranberry carbohydrates termed xyloglucans that are likely not digested prior to reaching the colon. This is significant, as bifidobacteria interact with this dietary compound to potentially impact human host health through energy and metabolite production by utilizing these substrates. Specific bacterial strains utilize cranberry xyloglucans as a nutritive source, indicating unknown mechanisms that are not universal in bifidobacteria. In addition, xyloglucan metabolism proceeds by using an alternative pathway that could lead to further research to investigate mechanisms underlying this interaction. Finally, we observed cross-feeding between bacteria in which one strain degrades the cranberry xyloglucan to make it available to a second strain. Similar nutritive strategies are known to occur within the gut. In aggregate, this study may lead to novel foods or supplements used to impact human health through rational manipulation of the human microbiome.

FOOTNOTES

    • Received 15 May 2017.
    • Accepted 22 June 2017.
    • Accepted manuscript posted online 30 June 2017.
  • Supplemental material for this article may be found at https://doi.org/10.1128/AEM.01097-17 .

  • Copyright © 2017 American Society for Microbiology.

All Rights Reserved .

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A Human Gut Commensal Ferments Cranberry Carbohydrates To Produce Formate
Ezgi Özcan, Jiadong Sun, David C. Rowley, David A. Sela
Applied and Environmental Microbiology Aug 2017, 83 (17) e01097-17; DOI: 10.1128/AEM.01097-17

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A Human Gut Commensal Ferments Cranberry Carbohydrates To Produce Formate
Ezgi Özcan, Jiadong Sun, David C. Rowley, David A. Sela
Applied and Environmental Microbiology Aug 2017, 83 (17) e01097-17; DOI: 10.1128/AEM.01097-17
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KEYWORDS

bifidobacteria
food microbiology
prebiotics

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