Sex, body mass index, and dietary fiber intake influence the human gut microbiome

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Dominianni, Christine ^a   Sinha, Rashmi ^c   Goedert, James J ^c   Pei, Zhiheng ^a,b,d   Yang, Liying ^a   Hayes, Richard B ^a,b   Ahn, Jiyoung ^a,b  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RNA 16S;

ACTINOBACTERIA; ADULT; ARTICLE; ASIAN; BACTEROIDETES; BEAN; BLACK PERSON; BODY MASS; CAUCASIAN; CLOSTRIDIA; DIETARY FIBER; FECES ANALYSIS; FEMALE; FRUIT; GASTROINTESTINAL TRACT FUNCTION; GENE CLUSTER; GENE SEQUENCE; HISPANIC; HUMAN; INTESTINE FLORA; MALE; MICROBIAL GENOME; MULTIVARIATE ANALYSIS OF VARIANCE; MULTIVARIATE LOGISTIC REGRESSION ANALYSIS; NORMAL HUMAN; PACIFIC ISLANDER; POPULATION ABUNDANCE; SEX DIFFERENCE; TAXONOMY; VEGETABLE; ADMINISTRATION AND DOSAGE; AGED; ANIMAL; BACTERIAL GENE; CHEMISTRY; CLASSIFICATION; CLOSTRIDIUM; FECES; GASTROINTESTINAL TRACT; GENETICS; MICROBIOLOGY; MICROFLORA; MIDDLE AGED; STATISTICAL MODEL;

ACTINOBACTERIA; ANIMALIA; BACTEROIDETES; CLOSTRIDIA;

ACTINOBACTERIA; AGED; ANIMALS; BACTEROIDETES; BODY MASS INDEX; CLOSTRIDIUM; DIETARY FIBER; FECES; FEMALE; FRUIT; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; GENES, BACTERIAL; HUMANS; LOGISTIC MODELS; MALE; MICROBIOTA; MIDDLE AGED; RNA, RIBOSOMAL, 16S; SEX FACTORS; VEGETABLES;

EID: 84928902130     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0124599     Document Type: Article

References (58)

