The Controversial Role of Human Gut Lachnospiraceae

Mirco Vacca, Giuseppe Celano, Francesco Maria Calabrese, Piero Portincasa, Marco Gobbetti, Maria De Angelis, Mirco Vacca, Giuseppe Celano, Francesco Maria Calabrese, Piero Portincasa, Marco Gobbetti, Maria De Angelis

Abstract

The complex polymicrobial composition of human gut microbiota plays a key role in health and disease. Lachnospiraceae belong to the core of gut microbiota, colonizing the intestinal lumen from birth and increasing, in terms of species richness and their relative abundances during the host's life. Although, members of Lachnospiraceae are among the main producers of short-chain fatty acids, different taxa of Lachnospiraceae are also associated with different intra- and extraintestinal diseases. Their impact on the host physiology is often inconsistent across different studies. Here, we discuss changes in Lachnospiraceae abundances according to health and disease. With the aim of harnessing Lachnospiraceae to promote human health, we also analyze how nutrients from the host diet can influence their growth and how their metabolites can, in turn, influence host physiology.

Keywords: Lachnospiraceae; disease; gut microbial metabolites; gut microbial pathways; gut microbiota; health.

Conflict of interest statement

The authors declare no conflicts of interest.

Figures

Figure 1
Figure 1
Phylogeny of taxa belonging to the Lachnospiraceae family. Sequences have been retrieved from the RefSeq Targeted Loci Project included in the National Center for Biotechnology Information (NCBI) database using the following combined search: txid186803[ORGN] AND (33175[Bioproject] OR 33317[Bioproject] of bacterial 16S ribosomal RNA. The nucleotide sequences have been multiply aligned using MAFFT tool version 7.427 (https://mafft.cbrc.jp/alignment/software/) and the approximately-maximum-likelihood phylogenetic tree has been inferred from the nucleotide alignments by using the general time-reversible model (GTR).
Figure 2
Figure 2
Reconstruction of the main microbial pathways associated to Lachnospiraceae in human gut. The panel in blue shows a schematic representation of the metabolic pathways involved in the biosynthesis of acetate and butyrate, as well as the main pathways of carbohydrate degradation (yellow). The green panel shows a schematic representation of metabolic pathways of aromatic amino acids involved in the biosynthesis of indole-propionic acid, indole, phenol, and p-cresol.

