Role of the gut microbiota in human nutrition and metabolism

Journal of Gastroenterology and Hepatology (Australia)

Volumn 28, Issue S4, 2013, Pages 9-17

  Ramakrishna, Balakrishnan S ^a,b  

^a SRM INSTITUTE OF SCIENCE AND TECHNOLOGY   (India)

^b FLINDERS UNIVERSITY   (Australia)

Author keywords

Bacteroides; Clostridia; Diabetes; Faecalibacterium; Firmicutes; Metabolic syndrome; Non alcoholic steatohepatitis; Obesity

Indexed keywords

MINERAL; SHORT CHAIN FATTY ACID;

ARTICLE; FERMENTATION; GLUCOSE METABOLISM; HUMAN; INTESTINE ABSORPTION; INTESTINE FLORA; LIPID METABOLISM; METABOLIC CAPACITY; NONHUMAN; NUTRITION; OBESITY; PRIORITY JOURNAL; PROTEIN CALORIE MALNUTRITION; PROTEIN METABOLISM;

BACTEROIDES; CLOSTRIDIA; DIABETES; FAECALIBACTERIUM; FIRMICUTES; METABOLIC SYNDROME; NON-ALCOHOLIC STEATOHEPATITIS; OBESITY;

ANIMALS; BACTERIAL PHYSIOLOGICAL PHENOMENA; CARBOHYDRATE METABOLISM; COGNITION DISORDERS; DIABETES MELLITUS; ENERGY METABOLISM; EPITHELIAL CELLS; FATTY ACIDS, VOLATILE; FATTY LIVER; FERMENTATION; FOOD; GASTROINTESTINAL TRACT; HUMANS; INTESTINAL ABSORPTION; LIPID METABOLISM; METABOLIC SYNDROME X; MICE; MINERALS; NUTRITIONAL PHYSIOLOGICAL PHENOMENA; OBESITY; PROTEINS; VITAMIN B COMPLEX; VITAMIN K;

EID: 84897628732     PISSN: 08159319     EISSN: 14401746     Source Type: Journal    
DOI: 10.1111/jgh.12294     Document Type: Article

References (88)

