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Protein & Cell

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ISSN 1674-8018(Online)

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Prot Cell    2013, Vol. 4 Issue (6) : 403-414    https://doi.org/10.1007/s13238-013-3017-x      PMID: 23686721
REVIEW
The role of gut microbiota in the gut-brain axis: current challenges and perspectives
Xiao Chen1, Roshan D’Souza2, Seong-Tshool Hong1()
1. BDRD Research Institute, JINIS Biopharmaceuticals Inc, 948-9 Dunsan, Bongdong, Wanju, Chonbuk 565-902, South Korea; 2. Department of Microbiology and Genetics and Institute for Medical Science, Chonbuk National University Medical School, Jeonju 561-712, South Korea
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Abstract

Brain and the gastrointestinal (GI) tract are intimately connected to form a bidirectional neurohumoral communication system. The communication between gut and brain, knows as the gut-brain axis, is so well established that the functional status of gut is always related to the condition of brain. The researches on the gut-brain axis were traditionally focused on the psychological status affecting the function of the GI tract. However, recent evidences showed that gut microbiota communicates with the brain via the gut-brain axis to modulate brain development and behavioral phenotypes. These recent fi ndings on the new role of gut microbiota in the gut-brain axis implicate that gut microbiota could associate with brain functions as well as neurological diseases via the gut-brain axis. To elucidate the role of gut microbiota in the gut-brain axis, precise identification of the composition of microbes constituting gut microbiota is an essential step. However, identifi cation of microbes constituting gut microbiota has been the main technological challenge currently due to massive amount of intestinal microbes and the diffi culties in culture of gut microbes. Current methods for identifi cation of microbes constituting gut microbiota are dependent on omics analysis methods by using advanced high tech equipment. Here, we review the association of gut microbiota with the gut-brain axis, including the pros and cons of the current high throughput methods for identifi cation of microbes constituting gut microbiota to elucidate the role of gut microbiota in the gut-brain axis.

Keywords gut microbiota      the gut-brain axis      central nervous system      high throughput methods      next-generation sequencings     
Corresponding Author(s): Hong Seong-Tshool,Email:seonghong@chonbuk.ac.kr   
Issue Date: 01 June 2013
 Cite this article:   
Xiao Chen,Roshan D’Souza,Seong-Tshool Hong. The role of gut microbiota in the gut-brain axis: current challenges and perspectives[J]. Prot Cell, 2013, 4(6): 403-414.
 URL:  
https://academic.hep.com.cn/pac/EN/10.1007/s13238-013-3017-x
https://academic.hep.com.cn/pac/EN/Y2013/V4/I6/403
1 Albesharat, R., Ehrmann, M.A., Korakli, M., Yazaji, S., and Vogel, R.F. (2011). Phenotypic and genotypic analyses of lactic acid bacteria in local fermented food, breast milk and feces of mothers and their babies. Syst Appl Microbiol 34, 148-155
doi: 10.1016/j.syapm.2010.12.001
2 Andrew, J.W. (2002). The gut-brain axis in childhood developmental disorders. J Pediatr Gastroenterol Nutr 34, S14-17
doi: 10.1097/00005176-200205001-00004
3 Angelakis, E., Million, M., Henry, M., and Raoult, D. (2011). Rapid and accurate bacterial identification in probiotics and yoghurts by MALDI-TOF mass spectrometry. J Food Sci 76, M568-572
doi: 10.1111/j.1750-3841.2011.02369.x
4 Anhalt, J.P., and Fenselau, C. (1975). Identification of bacteria using mass spectrometry. Anal Chem 47, 219-225
doi: 10.1021/ac60352a007
5 Barbara, G., Brummer, R.J., and Delzenne, N. (2007). Investigating the crosstalk between the gut microbiota and the host: the gut-brain axis. Consensus Report . Warsaw.
