Current Diabetes Reports

, 16:93 | Cite as

Diet and Gut Microbial Function in Metabolic and Cardiovascular Disease Risk

Lifestyle Management to Reduce Diabetes/Cardiovascular Risk (C Shay and B Conway, Section Editors)
Part of the following topical collections:
  1. Topical Collection on Lifestyle Management to Reduce Diabetes/Cardiovascular Risk

Abstract

Over the past decade, the gut microbiome has emerged as a novel and largely unexplored source of variability for metabolic and cardiovascular disease risk, including diabetes. Animal and human studies support several possible pathways through which the gut microbiome may impact health, including the production of health-related metabolites from dietary sources. Diet is considered important to shaping the gut microbiota; in addition, gut microbiota influence the metabolism of many dietary components. In the present paper, we address the distinction between compositional and functional analysis of the gut microbiota. We focus on literature that highlights the value of moving beyond surveys of microbial composition to measuring gut microbial functioning to delineate mechanisms related to the interplay between diet and gut microbiota in cardiometabolic health.

Keywords

Gut microbiota Metabolites Nutrition Diabetes Cardiovascular disease 

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 1.
    Ley RE, Hamady M, Lozupone C, et al. Evolution of mammals and their gut microbes. Science. 2008;320:1647–51.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Muegge BD, Kuczynski J, Knights D, et al. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science. 2011;332:970–4.CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    De Filippo C, Cavalieri D, Di Paola M, 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 U S A. 2010;107:14691–6.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Yatsunenko T, Rey FE, Manary MJ, et al. Human gut microbiome viewed across age and geography. Nature. 2012;486:222–7.PubMedPubMedCentralGoogle Scholar
  5. 5.
    Schnorr SL, Candela M, Rampelli S, et al. Gut microbiome of the Hadza hunter-gatherers. Nat Commun. 2014;5:3654.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.••
    Xu Z, Knight R. Dietary effects on human gut microbiome diversity. Br J Nutr. 2015;113:S1–5. This is a review of how diet may influence the composition of the gut microbiota. CrossRefPubMedGoogle Scholar
  7. 7.••
    Wong JM. Gut microbiota and cardiometabolic outcomes: influence of dietary patterns and their associated components. Am J Clin Nutr. 2014;100:369S–77S. A review of how diet may influence the composition of the gut microbiota. CrossRefPubMedGoogle Scholar
  8. 8.
    Graf D, Di Cagno R, Fak F, et al. Contribution of diet to the composition of the human gut microbiota. Microb Ecol Health Dis. 2015;26:26164.PubMedGoogle Scholar
  9. 9.
    Nicholson JK, Holmes E, Kinross J, et al. Host-gut microbiota metabolic interactions. Science. 2012;336:1262–7.CrossRefPubMedGoogle Scholar
  10. 10.
    Wikoff WR, Anfora AT, Liu J, et al. Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proc Natl Acad Sci U S A. 2009;106:3698–703.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.•
    Hullar MA, Lancaster SM, Li F, et al. Enterolignan-producing phenotypes are associated with increased gut microbial diversity and altered composition in premenopausal women in the United States. Cancer Epidemiol Biomarkers Prev. 2015;24:546–54. A population-based study of the association between metabolite production and gut microbiota composition. CrossRefPubMedGoogle Scholar
  12. 12.
    Koeth RA, Wang Z, Levison BS, et al. Intestinal microbiota metabolism of L-carnitine, a nutrient in red meat, promotes atherosclerosis. Nat Med. 2013;19:576–85.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Delzenne NM, Cani PD. Gut microbiota and the pathogenesis of insulin resistance. Curr Diab Rep. 2011;11:154–9.CrossRefPubMedGoogle Scholar
  14. 14.••
    Li D, Kirsop J, Tang WH. Listening to our gut: contribution of gut microbiota and cardiovascular risk in diabetes pathogenesis. Curr Diab Rep. 2015;15:63. An excellent review of possible pathways from gut microbiota to cardiovascular disease.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Cox AJ, West NP, Cripps AW. Obesity, inflammation, and the gut microbiota. Lancet Diabetes Endocrinol. 2015;3:207–15.CrossRefPubMedGoogle Scholar