References

    1. Baquero F., Nombela C. The microbiome as a human organ. Clin. Microbiol. Infect. 2012;18:2–4. doi: 10.1111/j.1469-0691.2012.03916.x.
    1. Atarashi K., Tanoue T., Ando M., Kamada N., Nagano Y., Narushima S., Suda W., Imaoka A., Setoyama H., Nagamori T., et al. Th17 Cell Induction by Adhesion of Microbes to Intestinal Epithelial Cells. Cell. 2015;163:367–380. doi: 10.1016/j.cell.2015.08.058.
    1. Gensollen T., Iyer S.S., Kasper D.L., Blumberg R.S. How colonization by microbiota in early life shapes the immune system. Science. 2016;352:539–544. doi: 10.1126/science.aad9378.
    1. Power S.E., O’Toole P.W., Stanton C., Ross R.P., Fitzgerald G.F. Intestinal microbiota, diet and health. Br. J. Nutr. 2014;111:387–402. doi: 10.1017/S0007114513002560.
    1. Valdes A.M., Walter J., Segal E., Spector T.D. Role of the gut microbiota in nutrition and health. BMJ. 2018;361:k2179. doi: 10.1136/bmj.k2179.
    1. Gentile C.L., Weir T.L. The gut microbiota at the intersection of diet and human health. Science. 2018;362:776–780. doi: 10.1126/science.aau5812.
    1. Zhang N., Ju Z., Zuo T. Time for food: The impact of diet on gut microbiota and human health. Nutrition. 2018;51:80–85. doi: 10.1016/j.nut.2017.12.005.
    1. Crittenden R.G., Martinez N.R., Playne M.J. Synthesis and utilisation of folate by yoghurt starter cultures and probiotic bacteria. Int. J. Food Microbiol. 2003;80:217–222. doi: 10.1016/S0168-1605(02)00170-8.
    1. Riwes M., Reddy P. Microbial metabolites and graft versus host disease. Am. J. Transplant. 2018;18:23–29. doi: 10.1111/ajt.14443.
    1. Huttenhower C., Gevers D., Knight R., Abubucker S., Badger J.H., Chinwalla A.T., Creasy H.H., Earl A.M., FitzGerald M.G., Fulton R.S., et al. Structure, function and diversity of the healthy human microbiome. Nature. 2012;486:207. doi: 10.1038/nature11234.
    1. 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. doi: 10.1038/nbt.2942.
    1. Lozupone C.A., Stombaugh J.I., Gordon J.I., Jansson J.K., Knight R. Diversity, stability and resilience of the human gut microbiota. Nature. 2012;489:220–230. doi: 10.1038/nature11550.
    1. Rainey F.A., Family V. Lachnospiraceae fam. nov. In: De Vos P., Garrity G.M., Jones D., Krieg N.R., Ludwig W., Rainey F.A., Schleifer K.H., Whitman W.B., editors. Bergey’s Manual of Systematic Bacteriology. 3rd ed. Springer; Berlin/Heidelberg, Germany: 2009. pp. 921–968.
    1. Sayers E.W., Barrett T., Benson D.A., Bolton E., Bryant S.H., Canese K., Chetvernin V., Church D.M., DiCuccio M., Federhen S., et al. Database resources of the national center for biotechnology information. Nucleic Acids Res. 2009;38:D5–D16. doi: 10.1093/nar/gkp967.
    1. Stackebrandt E. The Family Lachnospiraceae. In: Rosenberg E., DeLong E.F., Lory S., Stackebrandt E., Thompson F., editors. The Prokaryotes. Springer; Berlin/Heidelberg, Germany: 2014. pp. 197–201.
    1. Ding Y., Xiao L., Guo J., Jiong L.U., Hao X.U., Hou M., Ben X. Intestinal microbiota in neonates within three days after birth. Chin. J. Perinat. Med. 2017;20:507–514.
    1. Sagheddu V., Patrone V., Miragoli F., Puglisi E., Morelli L. Infant early gut colonization by Lachnospiraceae: High frequency of Ruminococcus gnavus. Front. Pediatr. 2016;4:57. doi: 10.3389/fped.2016.00057.
    1. Sohn K., Underwood M.A. Prenatal and postnatal administration of prebiotics and probiotics. Semin Fetal Neonatal Med. 2017;22:284–289. doi: 10.1016/j.siny.2017.07.002.
    1. Odamaki T., Kato K., Sugahara H., Hashikura N., Takahashi S., Xiao J.Z., Abe F., Osawa R. Age-related changes in gut microbiota composition from newborn to centenarian: A cross-sectional study. BMC Microbiol. 2016;16:90. doi: 10.1186/s12866-016-0708-5.