1. Savage DC. Microbial ecology of the gastrointestinal tract. Annual review of microbiology. 1977; 31:107-33. PMID: 334036
2. Kau AL, Ahern PP, Griffin NW, Goodman AL, Gordon JI. Human nutrition, the gut microbiome and the immune system. Nature. 2011; 474(7351):327-36. doi: 10.1038/nature10213 PMID: 21677749
3. Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R. Bacterial community variation in human body habitats across space and time. Science. 2009; 326(5960):1694-7. doi: 10.1126/science.1177486 PMID: 19892944
4. Salonen A, de Vos WM, Palva A. Gastrointestinal microbiota in irritable bowel syndrome: present state and perspectives. Microbiology. 2010; 156(Pt 11):3205-15. doi: 10.1099/mic.0.043257-0 PMID: 20705664
5. Morgan XC, Tickle TL, Sokol H, Gevers D, Devaney KL, Ward DV, et al. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome biology. 2012; 13(9):R79. doi: 10.1186/gb-2012-13-9-r79 PMID: 23013615
6. Sobhani I, Tap J, Roudot-Thoraval F, Roperch JP, Letulle S, Langella P, et al. Microbial dysbiosis in colorectal cancer (CRC) patients. PloS one. 2011; 6(1):e16393. doi: 10.1371/journal.pone.0016393 PMID: 21297998
7. Kostic AD, Gevers D, Pedamallu CS, Michaud M, Duke F, Earl AM, et al. Genomic analysis identifies association of Fusobacterium with colorectal carcinoma. Genome research. 2012; 22(2):292-8. doi: 10.1101/gr.126573.111 PMID: 22009990
8. Ahn J, Sinha R, Pei Z, Dominianni C, Wu J, Shi J, et al. Human gut microbiome and risk for colorectal cancer. Journal of the National Cancer Institute. 2013; 105(24):1907-11. doi: 10.1093/jnci/djt300 PMID: 24316595
9. Flores R, Shi J, Fuhrman B, Xu X, Veenstra TD, Gail MH, et al. Fecal microbial determinants of fecal and systemic estrogens and estrogen metabolites: a cross-sectional study. Journal of translational medicine. 2012; 10:253. doi: 10.1186/1479-5876-10-253 PMID: 23259758
10. Markle JG, Frank DN, Mortin-Toth S, Robertson CE, Feazel LM, Rolle-Kampczyk U, et al. Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science. 2013; 339 (6123):1084-8. doi: 10.1126/science.1233521 PMID: 23328391
11. Bulun SE, Chen D, Moy I, Brooks DC, Zhao H. Aromatase, breast cancer and obesity: a complex interaction. Trends in endocrinology and metabolism: TEM. 2012; 23(2):83-9. doi: 10.1016/j.tem.2011.10.003 PMID: 22169755
12. Ley RE, Backhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. Proceedings of the National Academy of Sciences of the United States of America. 2005; 102(31):11070-5. PMID: 16033867
13. Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature. 2006; 444(7122):1022-3. PMID: 17183309
14. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, et al. A core gut microbiome in obese and lean twins. Nature. 2009; 457(7228):480-4. doi: 10.1038/nature07540 PMID: 19043404
15. Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE, Kau AL, et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science. 2013; 341(6150):1241214. doi: 10.1126/science.1241214 PMID: 24009397
16. Tuohy KM, Conterno L, Gasperotti M, Viola R. Up-regulating the human intestinal microbiome using whole plant foods, polyphenols, and/or fiber. Journal of agricultural and food chemistry. 2012; 60(36):8776-82. doi: 10.1021/jf2053959 PMID: 22607578
17. Gaskins AJ, Mumford SL, Zhang C, Wactawski-Wende J, Hovey KM, Whitcomb BW, et al. Effect of daily fiber intake on reproductive function: the BioCycle Study. The American journal of clinical nutrition. 2009; 90(4):1061-9. doi: 10.3945/ajcn.2009.27990 PMID: 19692496
18. Gibson GR, Beatty ER, Wang X, Cummings JH. Selective stimulation of bifidobacteria in the human colon by oligofructose and inulin. Gastroenterology. 1995; 108(4):975-82. PMID: 7698613
19. Bouhnik Y, Raskine L, Simoneau G, Vicaut E, Neut C, Flourie B, et al. The capacity of nondigestible carbohydrates to stimulate fecal bifidobacteria in healthy humans: a double-blind, randomized, placebo-controlled, parallel-group, dose-response relation study. The American journal of clinical nutrition. 2004; 80(6):1658-64. PMID: 15585783
