Home LiteratureArticle Details
PMID: 24336217 Published · ppublish English Clinical Trial Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Diet rapidly and reproducibly alters the human gut microbiome.

Nature ·Vol. 505 ·No. 7484 ·2014-01-23 ·Pages 559-63

David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA, Biddinger SB, Dutton RJ, Turnbaugh PJ

Abstract

Long-term dietary intake influences the structure and activity of the trillions of microorganisms residing in the human gut, but it remains unclear how rapidly and reproducibly the human gut microbiome responds to short-term macronutrient change. Here we show that the short-term consumption of diets composed entirely of animal or plant products alters microbial community structure and overwhelms inter-individual differences in microbial gene expression. The animal-based diet increased the abundance of bile-tolerant microorganisms (Alistipes, Bilophila and Bacteroides) and decreased the levels of Firmicutes that metabolize dietary plant polysaccharides (Roseburia, Eubacterium rectale and Ruminococcus bromii). Microbial activity mirrored differences between herbivorous and carnivorous mammals, reflecting trade-offs between carbohydrate and protein fermentation. Foodborne microbes from both diets transiently colonized the gut, including bacteria, fungi and even viruses. Finally, increases in the abundance and activity of Bilophila wadsworthia on the animal-based diet support a link between dietary fat, bile acids and the outgrowth of microorganisms capable of triggering inflammatory bowel disease. In concert, these results demonstrate that the gut microbiome can rapidly respond to altered diet, potentially facilitating the diversity of human dietary lifestyles.

