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Open Access 01-02-2018 | Review

Gut microbiota functions: metabolism of nutrients and other food components

Authors: Ian Rowland, Glenn Gibson, Almut Heinken, Karen Scott, Jonathan Swann, Ines Thiele, Kieran Tuohy

Published in: European Journal of Nutrition | Issue 1/2018

Abstract

The diverse microbial community that inhabits the human gut has an extensive metabolic repertoire that is distinct from, but complements the activity of mammalian enzymes in the liver and gut mucosa and includes functions essential for host digestion. As such, the gut microbiota is a key factor in shaping the biochemical profile of the diet and, therefore, its impact on host health and disease. The important role that the gut microbiota appears to play in human metabolism and health has stimulated research into the identification of specific microorganisms involved in different processes, and the elucidation of metabolic pathways, particularly those associated with metabolism of dietary components and some host-generated substances. In the first part of the review, we discuss the main gut microorganisms, particularly bacteria, and microbial pathways associated with the metabolism of dietary carbohydrates (to short chain fatty acids and gases), proteins, plant polyphenols, bile acids, and vitamins. The second part of the review focuses on the methodologies, existing and novel, that can be employed to explore gut microbial pathways of metabolism. These include mathematical models, omics techniques, isolated microbes, and enzyme assays.

Rajilić-Stojanović M, de Vos WM (2014) The first 1000 cultured species of the human gastrointestinal microbiota. FEMS Microbiol Rev 38:996–1047CrossRef

Zhang Q, Raoof M, Chen Y et al (2010) Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature 464:104–107CrossRef

Nicholson JK, Holmes E, Kinross J et al (2012) Host-gut microbiota metabolic interactions. Science 336:1262–1267CrossRef

Greenblum S, Turnbaugh PJ, Borenstein E (2012) Metagenomic systems biology of the human gut microbiome reveals topological shifts associated with obesity and inflammatory bowel disease. Proc Natl Acad Sci U S A 109:594–599CrossRef

Marchesi JR, Adams DH, Fava F et al (2016) The gut microbiota and host health: a new clinical frontier. Gut 65:330–339CrossRef

Boyd SD, Liu Y, Wang C et al (2013) Human lymphocyte repertoires in ageing. Curr Opin Immunol 25:511–515CrossRef

Macfarlane GT, Gibson GR, Cummings JH (1992) Comparison of fermentation reactions in different regions of the human colon. J Appl Bacteriol 72:57–64

Steliou K, Boosalis MS, Perrine SP et al (2012) Butyrate histone deacetylase inhibitors. Biores Open Access 1:192–198CrossRef

De Vadder F, Kovatcheva-Datchary P, Goncalves D et al (2014) Microbiota-generated metabolites promote metabolic benefits via gut-brain neural circuits. Cell 156:84–96CrossRef

10.

Brown AJ, Goldsworthy SM, Barnes AA et al (2003) The Orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids. J Biol Chem 278:11312–11319CrossRef

11.

Tazoe H, Otomo Y, Kaji I et al (2008) Roles of short-chain fatty acids receptors, GPR41 and GPR43 on colonic functions. J Physiol Pharmacol 59(Suppl 2):251–262

12.

Duncan SH, Holtrop G, Lobley GE et al (2004) Contribution of acetate to butyrate formation by human faecal bacteria. Br J Nutr 91:915–923CrossRef

13.

Frost G, Sleeth ML, Sahuri-Arisoylu M et al (2014) The short-chain fatty acid acetate reduces appetite via a central homeostatic mechanism. Nat Commun 5:3611CrossRef

14.

Bjerrum JT, Wang Y, Hao F et al (2015) Metabonomics of human fecal extracts characterize ulcerative colitis, Crohn’s disease and healthy individuals. Metabolomics 11:122–133CrossRef

15.

Belenguer A, Duncan SH, Calder AG et al (2006) Two routes of metabolic cross-feeding between Bifidobacterium adolescentis and butyrate-producing anaerobes from the human gut. Appl Environ Microbiol 72:3593–3599CrossRef

16.

Falony G, Vlachou A, Verbrugghe K, De Vuyst L (2006) Cross-feeding between Bifidobacterium longum BB536 and acetate-converting, butyrate-producing colon bacteria during growth on oligofructose. Appl Environ Microbiol 72:7835–7841CrossRef

17.

Louis P, Young P, Holtrop G, Flint HJ (2010) Diversity of human colonic butyrate-producing bacteria revealed by analysis of the butyryl-CoA: acetate CoA-transferase gene. Environ Microbiol 12:304–314CrossRef

18.