6 Ben, X.M, and Li, J. (2008). Low level of galacto-oligosaccharide in infant formula stimulates growth of intestinal Bifidobacteria and Lactobacilli. World J Gastroenterol 14, 6564-6568
doi: 10.3748/wjg.14.6564
7 Beraza, N., and Trautwein, C. (2008). The Gut-Brain-Liver Axis: A New Option to Treat Obesity and Diabetes? Hepatology 48, 1011-1013 .
doi: 10.1002/hep.22478
8 Bercik, P., Collins, S.M., and Verdu, E.F. (2012). Microbes and the gutbrain axis. Neurogastroenterol Motil 224, 405-413
doi: 10.1111/j.1365-2982.2012.01906.x
9 Bercik, P., Denou, E., Collins, J., Jackson, W., Lu, J., Jury, J., Deng, Y., Blennerhassett, P., Macri, J., McCoy, K.D., . (2011). The Intestinal Microbiota Affect Central Levels of Brain-Derived Neurotropic Factor and Behavior in Mice. Gastroenterology 141, 599-609
doi: 10.1053/j.gastro.2011.04.052
10 Bishop, R. (2010). Applications of fluorescence in situ hybridization(FISH) in detecting genetic aberrations of medical significance. Biosci Horizons 3, 95-85
11 Blaut, M., Collins, M.D., Welling, G.W., Doré, J., van, L.J., and de Vos, W. (2004). Molecular methods for the analysis of gut microbiota. Microbial Ecology Health Disease 16, 71-85
doi: 10.1080/08910600410032367
12 Bocci, V. (1992). The neglected organ: bacterial fiora has a crucial immunostimulatory role. Perspect Biol Med 35, 251-260
13 Brian, W. P., Elizabeth, N., Elin, O., Emrah, K., Frode, N., Simon, T.H., Calvin, P., Mete, C., Christoph, D.R., Brian, J.B., . (2013). Genetic control of obesity and gut microbiota composition in response to high-fat, high-sucrose diet in mice. Cell Metab 17, 141-152
doi: 10.1016/j.cmet.2012.12.007
14 Burcelin, R., Serino, M., Chabo, C., Blasco-Baque, V., and Amar, J. (2011). Gut microbiota and diabetes: from pathogenesis to therapeutic perspective. Acta Diabetol 4, 257-273
doi: 10.1007/s00592-011-0333-6
15 Cattell, M., Lai, S., Cerny, R., and Medeiros, D.M. (2011). A new mechanistic scenario for the origin and evolution of vertebrate cartilage. PLoS ONE 6, e22474.
doi: 10.1371/journal.pone.0022474
16 Cecilia, J., and Sonja, L. (2010). Long-term impacts of antibiotic exposure on the human intestinal microbiota. Microbiology 156, 113216-3223
17 Chong, B.E., Wall, D.B., Lubman, D.M., and Flynn, S.J. (1997). Rapid profiling of E. coli proteins up to 500 kDa from whole cell lysates using matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Rapid Commun Mass Spectrom 11, 1900-1908
doi: 10.1002/(SICI)1097-0231(199711)11:17<1900::AID-RCM95>3.0.CO;2-K
18 Claesson, M.J., O’ Sullivan, O., Wang, Q., Nikkil?, J., Marchesi, J.R., Smidt, H., De Vos, W.M., Ross R .P.,and O’Toole, P.W. (2009). Comparative analysis of Pyrosequencing and a phylogenetic mi-croarray for exploring microbial community structures in the human distal intestine. PLoS One 4, e6669.
doi: 10.1371/journal.pone.0006669
19 Claesson, M.J., Wang, Q., O’Sullivan, O., Greene-Diniz, R., Cole, J.R., Ross, R.P., and O’Toole, P.W. (2010). Comparison of two nextgeneration sequencing technologies for resolving highly complex microbiota composition using tandem variable 16S rRNA gene re-gions. Nucleic Acids Res 38, e200.
doi: 10.1093/nar/gkq873
20 Claydon, M.A., Davey, S.N., Edwards, J.V., and Gordon, D.B. (1996). The rapid identification of intact microorganisms using mass spec-trometry. Nat Biotechnol 14, 1584-1586 .
doi: 10.1038/nbt1196-1584
21 Collado, M.C., Isolauri, E., Laitinen, K., and Salminen, S. (2008). Dis-tinct composition of gut microbiota during pregnancy in overweight and normal-weight women. Am J Clin Nutr 88, 894-899
22 Collins, S.M., Surette, M., and Bercik, P. (2012). The interplay between the intestinal microbiota and the brain. Nat Rev Microbiol 10, 735-742 .