  16. 16.••
    Hartstra AV, Bouter KE, Backhed F, et al. Insights into the role of the microbiome in obesity and type 2 diabetes. Diabetes Care. 2015;38:159–65. An excellent review of possible pathways from gut microbiota to obesity and type 2 diabetes. CrossRefPubMedGoogle Scholar
  17. 17.
    Qin J, Li Y, Cai Z, et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature. 2012;490:55–60.CrossRefPubMedGoogle Scholar
  18. 18.
    Karlsson FH, Tremaroli V, Nookaew I, et al. Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature. 2013;498:99–103.CrossRefPubMedGoogle Scholar
  19. 19.
    Larsen N, Vogensen FK, van den Berg FW, et al. Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS One. 2010;5:e9085.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Ley RE, Turnbaugh PJ, Klein S, et al. Microbial ecology: human gut microbes associated with obesity. Nature. 2006;444:1022–3.CrossRefPubMedGoogle Scholar
  21. 21.
    Turnbaugh PJ, Hamady M, Yatsunenko T, et al. A core gut microbiome in obese and lean twins. Nature. 2009;457:480–4.CrossRefPubMedGoogle Scholar
  22. 22.
    Turnbaugh PJ, Ley RE, Mahowald MA, et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444:1027–31.CrossRefPubMedGoogle Scholar
  23. 23.
    Dumas ME, Barton RH, Toye A, et al. Metabolic profiling reveals a contribution of gut microbiota to fatty liver phenotype in insulin-resistant mice. Proc Natl Acad Sci U S A. 2006;103:12511–6.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Cani PD, Bibiloni R, Knauf C, et al. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes. 2008;57:1470–81.CrossRefPubMedGoogle Scholar
  25. 25.
    Karlsson FH, Fak F, Nookaew I, et al. Symptomatic atherosclerosis is associated with an altered gut metagenome. Nat Commun. 2012;3:1245.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Yang T, Santisteban MM, Rodriguez V, et al. Gut dysbiosis is linked to hypertension. Hypertension. 2015;65:1331–40.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Holmes E, Loo RL, Stamler J, et al. Human metabolic phenotype diversity and its association with diet and blood pressure. Nature. 2008;453:396–400.CrossRefPubMedGoogle Scholar
  28. 28.
    Fu J, Bonder MJ, Cenit MC, et al. The gut microbiome contributes to a substantial proportion of the variation in blood lipids. Circ Res. 2015;117:817–24.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Tang WH, Wang Z, Levison BS, et al. Intestinal microbial metabolism of phosphatidylcholine and cardiovascular risk. N Engl J Med. 2013;368:1575–84.CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Wang Z, Klipfell E, Bennett BJ, et al. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature. 2011;472:57–63.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Zoetendal EG, Collier CT, Koike S, et al. Molecular ecological analysis of the gastrointestinal microbiota: a review. J Nutr. 2004;134:465–72.PubMedGoogle Scholar
  32. 32.
    Savage DC. Microbial ecology of the gastrointestinal tract. Annu Rev Microbiol. 1977;31:107–33.CrossRefPubMedGoogle Scholar
  33. 33.
    Finegold SM, Attebery HR, Sutter VL. Effect of diet on human fecal flora: comparison of Japanese and American diets. Am J Clin Nutr. 1974;27:1456–69.PubMedGoogle Scholar
  34. 34.
    Suau A, Bonnet R, Sutren M, et al. Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut. Appl Environ Microbiol. 1999;65:4799–807.PubMedPubMedCentralGoogle Scholar
  35. 35.
    Eckburg PB, Bik EM, Bernstein CN, et al. Diversity of the human intestinal microbial flora. Science. 2005;308:1635–8.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Tringe SG, von Mering C, Kobayashi A, et al. Comparative metagenomics of microbial communities. Science. 2005;308:554–7.CrossRefPubMedGoogle Scholar
  37. 37.
    Olsen GJ, Lane DJ, Giovannoni SJ, et al. Microbial ecology and evolution: a ribosomal RNA approach. Annu Rev Microbiol. 1986;40:337–65.CrossRefPubMedGoogle Scholar
  38. 38.
    Caporaso JG, Kuczynski J, Stombaugh J, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335–6.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Caporaso JG, Lauber CL, Walters WA, et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 2012;6:1621–4.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Morgan XC, Huttenhower C. Chapter 12: human microbiome analysis. PLoS Comput Biol. 2012;8:e1002808.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Weisburg WG, Barns SM, Pelletier DA, et al. 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol. 1991;173:697–703.PubMedPubMedCentralGoogle Scholar