Reichardt N, Duncan SH, Young P et al (2014) Phylogenetic distribution of three pathways for propionate production within the human gut microbiota. ISME J 8:1323–1335CrossRef

19.

Vital M, Howe AC, Tiedje JM (2014) Revealing the bacterial butyrate synthesis pathways by analyzing (meta)genomic data. MBio 5:e00889CrossRef

20.

Louis P, Duncan SH, McCrae SI et al (2004) Restricted distribution of the butyrate kinase pathway among butyrate-producing bacteria from the human colon. J Bacteriol 186:2099–2106CrossRef

21.

Louis P, Flint HJ (2017) Formation of propionate and butyrate by the human colonic microbiota. Environ Microbiol 19(1):29–41CrossRef

22.

Scott KP, Martin JC, Campbell G et al (2006) Whole-genome transcription profiling reveals genes up-regulated by growth on fucose in the human gut bacterium ‘Roseburia inulinivorans’. J Bacteriol 188:4340–4349CrossRef

23.

Hooper LV, Xu J, Falk PG et al (1999) A molecular sensor that allows a gut commensal to control its nutrient foundation in a competitive ecosystem. Proc Natl Acad Sci USA 96:9833–9838CrossRef

24.

El Aidy S, Van den Abbeele P, Van de Wiele T et al (2013) Intestinal colonization: how key microbial players become established in this dynamic process. Bioessays 35:913–923

25.

Duncan SH, Belenguer A, Holtrop G et al (2007) Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces. Appl Env Microbiol 73:1073–1078CrossRef

26.

Francois IEJA, Lescroart O, Veraverbeke WS et al (2012) Effects of a wheat bran extract containing arabinoxylan oligosaccharides on gastrointestinal health parameters in healthy adult human volunteers: a double-blind, randomised, placebo-controlled, cross-over trial. Br J Nutr 108:2229–2242CrossRef

27.

Halmos EP, Christophersen CT, Bird AR et al (2015) Diets that differ in their FODMAP content alter the colonic luminal microenvironment. Gut 64:93–100CrossRef

28.

Levitt MD, Bond JH Jr (1970) Volume, composition, and source of intestinal gas. Gastroenterology 59:921–929

29.

Cummings JH, Macfarlane GT (1991) The control and consequences of bacterial fermentation in the human colon. J Appl Bacteriol 70:443–459CrossRef

30.

Suarez F, Furne J, Springfield J, Levitt M (1997) Insights into human colonic physiology obtained from the study of flatus composition. Am J Physiol 272:G1028–G1033

31.

Gibson GR (1990) Physiology and ecology of the sulphate-reducing bacteria. J Appl Bacteriol 69:769–797CrossRef

32.

Wolf PG, Biswas A, Morales SE, Greening C, Gaskins HR (2016) H2 metabolism is widespread and diverse among human colonic microbes. Gut Microbes 3:235–245CrossRef

33.

Christl SU, Murgatroyd PR, Gibson GR, Cummings JH (1992) Production, metabolism, and excretion of hydrogen in the large intestine. Gastroenterology 102:1269–1277CrossRef

34.

Tomasova L, Konopelski P, Ufnal M (2016) Gut bacteria and hydrogen sulfide: the new old players in circulatory system homeostasis. Molecules 17:E1558CrossRef

35.

Gibson GR, Cummings JH, Macfarlane GT (1988) Use of a three-stage continuous culture system to study the effect of mucin on dissimilatory sulfate reduction and methanogenesis by mixed populations of human gut bacteria. Appl Environ Microbiol 54:2750–2755

36.

Lajoie SF, Bank S, Miller TL, Wolin MJ (1988) Acetate production from hydrogen and [13C] carbon dioxide by the microflora of human feces. Appl Environ Microbiol 54:2723–2727

37.

Christl SU, Gibson GR, Murgatroyd PR et al (1993) Impaired hydrogen metabolism in pneumatosis cystoides intestinalis. Gastroenterology 104:392–397CrossRef

38.

Shen X, Carlstrom M, Borniquel S et al (2013) Microbial regulation of host hydrogen sulfide bioavailability and metabolism. Free Radic Biol Med 60:195–200CrossRef

39.

Watanabe K, Mikamo H, Tanaka K (2007) [Clinical significance of sulfate-reducing bacteria for ulcerative colitis]. Nihon Rinsho 65:1337–1346.