doi: 10.1038/nrmicro2876
23 Cryan, J.F., and Dinan, T.G. (2012). Mind-altering microorganisms: the impact of the gut microbiota on brain and behavior. Nat Rev Neuro-sci 13, 701-712
doi: 10.1038/nrn3346
24 Cryan, J.F., and O’Mahony, S.M., (2011). The microbiome-gut-brain axis: from bowel to behavior. Neurogastroenterol Motil 23, 187-192 .
doi: 10.1111/j.1365-2982.2010.01664.x
25 Desbonnet, L., Garrett, L., Clarke, G., Bienenstock, J., and Dinan, T.G. (2008). The probiotic Bifidobacteria infantis: An assessment of potential antidepressant properties in the rat. J Psychiatr Res 43, 164-174
doi: 10.1016/j.jpsychires.2008.03.009
26 Dethlefsen, L., Sue, H., Mitchell, L.S., and Relman, D.A. (2008). The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol 6, e280.
doi: 10.1371/journal.pbio.0060280
27 Dumont, M.G., Neufeld, J.D., and Murrell, J.C. (2006). Isotopes as tools for microbial ecologists. Curr Opin Biotech 17, 57-58
doi: 10.1016/j.copbio.2006.01.004
28 Eckburg, P.B., Elisabeth, M.B., Charles, N.B., Elizabeth, P., Dethlefsen, L., Sargent, M., Gill, R.S., Nelson, K.E., and Relman, D.A. (2005). Diversity of the human intestinal microbial flora. Science 308, 1635-1638
doi: 10.1126/science.1110591
29 Zhang, S. M., Tian, F., Huang,Q. F., Zhao, Y.F., Guo, X.K. and Zhang, F. Q. (2011). Bacterial diversity of subgingival plaque in 6 healthy Chinese individuals. Exp Ther Med 2, 1023-1029
30 Finegold, S.M., Molitoris, D., Song, Y., Liu, C., Vaisanen, M.L., Bolte, E., McTeague, M., Sandler, R., Wexler, H., Marlowe, E.M., . (2002). Gastrointestinal microfiora studies in late-onset autism. Clin Infect Dis 35, S6-16 .
doi: 10.1086/341914
31 Fredrik, B., Ruth, E.L., Justin, L.S., Daniel, A.P., and Jeffrey, I.G. (2005). Host-bacterial mutualism in the human intestine. Science 307, 1915-1920
doi: 10.1126/science.1104816
32 Gill, S.R., Pop, M., DeBoy, R.T., Eckburg, P.B., Turnbaugh, P.J., Sam-uel, B.S., Gordon, J.I, Relman, D.A., Fraser-Liggett, C.M., and Ka-ren, E. (2006). Nelson metagenomic analysis of the human distal gut microbiome. Science 312, 1355-1359
doi: 10.1126/science.1124234
33 Greenblum, S., Turnbaugh, P.J., and Borenstein, E. (2012). Metagen-omic systems biology of the human gut microbiome reveals topological shifts associated with obesity and infiammatory bowel disease. Proc Natl Acad Sci U S A 109, 594-599
doi: 10.1073/pnas.1116053109
34 Greiner, T., Bfickhed, F. (2011). Effects of the gut microbiota on obesity and glucose homeostasis. Trends Endocrinol Metab 22, 117-123
doi: 10.1016/j.tem.2011.01.002
35 Hamady, M., Walker, J.J., Harris, J.K., Gold, N.J., and Knight, R. (2008). Error correcting barcoded primers for pyrosequencing hundreds of samples in multiplex. Nat Methods 5, 235-237
doi: 10.1038/nmeth.1184
36 He, Z., Gentry, T.J., Schadt, C.W., Wu, L., Liebich, J., Chong, S.C., Huang, Z., Wu, W., Gu, B., Jardine, P., . (2007). GeoChip: a comprehensive microarray for investigating biogeochemical, eco-logical and environmental processes. ISME J 1, 67-77
doi: 10.1038/ismej.2007.2
37 Heijtz, R.D., Wang, S., Anuar, F., Qian, Y., Bj?rkholm, B., Samuelsson, A., Hibberd, M.L., Forssberg, H., and Pettersson, S. (2011). Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci U S A 108, 3047-3052