MeSH Terms
Adult Bacteria/drug effects,genetics,isolation & purification Bacteroides/drug effects,genetics,isolation & purification Bile Acids and Salts/analysis,metabolism Bilophila/drug effects,genetics,isolation & purification Carnivory Diet/adverse effects Diet, Vegetarian Dietary Fats/adverse effects,pharmacology Feces/chemistry,microbiology Female Fermentation/drug effects Food Microbiology Gastrointestinal Tract/drug effects,microbiology,virology Gene Expression Regulation, Bacterial/drug effects Herbivory Humans Inflammatory Bowel Diseases/microbiology Male Metagenome/drug effects,genetics Microbiota/drug effects,genetics Time Factors Young Adult
Chemicals
Bile Acids and Salts Dietary Fats
Authors & Affiliations
13 authors, click to expand affiliations / ORCID
David Lawrence A
1] FAS Center for Systems Biology, Harvard University, Cambridge, Massachusetts 02138, USA [2] Society of Fellows, Harvard University, Cambridge, Massachusetts 02138, USA [3] Molecular Genetics & Microbiology and Institute for Genome Sciences & Policy, Duke University, Durham, North Carolina 27708, USA.
Maurice Corinne F
FAS Center for Systems Biology, Harvard University, Cambridge, Massachusetts 02138, USA.
Carmody Rachel N
FAS Center for Systems Biology, Harvard University, Cambridge, Massachusetts 02138, USA.
Gootenberg David B
FAS Center for Systems Biology, Harvard University, Cambridge, Massachusetts 02138, USA.
Button Julie E
FAS Center for Systems Biology, Harvard University, Cambridge, Massachusetts 02138, USA.
Wolfe Benjamin E
FAS Center for Systems Biology, Harvard University, Cambridge, Massachusetts 02138, USA.
Ling Alisha V
Division of Endocrinology, Children's Hospital Boston, Harvard Medical School, Boston, Massachusetts 02115, USA.
Devlin A Sloan
Department of Bioengineering & Therapeutic Sciences and the California Institute for Quantitative Biosciences, University of California, San Francisco, San Francisco, California 94158, USA.
Varma Yug
Department of Bioengineering & Therapeutic Sciences and the California Institute for Quantitative Biosciences, University of California, San Francisco, San Francisco, California 94158, USA.
Fischbach Michael A
Department of Bioengineering & Therapeutic Sciences and the California Institute for Quantitative Biosciences, University of California, San Francisco, San Francisco, California 94158, USA.
Biddinger Sudha B
Division of Endocrinology, Children's Hospital Boston, Harvard Medical School, Boston, Massachusetts 02115, USA.
Dutton Rachel J
FAS Center for Systems Biology, Harvard University, Cambridge, Massachusetts 02138, USA.
Turnbaugh Peter J
FAS Center for Systems Biology, Harvard University, Cambridge, Massachusetts 02138, USA.
References (48)
48 references, click to expand
  1. RNA viral community in human feces: prevalence of plant pathogenic viruses.
    PLoS Biol. 2006 Jan;4(1):e3 PMID: 16336043
  2. fdrtool: a versatile R package for estimating local and tail area-based false discovery rates.
    Bioinformatics. 2008 Jun 15;24(12):1461-2 PMID: 18441000
  3. An obesity-associated gut microbiome with increased capacity for energy harvest.
    Nature. 2006 Dec 21;444(7122):1027-31 PMID: 17183312
  4. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms.
    ISME J. 2012 Aug;6(8):1621-4 PMID: 22402401
  5. Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10-/- mice.
    Nature. 2012 Jul 5;487(7405):104-8 PMID: 22722865
  6. ITS primers with enhanced specificity for basidiomycetes--application to the identification of mycorrhizae and rusts.
    Mol Ecol. 1993 Apr;2(2):113-8 PMID: 8180733
  7. High concentrations of the carcinogen 2-amino-1-methyl-6-phenylimidazo- [4,5-b]pyridine (PhIP) occur in chicken but are dependent on the cooking method.
    Cancer Res. 1995 Oct 15;55(20):4516-9 PMID: 7553619
  8. Fast gapped-read alignment with Bowtie 2.
    Nat Methods. 2012 Mar 04;9(4):357-9 PMID: 22388286
  9. Distribution and function of genes concerned with aromatic biosynthesis in Escherichia coli.
    J Bacteriol. 1966 Apr;91(4):1494-508 PMID: 5326114
  10. Xenobiotics shape the physiology and gene expression of the active human gut microbiome.
    Cell. 2013 Jan 17;152(1-2):39-50 PMID: 23332745
  11. Bile acid is a host factor that regulates the composition of the cecal microbiota in rats.
    Gastroenterology. 2011 Nov;141(5):1773-81 PMID: 21839040
  12. SSAHA: a fast search method for large DNA databases.
    Genome Res. 2001 Oct;11(10):1725-9 PMID: 11591649
  13. General methods for the analysis of metabolic profiles of bile acids and related compounds in feces.
    J Lipid Res. 1983 Aug;24(8):1085-100 PMID: 6631236
  14. Carriage, quantification, and predominance of methanogens and sulfate-reducing bacteria in faecal samples.
    Lett Appl Microbiol. 2006 Jul;43(1):58-63 PMID: 16834722
  15. Metabolic reconstruction for metagenomic data and its application to the human microbiome.
    PLoS Comput Biol. 2012;8(6):e1002358 PMID: 22719234
  16. Inferring correlation networks from genomic survey data.
    PLoS Comput Biol. 2012;8(9):e1002687 PMID: 23028285