1. Ramakrishna BS. The normal bacterial flora of the human intestine and its regulation. J. Clin. Gastroenterol. 2007; 41: S2-6.
2. Shanahan F. The colonic microbiota in health and disease. Curr. Opin. Gastroenterol. 2013; 29: 49-54.
3. Goodman AL, Gordon JI. Our unindicted coconspirators: human metabolism from a microbial perspective. Cell Metab. 2010; 12: 111-116.
4. Eckburg PB, Bik EM, Bernstein CN etal. Diversity of the human intestinal microbial flora. Science 2005; 308: 1635-1638.
5. Gill SR, Pop M, Deboy RT etal. Metagenomic analysis of the human distal gut microbiome. Science 2006; 312: 1355-1359.
6. Faith JJ, Rey FE, O'Donnell D etal. Creating and characterizing communities of human gut microbes in gnotobiotic mice. ISME J. 2010; 4: 1094-1098.
7. Hamer HM, De Preter V, Windey K, Verbeke K. Functional analysis of colonic bacterial metabolism: relevant to health? Am. J. Physiol. Gastrointest. Liver Physiol. 2012; 302: G1-9.
8. Kau AL, Ahern PP, Griffin NW, Goodman AL, Gordon JI. Human nutrition, the gut microbiome and the immune system. Nature 2011; 474: 327-336.
9. Flint HJ, Scott KP, Louis P, Duncan SH. The role of the gut microbiota in nutrition and health. Nat. Rev. Gastroenterol. Hepatol. 2012; 9: 577-589.
10. Dutton RJ, Turnbaugh PJ. Taking a metagenomic view of human nutrition. Curr. Opin. Clin. Nutr. Metab. Care 2012; 15: 448-454.
11. Yatsunenko T, Rey FE, Manary MJ etal. Human gut microbiome viewed across age and geography. Nature 2012; 486: 222-227.
12. Arumugam M, Raes J, Pelletier E etal. Enterotypes of the human gut microbiome. Nature 2011; 473: 174-180.
13. Wu GD, Chen J, Hoffmann C etal. Linking long-term dietary patterns with gut microbial enterotypes. Science 2011; 334: 105-108.
14. Mountzouris KC, McCartney AL, Gibson GR. Intestinal microflora of human infants and current trends for its nutritional modulation. Br. J. Nutr. 2002; 87: 405-420.
15. Balamurugan R, Magne F, Balakrishnan D etal. Faecal bifidobacteria in Indian neonates & the effect of asymptomatic rotavirus infection during the first month of life. Indian J. Med. Res. 2010; 132: 721-727.
16. Jost T, Lacroix C, Braegger CP, Chassard C. New insights in gut microbiota establishment in healthy breast fed neonates. PLoS ONE 2012; 7: e44595.
17. Kabeerdoss J, Ferdous S, Balamurugan R etal. Development of the gut microbiota in southern Indian infants from birth to six months: a molecular analysis. J. Nutr. Sci. 2013.
18. Balamurugan R, Janardhan HP, George S, Chittaranjan SP, Ramakrishna BS. Bacterial succession in the colon during childhood and adolescence: molecular studies in a southern Indian village. Am. J. Clin. Nutr. 2008; 88: 1643-1647.
19. Ramakrishna BS, Roediger WE. Bacterial short chain fatty acids: their role in gastrointestinal disease. Dig. Dis. 1990; 8: 337-345.
20. Windey K, De Preter V, Verbeke K. Relevance of protein fermentation to gut health. Mol. Nutr. Food Res. 2012; 56: 184-196.
21. Ramakrishna BS, Gee D, Weiss A, Pannall P, Roberts-Thomson IC, Roediger WE. Estimation of phenolic conjugation by colonic mucosa. J. Clin. Pathol. 1989; 42: 620-623.
22. Leblanc JG, Milani C, de Giori GS, Sesma F, van Sinderen D, Ventura M. Bacteria as vitamin suppliers to their host: a gut microbiota perspective. Curr. Opin. Biotechnol. 2013; 24: 160-168.
23. Albert MJ, Mathan VI, Baker SJ. Vitamin B12 synthesis by human small intestinal bacteria. Nature 1980; 283: 781-782.
24. Bird AR, Brown IL, Topping DL. Starches, resistant starches, the gut microflora and human health. Curr. Issues Intest. Microbiol. 2000; 1: 25-37.
25. Kumar V, Sinha AK, Makkar HP, de Boeck G, Becker K. Dietary roles of non-starch polysaccharides in human nutrition: a review. Crit. Rev. Food Sci. Nutr. 2012; 52: 899-935.