doi: 10.1073/pnas.1010529108
38 Hernandez-Sanabria, E., Guan, L.L., Laksiri, A., Li, M., Mujibi, D.F., Stothard, P., Moore, S.S., and Leon-Quintero, M.C. (2010). Cor-relation of particular bacterial PCR-denaturing gradient gel electro-phoresis patterns with bovine ruminal fermentation parameters and feed efficiency traits. App Envior Biol 76, 6338-6350
doi: 10.1128/AEM.01052-10
39 Holland, R.D., Wilkes, J.G., Rafii, F., Sutherland, J.B., Persons, C.C., Voorhees, K.J., and Lay J .O. Jr. (1996). Rapid identification of intact whole bacteria based on spectral patterns using matrix-assisted laser desorption/ionization with time-of-flight mass spectrometry. Rapid Commun Mass Spectrom 10, 1227-1232
doi: 10.1002/(SICI)1097-0231(19960731)10:10<1227::AID-RCM659>3.0.CO;2-6
40 Hopkins, M.J., and Sharp, R. (2001). Age and disease related changes in intestinal bacterial populations assessed by cell culture, 16S rRNA abundance, and community cellular fatty acid profiles. Gut 48, 198-205
doi: 10.1136/gut.48.2.198
41 Huang, W.E., Stoecker, K., Griffiths, R., Newbold, L., Daims, H., White-ley, A.S., and Wagner, M. (2007). Raman-fish: Combining stable-isotope Raman spectroscopy and fiuorescence in situ hybridization for the single cell analysis of identity and function. Environ Microbiol 9, 1878-1889
doi: 10.1111/j.1462-2920.2007.01352.x
42 Jock, S., and Geider, K. (2004). Molecular differentiation of Erwinia amylovora strains from North America and of two Asian pear patho-gens by analyses of PFGE patterns and hrpN genes. Environ Mi-crobiol 6, 480-490
doi: 10.1111/j.1462-2920.2004.00583.x
43 Kim, P.I., Erickson, B.D., and Cerniglia, C.E. (2005). A membrane-array method to detect specific human intestinal bacteria in fecal samples using reverse transcriptase-PCR and chemiluminescence. J Microbiol Biotechnol 15, 310-320
44 Krishnamurthy, T., and Ross, P.L. (1996). Rapid identification of bacte-ria by direct matrix-assisted laser desorption/ionization mass spec-trometric analysis of whole cells. Rapid Commun Mass Spectrom 10, 1992-1996
doi: 10.1002/(SICI)1097-0231(199612)10:15<1992::AID-RCM789>3.0.CO;2-V
45 Kurz, C.M., Moosdijk, S.V., Thielecke, H., and Velten, T. (2011). To-wards a cellular multi-parameter analysis platform: fluorescence in situ hybridization (FISH) on microhole-array chips. Conf Proc IEEE Eng Med Biol Soc , 8408-8411
46 Kuypers, M.M.M., and J?rgensen, B.B. (2007). The future of single-cell environmental microbiology. Environ Microbiol 9, 6-7
doi: 10.1111/j.1462-2920.2006.01222_5.x
47 Lagier, J.C., Million, M., Hugon, P., Armougom, F., and Raoult, D. (2012). Human Gut Microbiota: Repertoire and Variations. Front Cell Infect Microbiol 2, 136.
doi: 10.3389/fcimb.2012.00136
48 Lewis, S., and Cochrane, S. (2007). Alteration of sulfate and hydrogen metabolism in the human colon by changing intestinal transit rate. Am J Gastroenterol 102, 624-633
doi: 10.1111/j.1572-0241.2006.01020.x
49 Lotta, N., Reetta, S., and Janne, N. (2013). Microarray analysis reveals marked intestinal microbiota aberrancy in infants having eczema compared to healthy children in at-risk for atopic disease. BMC Mi-crobiology 13, 12.
