skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

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 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)},
issn = {2150-7511},
number = 5,
volume = 8,
place = {United States},
year = {2017},
month = {10}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 56 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

The influence of diet on the gut microbiota
journal, March 2013


Dominant and diet-responsive groups of bacteria within the human colonic microbiota
journal, August 2010

  • Walker, Alan W.; Ince, Jennifer; Duncan, Sylvia H.
  • The ISME Journal, Vol. 5, Issue 2
  • DOI: 10.1038/ismej.2010.118

Microbial degradation of complex carbohydrates in the gut
journal, July 2012

  • Flint, Harry J.; Scott, Karen P.; Duncan, Sylvia H.
  • Gut Microbes, Vol. 3, Issue 4
  • DOI: 10.4161/gmic.19897

Impact of dietary resistant starch type 4 on human gut microbiota and immunometabolic functions
journal, June 2016

  • Upadhyaya, Bijaya; McCormack, Lacey; Fardin-Kia, Ali Reza
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep28797

Resistant Starches Types 2 and 4 Have Differential Effects on the Composition of the Fecal Microbiota in Human Subjects
journal, November 2010


Butyrate Improves Insulin Sensitivity and Increases Energy Expenditure in Mice
journal, April 2009


Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine
journal, May 2009


Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients
journal, October 2008

  • Sokol, H.; Pigneur, B.; Watterlot, L.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 43
  • DOI: 10.1073/pnas.0804812105

Ruminococcus bromii is a keystone species for the degradation of resistant starch in the human colon
journal, February 2012

  • Ze, Xiaolei; Duncan, Sylvia H.; Louis, Petra
  • The ISME Journal, Vol. 6, Issue 8
  • DOI: 10.1038/ismej.2012.4

The gut anaerobe Faecalibacterium prausnitzii uses an extracellular electron shuttle to grow at oxic–anoxic interphases
journal, February 2012

  • Khan, M. Tanweer; Duncan, Sylvia H.; Stams, Alfons J. M.
  • The ISME Journal, Vol. 6, Issue 8
  • DOI: 10.1038/ismej.2012.5

Molecular details of a starch utilization pathway in the human gut symbiont E ubacterium rectale : Starch utilization by
journal, December 2014

  • Cockburn, Darrell W.; Orlovsky, Nicole I.; Foley, Matthew H.
  • Molecular Microbiology, Vol. 95, Issue 2
  • DOI: 10.1111/mmi.12859

Shotgun metaproteomics of the human distal gut microbiota
journal, October 2008

  • Verberkmoes, Nathan C.; Russell, Alison L.; Shah, Manesh
  • The ISME Journal, Vol. 3, Issue 2
  • DOI: 10.1038/ismej.2008.108

Metabolomics Reveals Metabolic Biomarkers of Crohn's Disease
journal, July 2009


Diets High in Protein or Saturated Fat Do Not Affect Insulin Sensitivity or Plasma Concentrations of Lipids and Lipoproteins in Overweight and Obese Adults
journal, September 2014

  • Chiu, Sally; Williams, Paul T.; Dawson, Taylor
  • The Journal of Nutrition, Vol. 144, Issue 11
  • DOI: 10.3945/jn.114.197624

Resistant starch: the effect on postprandial glycemia, hormonal response, and satiety
journal, October 1994

  • Raben, A.; Tagliabue, A.; Christensen, N. J.
  • The American Journal of Clinical Nutrition, Vol. 60, Issue 4
  • DOI: 10.1093/ajcn/60.4.544

Plasma glucose and insulin reduction after consumption of breads varying in amylose content
journal, September 2002


Insulin-sensitizing effects of dietary resistant starch and effects on skeletal muscle and adipose tissue metabolism
journal, September 2005

  • Robertson, M. Denise; Bickerton, Alex S.; Dennis, A. Louise
  • The American Journal of Clinical Nutrition, Vol. 82, Issue 3
  • DOI: 10.1093/ajcn/82.3.559

Diets high in resistant starch increase plasma levels of trimethylamine- N -oxide, a gut microbiome metabolite associated with CVD risk
journal, December 2016