  42. 42.
    Gill SR, Pop M, Deboy RT, et al. Metagenomic analysis of the human distal gut microbiome. Science. 2006;312:1355–9.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature. 2012;486:207–14.CrossRefGoogle Scholar
  44. 44.
    Turnbaugh PJ, Ley RE, Hamady M, et al. The human microbiome project. Nature. 2007;449:804–10.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Ley RE, Backhed F, Turnbaugh P, et al. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A. 2005;102:11070–5.CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Walters WA, Xu Z, Knight R. Meta-analyses of human gut microbes associated with obesity and IBD. FEBS Lett. 2014;588:4223–33.CrossRefPubMedGoogle Scholar
  47. 47.
    Turnbaugh PJ, Backhed F, Fulton L, et al. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe. 2008;3:213–23.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Hildebrandt MA, Hoffmann C, Sherrill-Mix SA, et al. High-fat diet determines the composition of the murine gut microbiome independently of obesity. Gastroenterology. 2009;137:1716–24.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Walker AW, Ince J, Duncan SH, et al. Dominant and diet-responsive groups of bacteria within the human colonic microbiota. ISME J. 2011;5:220–30.CrossRefPubMedGoogle Scholar
  50. 50.
    Wu GD, Chen J, Hoffmann C, et al. Linking long-term dietary patterns with gut microbial enterotypes. Science. 2011;334:105–8.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    De Filippis F, Pellegrini N, Vannini L, et al. High-level adherence to a Mediterranean diet beneficially impacts the gut microbiota and associated metabolome. Gut. 2015. doi:10.1136/gutjnl-2015-309957.PubMedGoogle Scholar
  52. 52.
    Kovatcheva-Datchary P, Nilsson A, Akrami R, et al. Dietary fiber-induced improvement in glucose metabolism is associated with increased abundance of prevotella. Cell Metab. 2015;22:971–82.CrossRefPubMedGoogle Scholar
  53. 53.
    Dillon SM, Lee EJ, Kotter CV, et al. Gut dendritic cell activation links an altered colonic microbiome to mucosal and systemic T-cell activation in untreated HIV-1 infection. Mucosal Immunol. 2016;9:24–37.CrossRefPubMedGoogle Scholar
  54. 54.•
    Forslund K, Hildebrand F, Nielsen T, et al. Disentangling type 2 diabetes and metformin treatment signatures in the human gut microbiota. Nature. 2015;528:262–6. A study illustrating the potential for medication to confound associations between the gut microbiota and the health outcomes.CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Integrative HMP Research Network Consortium. The integrative human microbiome project: dynamic analysis of microbiome-host omics profiles during periods of human health and disease. Cell Host Microbe. 2014;16:276–89.CrossRefGoogle Scholar
  56. 56.
    Chen R, Mias GI, Li-Pook-Than J, et al. Personal omics profiling reveals dynamic molecular and medical phenotypes. Cell. 2012;148:1293–307.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Kussmann M, Raymond F, Affolter M. OMICS-driven biomarker discovery in nutrition and health. J Biotechnol. 2006;124:758–87.CrossRefPubMedGoogle Scholar
  58. 58.•
    Duffy LC, Raiten DJ, Hubbard VS, et al. Progress and challenges in developing metabolic footprints from diet in human gut microbial cometabolism. J Nutr. 2015;145:1123S–30S. A review of pathways to dietary metabolites through gut microbiota metabolism.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    den Besten G, van Eunen K, Groen AK, et al. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J Lipid Res. 2013;54:2325–40.CrossRefGoogle Scholar
  60. 60.
    Manach C, Scalbert A, Morand C, et al. Polyphenols: food sources and bioavailability. Am J Clin Nutr. 2004;79:727–47.PubMedGoogle Scholar
  61. 61.•