doi: 10.1186/1471-2180-13-12
50 Loy, A., Lehner, A., and Lee, N. (2002). Oligonucleotide microarray for 16S rRNA gene-based detection of all recognized lineages of sulfate-reducing prokaryotes in the environment. Appl Environ Mi-crobiol 68, 5064-5081
doi: 10.1128/AEM.68.10.5064-5081.2002
51 Manco, M. (2012). Gut microbiota and developmental programming of the brain: from evidence in behavioral endophenotypes to novel perspective in obesity. Front Cell Inf Microbio 2, 109.
doi: 10.3389/fcimb.2012.00109
52 Migrenne, S., Marsollier, N., Cruciani-Guglielmacci, C., Magnan, C. (2006). Importance of the gut-brain axis in the control of glucose Homeostasis. Curr Opin Pharmacol 6, 592-597 .
doi: 10.1016/j.coph.2006.08.004
53 Musso, G., Gambino, M., and Cassader, M. (2010). Obesity, diabetes, and gut microbiota. Diabetes Care 33, 2277-2284
doi: 10.2337/dc10-0556
54 Neufeld, K.M., Kang, N., Bienenstock, J., and Foster, J.A. (2011). Re-duced anxiety-like behavior and central neurochemical change in germ-free mice. Neurogastroenterol Motil 23, 255-264
doi: 10.1111/j.1365-2982.2010.01620.x
55 Nordlie, R.C., and Foster, J.D. (1999). Regulation of glucose produc-tion by the liver. Annu Rev Nutr 19, 379-406
doi: 10.1146/annurev.nutr.19.1.379
56 Paliy, O., Kenche, H., Abernathy, F., and Michail, S. (2009). High-throughput quantitative analysis of the human intestinal microbiota with a phylogenetic microarray. Appl Environ Microbiol 75, 3572-3579 .
doi: 10.1128/AEM.02764-08
57 Palmer, C., Bik, E.M., and DiGiulio, D.B. (2007). Development of the human infant intestinal microbiota. PLoS Biol 5, e177.
doi: 10.1371/journal.pbio.0050177
58 Palmer, C., Bik, E.M., and Eisen, M.B. (2006). Rapid quantitative profil-ing of complex microbial populations. Nucleic Acids Res 34, e5.
doi: 10.1093/nar/gnj007
59 Peterson, D.A., Frank, D.N., Pace, N.R., and Gordon, J.I. (2008). Metagenomic approaches for defining the pathogenesis of inflam-matory bowel diseases. Cell Host Microbe 3, 417-427
doi: 10.1016/j.chom.2008.05.001
60 Rakoff, N.S., Paglino, J., Eslami, V.F., Edberg, S., and Medzhitov, R. (2004). Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118, 229-241
doi: 10.1016/j.cell.2004.07.002
61 Sam, A.H., Troke, R.C., Tan, T.M., and Bewick, G.A. (2012). The role of the gut/brain axis in modulating food intake. Neuropharmacology 63, 46-56 .
doi: 10.1016/j.neuropharm.2011.10.008
62 Savage, D.C. (1977). Microbial ecology of the gastrointestinal tract. Annu Rev Microbiol 31, 107-133
doi: 10.1146/annurev.mi.31.100177.000543
63 Shanahan, F. (2002). The host-microbe interface within the gut. Best Pract Res Clin Gastroenterol 16, 915-931 .
doi: 10.1053/bega.2002.0342
64 Sintchenko, V., Iredell, J.R., and Gilbert, G.L. (2007). Pathogen profil-ing for disease management and surveillance. Nat Rev Microbiol 5, 464-470
doi: 10.1038/nrmicro1656
65 Sogin, L.M., Morrison, H.G., Huber, J.A., Welch, D.M., Huse, S.M., Neal, P.R., Arrieta, J.M., and Herndl, J.G. (2006). Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc NatAcad Sci U S A 103, 12115-12120
doi: 10.1073/pnas.0605127103
66 Stappenbeck, T.S., Hooper, L.V., and Gordon, J.I. (2001). Commensal host-bacterial relationships in the gut. Science 292, 1115-1118 .