40.

Rowan FE, Docherty NG, Coffey JC, O’Connell PR (2009) Sulphate-reducing bacteria and hydrogen sulphide in the aetiology of ulcerative colitis. Br J Surg 96:151–158CrossRef

41.

Flick JA, Hamilton SR, Rosales FJ, Perman JA (1990) Methane excretion and experimental colonic carcinogenesis. Dig Dis Sci 35:221–224CrossRef

42.

Macfarlane GT, Cummings JH, Allison C (1986) Protein degradation by human intestinal bacteria. Microbiology 132:1647–1656CrossRef

43.

Gibson SA, McFarlan C, Hay S, MacFarlane GT (1989) Significance of microflora in proteolysis in the colon. Appl Environ Microbiol 55:679–683

44.

Smith EA, Macfarlane GT (1996) 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 81:288–302CrossRef

45.

Russell WR, Duncan SH, Scobbie L, Duncan G, Cantlay L, Calder AG, Anderson SE, Flint HJ (2013) Major phenylpropanoid-derived metabolites in the human gut can arise from microbial fermentation of protein. Mol Nutr Food Res 57:523–535CrossRef

46.

Davila A-M, Blachier F, Gotteland M et al (2013) Intestinal luminal nitrogen metabolism: role of the gut microbiota and consequences for the host. Pharmacol Res 68:95–107CrossRef

47.

Dai Z-L, Zhang J, Wu G, Zhu W-Y (2010) Utilization of amino acids by bacteria from the pig small intestine. Amino Acids 39:1201–1215CrossRef

48.

Dai Z-L, Li X-L, Xi P-B et al (2013) L-Glutamine regulates amino acid utilization by intestinal bacteria. Amino Acids 45:501–512CrossRef

49.

Hermanussen M, Gonder U, Jakobs C et al (2010) Patterns of free amino acids in German convenience food products: marked mismatch between label information and composition. Eur J Clin Nutr 64:88–98CrossRef

50.

Wu G, Wu Z, Dai Z et al (2013) Dietary requirements of ‘nutritionally non-essential amino acids’ by animals and humans. Amino Acids 44:1107–1113CrossRef

51.

Karau A, Grayson I (2014) Amino acids in human and animal nutrition. Adv Biochem Eng Biotechnol 143:189–228

52.

Hill MJ (1997) Intestinal flora and endogenous vitamin synthesis. Eur J Cancer Prev 6:S43–S45CrossRef

53.

Gustafsson BE, Daft FS, McDaniel EG et al (1962) Effects of vitamin K-active compounds and intestinal micro-organisms in vitamin K-deficient germfree rats. J Nutr 78:461–468CrossRef

54.

Frick PG, Riedler G, Brögli H (1967) Dose response and minimal daily requirement for vitamin K in man. J Appl Physiol 23:387–389CrossRef

55.

Le Blanc JG, Milani C, de Giori GS et al (2013) Bacteria as vitamin suppliers to their host: a gut microbiota perspective. Curr Opin Biotechnol 24:160–168CrossRef

56.

Magnúsdóttir S, Ravcheev D, de Crécy-Lagard V, Thiele I (2015) Systematic genome assessment of B-vitamin biosynthesis suggests co-operation among gut microbes. Front Genet 6:148CrossRef

57.

Said HM (2013) Recent advances in transport of water-soluble vitamins in organs of the digestive system: a focus on the colon and the pancreas. Am J Physiol Gastrointest Liver Physiol 305:G601–G610CrossRef

58.

Kandell RL, Bernstein C (1991) Bile salt/acid induction of DNA damage in bacterial and mammalian cells: implications for colon cancer. Nutr Cancer 16:227–238CrossRef

59.

Bernstein H, Payne CM, Bernstein C et al (1999) Activation of the promoters of genes associated with DNA damage, oxidative stress, ER stress and protein malfolding by the bile salt, deoxycholate. Toxicol Lett 108:37–46CrossRef

60.

Begley M, Gahan CGM, Hill C (2005) The interaction between bacteria and bile. FEMS Microbiol Rev 29:625–651CrossRef

61.

Kurdi P, Kawanishi K, Mizutani K, Yokota A (2006) Mechanism of growth inhibition by free bile acids in lactobacilli and bifidobacteria. J Bacteriol 188:1979–1986CrossRef

62.

Kellogg TF (1971) Microbiological aspects of enterohepatic neutral sterol and bile acid metabolism. In: Fed. Proceedings. Fed. Am. Soc. Exp. Biol. pp 1808–1814

63.

