Diet rapidly and reproducibly alters the human gut microbiome

Nature

Volumn 505, Issue 7484, 2014, Pages 559-563

  David, Lawrence A ^a,b,e   Maurice, Corinne F ^a   Carmody, Rachel N ^a   Gootenberg, David B ^a   Button, Julie E ^a   Wolfe, Benjamin E ^a   Ling, Alisha V ^c   Devlin, A Sloan ^d   Varma, Yug ^d   Fischbach, Michael A ^d   Biddinger, Sudha B ^c   Dutton, Rachel J ^a   Turnbaugh, Peter J ^a  

^a HARVARD UNIVERSITY   (United States)

^b HARVARD UNIVERSITY   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

POLYSACCHARIDE;

CARBOHYDRATE; CARNIVORY; COMMUNITY RESPONSE; DIET; DIETARY SHIFT; FERMENTATION; FOOD INTAKE; GENE EXPRESSION; HERBIVORE; HOMINID; LIFESTYLE; METABOLISM; MICROBIAL COMMUNITY; MICROBIOLOGY; NUTRITION; POLYSACCHARIDE; STOMACH CONTENT;

ARTICLE; BACTEROIDES; BILOPHILA; BILOPHILA WADSWORTHIA; CARNIVORY; CLINICAL ARTICLE; DIETARY INTAKE; EUBACTERIUM; FERMENTATION; FIRMICUTES; FUNGUS; GENE EXPRESSION; HERBIVORY; HUMAN; HUMAN EXPERIMENT; INTESTINE FLORA; LIFESTYLE; MICROBIAL ACTIVITY; MICROBIAL COMMUNITY; MICROBIAL GENE; NONHUMAN; PLANT PRODUCT; PRIORITY JOURNAL; RUMINOCOCCUS; VIRUS;

ADULT; BACTERIA; BACTEROIDES; BILE ACIDS AND SALTS; BILOPHILA; CARNIVORY; DIET; DIET, VEGETARIAN; DIETARY FATS; FECES; FEMALE; FERMENTATION; FOOD MICROBIOLOGY; GASTROINTESTINAL TRACT; GENE EXPRESSION REGULATION, BACTERIAL; HERBIVORY; HUMANS; INFLAMMATORY BOWEL DISEASES; MALE; METAGENOME; MICROBIOTA; TIME FACTORS; YOUNG ADULT;

ALISTIPES; ANIMALIA; BACTERIA (MICROORGANISMS); BACTEROIDES; BILOPHILA; BILOPHILA WADSWORTHIA; EUBACTERIUM RECTALE; FIRMICUTES; FUNGI; MAMMALIA; ROSEBURIA; RUMINOCOCCUS BROMII;

EID: 84892828465     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature12820     Document Type: Article

References (56)