    1. Van Treuren W., Dodd D. Microbial contribution to the human metabolome: Implications for health and disease. Annu. Rev. Pathol. Mech. Dis. 2020;15:345–369. doi: 10.1146/annurev-pathol-020117-043559.
    1. Biddle A., Stewart L., Blanchard J., Leschine S. Untangling the genetic basis of fibrolytic specialization by Lachnospiraceae and Ruminococcaceae in diverse gut communities. Diversity. 2013;5:627–640. doi: 10.3390/d5030627.
    1. Devillard E., McIntosh F.M., Duncan S.H., Wallace R.J. Metabolism of linoleic acid by human gut bacteria: Different routes for biosynthesis of conjugated linoleic acid. J. Bacteriol. 2007;189:2566–2570. doi: 10.1128/JB.01359-06.
    1. Wong J., Piceno Y.M., DeSantis T.Z., Pahl M., Andersen G.L., Vaziri N.D. Expansion of urease-and uricase-containing, indole-and p-cresol-forming and contraction of short-chain fatty acid-producing intestinal microbiota in ESRD. Am. J. Nephrol. 2014;39:230–237. doi: 10.1159/000360010.
    1. Sheridan P.O., Martin J.C., Lawley T.D., Browne H.P., Harris H.M., Bernalier-Donadille A., Duncan S.H., O’Toole P.W., Scott K.P., Flint H.J. Polysaccharide utilization loci and nutritional specialization in a dominant group of butyrate-producing human colonic Firmicutes. Microb. Genom. 2016;2:e000043. doi: 10.1099/mgen.0.000043.
    1. Scott K.P., Martin J.C., Chassard C., Clerget M., Potrykus J., Campbell G., Mayer C.D., Young P., Rucklidge G., Ramsay A.G., et al. Substrate-driven gene expression in Roseburia inulinivorans: Importance of inducible enzymes in the utilization of inulin and starch. Proc. Natl. Acad. Sci. USA. 2011;108:4672–4679. doi: 10.1073/pnas.1000091107.
    1. Ramsay A.G., Scott K.P., Martin J.C., Rincon M.T., Flint H.J. Cell-associated α-amylases of butyrate-producing Firmicute bacteria from the human colon. Microbiology. 2006;152:3281–3290. doi: 10.1099/mic.0.29233-0.
    1. Scott K.P., Martin J.C., Campbell G., Mayer C.D., Flint H.J. Whole-genome transcription profiling reveals genes up-regulated by growth on fucose in the human gut bacterium “Roseburia inulinivorans”. J. Bacteriol. 2006;188:4340–4349. doi: 10.1128/JB.00137-06.
    1. Chassard C., Goumy V., Leclerc M., Del’homme C., Bernalier-Donadille A. Characterization of the xylan-degrading microbial community from human faeces. FEMS Microbiol. Ecol. 2007;61:121–131. doi: 10.1111/j.1574-6941.2007.00314.x.
    1. Flint H.J., Scott K.P., Duncan S.H., Louis P., Forano E. Microbial degradation of complex carbohydrates in the gut. Gut Microbes. 2012;3:289–306. doi: 10.4161/gmic.19897.
    1. Duncan S.H., Scott K.P., Ramsay A.G., Harmsen H.J., Welling G.W., Stewart C.S., Flint H.J. Effects of alternative dietary substrates on competition between human colonic bacteria in an anaerobic fermentor system. Appl. Environ. Microbiol. 2003;69:1136–1142. doi: 10.1128/AEM.69.2.1136-1142.2003.
    1. Rossi M., Corradini C., Amaretti A., Nicolini M., Pompei A., Zanoni S., Matteuzzi D. Fermentation of fructooligosaccharides and inulin by bifidobacteria: A comparative study of pure and fecal cultures. Appl. Environ. Microbiol. 2005;71:6150–6158. doi: 10.1128/AEM.71.10.6150-6158.2005.
    1. Louis P., Young P., Holtrop G., Flint H.J. Diversity of human colonic butyrate-producing bacteria revealed by analysis of the butyryl-CoA: Acetate CoA-transferase gene. Environ. Microbiol. 2010;12:304–314. doi: 10.1111/j.1462-2920.2009.02066.x.
    1. Wolin M.J., Miller T.L., Collins M.D., Lawson P.A. Formate-Dependent Growth and Homoacetogenic Fermentation by a Bacterium from Human Feces: Description of Bryantella formatexigens gen. nov., sp. nov. Appl. Environ. Microbiol. 2003;69:6321–6326. doi: 10.1128/AEM.69.10.6321-6326.2003.