  • Bergeron, Nathalie; Williams, Paul T.; Lamendella, Regina
  • British Journal of Nutrition, Vol. 116, Issue 12
  • DOI: 10.1017/S0007114516004165

Identification of Metabolic Signatures Linked to Anti-Inflammatory Effects of Faecalibacterium prausnitzii
journal, April 2015


Diversity of human colonic butyrate-producing bacteria revealed by analysis of the butyryl-CoA:acetate CoA-transferase gene
journal, February 2010


A metagenome-wide association study of gut microbiota in type 2 diabetes
journal, September 2012


Two Routes of Metabolic Cross-Feeding between Bifidobacterium adolescentis and Butyrate-Producing Anaerobes from the Human Gut
journal, May 2006


Hydrolytic action of α-amylase on high-amylose starch of low molecular mass
journal, June 2000

  • Rendleman, Jr., Jacob A.
  • Biotechnology and Applied Biochemistry, Vol. 31, Issue 3
  • DOI: 10.1042/BA19990100

Cell-associated  -amylases of butyrate-producing Firmicute bacteria from the human colon
journal, November 2006


MassTRIX: mass translator into pathways
journal, May 2008

  • Suhre, K.; Schmitt-Kopplin, P.
  • Nucleic Acids Research, Vol. 36, Issue Web Server
  • DOI: 10.1093/nar/gkn194

KEGG: Kyoto Encyclopedia of Genes and Genomes
journal, January 2000

  • Kanehisa, Minoru; Goto, Susumu
  • Nucleic Acids Research, Vol. 28, Issue 1, p. 27-30
  • DOI: 10.1093/nar/28.1.27

Dealing with the unknown: Metabolomics and Metabolite Atlases
journal, September 2010

  • Bowen, Benjamin P.; Northen, Trent R.
  • Journal of the American Society for Mass Spectrometry, Vol. 21, Issue 9
  • DOI: 10.1016/j.jasms.2010.04.003

Mass-spectrometry-based metabolomics: limitations and recommendations for future progress with particular focus on nutrition research
journal, June 2009


Large-Scale Mapping and Validation of Escherichia coli Transcriptional Regulation from a Compendium of Expression Profiles
journal, January 2007


A Diet High in Resistant Starch Modulates Microbiota Composition, SCFA Concentrations, and Gene Expression in Pig Intestine
journal, January 2013

  • Haenen, Daniëlle; Zhang, Jing; Souza da Silva, Carol
  • The Journal of Nutrition, Vol. 143, Issue 3
  • DOI: 10.3945/jn.112.169672

Faecalibacterium prausnitzii and human intestinal health
journal, June 2013


Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample
journal, June 2010

  • Caporaso, J. G.; Lauber, C. L.; Walters, W. A.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue Supplement_1
  • DOI: 10.1073/pnas.1000080107

Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms
journal, March 2012

  • Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A.
  • The ISME Journal, Vol. 6, Issue 8
  • DOI: 10.1038/ismej.2012.8

QIIME allows analysis of high-throughput community sequencing data
journal, April 2010

  • Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse
  • Nature Methods, Vol. 7, Issue 5
  • DOI: 10.1038/nmeth.f.303

UniFrac: a New Phylogenetic Method for Comparing Microbial Communities
journal, December 2005


phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data
journal, April 2013


Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014


Colonization State Influences the Hemocyte Proteome in a Beneficial Squid–Vibrio Symbiosis
journal, July 2014

  • Schleicher, Tyler R.; VerBerkmoes, Nathan C.; Shah, Manesh
  • Molecular & Cellular Proteomics, Vol. 13, Issue 10
  • DOI: 10.1074/mcp.M113.037259

Integrated Metagenomics/Metaproteomics Reveals Human Host-Microbiota Signatures of Crohn's Disease
journal, November 2012


An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database
journal, November 1994

  • Eng, Jimmy K.; McCormack, Ashley L.; Yates, John R.
  • Journal of the American Society for Mass Spectrometry, Vol. 5, Issue 11
  • DOI: 10.1016/1044-0305(94)80016-2