    Marcobal A, Kashyap PC, Nelson TA, et al. A metabolomic view of how the human gut microbiota impacts the host metabolome using humanized and gnotobiotic mice. ISME J. 2013;7:1933–43. An example of the integration of human samples and animal models for mechanistic understanding of gut microbiota-metabolome pathways.CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Turnbaugh PJ, Ridaura VK, Faith JJ, et al. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med. 2009;1:6ra14.CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Tang WH, Wang Z, Kennedy DJ, et al. Gut microbiota-dependent trimethylamine N-oxide (TMAO) pathway contributes to both development of renal insufficiency and mortality risk in chronic kidney disease. Circ Res. 2015;116:448–55.CrossRefPubMedGoogle Scholar
  64. 64.
    Rhee EP, Ho JE, Chen MH, et al. A genome-wide association study of the human metabolome in a community-based cohort. Cell Metab. 2013;18:130–43.CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Lever M, George PM, Slow S, et al. Betaine and trimethylamine-N-oxide as predictors of cardiovascular outcomes show different patterns in diabetes mellitus: An observational study. PLoS One. 2014;9:e114969.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Miao J, Ling AV, Manthena PV, et al. Flavin-containing monooxygenase 3 as a potential player in diabetes-associated atherosclerosis. Nat Commun. 2015;6:6498.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Gao X, Xu J, Jiang C, et al. Fish oil ameliorates trimethylamine N-oxide-exacerbated glucose intolerance in high-fat diet-fed mice. Food Funct. 2015;6:1117–25.CrossRefPubMedGoogle Scholar
  68. 68.
    Mueller DM, Allenspach M, Othman A, et al. Plasma levels of trimethylamine-N-oxide are confounded by impaired kidney function and poor metabolic control. Atherosclerosis. 2015;243:638–44.CrossRefPubMedGoogle Scholar
  69. 69.
    Wang TJ, Larson MG, Vasan RS, et al. Metabolite profiles and the risk of developing diabetes. Nat Med. 2011;17:448–53.CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Zhu W, Gregory JC, Org E, et al. Gut microbial metabolite TMAO enhances platelet hyperreactivity and thrombosis risk. Cell. 2016;165:111–24.CrossRefPubMedGoogle Scholar
  71. 71.
    Bennett BJ, de Aguiar Vallim TQ, Wang Z, et al. Trimethylamine-N-oxide, a metabolite associated with atherosclerosis, exhibits complex genetic and dietary regulation. Cell Metab. 2013;17:49–60.CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Hartiala J, Bennett BJ, Tang WH, et al. Comparative genome-wide association studies in mice and humans for trimethylamine N-oxide, a proatherogenic metabolite of choline and L-carnitine. Arterioscler Thromb Vasc Biol. 2014;34:1307–13.CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Craciun S, Balskus EP. Microbial conversion of choline to trimethylamine requires a glycyl radical enzyme. Proc Natl Acad Sci U S A. 2012;109:21307–12.CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Koeth RA, Levison BS, Culley MK, et al. gamma-Butyrobetaine is a proatherogenic intermediate in gut microbial metabolism of L-carnitine to TMAO. Cell Metab. 2014;20:799–812.CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Zhu Y, Jameson E, Crosatti M, et al. Carnitine metabolism to trimethylamine by an unusual Rieske-type oxygenase from human microbiota. Proc Natl Acad Sci U S A. 2014;111:4268–73.CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Falony G, Vieira-Silva S, Raes J. Microbiology meets big data: the case of gut microbiota-derived trimethylamine. Annu Rev Microbiol. 2015;69:305–21.CrossRefPubMedGoogle Scholar
  77. 77.•
    Miller CA, Corbin KD, da Costa KA, et al. Effect of egg ingestion on trimethylamine-N-oxide production in humans: a randomized, controlled, dose-response study. Am J Clin Nutr. 2014;100:778–86. A controlled feeding study demonstrating variable production of trimethylamine N-oxide, a gut microbiota-dependent nutrient metabolite.CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Chen ML, Yi L, Zhang Y, et al. Resveratrol attenuates trimethylamine-N-oxide (TMAO)-induced atherosclerosis by regulating TMAO synthesis and bile acid metabolism via remodeling of the gut microbiota. MBio. 2016;7:e02210–5.PubMedPubMedCentralGoogle Scholar
  79. 79.
    Wu WK, Panyod S, Ho CT, et al. Dietary allicin reduces transformation of L-carnitine to TMAO through impact on gut microbiota. J Funct Foods. 2015;15:408–17.CrossRefGoogle Scholar
  80. 80.
    Cho CE, Taesuwan S, Malysheva OV, et al. Trimethylamine-N-oxide biomarker response is a function of dietary precursor intake and gut microbiota composition in healthy young men. FASEB J. 2016;30(1):Supplement 406.6.Google Scholar
  81. 81.