1. Wu, G. D. et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 334, 105-108 (2011).
2. Muegge, B. D. et al. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332, 970-974 (2011).
3. Duncan, S. H. et al. Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces. Appl. Environ. Microbiol. 73, 1073-1078 (2007).
4. Ley, R. E., Turnbaugh, P. J., Klein, S. & Gordon, J. I. Microbial ecology: human gut microbes associated with obesity. Nature 444, 1022-1023 (2006).
5. Walker, A. W. et al. Dominant and diet-responsive groups of bacteria within the human colonic microbiota. ISME J. 5, 220-230 (2011).
6. 2/2 mice. Nature 487, 104-108 (2012).
7. Turnbaugh, P. J. et al. The effectofdietonthe human gut microbiome:ametagenomic analysis in humanized gnotobiotic mice. Sci. Transl. Med. 1, 6ra14 (2009).
8. Turnbaugh, P. J. et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444, 1027-1031 (2006).
9. Faith, J. J., McNulty, N. P., Rey, F. E. & Gordon, J. I. Predicting a human gut microbiota's response to diet in gnotobiotic mice. Science 333, 101-104 (2011).
10. Russell, W. R. et al. High-protein, reduced-carbohydrate weight-loss diets promote metabolite profiles likely to be detrimental to colonic health. Am. J. Clin. Nutr. 93, 1062-1072 (2011).
11. Cordain, L. et al. Plant-animal subsistence ratios and macronutrient energy estimations in worldwide hunter-gatherer diets. Am. J. Clin. Nutr. 71, 682-692 (2000).
12. Arumugam, M. et al. Enterotypes of the human gut microbiome. Nature 473, 174-180 (2011).
13. De Filippo, C. et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc. Natl Acad. Sci. USA 107, 14691-14696 (2010).
14. Reddy, B. S. Diet and excretion of bile acids. Cancer Res. 41, 3766-3768 (1981).
15. Smith, E. A. & Macfarlane, G. T. Enumeration of amino acid fermenting bacteria in the human large intestine: effects of pH and starch on peptide metabolism and dissimilation of amino acids. FEMS Microbiol. Ecol. 25, 355-368 (1998).
16. Smith, E. A. & Macfarlane, G. T. Enumerationof 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. 81, 288-302 (1996).
17. Sinha, R. et al. 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. 55, 4516-4519 (1995).
18. Langille, M. G. I. et al. Predictive functional profilingofmicrobial communities using 16S rRNA marker gene sequences. Nature Biotechnol. 31, 814-821 (2013).
19. Kanehisa, M. & Goto, S. KEGG:KyotoEncyclopediaofGenesandGenomes. Nucleic Acids Res. 28, 27-30 (2000).
20. Pittard, J. & Wallace, B. J. Distribution and function of genes concerned with aromatic biosynthesis in Escherichia coli. J. Bacteriol. 91, 1494-1508 (1966).
21. Hawkes, K., O'Connell, J. F. & Jones, N. G. 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. 334, 243-250 (1991).
22. Bourdichon, F., Berger, B. & Casaregola, S. Safety demonstration of microbial food cultures (MFC) in fermented food products. Bull. Int. Dairy Fed. 455, 1-66 (2012).
23. Nychas, G. J. & Arkoudelos, J. S. Staphylococci: their role in fermented sausages. Soc. Appl. Bacteriol. Symp. Ser. 19, 167S-188S (1990).
24. McGavin, W. J. & Macfarlane, S. A. Rubuschlorotic mottlevirus, anew sobemovirus infecting raspberry and bramble. Virus Res. 139, 10-13 (2009).
25. Zhang, T. et al. RNA viral community in human feces: prevalence of plant pathogenic viruses. PLoS Biol. 4, e3 (2006).
26. Yoshimoto, S. et al. Obesity-induced gut microbial metabolite promotes liver cancer through senescence secretome. Nature 499, 97-101 (2013).
27. Ridlon, J. M., Kang, D. J. & Hylemon, P. B. Bile salt biotransformations by human intestinal bacteria. J. Lipid Res. 47, 241-259 (2006).
28. Islam, K. B. et al. Bile acid isa host factor that regulates the composition ofthe cecal microbiota in rats. Gastroenterology 141, 1773-1781 (2011).
29. Maurice, C. F., Haiser, H. J. & Turnbaugh, P. J. Xenobiotics shape the physiology andgeneexpressionoftheactivehumangutmicrobiome. Cell152, 39-50(2013).
30. Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7, 335-336 (2010).
31. Lewis, S. J. & Heaton, K. W. Stool form scale as a useful guide to intestinal transit time. Scand. J. Gastroenterol. 32, 920-924 (1997).
32. National Institutes of Health. Diet History Questionnaire Version 2. 0 (National Institutes of Health, Applied Research Program, National Cancer Institute, 2010).
33. Caporaso, J. G. et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl Acad. Sci. USA 108 (suppl. 1), 4516-4522 (2011).
34. Caporaso, J. G. et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 6, 1621-1624 (2012).
35. DeSantis, T. Z. et al. Greengenes, achimera-checked 16S rRNA genedatabase and workbench compatible with ARB. Appl. Environ. Microbiol. 72, 5069-5072 (2006).
36. Jones, E. et al. SciPy: open source scientific tools for Python (2001).
37. McKinney, W. Data structures for statistical computing in Python. Proc. 9th Python Sci. Conf. 51-56 (2010).
38. Strimmer, K. fdrtool: a versatile R package for estimating local and tail areabased false discovery rates. Bioinformatics 24, 1461-1462 (2008).
39. Friedman, J. & Alm, E. J. Inferring correlation networks from genomic survey data. PLoS Comput. Biol. 8, e1002687 (2012).
40. Turnbaugh, P. J. et al. Organismal, genetic, and transcriptional variation in the deeply sequenced gut microbiomes of identical twins. Proc. Natl Acad. Sci. USA 107, 7503-7508 (2010).
41. Rey, F. E. et al. Dissecting the in vivo metabolic potential of two human gut acetogens. J. Biol. Chem. 285, 22082-22090 (2010).
42. Nelson, K. E. et al. A catalog of reference genomes from the human microbiome. Science 328, 994-999 (2010).
43. Ning, Z., Cox, A. J. & Mullikin, J. C. SSAHA: a fast search method for large DNA databases. Genome Res. 11, 1725-1729 (2001).
44. Abubucker, S. et al. Metabolic reconstruction for metagenomic data and its application to the human microbiome. PLOS Comput. Biol. 8, e1002358 (2012).
45. Segata, N. et al. Metagenomic biomarker discovery and explanation. Genome Biol. 12, R60 (2011).
46. Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie2. Nature Methods 9, 357-359 (2012)
47. Markowitz, V. M. et al. IMG: the Integrated Microbial Genomes database and comparative analysis system. Nucleic Acids Res. 40, D115-D122 (2012).
48. Martin, J. et al. Optimizing read mapping to reference genomes to determine composition and species prevalence in microbial communities. PLoS ONE 7, e36427 (2012).
49. Deplancke, B. et al. Molecular ecological analysis of the succession and diversity of sulfate-reducing bacteria in the mouse gastrointestinal tract. Appl. Environ. Microbiol. 66, 2166-2174 (2000).
50. Stewart, J. A., Chadwick, V. S. & Murray, A. Carriage, quantification, and predominance of methanogens and sulfate-reducing bacteria in faecal samples. Lett. Appl. Microbiol. 43, 58-63 (2006).
51. Porter, J. L. et al. Accurate enzymatic measurement of fecal bile acids in patients with malabsorption. J. Lab. Clin. Med. 141, 411-418 (2003).
52. Setchell, K. D., Lawson, A. M., Tanida, N. & Sjovall, J. General methods for the analysis ofmetabolic profiles of bile acids and related compounds infeces. J. Lipid Res. 24, 1085-1100 (1983).
53. Schoch, C. L. et al. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc. Natl Acad. Sci. USA 109, 6241-6246 (2012).
54. Gardes, M. & Bruns, T. D. ITS primers with enhanced specificityfor basidiomycetes application to the identification of mycorrhizae and rusts. Mol. Ecol. 2, 113-118 (1993).
55. White, T. J., Bruns, T., Lee, S. & Taylor, J. in PCR Protocols: A Guide to Methods and Applications (eds Gelfand, D. H., Innis, M. A., Shinsky, J. J. & White, T. J.) 315-322 (1990).
56. Walker, H. K., Hall, W. D., Hurst, J. W., Comstock, J. P. & Garber, A. J. Ketonuria 3rd edn (Butterworths, 1990).