DTASelect and Contrast:  Tools for Assembling and Comparing Protein Identifications from Shotgun Proteomics
journal, February 2002

  • Tabb, David L.; McDonald, W. Hayes; Yates, John R.
  • Journal of Proteome Research, Vol. 1, Issue 1, p. 21-26
  • DOI: 10.1021/pr015504q

HMDB: the Human Metabolome Database
journal, January 2007

  • Wishart, D. S.; Tzur, D.; Knox, C.
  • Nucleic Acids Research, Vol. 35, Issue Database
  • DOI: 10.1093/nar/gkl923

MassTRIX Reloaded: Combined Analysis and Visualization of Transcriptome and Metabolome Data
journal, July 2012


Interactively exploring hierarchical clustering results [gene identification]
journal, July 2002


Data visualization in environmental proteomics
journal, August 2013


Systems-wide temporal proteomic profiling in glucose-starved Bacillus subtilis
journal, December 2010

  • Otto, Andreas; Bernhardt, Jörg; Meyer, Hanna
  • Nature Communications, Vol. 1, Issue 1
  • DOI: 10.1038/ncomms1137

Tree visualization with tree-maps: 2-d space-filling approach
journal, January 1992


Voronoi Treemaps
conference, January 2005


KEGG for integration and interpretation of large-scale molecular data sets
journal, November 2011

  • Kanehisa, M.; Goto, S.; Sato, Y.
  • Nucleic Acids Research, Vol. 40, Issue D1
  • DOI: 10.1093/nar/gkr988

KEGG: new perspectives on genomes, pathways, diseases and drugs
journal, November 2016

  • Kanehisa, Minoru; Furumichi, Miho; Tanabe, Mao
  • Nucleic Acids Research, Vol. 45, Issue D1
  • DOI: 10.1093/nar/gkw1092

Identification and Validation of Ifit1 as an Important Innate Immune Bottleneck
journal, June 2012


Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks
journal, November 2003


    Works referencing / citing this record:

    Current understanding of the human microbiome
    journal, April 2018

    • Gilbert, Jack A.; Blaser, Martin J.; Caporaso, J. Gregory
    • Nature Medicine, Vol. 24, Issue 4
    • DOI: 10.1038/nm.4517

    Modulation of the Gut Microbiota by Resistant Starch as a Treatment of Chronic Kidney Diseases: Evidence of Efficacy and Mechanistic Insights
    journal, January 2019

    • Snelson, Matthew; Kellow, Nicole J.; Coughlan, Melinda T.
    • Advances in Nutrition, Vol. 10, Issue 2
    • DOI: 10.1093/advances/nmy068

    The Microbiota-Gut-Brain Axis
    journal, October 2019

    • Cryan, John F.; O'Riordan, Kenneth J.; Cowan, Caitlin S. M.
    • Physiological Reviews, Vol. 99, Issue 4
    • DOI: 10.1152/physrev.00018.2018

    Current understanding of the human microbiome
    journal, April 2018

    • Gilbert, Jack A.; Blaser, Martin J.; Caporaso, J. Gregory
    • Nature Medicine, Vol. 24, Issue 4
    • DOI: 10.1038/nm.4517

    Modulation of the Gut Microbiota by Resistant Starch as a Treatment of Chronic Kidney Diseases: Evidence of Efficacy and Mechanistic Insights
    journal, January 2019

    • Snelson, Matthew; Kellow, Nicole J.; Coughlan, Melinda T.
    • Advances in Nutrition, Vol. 10, Issue 2
    • DOI: 10.1093/advances/nmy068

    Impact of Individual Traits, Saturated Fat, and Protein Source on the Gut Microbiome
    journal, December 2018


    The Microbiota-Gut-Brain Axis
    journal, October 2019

    • Cryan, John F.; O'Riordan, Kenneth J.; Cowan, Caitlin S. M.
    • Physiological Reviews, Vol. 99, Issue 4
    • DOI: 10.1152/physrev.00018.2018