26. Flint HJ, Scott KP, Duncan SH, Louis P, Forano E. Microbial degradation of complex carbohydrates in the gut. Gut Microbes 2012; 3: 289-306.
27. Bird AR, Conlon MA, Christophersen CT, Topping DL. Resistant starch, large bowel fermentation and a broader perspective of prebiotics and probiotics. Benef. Microbes 2010; 1: 423-431.
28. Louis P, Scott KP, Duncan SH, Flint HJ. Understanding the effects of diet on bacterial metabolism in the large intestine. J. Appl. Microbiol. 2007; 102: 1197-1208.
29. Kaur A, Rose DJ, Rumpagaporn P, Patterson JA, Hamaker BR. In vitro batch fecal fermentation comparison of gas and short-chain fatty acid production using "slowly fermentable" dietary fibers. J. Food Sci. 2011; 76: H137-142.
30. Atia A, Girard-Pipau F, Hébuterne X etal. Macronutrient absorption characteristics in humans with short bowel syndrome and jejunocolonic anastomosis: starch is the most important carbohydrate substrate, although pectin supplementation may modestly enhance short chain fatty acid production and fluid absorption. JPEN J. Parenter. Enteral Nutr. 2011; 35: 229-240.
31. Muir JG, Lu ZX, Young GP, Cameron-Smith D, Collier GR, O'Dea K. Resistant starch in the diet increases breath hydrogen and serum acetate in human subjects. Am. J. Clin. Nutr. 1995; 61: 792-799.
32. Hosseini E, Grootaert C, Verstraete W, Van de Wiele T. Propionate as a health-promoting microbial metabolite in the human gut. Nutr. Rev. 2011; 69: 245-258.
33. Arora T, Sharma R. Fermentation potential of the gut microbiome: implications for energy homeostasis and weight management. Nutr. Rev. 2011; 69: 99-106.
34. Kovatcheva-Datchary P, Egert M, Maathuis A etal. Linking phylogenetic identities of bacteria to starch fermentation in an in vitro model of the large intestine by RNA-based stable isotope probing. Environ. Microbiol. 2009; 11: 914-926.
35. Zhang C, Brandt MJ, Schwab C, Gänzle MG. Propionic acid production by cofermentation of Lactobacillus buchneri and Lactobacillus diolivorans in sourdough. Food Microbiol. 2010; 27: 390-395.
36. Wang X, Conway PL, Brown IL, Evans AJ. In vitro utilization of amylopectin and high-amylose maize (Amylomaize) starch granules by human colonic bacteria. Appl. Environ. Microbiol. 1999; 65: 4848-4854.
37. Fushinobu S. Unique sugar metabolic pathways of bifidobacteria. Biosci. Biotechnol. Biochem. 2010; 74: 2374-2384.
38. Fukuda S, Toh H, Hase K etal. Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature 2011; 469: 543-547.
39. Ze X, Duncan SH, Louis P, Flint HJ. Ruminococcus bromii is a keystone species for the degradation of resistant starch in the human colon. ISME J. 2012; 6: 1535-1543.
40. Bäckhed F, Ding H, Wang T etal. The gut microbiota as an environmental factor that regulates fat storage. Proc. Natl. Acad. Sci. U.S.A. 2004; 101: 15718-15723.
41. Ley RE, Bäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. Proc. Natl. Acad. Sci. U.S.A. 2005; 102: 11070-11075.
42. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 2006; 444: 1027-1031.
43. Waldram A, Holmes E, Wang Y etal. Top-down systems biology modeling of host metabotype-microbiome associations in obese rodents. J. Proteome Res. 2009; 8: 2361-2375.
44. Balamurugan R, George G, Kabeerdoss J, Hepsiba J, Chandragunasekaran AM, Ramakrishna BS. Quantitative differences in intestinal Faecalibacterium prausnitzii in obese Indian children. Br. J. Nutr. 2010; 103: 335-338.
45. Armougom F, Henry M, Vialettes B, Raccah D, Raoult D. Monitoring bacterial community of human gut microbiota reveals an increase in Lactobacillus in obese patients and methanogens in anorexic patients. PLoS ONE 2009; 4: e7125.
46. Karlsson CL, Onnerfält J, Xu J, Molin G, Ahrné S, Thorngren-Jerneck K. The microbiota of the gut in preschool children with normal and excessive body weight. Obesity (Silver Spring) 2012; 20: 2257-2261.