Jones BV, Begley M, Hill C et al (2008) Functional and comparative metagenomic analysis of bile salt hydrolase activity in the human gut microbiome. Proc Natl Acad Sci USA 105:13580–13585CrossRef

64.

Van Eldere J, Celis P, De Pauw G et al (1996) Tauroconjugation of cholic acid stimulates 7 alpha-dehydroxylation by fecal bacteria. Appl Environ Microbiol 62:656–661

65.

Ridlon JM, Kang D-J, Hylemon PB (2006) Bile salt biotransformations by human intestinal bacteria. J Lipid Res 47:241–259CrossRef

66.

Gustafsson BE, Angelin B, Einarsson K, Gustafsson JA (1977) Effects of cholesterol feeding on synthesis and metabolism of cholesterol and bile acids in germfree rats. J Lipid Res 18:717–721

67.

Mallonee DH, Hylemon PB (1996) Sequencing and expression of a gene encoding a bile acid transporter from Eubacterium sp. strain VPI 12708. J Bacteriol 178:7053–7058CrossRef

68.

Hussaini SH, Pereira SP, Murphy GM, Dowling RH (1995) Deoxycholic acid influences cholesterol solubilization and microcrystal nucleation time in gallbladder bile. Hepatology 22:1735–1744

69.

Ridlon JM, Wolf PG, Gaskins R (2016) Taurocholic acid metabolism by gut microbes and colon cancer. Gut Microbes 7:201–215CrossRef

70.

Hofmann AF (2004) Detoxification of lithocholic acid, a toxic bile acid: relevance to drug hepatotoxicity. Drug Metab Rev 36:703–722CrossRef

71.

Woollett LA, Buckley DD, Yao L et al (2003) Effect of ursodeoxycholic acid on cholesterol absorption and metabolism in humans. J Lipid Res 44:935–942CrossRef

72.

Garcia-Canaveras JC, Donato MT, Castell JV, Lahoz A (2012) Targeted profiling of circulating and hepatic bile acids in human, mouse, and rat using a UPLC-MRM-MS-validated method. J Lipid Res 53:2231–2241CrossRef

73.

Houten SM, Watanabe M, Auwerx J (2006) Endocrine functions of bile acids. EMBO J 25:1419–1425CrossRef

74.

Eloranta JJ, Kullak-Ublick GA (2008) The role of FXR in disorders of bile acid homeostasis. Physiology 23:286–295CrossRef

75.

Goodwin B, Jones SA, Price RR et al (2000) A regulatory cascade of the nuclear receptors FXR, SHP-1, and LRH-1 represses bile acid biosynthesis. Mol Cell 6:517–526CrossRef

76.

Pircher PC, Kitto JL, Petrowski ML et al (2003) Farnesoid X receptor regulates bile acid-amino acid conjugation. J Biol Chem 278:27703–27711CrossRef

77.

Song CS, Echchgadda I, Baek BS et al (2001) Dehydroepiandrosterone sulfotransferase gene induction by bile acid activated farnesoid X receptor. J Biol Chem 276:42549–42556CrossRef

78.

Hirokane H, Nakahara M, Tachibana S et al (2004) Bile acid reduces the secretion of very low density lipoprotein by repressing microsomal triglyceride transfer protein gene expression mediated by hepatocyte nuclear factor-4. J Biol Chem 279:45685–45692CrossRef

79.

Watanabe M, Houten SM, Wang L et al (2004) Bile acids lower triglyceride levels via a pathway involving FXR, SHP, and SREBP-1c. J Clin Invest 113:1408–1418CrossRef

80.

Katsuma S, Hirasawa A, Tsujimoto G (2005) Bile acids promote glucagon-like peptide-1 secretion through TGR5 in a murine enteroendocrine cell line STC-1. Biochem Biophys Res Commun 329:386–390CrossRef

81.

Stayrook KR, Bramlett KS, Savkur RS et al (2005) Regulation of carbohydrate metabolism by the farnesoid X receptor. Endocrinology 146:984–991CrossRef

82.

Watanabe M, Houten SM, Mataki C et al (2006) Bile acids induce energy expenditure by promoting intracellular thyroid hormone activation. Nature 439:484–489CrossRef

83.

Swann JR, Tuohy KM, Lindfors P et al (2011) Variation in antibiotic-induced microbial recolonization impacts on the host metabolic phenotypes of rats. J Proteome Res 10:3590–3603CrossRef

84.

