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Title: Impact of Dietary Resistant Starch on the Human Gut Microbiome, Metaproteome, and Metabolome

Abstract

Diet can influence the composition of the human microbiome, and yet relatively few dietary ingredients have been systematically investigated with respect to their impact on the functional potential of the microbiome. Dietary resistant starch (RS) has been shown to have health benefits, but we lack a mechanistic understanding of the metabolic processes that occur in the gut during digestion of RS. Here, we collected samples during a dietary crossover study with diets containing large or small amounts of RS. We determined the impact of RS on the gut microbiome and metabolic pathways in the gut, using a combination of “omics” approaches, including 16S rRNA gene sequencing, metaproteomics, and metabolomics. This multiomics approach captured changes in the abundance of specific bacterial species, proteins, and metabolites after a diet high in resistant starch (HRS), providing key insights into the influence of dietary interventions on the gut microbiome. The combined data showed that a high-RS diet caused an increase in the ratio of Firmicutes to Bacteroidetes, including increases in relative abundances of some specific members of the Firmicutes and concurrent increases in enzymatic pathways and metabolites involved in lipid metabolism in the gut. IMPORTANCEThis work was undertaken to obtain a mechanistic understanding ofmore » the complex interplay between diet and the microorganisms residing in the intestine. Although it is known that gut microbes play a key role in digestion of the food that we consume, the specific contributions of different microorganisms are not well understood. In addition, the metabolic pathways and resultant products of metabolism during digestion are highly complex. To address these knowledge gaps, we used a combination of molecular approaches to determine the identities of the microorganisms in the gut during digestion of dietary starch as well as the metabolic pathways that they carry out. Together, these data provide a more complete picture of the function of the gut microbiome in digestion, including links between an RS diet and lipid metabolism and novel linkages between specific gut microbes and their metabolites and proteins produced in the gut.« less

Authors:
 [1];  [1];  [2];  [3];  [4];  [5];  [6];  [7];  [8];  [1];  [9];  [9];  [9];  [9];  [5];  [10];  [11];  [4];  [12]
  1. Helmholtz Zentrum Munchen, Neuherberg (Germany)
  2. Brigham and Women's Hospital and Harvard Medical School, Boston, MA (United States); Harvard Medical School, Boston, MA (United States)
  3. The Univ. of Texas, El Paso, TX (United States)
  4. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  5. Greifswald Univ., Greifswald (Germany)
  6. Juniata College, Huntingdon, PA (United States)
  7. Pacific Northwest National Lab. (PNNL), Richland, WA (United States); Oregon Health & Sciences Univ., Portland, OR (United States)
  8. Children's Hospital Oakland Research Institute, Oakland, CA (United States); Touro Univ. California, Vallejo, CA (United States)
  9. Univ. of California, San Diego, CA (United States)
  10. Children's Hospital Oakland Research Institute, Oakland, CA (United States)
  11. Helmholtz Zentrum Munchen, Neuherberg (Germany); Technische Univ. Munchen, Freising (Germany)
  12. Univ. of Georgia, Athens, GA (United States)
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1406729
Report Number(s):
PNNL-SA-126751
Journal ID: ISSN 2150-7511
Grant/Contract Number:  
AC05-76RL01830
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online); Journal Volume: 8; Journal Issue: 5; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; clinical; proteomics; metabolomics; human microbiome; diet; gut microbiome; multiomics; resistant starch