47. Patil DP, Dhotre DP, Chavan SG etal. Molecular analysis of gut microbiota in obesity among Indian individuals. J. Biosci. 2012; 37: 647-657.
48. Ferrer M, Ruiz A, Lanza F etal. Microbiota from the distal guts of lean and obese adolescents exhibit partial functional redundancy besides clear differences in community structure. Environ. Microbiol. 2013; 15: 211-226.
49. Turnbaugh PJ, Hamady M, Yatsunenko T etal. A core gut microbiome in obese and lean twins. Nature 2009; 457: 480-484.
50. Liou AP, Paziuk M, Luevano JM Jr, Machineni S, Turnbaugh PJ, Kaplan LM. Conserved shifts in the gut microbiota due to gastric bypass reduce host weight and adiposity. Sci. Transl. Med. 2013; 5: 178ra41.
51. Krajmalnik-Brown R, Ilhan ZE, Kang DW, DiBaise JK. Effects of gut microbes on nutrient absorption and energy regulation. Nutr. Clin. Pract. 2012; 27: 201-214.
52. Venema K. Role of gut microbiota in the control of energy and carbohydrate metabolism. Curr. Opin. Clin. Nutr. Metab. Care 2010; 13: 432-438.
53. Jumpertz R, Le DS, Turnbaugh PJ etal. Energy-balance studies reveal associations between gut microbes, caloric load, and nutrient absorption in humans. Am. J. Clin. Nutr. 2011; 94: 58-65.
54. van Tongeren SP, Slaets JP, Harmsen HJ, Welling GW. Fecal microbiota composition and frailty. Appl. Environ. Microbiol. 2005; 71: 6438-6442.
55. Samuel BS, Shaito A, Motoike T etal. Effects of the gut microbiota on host adiposity are modulated by the short-chain fatty-acid binding G protein-coupled receptor, Gpr41. Proc. Natl. Acad. Sci. U.S.A. 2008; 105: 16767-16772.
56. Tolhurst G, Heffron H, Lam YS etal. Short-chain fatty acids stimulate glucagon-like peptide-1 secretion via the G-protein-coupled receptor FFAR2. Diabetes 2012; 61: 364-371.
57. Bellahcene M, O'Dowd JF, Wargent ET etal. Male mice that lack the G-protein-coupled receptor GPR41 have low energy expenditure and increased body fat content. Br. J. Nutr. 2012; 31: 1-10.
58. Lin HV, Frassetto A, Kowalik EJ Jr etal. Butyrate and propionate protect against diet-induced obesity and regulate gut hormones via free fatty acid receptor 3-independent mechanisms. PLoS ONE 2012; 7: e35240.
59. Backhed F, Manchester JK, Semenkovich CF, Gordon JI. Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc. Natl. Acad. Sci. U.S.A. 2007; 104: 979-984.
60. Verdam FJ, Fuentes S, de Jonge C etal. Human intestinal microbiota composition is associated with local and systemic inflammation in obesity. Obesity (Silver Spring) 2013. doi: 10.1002/oby.20466. [Epub ahead of print].
61. Teixeira TF, Collado MC, Ferreira CL, Bressan J, Peluzio Mdo C. Potential mechanisms for the emerging link between obesity and increased intestinal permeability. Nutr. Res. 2012; 32: 637-647.
62. Kim KA, Gu W, Lee IA, Joh EH, Kim DH. High fat diet-induced gut microbiota exacerbates inflammation and obesity in mice via the TLR4 signaling pathway. PLoS ONE 2012; 7: e47713.
63. Henao-Mejia J, Elinav E, Jin C etal. Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity. Nature 2012; 482: 179-185.
64. Fredborg M, Theil PK, Jensen BB, Purup S. G protein-coupled receptor120 (GPR120) transcription in intestinal epithelial cells is significantly affected by bacteria belonging to the Bacteroides, Proteobacteria, and Firmicutes phyla. J. Anim. Sci. 2012; 90 (Suppl. 4): 10-12.
65. Zhu L, Baker SS, Gill C etal. Characterization of gut microbiomes in nonalcoholic steatohepatitis (NASH) patients: a connection between endogenous alcohol and NASH. Hepatology 2013; 57: 601-609.
66. Ramakrishna BS, Venkataraman S, Mukhopadhya A. Tropical malabsorption. Postgrad. Med. J. 2006; 82: 779-787.