Pérez-Jiménez J, Fezeu L, Touvier M et al (2011) Dietary intake of 337 polyphenols in French adults. Am J Clin Nutr 93:1220–1228CrossRef

85.

Manach C, Scalbert A, Morand C et al (2004) Polyphenols: food sources and bioavailability. Am J Clin Nutr 79:727–747CrossRef

86.

Russell WR, Scobbie L, Chesson A et al (2008) Anti-inflammatory implications of the microbial transformation of dietary phenolic compounds. Nutr Cancer 60:636–642CrossRef

87.

Duda-Chodak A, Tarko T, Satora P, Sroka P (2015) Interaction of dietary compounds, especially polyphenols, with the intestinal microbiota: a review. Eur J Nutr 54:325–341CrossRef

88.

Marín L, Miguélez EM, Villar CJ, Lombó F (2015) Bioavailability of dietary polyphenols and gut microbiota metabolism: antimicrobial properties. Biomed Res Int 2015:905215CrossRef

89.

Braune A, Engst W, Blaut M (2015) Identification and functional expression of genes encoding flavonoid O-and C-glycosidases in intestinal bacteria. Environ Microbiol 18:2117–2129CrossRef

90.

Rechner AR, Smith MA, Kuhnle G et al (2004) Colonic metabolism of dietary polyphenols: influence of structure on microbial fermentation products. Free Radic Biol Med 36:212–225CrossRef

91.

Braune A, Blaut M (2016) Bacterial species involved in the conversion of dietary flavonoids in the human gut. Gut Microbes 7:216–234CrossRef

92.

Clavel T, Henderson G, Engst W et al (2006) Phylogeny of human intestinal bacteria that activate the dietary lignan secoisolariciresinol diglucoside. FEMS Microbiol Ecol 55:471–478CrossRef

93.

Clavel T, Lippman R, Gavini F et al (2007) Clostridium saccharogumia sp. nov. and Lactonifactor longoviformis gen. nov., sp. nov., two novel human faecal bacteria involved in the conversion of the dietary phytoestrogen secoisolariciresinol diglucoside. Syst Appl Microbiol 30:16–26CrossRef

94.

Quartieri A, García-Villalba R, Amaretti A et al (2016) Detection of novel metabolites of flaxseed lignans in vitro and in vivo. Mol Nutr Food Res 60:1590–1601CrossRef

95.

Gill CIR, McDougall GJ, Glidewell S et al (2010) Profiling of phenols in human fecal water after raspberry supplementation. J Agric Food Chem 58:10389–10395CrossRef

96.

Rowland I, Faughnan M, Hoey L et al (2003) Bioavailability of phyto-oestrogens. Br J Nutr 89(Suppl 1):S45–S58

97.

Tomas-Barberan F, Garcia-Villalba R, Quartieri A et al (2014) In vitro transformation of chlorogenic acid by human gut microbiota. Mol Nutr Food Res 58:1122–1131CrossRef

98.

Decroos K, Vanhemmens S, Cattoir S et al (2005) Isolation and characterisation of an equol-producing mixed microbial culture from a human faecal sample and its activity under gastrointestinal conditions. Arch Microbiol 183:45–55CrossRef

99.

Landete JM, Arqués J, Medina M et al (2015) Bioactivation of phytoestrogens: intestinal bacteria and health. Crit Rev Food Sci Nutr 56:1826–1843CrossRef

100.

Lampe JW (2009) Is equol the key to the efficacy of soy foods? Am J Clin Nutr 89:1664S–1667SCrossRef

101.

Tomas-Barberan FA, Gonzalez-Sarrias A, Garcia-Villalba R et al. (2016) Urolithins, the rescue of ‘old’ metabolites to understand a ‘new’ concept: metabotypes as a nexus between phenolic metabolism, microbiota dysbiosis and host health status. Mol Nutr Food Res 61:1500901CrossRef

102.

Matthies A, Blaut M, Braune A (2009) Isolation of a human intestinal bacterium capable of daidzein and genistein conversion. Appl Environ Microbiol 75:1740–1744CrossRef

103.

Bastos F, Bessa J, Pacheco CC et al (2002) Enrichment of microbial cultures able to degrade 1,3-dichloro-2-propanol: a comparison between batch and continuous methods. Biodegradation 13:211–220CrossRef

104.

Ziemer CJ (2014) Newly cultured bacteria with broad diversity isolated from eight-week continuous culture enrichments of cow feces on complex polysaccharides. Appl Environ Microbiol 80:574–585CrossRef

105.