    1. Cummings J., Pomare E.W., Branch W.J., Naylor C.P., Macfarlane G.T. Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut. 1987;28:1221–1227. doi: 10.1136/gut.28.10.1221.
    1. Den Besten G., Lange K., Havinga R., van Dijk T.H., Gerding A., van Eunen K., Reijngoud D.J. Gut-derived short-chain fatty acids are vividly assimilated into host carbohydrates and lipids. Am. J. Physiol. 2013;305:G900–G910. doi: 10.1152/ajpgi.00265.2013.
    1. Macfarlane G.T., Gibson G.R., Cummings J.H. Comparison of fermentation reactions in different regions of the human colon. J. Appl. Bacteriol. 1992;72:57–64. doi: 10.1111/j.1365-2672.1992.tb04882.x.
    1. Kettle H., Louis P., Holtrop G., Duncan S.H., Flint H.J. Modelling the emergent dynamics and major metabolites of the human colonic microbiota. Environ. Microbiol. 2015;17:1615–1630. doi: 10.1111/1462-2920.12599.
    1. Tamanai-Shacoori Z., Smida I., Bousarghin L., Loreal O., Meuric V., Fong S.B., Bonnaure-Mallet M., Jolivet-Gougeon A. Roseburia spp.: A marker of health? Future Microbiol. 2017;12:157–170. doi: 10.2217/fmb-2016-0130.
    1. Louis P., Flint H.J. Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine. FEMS Microbiol. Lett. 2009;294:1–8. doi: 10.1111/j.1574-6968.2009.01514.x.
    1. Louis P., Flint H.J. Formation of propionate and butyrate by the human colonic microbiota. Environ. Microbiol. 2017;19:29–41. doi: 10.1111/1462-2920.13589.
    1. Reichardt N., Duncan S.H., Young P., Belenguer A., Leitch C.M., 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. doi: 10.1038/ismej.2014.14.
    1. Louis P., Duncan S.H., McCrae S.I., Millar J., Jackson M.S., Flint H.J. Restricted distribution of the butyrate kinase pathway among butyrate-producing bacteria from the human colon. J. Bacteriol. 2004;186:2099–2106. doi: 10.1128/JB.186.7.2099-2106.2004.
    1. Chassard C., Bernalier-Donadille A. H2 and acetate transfers during xylan fermentation between a butyrate-producing xylanolytic species and hydrogenotrophic microorganisms from the human gut. FEMS Microbiol. Lett. 2006;254:116–122. doi: 10.1111/j.1574-6968.2005.00016.x.
    1. Allen-Vercoe E., Daigneault M., White A., Panaccione R., Duncan S.H., Flint H.J., O’Neal L., Lawson P.A. Anaerostipes hadrus comb. nov., a dominant species within the human colonic microbiota; reclassification of Eubacterium hadrum Moore et al. 1976. Anaerobe. 2012;18:523–529. doi: 10.1016/j.anaerobe.2012.09.002.
    1. Duncan S.H., Louis P., Flint H.J. Lactate-utilizing bacteria, isolated from human feces, that produce butyrate as a major fermentation product. Appl. Environ. Microbiol. 2004;70:5810–5817. doi: 10.1128/AEM.70.10.5810-5817.2004.
    1. Duncan S.H., Barcenilla A., Stewart C.S., Pryde S.E., Flint H.J. Acetate utilization and butyryl coenzyme A (CoA): Acetate-CoA transferase in butyrate-producing bacteria from the human large intestine. Appl. Environ. Microbiol. 2002;68:5186–5190. doi: 10.1128/AEM.68.10.5186-5190.2002.
    1. Schwab C., Ruscheweyh H.J., Bunesova V., Pham V.T., Beerenwinkel N., Lacroix C. Trophic interactions of infant bifidobacteria and Eubacterium hallii during L-fucose and fucosyllactose degradation. Front. Microbiol. 2017;8:95. doi: 10.3389/fmicb.2017.00095.
    1. Fekry M.I., Engels C., Zhang J., Schwab C., Lacroix C., Sturla S.J., Chassard C. The strict anaerobic gut microbe Eubacterium hallii transforms the carcinogenic dietary heterocyclic amine 2-amino-1-methyl-6-phenylimidazo [4, 5-b] pyridine (PhIP) Environ. Microbiol. Rep. 2016;8:201–209. doi: 10.1111/1758-2229.12369.