67. Venkatraman A, Ramakrishna BS, Shaji RV, Kumar NS, Pulimood A, Patra S. Amelioration of dextran sulfate colitis by butyrate: role of heat shock protein 70 and NF-kappaB. Am. J. Physiol. Gastrointest. Liver Physiol. 2003; 285: G177-184.
68. Nanda Kumar NS, Balamurugan R, Jayakanthan K, Pulimood A, Pugazhendhi S, Ramakrishna BS. Probiotic administration alters the gut flora and attenuates colitis in mice administered dextran sodium sulfate. J. Gastroenterol. Hepatol. 2008; 23: 1834-1839.
69. Gordon JI, Dewey KG, Mills DA, Medzhitov RM. The human gut microbiota and undernutrition. Sci. Transl. Med. 2012; 4: 137ps12.
70. Monira S, Nakamura S, Gotoh K etal. Gut microbiota of healthy and malnourished children in Bangladesh. Front. Microbiol. 2011; 2: 228.
71. Smith MI, Yatsunenko T, Manary MJ etal. Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. Science 2013; 339: 548-554.
72. Balamurugan R, Mary RR, Chittaranjan S, Jancy H, Shobana Devi R, Ramakrishna BS. Low levels of faecal lactobacilli in women with iron-deficiency anaemia in south India. Br. J. Nutr. 2010; 104: 931-934.
73. Scholz-Ahrens KE, Schrezenmeir J. Inulin and oligofructose and mineral metabolism: the evidence from animal trials. J. Nutr. 2007; 137 (11 Suppl.): 2513S-2523S.
74. Scholz-Ahrens KE, Schrezenmeir J. Inulin, oligofructose and mineral metabolism-experimental data and mechanism. Br. J. Nutr. 2002; 87 (Suppl. 2): S179-186.
75. Levrat MA, Remesy C, Demigne C. High propionic acid fermentations and mineral accumulation in the cecum of rats adapted to different levels of inulin. J. Nutr. 1991; 121: 1730-1737.
76. Caricilli AM, Saad MJ. The role of gut microbiota on insulin resistance. Nutrients 2013; 5: 829-851.
77. Munukka E, Wiklund P, Pekkal S etal. Women with and without metabolic disorder differ in their gut microbiota composition. Obesity (Silver Spring) 2012; 20: 1082-1087.
78. Caricilli AM, Picardi PK, de Abreu LL etal. Gut microbiota is a key modulator of insulin resistance in TLR 2 knockout mice. PLoS Biol. 2011; 9: e1001212.
79. Tremaroli V, Backhed F. Functional interactions between the gut microbiota and host metabolism. Nature 2012; 489: 242-249.
80. Vrieze A, Van Nood E, Holleman F etal. Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology 2012; 143: 913-967.
81. Kumar R, Grover S, Batish VK. Hypocholesterolaemic effect of dietary inclusion of two putative probiotic bile salt hydrolase-producing Lactobacillus plantarum strains in Sprague-Dawley rats. Br. J. Nutr. 2011; 105: 561-573.
82. Favier ML, Moundras C, Demigné C, Rémésy C. Fermentable carbohydrates exert a more potent cholesterol-lowering effect than cholestyramine. Biochim. Biophys. Acta 1995; 1258: 115-121.
83. Levrat MA, Favier ML, Moundras C, Rémésy C, Demigné C, Morand C. Role of dietary propionic acid and bile acid excretion in the hypocholesterolemic effects of oligosaccharides in rats. J. Nutr. 1994; 124: 531-538.
84. Lin Y, Vonk RJ, Slooff MJ, Kuipers F, Smit MJ. Differences in propionate-induced inhibition of cholesterol and triacylglycerol synthesis between human and rat hepatocytes in primary culture. Br. J. Nutr. 1995; 74: 197-207.
85. Nyangale EP, Mottram DS, Gibson GR. Gut microbial activity, implications for health and disease: the potential role of metabolite analysis. J. Proteome Res. 2012; 11: 5573-5585.
86. Davila AM, Blachier F, Gotteland M etal. Re-print of "Intestinal luminal nitrogen metabolism: role of the gut microbiota and consequences for the host." Pharmacol. Res. 2013; 69: 114-126.
87. Bajaj JS, Ridlon JM, Hylemon PB etal. Linkage of gut microbiome with cognition in hepatic encephalopathy. Am. J. Physiol. Gastrointest. Liver Physiol. 2012; 302: G168-175.
88. Bajaj JS, Heuman DM, Sanyal AJ etal. Modulation of the metabiome by rifaximin in patients with cirrhosis and minimal hepatic encephalopathy. PLoS ONE 2013; 8: e60042.