Cole CB, Fuller R, Mallet AK, Rowland IR (1985) The influence of the host on expression of intestinal microbial enzyme activities involved in metabolism of foreign compounds. J Appl Bacteriol 59:549–553CrossRef

106.

Mallett AK, Rowland IR (1990) Bacterial enzymes: their role in the formation of mutagens and carcinogens in the intestine. Dig Dis 8(2):71–79CrossRef

107.

Dabek M, McCrae SI, Stevens VJ et al (2008) Distribution of β-glucosidase and β-glucuronidase activity and of β-glucuronidase gene gus in human colonic bacteria. FEMS Microbiol Ecol 66:487–495CrossRef

108.

McIntosh FM, Maison N, Holtrop G et al (2012) Phylogenetic distribution of genes encoding β-glucuronidase activity in human colonic bacteria and the impact of diet on faecal glycosidase activities. Environ Microbiol 14:1876–1887CrossRef

109.

El Kaoutari A, Armougom F, Leroy Q et al (2013) Development and Validation of a Microarray for the Investigation of the CAZymes Encoded by the Human Gut Microbiome. PLoS One 8:e84033CrossRef

110.

Roume H, Muller EEL, Cordes T et al (2013) A biomolecular isolation framework for eco-systems biology. ISME J 7:110–121CrossRef

111.

Wang W-L, Xu S-Y, Ren Z-G et al (2015) Application of metagenomics in the human gut microbiome. World J Gastroenterol 21:803–814CrossRef

112.

Wei X, Yan X, Zou D et al (2013) Abnormal fecal microbiota community and functions in patients with hepatitis B liver cirrhosis as revealed by a metagenomic approach. BMC Gastroenterol 13:175CrossRef

113.

Mohammed A, Guda C (2015) Application of a hierarchical enzyme classification method reveals the role of gut microbiome in human metabolism. BMC Genomics 16:1CrossRef

114.

Tasse L, Bercovici J, Pizzut-Serin S et al (2010) Functional metagenomics to mine the human gut microbiome for dietary fiber catabolic enzymes. Genome Res 20:1605-1612-274CrossRef

115.

Walker AW, Duncan SH, Louis P, Flint HJ (2014) Phylogeny, culturing, and metagenomics of the approaches to unravel multi-species microbial community functioning. Comput Struct. Biotechnol J 13:24–32

116.

Abram F (2015) Systems-based approaches to unravel multi-species microbial community functioning. Comput Struct Biotechnol J 13:24–32CrossRef

117.

Turnbaugh PJ, Hamady M, Yatsunenko T et al (2009) A core gut microbiome in obese and lean twins. Nature 457:480–484CrossRef

118.

Gosalbes MJ, Durbán A, Pignatelli M et al (2011) Metatranscriptomic approach to analyze the functional human gut microbiota. PLoS One 6:e17447CrossRef

119.

Xiong W, Abraham PE, Li Z et al (2015) Microbial metaproteomics for characterizing the range of metabolic functions and activities of human gut microbiota. Proteomics 15:3424–3438CrossRef

120.

Young JC, Pan C, Adams RM et al (2015) Metaproteomics reveals functional shifts in microbial and human proteins during a preterm infant gut colonization case. Proteomics 15:3463–3473CrossRef

121.

Verberkmoes NC, Russell AL, Shah M et al (2009) Shotgun metaproteomics of the human distal gut microbiota. ISME J 3:179–189CrossRef

122.

Kolmeder CA, De Been M, Nikkilä J et al (2012) Comparative metaproteomics and diversity analysis of human intestinal microbiota testifies for its temporal stability and expression of core functions. PLoS One 7:e29913CrossRef

123.

Kolmeder CA, de Vos WM (2014) Metaproteomics of our microbiome—developing insight in function and activity in man and model systems. J Proteomics 97:3–16CrossRef

124.

Lenz EM, Wilson ID (2007) Analytical strategies in metabonomics. J Proteome Res 6:443–458CrossRef

125.

Wang Y, Liu S, Hu Y et al (2015) Current state of the art of mass spectrometry-based metabolomics studies—a review focusing on wide coverage, high throughput and easy identification. RSC Adv 5:78728–78737CrossRef

126.

Emwas A-HM (2015) The strengths and weaknesses of NMR spectroscopy and mass spectrometry with particular focus on metabolomics research. Metabonomics Methods Protoc 1277:161–193

127.