    Manach C, Williamson G, Morand C, et al. Bioavailability and bioefficacy of polyphenols in humans. I. Review of 97 bioavailability studies. Am J Clin Nutr. 2005;81:230S–42S.PubMedGoogle Scholar
  82. 82.
    Williamson G, Manach C. Bioavailability and bioefficacy of polyphenols in humans. II. Review of 93 intervention studies. Am J Clin Nutr. 2005;81:243S–55S.PubMedGoogle Scholar
  83. 83.
    Scalbert A, Manach C, Morand C, et al. Dietary polyphenols and the prevention of diseases. Crit Rev Food Sci Nutr. 2005;45:287–306.CrossRefPubMedGoogle Scholar
  84. 84.
    Manach C, Mazur A, Scalbert A. Polyphenols and prevention of cardiovascular diseases. Curr Opin Lipidol. 2005;16:77–84.CrossRefPubMedGoogle Scholar
  85. 85.
    Ding M, Franke AA, Rosner BA, et al. Urinary isoflavonoids and risk of type 2 diabetes: a prospective investigation in US women. Br J Nutr. 2015;114:1694–701.CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    Sun Q, Wedick NM, Pan A, et al. Gut microbiota metabolites of dietary lignans and risk of type 2 diabetes: a prospective investigation in two cohorts of U.S. women. Diabetes Care. 2014;37:1287–95.CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Bowey E, Adlercreutz H, Rowland I. Metabolism of isoflavones and lignans by the gut microflora: a study in germ-free and human flora associated rats. Food Chem Toxicol. 2003;41:631–6.CrossRefPubMedGoogle Scholar
  88. 88.
    Song KB, Atkinson C, Frankenfeld CL, et al. Prevalence of daidzein-metabolizing phenotypes differs between Caucasian and Korean American women and girls. J Nutr. 2006;136:1347–51.PubMedGoogle Scholar
  89. 89.
    Setchell KD, Cole SJ. Method of defining equol-producer status and its frequency among vegetarians. J Nutr. 2006;136:2188–93.PubMedGoogle Scholar
  90. 90.
    Rowland IR, Wiseman H, Sanders TA, et al. Interindividual variation in metabolism of soy isoflavones and lignans: influence of habitual diet on equol production by the gut microflora. Nutr Cancer. 2000;36:27–32.CrossRefPubMedGoogle Scholar
  91. 91.
    Atkinson C, Newton KM, Bowles EJ, et al. Demographic, anthropometric, and lifestyle factors and dietary intakes in relation to daidzein-metabolizing phenotypes among premenopausal women in the United States. Am J Clin Nutr. 2008;87:679–87.PubMedGoogle Scholar
  92. 92.
    Lampe JW, Skor HE, Li S, et al. Wheat bran and soy protein feeding do not alter urinary excretion of the isoflavan equol in premenopausal women. J Nutr. 2001;131:740–4.PubMedGoogle Scholar
  93. 93.
    Melby MK, Watanabe S. Soy isoflavones in epidemiologic serum samples: what are the optimal time window and concentration cutoffs for assignment of equol producer status? Austin J Nutr and Food Sci. 2014;2:id1034.Google Scholar
  94. 94.•
    Hanage WP. Microbiology: microbiome science needs a healthy dose of scepticism. Nature. 2014;512:247–8. An excellent summary of current challenges in microbiome research.CrossRefPubMedGoogle Scholar
  95. 95.
    Arrieta MC, Walter J, Finlay BB. Human microbiota-associated mice: a model with challenges. Cell Host Microbe. 2016;19:575–8.CrossRefPubMedGoogle Scholar
  96. 96.•
    David LA, Maurice CF, Carmody RN, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505:559–63. A controlled feeding study demonstrating changes in microbial metabolite production and gene expression within 24-h of shifting between plant- and animal-based diets.CrossRefPubMedGoogle Scholar
  97. 97.
    Brooks JP, Edwards DJ, Harwich Jr MD, et al. The truth about metagenomics: quantifying and counteracting bias in 16S rRNA studies. BMC Microbiol. 2015;15:66.CrossRefPubMedPubMedCentralGoogle Scholar
  98. 98.
    Sinha R, Abnet CC, White O, et al. The microbiome quality control project: baseline study design and future directions. Genome Biol. 2015;16:276.CrossRefPubMedPubMedCentralGoogle Scholar
  99. 99.
    Zeevi D, Korem T, Zmora N, et al. Personalized nutrition by prediction of glycemic responses. Cell. 2015;163:1079–94.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  1. 1.Department of Nutrition, Gillings School of Global Public HealthUniversity of North Carolina at Chapel HillChapel HillUSA
  2. 2.Nutrition Research InstituteUniversity of North Carolina at Chapel HillKannapolisUSA
  3. 3.Department of Genetics, School of MedicineUniversity of North Carolina at Chapel HillChapel HillUSA

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