doi: 10.1126/science.1058709
67 Stappenbeck, T.S., Hooper, L.V., and Gordon, J.I. (2002). Develop-mental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proc Natl Acad Sci U S A 99, 15451-15455
doi: 10.1073/pnas.202604299
68 Sudo, N., Chida, Y., Aiba, Y., Sonoda, J., Oyama, N., Yu, X.N., Kubo, C., and Koga, Y. (2004). Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J Physiol 558, 263-275 .
doi: 10.1113/jphysiol.2004.063388
69 Turnbaugh, P.J., Hamady, M., Yatsunenko, T., Cantarel, B.L., Duncan, A., Ley, R.E., Sogin, M.L., Jones, W.J., Roe, B.A., Affourtit, J.P., . (2008). A core gut microbiome in obese and lean twins. Nature 457, 480-484
doi: 10.1038/nature07540
70 Turnbull, A.V., and Rivier, C.L. (1999). Regulation of the hypothalamic-pituitary-adrenal axis by cytokines: actions and mechanisms of ac-tion. Physiol rev 79, 1-71 .
71 Walker, J.R., Ediger, J.P., Graff, L.A., Greenfeld, J.M., Clara, I., Lix, L., Rawsthorne, P., Miller, N., Rogala, L., McPhail, C.M., and Bern-stein, C.N. (2008). The Manitoba IBD cohort study: a population-based study of the prevalence of lifetime and 12-month anxiety and mood disorders. Am J Gastroenterol 103, 1989-1997
doi: 10.1111/j.1572-0241.2008.01980.x
72 Wang, P.Y., Caspi, L., Lam, C.K., Chari, M., Li, X., Light, P.E., Gutier-rez-Juarez, R., Ang, M., Schwartz, G.J., and Lam, T.K. (2008). Up-per intestinal lipids trigger a gut-brain-liver axis to regulate glucose production. Nature 452, 1012-1016
doi: 10.1038/nature06852
73 Welker, M. (2012). MALDI-TOF MS for identification of microorgan-isms: a new era in clinical microbiological research and diagnosis. In: Hays, J.P., van Leeuwen, W.B. (Eds.), The Role of New Tech-nologies in Medical Microbiological Research and Diagnosis, Ben-tham Science Publishers, Bussum .
74 Whitehead, W.E., Palsson, O., and Jones, K.R. (2002). Systematic re-view of the comorbidity of irritable bowel syndrome with other disor-ders: what are the causes and implications. Gastroenterology 122, 1140-1156
doi: 10.1053/gast.2002.32392
75 Wook, H.S., Kim, I.S., Lee, J.S., and Chung, K.S. (2011). Culture-Based and Denaturing Gradient Gel Electrophoresis Analysis of the Bacterial Community Structure from the Intestinal Tracts of Earth-worms (Eisenia fetida). J Microbiol Biotechnol 21, 885-892
doi: 10.4014/jmb.1009.09041
76 Wu, L., Thompson, D.K., Liu, X., Fields, M.W., Bagwell, C.E., Tiedje, J.M., and Zhou, J. (2004). Development and evaluation of microar-ray-based whole genome hybridization for detection of microorgan-isms within the context of environmental applications. Environ Sci Technol 38, 6775-6782
doi: 10.1021/es049508i
77 Zhang, H., DiBaise, J.K, Zuccolo, A., Kudrna, D., Braidotti, M., Yu, Y., Parameswaran, P., Crowell, M.D., Wing, R., and Rittmann, B.E. (2009). Human gut microbiota in obesity and after gastric bypass. Proc Natl Acad Sci U S A 106, 2365-2370
doi: 10.1073/pnas.0812600106
78 Zimmer, C. (2010). How microbes defend and define us. New York Times . 17 July.
79 Simrén, M., Barbara, G., Flint, H.J., Spiegel, B.M., Spiller, R.C., Vanner, S., Verdu, E.F., Whorwell, P. J., and Zoetendal, E. G. (2013). Intestinal microbiota in functional bowel disorders: a Rome founda-tion report. Gut 62, 159-176
doi: 10.1136/gutjnl-2012-302167
80 Sekirov, I., Russell, S. L., Antunes, L. C. M., and Brett Finlay, B. (2010). Gut Microbiota in Health and Disease. Physiol Rev 90, 859-904
doi: 10.1152/physrev.00045.2009
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