Pathways and functions of gut microbiota metabolism impacting host physiology

Current Opinion in Biotechnology

Volumn 36, Issue , 2015, Pages 137-145

  Krishnan, Smitha ^a   Alden, Nicholas ^a   Lee, Kyongbum ^a  

^a Tufts University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHYSIOLOGY;

ANALYTICAL APPROACH; BACTERIAL POPULATION; BIOLOGICAL FUNCTIONS; METABOLIC ACTIVITY; METABOLIC MODELING; METABOLIC PRODUCTS; PHYSIOLOGICAL FUNCTIONS; SYNTHETIC SYSTEMS;

METABOLISM;

ACETIC ACID; ACETYL COENZYME A; AROMATIC AMINO ACID; BILE ACID; BUTYRIC ACID; CHENODEOXYCHOLIC ACID; CHOLIC ACID; CHOLINE; FARNESOID X RECEPTOR; G PROTEIN COUPLED RECEPTOR; INDOLEACETIC ACID; INDOLEAMINE 2,3 DIOXYGENASE; KYNURENINE; PROPIONIC ACID; SHORT CHAIN FATTY ACID; TRYPTAMINE; TRYPTOPHAN;

AMINO ACID METABOLISM; BACTERIAL METABOLISM; BACTEROIDES; BIFIDOBACTERIUM; BILE ACID METABOLISM; BILE ACID SYNTHESIS; CLOSTRIDIUM; ENERGY BALANCE; FATTY ACID SYNTHESIS; FIRMICUTES; HOST PATHOGEN INTERACTION; HUMAN; IMMUNE RESPONSE; INTESTINE FLORA; LACHNOSPIRACEAE; LACTOBACILLUS; METABOLOMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; ANIMAL; INTESTINE; METABOLISM; MICROBIOLOGY; MICROFLORA; PHYSIOLOGY;

AMINO ACIDS, AROMATIC; ANIMALS; BILE ACIDS AND SALTS; CHOLINE; GASTROINTESTINAL MICROBIOME; HUMANS; INTESTINES; MICROBIOTA;

EID: 84940560765     PISSN: 09581669     EISSN: 18790429     Source Type: Journal    
DOI: 10.1016/j.copbio.2015.08.015     Document Type: Review

References (50)