Citation Formats

Maier, Tanja V., Lucio, Marianna, Lee, Lang Ho, VerBerkmoes, Nathan C., Brislawn, Colin J., Bernhardt, Jorg, Lamendella, Regina, McDermott, Jason E., Bergeron, Nathalie, Heinzmann, Silke S., Morton, James T., Gonzalez, Antonio, Ackermann, Gail, Knight, Rob, Riedel, Katharina, Krauss, Ronald M., Schmitt-Kopplin, Philippe, Jansson, Janet K., and Moran, Mary Ann. Impact of Dietary Resistant Starch on the Human Gut Microbiome, Metaproteome, and Metabolome. United States: N. p., 2017. Web. doi:10.1128/mBio.01343-17.
Maier, Tanja V., Lucio, Marianna, Lee, Lang Ho, VerBerkmoes, Nathan C., Brislawn, Colin J., Bernhardt, Jorg, Lamendella, Regina, McDermott, Jason E., Bergeron, Nathalie, Heinzmann, Silke S., Morton, James T., Gonzalez, Antonio, Ackermann, Gail, Knight, Rob, Riedel, Katharina, Krauss, Ronald M., Schmitt-Kopplin, Philippe, Jansson, Janet K., & Moran, Mary Ann. Impact of Dietary Resistant Starch on the Human Gut Microbiome, Metaproteome, and Metabolome. United States. doi:10.1128/mBio.01343-17.
Maier, Tanja V., Lucio, Marianna, Lee, Lang Ho, VerBerkmoes, Nathan C., Brislawn, Colin J., Bernhardt, Jorg, Lamendella, Regina, McDermott, Jason E., Bergeron, Nathalie, Heinzmann, Silke S., Morton, James T., Gonzalez, Antonio, Ackermann, Gail, Knight, Rob, Riedel, Katharina, Krauss, Ronald M., Schmitt-Kopplin, Philippe, Jansson, Janet K., and Moran, Mary Ann. Tue . "Impact of Dietary Resistant Starch on the Human Gut Microbiome, Metaproteome, and Metabolome". United States. doi:10.1128/mBio.01343-17. https://www.osti.gov/servlets/purl/1406729.
@article{osti_1406729,
title = {Impact of Dietary Resistant Starch on the Human Gut Microbiome, Metaproteome, and Metabolome},
author = {Maier, Tanja V. and Lucio, Marianna and Lee, Lang Ho and VerBerkmoes, Nathan C. and Brislawn, Colin J. and Bernhardt, Jorg and Lamendella, Regina and McDermott, Jason E. and Bergeron, Nathalie and Heinzmann, Silke S. and Morton, James T. and Gonzalez, Antonio and Ackermann, Gail and Knight, Rob and Riedel, Katharina and Krauss, Ronald M. and Schmitt-Kopplin, Philippe and Jansson, Janet K. and Moran, Mary Ann},
abstractNote = {Diet can influence the composition of the human microbiome, and yet relatively few dietary ingredients have been systematically investigated with respect to their impact on the functional potential of the microbiome. Dietary resistant starch (RS) has been shown to have health benefits, but we lack a mechanistic understanding of the metabolic processes that occur in the gut during digestion of RS. Here, we collected samples during a dietary crossover study with diets containing large or small amounts of RS. We determined the impact of RS on the gut microbiome and metabolic pathways in the gut, using a combination of “omics” approaches, including 16S rRNA gene sequencing, metaproteomics, and metabolomics. This multiomics approach captured changes in the abundance of specific bacterial species, proteins, and metabolites after a diet high in resistant starch (HRS), providing key insights into the influence of dietary interventions on the gut microbiome. The combined data showed that a high-RS diet caused an increase in the ratio of Firmicutes to Bacteroidetes, including increases in relative abundances of some specific members of the Firmicutes and concurrent increases in enzymatic pathways and metabolites involved in lipid metabolism in the gut. IMPORTANCEThis work was undertaken to obtain a mechanistic understanding of the complex interplay between diet and the microorganisms residing in the intestine. Although it is known that gut microbes play a key role in digestion of the food that we consume, the specific contributions of different microorganisms are not well understood. In addition, the metabolic pathways and resultant products of metabolism during digestion are highly complex. To address these knowledge gaps, we used a combination of molecular approaches to determine the identities of the microorganisms in the gut during digestion of dietary starch as well as the metabolic pathways that they carry out. Together, these data provide a more complete picture of the function of the gut microbiome in digestion, including links between an RS diet and lipid metabolism and novel linkages between specific gut microbes and their metabolites and proteins produced in the gut.},
doi = {10.1128/mBio.01343-17},
journal = {mBio (Online)},
number = 5,
volume = 8,
place = {United States},
year = {Tue Oct 17 00:00:00 EDT 2017},
month = {Tue Oct 17 00:00:00 EDT 2017}
}

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