  17. Organismal, genetic, and transcriptional variation in the deeply sequenced gut microbiomes of identical twins.
    Proc Natl Acad Sci U S A. 2010 Apr 20;107(16):7503-8 PMID: 20363958
  18. Rubus chlorotic mottle virus, a new sobemovirus infecting raspberry and bramble.
    Virus Res. 2009 Jan;139(1):10-3 PMID: 18929604
  19. Bile salt biotransformations by human intestinal bacteria.
    J Lipid Res. 2006 Feb;47(2):241-59 PMID: 16299351
  20. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans.
    Science. 2011 May 20;332(6032):970-4 PMID: 21596990
  21. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB.
    Appl Environ Microbiol. 2006 Jul;72(7):5069-72 PMID: 16820507
  22. Diet and excretion of bile acids.
    Cancer Res. 1981 Sep;41(9 Pt 2):3766-8 PMID: 6266664
  23. Microbial ecology: human gut microbes associated with obesity.
    Nature. 2006 Dec 21;444(7122):1022-3 PMID: 17183309
  24. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample.
    Proc Natl Acad Sci U S A. 2011 Mar 15;108 Suppl 1:4516-22 PMID: 20534432
  25. Accurate enzymatic measurement of fecal bile acids in patients with malabsorption.
    J Lab Clin Med. 2003 Jun;141(6):411-8 PMID: 12819639
  26. Enumeration of human colonic bacteria producing phenolic and indolic compounds: effects of pH, carbohydrate availability and retention time on dissimilatory aromatic amino acid metabolism.
    J Appl Bacteriol. 1996 Sep;81(3):288-302 PMID: 8810056
  27. High-protein, reduced-carbohydrate weight-loss diets promote metabolite profiles likely to be detrimental to colonic health.
    Am J Clin Nutr. 2011 May;93(5):1062-72 PMID: 21389180
  28. A catalog of reference genomes from the human microbiome.
    Science. 2010 May 21;328(5981):994-9 PMID: 20489017
  29. Linking long-term dietary patterns with gut microbial enterotypes.
    Science. 2011 Oct 7;334(6052):105-8 PMID: 21885731
  30. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa.
    Proc Natl Acad Sci U S A. 2010 Aug 17;107(33):14691-6 PMID: 20679230
  31. Hunting income patterns among the Hadza: big game, common goods, foraging goals and the evolution of the human diet.
    Philos Trans R Soc Lond B Biol Sci. 1991 Nov 29;334(1270):243-50; discussion 250-1 PMID: 1685582
  32. Molecular ecological analysis of the succession and diversity of sulfate-reducing bacteria in the mouse gastrointestinal tract.
    Appl Environ Microbiol. 2000 May;66(5):2166-74 PMID: 10788396
  33. Stool form scale as a useful guide to intestinal transit time.
    Scand J Gastroenterol. 1997 Sep;32(9):920-4 PMID: 9299672
  34. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi.
    Proc Natl Acad Sci U S A. 2012 Apr 17;109(16):6241-6 PMID: 22454494
  35. Metagenomic biomarker discovery and explanation.
    Genome Biol. 2011 Jun 24;12(6):R60 PMID: 21702898
  36. Optimizing read mapping to reference genomes to determine composition and species prevalence in microbial communities.
    PLoS One. 2012;7(6):e36427 PMID: 22719831
  37. Plant-animal subsistence ratios and macronutrient energy estimations in worldwide hunter-gatherer diets.
    Am J Clin Nutr. 2000 Mar;71(3):682-92 PMID: 10702160
  38. Dominant and diet-responsive groups of bacteria within the human colonic microbiota.
    ISME J. 2011 Feb;5(2):220-30 PMID: 20686513
  39. IMG: the Integrated Microbial Genomes database and comparative analysis system.
    Nucleic Acids Res. 2012 Jan;40(Database issue):D115-22 PMID: 22194640
  40. Predicting a human gut microbiota's response to diet in gnotobiotic mice.
    Science. 2011 Jul 1;333(6038):101-4 PMID: 21596954
  41. Dissecting the in vivo metabolic potential of two human gut acetogens.
    J Biol Chem. 2010 Jul 16;285(29):22082-90 PMID: 20444704
  42. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice.
    Sci Transl Med. 2009 Nov 11;1(6):6ra14 PMID: 20368178
  43. Enterotypes of the human gut microbiome.
    Nature. 2011 May 12;473(7346):174-80 PMID: 21508958
  44. Staphylococci: their role in fermented sausages.
    Soc Appl Bacteriol Symp Ser. 1990;19:167S-188S PMID: 2119063
  45. Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces.
    Appl Environ Microbiol. 2007 Feb;73(4):1073-8 PMID: 17189447
  46. KEGG: kyoto encyclopedia of genes and genomes.
    Nucleic Acids Res. 2000 Jan 1;28(1):27-30 PMID: 10592173
  47. QIIME allows analysis of high-throughput community sequencing data.
    Nat Methods. 2010 May;7(5):335-6 PMID: 20383131
  48. Obesity-induced gut microbial metabolite promotes liver cancer through senescence secretome.
    Nature. 2013 Jul 4;499(7456):97-101 PMID: 23803760
Article Info
Journal
Nature
Abbr.
Nature
ISSN
1476-4687
Published
2014-01-23
Epub
2013-00-11
Pages
559-63
Language
English
Region
England
NLM ID
0410462
PMCID
PMC3957428
Subset
IM
Grants
NIGMS NIH HHS · P50 GM068763 · United States
NIDDK NIH HHS · DK0046200 · United States
NIDDK NIH HHS · P30 DK046200 · United States
NIDDK NIH HHS · P30 DK034854 · United States
NIDDK NIH HHS · R01 DK094162 · United States
Databases
GEO
Corrections
CommentIn
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com