20. Whelan K, Judd PA, Preedy VR, Simmering R, Jann A, Taylor MA. Fructooligosaccharides and fiber partially prevent the alterations in fecal microbiota and short-chain fatty acid concentrations caused by standard enteral formula in healthy humans. The Journal of nutrition. 2005; 135(8):1896-902. PMID: 16046714
21. Benus RF, van der Werf TS, Welling GW, Judd PA, Taylor MA, Harmsen HJ, et al. Association between Faecalibacterium prausnitzii and dietary fibre in colonic fermentation in healthy human subjects. The British journal of nutrition. 2010; 104(5):693-700. doi: 10.1017/S0007114510001030 PMID: 20346190
22. Hooda S, Boler BM, Serao MC, Brulc JM, Staeger MA, Boileau TW, et al. 454 pyrosequencing reveals a shift in fecal microbiota of healthy adult men consuming polydextrose or soluble corn fiber. The Journal of nutrition. 2012; 142(7):1259-65. doi: 10.3945/jn.112.158766 PMID: 22649263
23. Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA, et al. Linking long-term dietary patterns with gut microbial enterotypes. Science. 2011; 334(6052):105-8. doi: 10.1126/science.1208344 PMID: 21885731
24. Chen HM, Yu YN, Wang JL, Lin YW, Kong X, Yang CQ, et al. Decreased dietary fiber intake and structural alteration of gut microbiota in patients with advanced colorectal adenoma. The American journal of clinical nutrition. 2013; 97(5):1044-52. doi: 10.3945/ajcn.112.046607 PMID: 23553152
25. Romero-Corral A, Somers VK, Sierra-Johnson J, Thomas RJ, Collazo-Clavell ML, Korinek J, et al. Accuracy of body mass index in diagnosing obesity in the adult general population. Int J Obes (Lond). 2008; 32(6):959-66. doi: 10.1038/ijo.2008.11 PMID: 18283284
26. Schiffman MH, Andrews AW, Van Tassell RL, Smith L, Daniel J, Robinson A, et al. Case-control study of colorectal cancer and fecal mutagenicity. Cancer research. 1989; 49(12):3420-4. PMID: 2655896
27. Schiffman MH, Van Tassell RL, Robinson A, Smith L, Daniel J, Hoover RN, et al. Case-control study of colorectal cancer and fecapentaene excretion. Cancer research. 1989; 49(5):1322-6. PMID: 2917361
28. Classification BMI. Global Database on Body Mass Index World Health Organization. 2006.
29. Subar AF, Midthune D, Kulldorff M, Brown CC, Thompson FE, Kipnis V, et al. Evaluation of alternative approaches to assign nutrient values to food groups in food frequency questionnaires. American journal of epidemiology. 2000; 152(3):279-86. PMID: 10933275
30. Willett W. Nutritional Epidemiology: Oxford University Press; 1998.
31. Nossa CW, Oberdorf WE, Yang L, Aas JA, Paster BJ, Desantis TZ, et al. Design of 16S rRNA gene primers for 454 pyrosequencing of the human foregut microbiome. World journal of gastroenterology: WJG. 2010; 16(33):4135-44. PMID: 20806429
32. Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos G, et al. Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome research. 2011; 21(3):494-504. doi: 10.1101/gr.112730.110 PMID: 21212162
33. Kuczynski J, Stombaugh J, Walters WA, Gonzalez A, Caporaso JG, Knight R. Using QIIME to analyze 16S rRNA gene sequences from microbial communities. Current protocols in bioinformatics / editoral board, Andreas D Baxevanis [et al]. 2011;Chapter 10:Unit 10 7.
34. Lozupone C, Hamady M, Knight R. UniFrac-an online tool for comparing microbial community diversity in a phylogenetic context. BMC bioinformatics. 2006; 7:371. PMID: 16893466
35. Anderson BHMMJ. Fitting multivariate models to community data: a comment on distance based redundancy analysis. Ecology. 2001; 82(1):290-7.
36. Shannon CE. A Mathematical Theory of Communication. At&T Tech J. 1948; 27(4):623-56.
37. Benjamini Y, Y. H. Controlling the false discovery rate: A practical and powerful approach to multiple testing Journal of the Royal Statistical Society. 1995; 57(1):289-300.