Trygg J, Holmes E, Lundstedt T (2007) Chemometrics in metabonomics. J Proteome Res 6:469–479CrossRef

128.

Madsen R, Lundstedt T, Trygg J (2010) Chemometrics in metabolomics—a review in human disease diagnosis. Anal Chim Acta 659:23–33CrossRef

129.

Alonso A, Marsal S, Julia A (2015) Analytical methods in untargeted metabolomics: state of the art in 2015. Front Bioeng Biotechnol 3:23CrossRef

130.

Marcobal A, Yusufaly T, Higginbottom S et al (2015) Metabolome progression during early gut microbial colonization of gnotobiotic mice. Sci Rep 5:11589CrossRef

131.

Kok MGM, Ruijken MMA, Swann JR et al (2013) Anionic metabolic profiling of urine from antibiotic-treated rats by capillary electrophoresis-mass spectrometry. Anal Bioanal Chem 405:2585–2594CrossRef

132.

Wikoff WR, Anfora AT, Liu J et al (2009) Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proc Natl Acad Sci USA 106:3698–3703CrossRef

133.

Wang Z, Klipfell E, Bennett BJ et al (2011) Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature 472:57–63CrossRef

134.

Tannock GW, Lawley B, Munro K et al (2014) RNA-stable-isotope probing shows utilization of carbon from inulin by specific bacterial populations in the rat large bowel. Appl Environ Microbiol 80:2240–2247CrossRef

135.

Franzosa EA, Hsu T, Sirota-Madi A et al (2015) Sequencing and beyond: integrating molecular ‘omics’ for microbial community profiling. Nat Rev Microbiol 13:360–372CrossRef

136.

Manor O, Levy R, Borenstein E (2014) Mapping the inner workings of the microbiome: genomic- and metagenomic-based study of metabolism and metabolic interactions in the human microbiome. Cell Metab 20:742–752CrossRef

137.

Muñoz-Tamayo R, Laroche B, Walter E et al (2011) Kinetic modelling of lactate utilization and butyrate production by key human colonic bacterial species. FEMS Microbiol Ecol 76:615–624CrossRef

138.

Kettle H, Donnelly R, Flint HJ, Marion G (2014) pH feedback and phenotypic diversity within bacterial functional groups of the human gut. J Theor Biol 342:62–69CrossRef

139.

Kettle H, Louis P, Holtrop G et al (2015) Modelling the emergent dynamics and major metabolites of the human colonic microbiota. Environ Microbiol 17:1615–1630CrossRef

140.

Walker AW, Ince J, Duncan SH et al (2011) Dominant and diet-responsive groups of bacteria within the human colonic microbiota. ISME J 5:220–230CrossRef

141.

Shashkova T, Popenko A, Tyakht A et al (2016) Agent based modeling of human gut microbiome interactions and perturbations. PLoS One 11:e0148386CrossRef

142.

Heinken A, Thiele I (2015) Systems biology of host-microbe metabolomics. Syst Biol Med 7:195–219

143.

Steinway SN, Biggs MB, Loughran TPJ et al (2015) Inference of network dynamics and metabolic interactions in the gut microbiome. PLoS Comput Biol 11:e1004338CrossRef

144.

Noecker C, Eng A, Srinivasan S et al (2016) Metabolic model-based integration of microbiome taxonomic and metabolomic profiles elucidates mechanistic links between ecological and metabolic variation. mSystems 1:e00013–15CrossRef

145.

Palsson BØ (2006) Systems biology: properties of reconstructed networks. Cambridge University Press, Cambridge

146.

Bordbar A, Monk JM, King ZA, Palsson BO (2014) Constraint-based models predict metabolic and associated cellular functions. Nat Rev Genet 15:107–120CrossRef

147.

Heinken A, Khan MT, Paglia G et al (2014) Functional metabolic map of Faecalibacterium prausnitzii, a beneficial human gut microbe. J Bacteriol 196:3289–3302CrossRef

148.

Bauer E, Laczny CC, Magnusdottir S et al (2015) Phenotypic differentiation of gastrointestinal microbes is reflected in their encoded metabolic repertoires. Microbiome 3:55CrossRef

149.

Heinken A, Sahoo S, Fleming RMT, Thiele I (2013) Systems-level characterization of a host-microbe metabolic symbiosis in the mammalian gut. Gut Microbes 4:28–40CrossRef

150.

Heinken A, Thiele I (2015) Systematic prediction of health-relevant human-microbial co-metabolism through a computational framework. Gut Microbes 6:120–130CrossRef

151.