1. Human Microbiome Project C Structure, function and diversity of the healthy human microbiome. Nature 2012, 486:207-214.
2. Wikoff W.R., Anfora A.T., Liu J., Schultz P.G., Lesley S.A., Peters E.C., Siuzdak G. Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proc Natl Acad Sci U S A 2009, 106:3698-3703.
3. Turnbaugh P.J., Ley R.E., Mahowald M.A., Magrini V., Mardis E.R., Gordon J.I. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 2006, 444:1027-1031.
4. De Angelis M., Piccolo M., Vannini L., Siragusa S., De Giacomo A., Serrazzanetti D.I., Cristofori F., Guerzoni M.E., Gobbetti M., Francavilla R. Fecal microbiota and metabolome of children with autism and pervasive developmental disorder not otherwise specified. PLoS One 2013, 8:e76993.
5. Krajmalnik-Brown R., Lozupone C., Kang D.W., Adams J.B. Gut bacteria in children with autism spectrum disorders: challenges and promise of studying how a complex community influences a complex disease. Microb Ecol Health Dis 2015, 26:26914.
6. Hsiao E.Y., McBride S.W., Hsien S., Sharon G., Hyde E.R., McCue T., Codelli J.A., Chow J., Reisman S.E., Petrosino J.F., et al. Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell 2013, 155:1451-1463.
7. Nicholson J.K., Holmes E., Kinross J., Burcelin R., Gibson G., Jia W., Pettersson S. Host-gut microbiota metabolic interactions. Science 2012, 336:1262-1267.
8. Laparra J.M., Sanz Y. Interactions of gut microbiota with functional food components and nutraceuticals. Pharmacol Res 2010, 61:219-225.
9. Sanz Y., De Palma G. Gut microbiota and probiotics in modulation of epithelium and gut-associated lymphoid tissue function. Int Rev Immunol 2009, 28:397-413.
10. Vogt S.L., Pena-Diaz J., Finlay B.B. Chemical communication in the gut: effects of microbiota-generated metabolites on gastrointestinal bacterial pathogens. Anaerobe 2015, 34:106-115.
11. Segata N., Boernigen D., Tickle T.L., Morgan X.C., Garrett W.S., Huttenhower C. Computational meta'omics for microbial community studies. Mol Syst Biol 2013, 9:666.
12. Qin J., Li R., Raes J., Arumugam M., Burgdorf K.S., Manichanh C., Nielsen T., Pons N., Levenez F., Yamada T., et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 2010, 464:59-65.
13. Li J., Jia H., Cai X., Zhong H., Feng Q., Sunagawa S., Arumugam M., Kultima J.R., Prifti E., Nielsen T., et al. An integrated catalog of reference genes in the human gut microbiome. Nat Biotechnol 2014, 32:834-841.
14. Turnbaugh P.J., Ridaura V.K., Faith J.J., Rey F.E., Knight R., Gordon J.I. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med 2009, 1. 6ra14.
15. Druart C., Bindels L.B., Schmaltz R., Neyrinck A.M., Cani P.D., Walter J., Ramer-Tait A.E., Delzenne N.M. Ability of the gut microbiota to produce PUFA-derived bacterial metabolites: proof of concept in germ-free versus conventionalized mice. Mol Nutr Food Res 2015, 59:1603-1613.
16. van Duynhoven J., Vaughan E.E., Jacobs D.M., Kemperman R.A., van Velzen E.J., Gross G., Roger L.C., Possemiers S., Smilde A.K., Doré J., et al. Metabolic fate of polyphenols in the human superorganism. Proc Natl Acad Sci U S A 2011, 108:4531-4538.
17. Macfarlane G.T., Macfarlane S. Fermentation in the human large intestine: its physiologic consequences and the potential contribution of prebiotics. J Clin Gastroenterol 2011, 45:S120-S127.
18. De Preter V., Machiels K., Joossens M., Arijs I., Matthys C., Vermeire S., Rutgeerts P., Verbeke K. Faecal metabolite profiling identifies medium-chain fatty acids as discriminating compounds in IBD. Gut 2015, 64:447-458.
19. Reichardt N., Duncan S.H., Young P., Belenguer A., McWilliam Leitch C., Scott K.P., Flint H.J., Louis P. Phylogenetic distribution of three pathways for propionate production within the human gut microbiota. ISME J 2014, 8:1323-1335.
20. Vital M., Howe A.C., Tiedje J.M. Revealing the bacterial butyrate synthesis pathways by analyzing (meta)genomic data. MBio 2014, 5:e00889.
21. Samuel B.S., Shaito A., Motoike T., Rey F.E., Backhed F., Manchester J.K., Hammer R.E., Williams S.C., Crowley J., Yanagisawa M., et al. 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.
22. Kim M.H., Kang S.G., Park J.H., Yanagisawa M., Kim C.H. Short-chain fatty acids activate GPR41 and GPR43 on intestinal epithelial cells to promote inflammatory responses in mice. Gastroenterology 2013, 145:396-406. e1-10.
23. Nguyen N.T., Kimura A., Nakahama T., Chinen I., Masuda K., Nohara K., Fujii-Kuriyama Y., Kishimoto T. Aryl hydrocarbon receptor negatively regulates dendritic cell immunogenicity via a kynurenine-dependent mechanism. Proc Natl Acad Sci U S A 2010, 107:19961-19966.
24. Zelante T., Iannitti R.G., Cunha C., De Luca A., Giovannini G., Pieraccini G., Zecchi R., D'Angelo C., Massi-Benedetti C., Fallarino F., et al. Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22. Immunity 2013, 39:372-385.
25. Sridharan G.V., Choi K., Klemashevich C., Wu C., Prabakaran D., Pan L.B., Steinmeyer S., Mueller C., Yousofshahi M., Alaniz R.C., et al. Prediction and quantification of bioactive microbiota metabolites in the mouse gut. Nat Commun 2014, 5:5492.
26. Cheng Y., Jin U.H., Allred C.D., Jayraman A., Chapkin R.S., Safe S. Aryl hydrocarbon receptor activity of tryptophan metabolites in young adult mouse colonocytes. Drug Metab Dispos 2015.
