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

Journal Article · · mBio
 [1];  [1];  [2];  [3];  [4];  [5];  [6];  [7];  [8];  [1];  [9];  [9];  [9];  [9];  [5];  [10];  [11];  [4]; ; more »; « less
  1. Research Unit Analytical BioGeoChemistry, Helmholtz Zentrum München, Neuherberg, Germany
  2. Center for Interdisciplinary Cardiovascular Science (CICS), Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts, USA
  3. The University of Texas, El Paso, Texas, USA
  4. Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, Washington, USA
  5. Institute of Microbiology, Greifswald University, Greifswald, Germany
  6. Juniata College, Huntingdon, Pennsylvania, USA
  7. Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, Washington, USA, Department of Molecular Microbiology and Immunology, Oregon Health &, Sciences University, Portland, Oregon, USA
  8. Children’s Hospital Oakland Research Institute, Oakland, California, USA, College of Pharmacy, Touro University California, Vallejo, California, USA
  9. University of California, San Diego, California, USA
  10. Children’s Hospital Oakland Research Institute, Oakland, California, USA
  11. Research Unit Analytical BioGeoChemistry, Helmholtz Zentrum München, Neuherberg, Germany, Technische Universität München, Freising, Germany
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.

IMPORTANCE This 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.

Research Organization:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Sponsoring Organization:
USDOE
Grant/Contract Number:
AC05-76RL01830
OSTI ID:
1786916
Alternate ID(s):
OSTI ID: 1406729
Report Number(s):
PNNL-SA--126751; e01343-17
Journal Information:
mBio, Journal Name: mBio Journal Issue: 5 Vol. 8; ISSN 2161-2129
Publisher:
American Society for MicrobiologyCopyright Statement
Country of Publication:
United States
Language:
English

References (57)

Data visualization in environmental proteomics journal August 2013
Mass-spectrometry-based metabolomics: limitations and recommendations for future progress with particular focus on nutrition research journal June 2009
An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database journal November 1994
Optimizing a ultrahigh pressure liquid chromatography-time of flight-mass spectrometry approach using a novel sub-2μm core–shell particle for in depth lipidomic profiling of Caenorhabditis elegans journal September 2014
Dealing with the unknown: Metabolomics and Metabolite Atlases journal September 2010
Faecalibacterium prausnitzii and human intestinal health journal June 2013
Consumption of the slow-digesting waxy maize starch leads to blunted plasma glucose and insulin response but does not influence energy expenditure or appetite in humans journal June 2009
The influence of diet on the gut microbiota journal March 2013
Diets high in resistant starch increase plasma levels of trimethylamine- N -oxide, a gut microbiome metabolite associated with CVD risk journal December 2016
DTASelect and Contrast:  Tools for Assembling and Comparing Protein Identifications from Shotgun Proteomics journal February 2002
Shotgun metaproteomics of the human distal gut microbiota journal October 2008
Dominant and diet-responsive groups of bacteria within the human colonic microbiota journal August 2010
Ruminococcus bromii is a keystone species for the degradation of resistant starch in the human colon journal February 2012
The gut anaerobe Faecalibacterium prausnitzii uses an extracellular electron shuttle to grow at oxic–anoxic interphases journal February 2012
Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms journal March 2012
Structure, function and diversity of the healthy human microbiome journal June 2012
A metagenome-wide association study of gut microbiota in type 2 diabetes journal September 2012
Systems-wide temporal proteomic profiling in glucose-starved Bacillus subtilis journal December 2010
QIIME allows analysis of high-throughput community sequencing data journal April 2010
Plasma glucose and insulin reduction after consumption of breads varying in amylose content journal September 2002
Impact of dietary resistant starch type 4 on human gut microbiota and immunometabolic functions journal June 2016
Hydrolytic action of α-amylase on high-amylose starch of low molecular mass journal June 2000
Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients journal October 2008
Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample journal June 2010
Colonization State Influences the Hemocyte Proteome in a Beneficial Squid–Vibrio Symbiosis journal July 2014
Resistant starch: the effect on postprandial glycemia, hormonal response, and satiety journal October 1994
Insulin-sensitizing effects of dietary resistant starch and effects on skeletal muscle and adipose tissue metabolism journal September 2005
KEGG: Kyoto Encyclopedia of Genes and Genomes journal January 2000
HMDB: the Human Metabolome Database journal January 2007
MassTRIX: mass translator into pathways journal May 2008
KEGG for integration and interpretation of large-scale molecular data sets journal November 2011
KEGG: new perspectives on genomes, pathways, diseases and drugs journal November 2016
Cell-associated  -amylases of butyrate-producing Firmicute bacteria from the human colon journal November 2006
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks journal November 2003
Voronoi Treemaps conference January 2005
Visualizing Gene Expression Data via Voronoi Treemaps conference June 2009
Interactively exploring hierarchical clustering results [gene identification] journal July 2002
Diversity of human colonic butyrate-producing bacteria revealed by analysis of the butyryl-CoA:acetate CoA-transferase gene journal February 2010
Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine journal May 2009
Molecular details of a starch utilization pathway in the human gut symbiont E ubacterium rectale : Starch utilization by journal December 2014
UniFrac: a New Phylogenetic Method for Comparing Microbial Communities journal December 2005
Two Routes of Metabolic Cross-Feeding between Bifidobacterium adolescentis and Butyrate-Producing Anaerobes from the Human Gut journal May 2006
Identification of Metabolic Signatures Linked to Anti-Inflammatory Effects of Faecalibacterium prausnitzii journal April 2015
Tree visualization with tree-maps: 2-d space-filling approach journal January 1992
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 journal December 2014
Kendrick-Analogous Network Visualisation of Ion Cyclotron Resonance Fourier Transform Mass Spectra: Improved Options for the Assignment of Elemental Compositions and the Classification of Organic Molecular Complexity journal August 2011
Large-Scale Mapping and Validation of Escherichia coli Transcriptional Regulation from a Compendium of Expression Profiles journal January 2007
Metabolomics Reveals Metabolic Biomarkers of Crohn's Disease journal July 2009
Resistant Starches Types 2 and 4 Have Differential Effects on the Composition of the Fecal Microbiota in Human Subjects journal November 2010
Identification and Validation of Ifit1 as an Important Innate Immune Bottleneck journal June 2012
MassTRIX Reloaded: Combined Analysis and Visualization of Transcriptome and Metabolome Data journal July 2012
Integrated Metagenomics/Metaproteomics Reveals Human Host-Microbiota Signatures of Crohn's Disease journal November 2012
phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data journal April 2013
Butyrate Improves Insulin Sensitivity and Increases Energy Expenditure in Mice journal April 2009
A Diet High in Resistant Starch Modulates Microbiota Composition, SCFA Concentrations, and Gene Expression in Pig Intestine journal January 2013
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
Microbial degradation of complex carbohydrates in the gut journal July 2012