Biggs MB, Medlock GL, Kolling GL, Papin JA (2015) Metabolic network modeling of microbial communities. Syst Biol Med 7:317–334

152.

Zomorrodi AR, Segre D (2016) Synthetic ecology of microbes: mathematical models and applications. J Mol Biol 428:837–861CrossRef

153.

Heinken A, Thiele I (2015) Anoxic conditions promote species-specific mutualism between gut microbes in silico. Appl Environ Microbiol 81:4049–4061CrossRef

154.

Lewis NE, Nagarajan H, Palsson BO (2012) Constraining the metabolic genotype-phenotype relationship using a phylogeny of in silico methods. Nat Rev Microbiol 10:291–305CrossRef

155.

Joyce SA, MacSharry J, Casey PG et al (2014) Regulation of host weight gain and lipid metabolism by bacterial bile acid modification in the gut. Proc Natl Acad Sci USA 111:7421–7426CrossRef

156.

Louis P, Hold GL, Flint HJ (2014) The gut microbiota, bacterial metabolites and colorectal cancer. Nat Rev Microbiol 12:661–672CrossRef

157.

Selma M V, Beltran D, Garcia-Villalba R et al (2014) Description of urolithin production capacity from ellagic acid of two human intestinal Gordonibacter species. Food Funct 5:1779–1784CrossRef

158.

Tomas-Barberan FA, Garcia-Villalba R, Gonzalez-Sarrias A et al (2014) Ellagic acid metabolism by human gut microbiota: consistent observation of three urolithin phenotypes in intervention trials, independent of food source, age, and health status. J Agric Food Chem 62:6535–6538CrossRef

159.

Couteau D, McCartney AL, Gibson GR et al (2001) Isolation and characterization of human colonic bacteria able to hydrolyse chlorogenic acid. J Appl Microbiol 90:873–881CrossRef

160.

Possemiers S, Rabot S, Espín JC et al (2008) Eubacterium limosum activates isoxanthohumol from hops (Humulus lupulus L.) into the potent phytoestrogen 8-prenylnaringenin in vitro and in rat intestine. J Nutr 138:1310–1316CrossRef

161.

Hanske L, Loh G, Sczesny S et al (2009) The bioavailability of apigenin-7-glucoside is influenced by human intestinal microbiota in rats. J Nutr 139:1095–1102CrossRef

162.

Matthies A, Loh G, Blaut M, Braune A (2012) Daidzein and genistein are converted to equol and 5-hydroxy-equol by human intestinal Slackia isoflavoniconvertens in gnotobiotic rats. J Nutr 142:40–46CrossRef

163.

Blaut M, Schoefer L, Braune A (2003) Transformation of flavonoids by intestinal microorganisms. Int J Vitam Nutr Res 73:79–87CrossRef

164.

Hanske L, Engst W, Loh G et al (2013) Contribution of gut bacteria to the metabolism of cyanidin 3-glucoside in human microbiota-associated rats. Br J Nutr 109:1433–1441CrossRef

165.

Corona G, Tzounis X, Assunta Dessi M et al (2006) The fate of olive oil polyphenols in the gastrointestinal tract: implications of gastric and colonic microflora-dependent biotransformation. Free Radic Res 40:647–658CrossRef

166.

Lockyer S, Corona G, Yaqoob P et al (2015) Secoiridoids delivered as olive leaf extract induce acute improvements in human vascular function and reduction of an inflammatory cytokine: a randomised, double-blind, placebo-controlled, cross-over trial. Br J Nutr 114:75–83CrossRef

167.

Fiorucci S (2015) Bile acids receptors regulate the integrity of gastrointestinal mucosa. LinkedIn SlideShare. http://www.slideshare.net/StefanoFiorucci/bile-acids-microbiota-and-nuclear-receptors. Slide 4. Accessed 23 Apr 2015

Title: Gut microbiota functions: metabolism of nutrients and other food components
Authors: Ian Rowland
Glenn Gibson
Almut Heinken
Karen Scott
Jonathan Swann
Ines Thiele
Kieran Tuohy
Publication date: 01-02-2018
Publisher: Springer Berlin Heidelberg
Published in: European Journal of Nutrition / Issue 1/2018
Print ISSN: 1436-6207
Electronic ISSN: 1436-6215
DOI: https://doi.org/10.1007/s00394-017-1445-8

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Gut microbiota functions: metabolism of nutrients and other food components

Abstract

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Abstract

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