38. Mueller S, Saunier K, Hanisch C, Norin E, Alm L, Midtvedt T, et al. Differences in fecal microbiota in different European study populations in relation to age, gender, and country: a cross-sectional study. Applied and environmental microbiology. 2006; 72(2):1027-33. PMID: 16461645
39. Yurkovetskiy L, Burrows M, Khan AA, Graham L, Volchkov P, Becker L, et al. Gender bias in autoimmunity is influenced by microbiota. Immunity. 2013; 39(2):400-12. doi: 10.1016/j.immuni.2013.08.013 PMID: 23973225
40. Lampe JW, Fredstrom SB, Slavin JL, Potter JD. Sex differences in colonic function: a randomised trial. Gut. 1993; 34(4):531-6. PMID: 8387940
41. Degen LP, Phillips SF. Variability of gastrointestinal transit in healthy women and men. Gut. 1996; 39(2):299-305. PMID: 8977347
42. Stipanuk M, Caudill MA. Biochemical, Physiological, and Molecular Aspects of Human Nutrition. 3rd ed: Elsevier Saunders; 2013.
43. Duncan SH, Louis P, Thomson JM, Flint HJ. The role of pH in determining the species composition of the human colonic microbiota. Environmental microbiology. 2009; 11(8):2112-22. doi: 10.1111/j.1462-2920.2009.01931.x PMID: 19397676
44. Probert CS, Emmett PM, Heaton KW. Some determinants of whole-gut transit time: a population-based study. QJM: monthly journal of the Association of Physicians. 1995; 88(5):311-5. PMID: 7796084
45. Lewis SJ, Heaton KW. Increasing butyrate concentration in the distal colon by accelerating intestinal transit. Gut. 1997; 41(2):245-51. PMID: 9301506
46. Louis P, Flint HJ. Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine. FEMS microbiology letters. 2009; 294(1):1-8. doi: 10.1111/j.1574-6968.2009.01514.x PMID: 19222573
47. Hamer HM, Jonkers D, Venema K, Vanhoutvin S, Troost FJ, Brummer RJ. Review article: the role of butyrate on colonic function. Alimentary pharmacology & therapeutics. 2008; 27(2):104-19.
48. Landa-Habana L, Pina-Hernandez A, Agama-Acevedo E, Tovar J, Bello-Perez LA. Effect of cooking procedures and storage on starch bioavailability in common beans (Phaseolus vulgaris L.). Plant foods for human nutrition (Dordrecht, Netherlands). 2004; 59(4):133-6. PMID: 15678720
49. Yadav BS, Sharma A, Yadav RB. Studies on effect of multiple heating/cooling cycles on the resistant starch formation in cereals, legumes and tubers. International journal of food sciences and nutrition. 2009; 60 Suppl 4:258-72. doi: 10.1080/09637480902970975 PMID: 19562607
50. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, et al. Diversity of the human intestinal microbial flora. Science. 2005; 308(5728):1635-8. PMID: 15831718
51. Martinez I, Kim J, Duffy PR, Schlegel VL, Walter J. Resistant starches types 2 and 4 have differential effects on the composition of the fecal microbiota in human subjects. PloS one. 2010; 5(11):e15046. doi: 10.1371/journal.pone.0015046 PMID: 21151493
52. Walker AW, Ince J, Duncan SH, Webster LM, Holtrop G, Ze X, et al. Dominant and diet-responsive groups of bacteria within the human colonic microbiota. The ISME journal. 2011; 5(2):220-30. doi: 10.1038/ismej.2010.118 PMID: 20686513
53. Larsen N, Vogensen FK, van den Berg FW, Nielsen DS, Andreasen AS, Pedersen BK, et al. Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PloS one. 2010; 5(2):e9085. doi: 10.1371/journal.pone.0009085 PMID: 20140211
54. Nielsen DS, Krych L, Buschard K, Hansen CH, Hansen AK. Beyond genetics. Influence of dietary factors and gut microbiota on type 1 diabetes. FEBS letters. 2014.
55. Ngo ST, Steyn FJ, McCombe PA. Gender differences in autoimmune disease. Frontiers in neuroendocrinology. 2014; 35(3):347-69. doi: 10.1016/j.yfrne.2014.04.004 PMID: 24793874
56. Vucenik I, Stains JP. Obesity and cancer risk: evidence, mechanisms, and recommendations. Annals of the New York Academy of Sciences. 2012; 1271:37-43. doi: 10.1111/j.1749-6632.2012.06750.x PMID: 23050962
57. Versini M, Jeandel PY, Rosenthal E, Shoenfeld Y. Obesity in autoimmune diseases: Not a passive bystander. Autoimmunity reviews. 2014.
58. Slavin J. Fiber and prebiotics: mechanisms and health benefits. Nutrients. 2013; 5(4):1417-35. doi: 10.3390/nu5041417 PMID: 23609775