27. Bansal T., Alaniz R.C., Wood T.K., Jayaraman A. The bacterial signal indole increases epithelial-cell tight-junction resistance and attenuates indicators of inflammation. Proc Natl Acad Sci U S A 2010, 107:228-233.
28. Yano J.M., Yu K., Donaldson G.P., Shastri G.G., Ann P., Ma L., Nagler C.R., Ismagilov R.F., Mazmanian S.K., Hsiao E.Y. Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis. Cell 2015, 161:264-276.
29. Asano Y., Hiramoto T., Nishino R., Aiba Y., Kimura T., Yoshihara K., Koga Y., Sudo N. Critical role of gut microbiota in the production of biologically active, free catecholamines in the gut lumen of mice. Am J Physiol Gastrointest Liver Physiol 2012, 303:G1288-G1295.
30. Ridlon J.M., Hylemon P.B. Identification and characterization of two bile acid coenzyme A transferases from Clostridium scindens, a bile acid 7alpha-dehydroxylating intestinal bacterium. J Lipid Res 2012, 53:66-76.
31. Jones B.V., Begley M., Hill C., Gahan C.G., Marchesi J.R. Functional and comparative metagenomic analysis of bile salt hydrolase activity in the human gut microbiome. Proc Natl Acad Sci U S A 2008, 105:13580-13585.
32. Sayin S.I., Wahlstrom A., Felin J., Jantti S., Marschall H.U., Bamberg K., Angelin B., Hyotylainen T., Oresic M., Backhed F. Gut microbiota regulates bile acid metabolism by reducing the levels of tauro-beta-muricholic acid, a naturally occurring FXR antagonist. Cell Metab 2013, 17:225-235.
33. Chiang J.Y. Bile acids: regulation of synthesis. J Lipid Res 2009, 50:1955-1960.
34. Li F., Jiang C., Krausz K.W., Li Y., Albert I., Hao H., Fabre K.M., Mitchell J.B., Patterson A.D., Gonzalez F.J. Microbiome remodelling leads to inhibition of intestinal farnesoid X receptor signalling and decreased obesity. Nat Commun 2013, 4:2384.
35. Joyce S.A., MacSharry J., Casey P.G., Kinsella M., Murphy E.F., Shanahan F., Hill C., Gahan C.G. Regulation of host weight gain and lipid metabolism by bacterial bile acid modification in the gut. Proc Natl Acad Sci U S A 2014, 111:7421-7426.
36. Buffie C.G., Bucci V., Stein R.R., McKenney P.T., Ling L., Gobourne A., No D., Liu H., Kinnebrew M., Viale A., et al. Precision microbiome reconstitution restores bile acid mediated resistance to Clostridium difficile. Nature 2015, 517:205-208.
37. Martinez-del Campo A., Bodea S., Hamer H.A., Marks J.A., Haiser H.J., Turnbaugh P.J., Balskus E.P. Characterization and detection of a widely distributed gene cluster that predicts anaerobic choline utilization by human gut bacteria. MBio 2015, 6.
38. Reikvam D.H., Erofeev A., Sandvik A., Grcic V., Jahnsen F.L., Gaustad P., McCoy K.D., Macpherson A.J., Meza-Zepeda L.A., Johansen F.E. Depletion of murine intestinal microbiota: effects on gut mucosa and epithelial gene expression. PLoS One 2011, 6:e17996.
39. Goodman A.L., Kallstrom G., Faith J.J., Reyes A., Moore A., Dantas G., Gordon J.I. Extensive personal human gut microbiota culture collections characterized and manipulated in gnotobiotic mice. Proc Natl Acad Sci U S A 2011, 108:6252-6257.
40. Ridaura V.K., Faith J.J., Rey F.E., Cheng J., Duncan A.E., Kau A.L., Griffin N.W., Lombard V., Henrissat B., Bain J.R., et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 2013, 341:1241214.
41. Stearns J.C., Lynch M.D., Senadheera D.B., Tenenbaum H.C., Goldberg M.B., Cvitkovitch D.G., Croitoru K., Moreno-Hagelsieb G., Neufeld J.D. Bacterial biogeography of the human digestive tract. Sci Rep 2011, 1:170.
42. Feria-Gervasio D., Tottey W., Gaci N., Alric M., Cardot J.M., Peyret P., Martin J.F., Pujos E., Sebedio J.L., Brugere J.F. Three-stage continuous culture system with a self-generated anaerobia to study the regionalized metabolism of the human gut microbiota. J Microbiol Methods 2014, 96:111-118.
43. Marcobal A., Kashyap P.C., Nelson T.A., Aronov P.A., Donia M.S., Spormann A., Fischbach M.A., Sonnenburg J.L. A metabolomic view of how the human gut microbiota impacts the host metabolome using humanized and gnotobiotic mice. ISME J 2013, 7:1933-1943.
44. Fischbach M.A., Sonnenburg J.L. Eating for two: how metabolism establishes interspecies interactions in the gut. Cell Host Microbe 2011, 10:336-347.
45. Magnusdottir S., Ravcheev D., de Crecy-Lagard V., Thiele I. Systematic genome assessment of B-vitamin biosynthesis suggests co-operation among gut microbes. Front Genet 2015, 6:148.
46. Heinken A., Sahoo S., Fleming R.M., Thiele I. Systems-level characterization of a host-microbe metabolic symbiosis in the mammalian gut. Gut Microbes 2013, 4:28-40.
47. Shoaie S., Karlsson F., Mardinoglu A., Nookaew I., Bordel S., Nielsen J. Understanding the interactions between bacteria in the human gut through metabolic modeling. Sci Rep 2013, 3:2532.
48. Jiao D., Ye Y., Tang H. Probabilistic inference of biochemical reactions in microbial communities from metagenomic sequences. PLoS Comput Biol 2013, 9:e1002981.
49. Greenblum S., Turnbaugh P.J., Borenstein E. 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 2012, 109:594-599.
50. Donia M.S., Cimermancic P., Schulze C.J., Wieland Brown L.C., Martin J., Mitreva M., Clardy J., Linington R.G., Fischbach M.A. A systematic analysis of biosynthetic gene clusters in the human microbiome reveals a common family of antibiotics. Cell 2014, 158:1402-1414.