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Title: Metagenomic Insights into the Degradation of Resistant Starch by Human Gut Microbiota

Abstract

ABSTRACT Several studies monitoring alterations in the community structure upon resistant starch (RS) interventions are available, although comprehensive function-based analyses are lacking. Recently, a multiomics approach based on 16S rRNA gene sequencing, metaproteomics, and metabolomics on fecal samples from individuals subjected to high and low doses of type 2 RS (RS2; 48 g and 3 g/2,500 kcal, respectively, daily for 2 weeks) in a crossover intervention experiment was performed. In the present study, we did pathway-based metagenomic analyses on samples from a subset of individuals (n= 12) from that study to obtain additional detailed insights into the functional structure at high resolution during RS2 intervention. A mechanistic framework based on obtained results is proposed where primary degradation was governed byFirmicutes, withRuminococcus bromiias a major taxon involved, providing fermentation substrates and increased acetate concentrations for the growth of various major butyrate producers exhibiting the enzyme butyryl-coenzyme A (CoA):acetate CoA-transferase. H 2-scavenging sulfite reducers and acetogens concurrently increased. Individual responses of gut microbiota were noted, where seven of the 12 participants displayed all features of the outlined pattern, whereas four individuals showed mixed behavior and one subject was unresponsive. Intervention order did not affect the outcome, emphasizing a constant substrate supply formore » maintaining specific functional communities. IMPORTANCEManipulation of gut microbiota is increasingly recognized as a promising approach to reduce various noncommunicable diseases, such as obesity and type 2 diabetes. Specific dietary supplements, including resistant starches (RS), are often a focus, yet comprehensive insights into functional responses of microbiota are largely lacking. Furthermore, unresponsiveness in certain individuals is poorly understood. Our data indicate that distinct parts of microbiota work jointly to degrade RS and successively form health-promoting fermentation end products. It highlights the need to consider both primary degraders and specific more-downstream-acting bacterial groups in order to achieve desired intervention outcomes. The gained insights will assist the design of personalized treatment strategies based on an individual's microbiota.« less

Authors:
; ; ; ; ; ;
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1503607
Report Number(s):
PNNL-SA-134050
Journal ID: ISSN 0099-2240
DOE Contract Number:  
AC05-76RL01830
Resource Type:
Journal Article
Journal Name:
Applied and Environmental Microbiology
Additional Journal Information:
Journal Volume: 84; Journal Issue: 23; Journal ID: ISSN 0099-2240
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English

Citation Formats

Vital, Marius, Howe, Adina, Bergeron, Nathalie, Krauss, Ronald M., Jansson, Janet K., Tiedje, James M., and Drake, Harold L. Metagenomic Insights into the Degradation of Resistant Starch by Human Gut Microbiota. United States: N. p., 2018. Web. doi:10.1128/AEM.01562-18.
Vital, Marius, Howe, Adina, Bergeron, Nathalie, Krauss, Ronald M., Jansson, Janet K., Tiedje, James M., & Drake, Harold L. Metagenomic Insights into the Degradation of Resistant Starch by Human Gut Microbiota. United States. doi:10.1128/AEM.01562-18.
Vital, Marius, Howe, Adina, Bergeron, Nathalie, Krauss, Ronald M., Jansson, Janet K., Tiedje, James M., and Drake, Harold L. Fri . "Metagenomic Insights into the Degradation of Resistant Starch by Human Gut Microbiota". United States. doi:10.1128/AEM.01562-18.
@article{osti_1503607,
title = {Metagenomic Insights into the Degradation of Resistant Starch by Human Gut Microbiota},
author = {Vital, Marius and Howe, Adina and Bergeron, Nathalie and Krauss, Ronald M. and Jansson, Janet K. and Tiedje, James M. and Drake, Harold L.},
abstractNote = {ABSTRACT Several studies monitoring alterations in the community structure upon resistant starch (RS) interventions are available, although comprehensive function-based analyses are lacking. Recently, a multiomics approach based on 16S rRNA gene sequencing, metaproteomics, and metabolomics on fecal samples from individuals subjected to high and low doses of type 2 RS (RS2; 48 g and 3 g/2,500 kcal, respectively, daily for 2 weeks) in a crossover intervention experiment was performed. In the present study, we did pathway-based metagenomic analyses on samples from a subset of individuals (n= 12) from that study to obtain additional detailed insights into the functional structure at high resolution during RS2 intervention. A mechanistic framework based on obtained results is proposed where primary degradation was governed byFirmicutes, withRuminococcus bromiias a major taxon involved, providing fermentation substrates and increased acetate concentrations for the growth of various major butyrate producers exhibiting the enzyme butyryl-coenzyme A (CoA):acetate CoA-transferase. H2-scavenging sulfite reducers and acetogens concurrently increased. Individual responses of gut microbiota were noted, where seven of the 12 participants displayed all features of the outlined pattern, whereas four individuals showed mixed behavior and one subject was unresponsive. Intervention order did not affect the outcome, emphasizing a constant substrate supply for maintaining specific functional communities. IMPORTANCEManipulation of gut microbiota is increasingly recognized as a promising approach to reduce various noncommunicable diseases, such as obesity and type 2 diabetes. Specific dietary supplements, including resistant starches (RS), are often a focus, yet comprehensive insights into functional responses of microbiota are largely lacking. Furthermore, unresponsiveness in certain individuals is poorly understood. Our data indicate that distinct parts of microbiota work jointly to degrade RS and successively form health-promoting fermentation end products. It highlights the need to consider both primary degraders and specific more-downstream-acting bacterial groups in order to achieve desired intervention outcomes. The gained insights will assist the design of personalized treatment strategies based on an individual's microbiota.},
doi = {10.1128/AEM.01562-18},
journal = {Applied and Environmental Microbiology},
issn = {0099-2240},
number = 23,
volume = 84,
place = {United States},
year = {2018},
month = {9}
}

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