    1. Morita H., Toh H., Fukuda S., Horikawa H., Oshima K., Suzuki T., Murakami M., Hisamatsu S., Kato Y., Takizawa T., et al. Comparative genome analysis of Lactobacillus reuteri and Lactobacillus fermentum reveal a genomic island for reuterin and cobalamin production. DNA Res. 2008;15:151–161. doi: 10.1093/dnares/dsn009.
    1. Engels C., Ruscheweyh H.J., Beerenwinkel N., Lacroix C., Schwab C. The common gut microbe Eubacterium hallii also contributes to intestinal propionate formation. Front. Microbiol. 2016;7:713. doi: 10.3389/fmicb.2016.00713.
    1. Belzer C., Chia L.W., Aalvink S., Chamlagain B., Piironen V., Knol J., de Vos W.M. Microbial metabolic networks at the mucus layer lead to diet-independent butyrate and vitamin B12 production by intestinal symbionts. MBio. 2017;8:e00770-17. doi: 10.1128/mBio.00770-17.
    1. Crost E.H., Tailford L.E., Le Gall G., Fons M., Henrissat B., Juge N. Utilisation of mucin glycans by the human gut symbiont Ruminococcus gnavus is strain-dependent. PLoS ONE. 2013;8:e76341. doi: 10.1371/journal.pone.0076341.
    1. Crost E.H., Tailford L.E., Monestier M., Swarbreck D., Henrissat B., Crossman L.C., Juge N. The mucin-degradation strategy of Ruminococcus gnavus: The importance of intramolecular trans-sialidases. Gut Microbes. 2016;7:302–312. doi: 10.1080/19490976.2016.1186334.
    1. Meyer T.W., Hostetter T.H. Uremic solutes from colon microbes. Kidney Int. 2012;81:949–954. doi: 10.1038/ki.2011.504.
    1. Saito Y., Sato T., Nomoto K., Tsuji H. Identification of phenol-and p-cresol-producing intestinal bacteria by using media supplemented with tyrosine and its metabolites. FEMS Microbiol. Ecol. 2018;94:125. doi: 10.1093/femsec/fiy125.
    1. Nazzal L., Roberts J., Singh P., Jhawar S., Matalon A., Gao Z., Holzman R., Liebes L., Blaser M.J., Lowenstein J. Microbiome perturbation by oral vancomycin reduces plasma concentration of two gut-derived uremic solutes, indoxyl sulfate and p-cresyl sulfate, in end-stage renal disease. Nephrol. Dial. Transpl. 2017;32:1809–1817. doi: 10.1093/ndt/gfx029.
    1. Feng Y.L., Cao G., Chen D.Q., Vaziri N.D., Chen L., Zhang J., Wang M., Guo Y., Zhao Y.Y. Microbiome–metabolomics reveals gut microbiota associated with glycine-conjugated metabolites and polyamine metabolism in chronic kidney disease. Cell Mol. Life Sci. 2019;76:1–18. doi: 10.1007/s00018-019-03155-9.
    1. Menni C., Hernandez M.M., Vital M., Mohney R.P., Spector T.D., Valdes A.M. Circulating levels of the anti-oxidant indoleproprionic acid are associated with higher gut microbiome diversity. Gut Microbes. 2019;10:1–8. doi: 10.1080/19490976.2019.1586038.
    1. Possemiers S., Heyerick A., Robbens V., De Keukeleire D., Verstraete W. Activation of proestrogens from hops (Humulus lupulus L.) by intestinal microbiota; conversion of isoxanthohumol into 8-prenylnaringenin. J. Agric. Food Chem. 2005;53:6281–6288. doi: 10.1021/jf0509714.
    1. Burapan S., Kim M., Han J. Demethylation of polymethoxyflavones by human gut bacterium, Blautia sp. MRG-PMF1. J. Agric. Food Chem. 2017;65:1620–1629. doi: 10.1021/acs.jafc.7b00408.
    1. Brahe L.K., Astrup A., Larsen L.H. Is butyrate the link between diet, intestinal microbiota and obesity-related metabolic diseases? Obes. Rev. 2013;14:950–959. doi: 10.1111/obr.12068.
    1. Portune K.J., Benítez-Páez A., Del Pulgar E.M.G., Cerrudo V., Sanz Y. Gut microbiota, diet, and obesity-related disorders—The good, the bad, and the future challenges. Mol. Nutr. Food Res. 2017;61:1600252. doi: 10.1002/mnfr.201600252.
    1. Layden B.T., Angueira A.R., Brodsky M., Durai V., Lowe W.L. Short chain fatty acids and their receptors: New metabolic targets. Transl. Res. 2013;161:131–140. doi: 10.1016/j.trsl.2012.10.007.
    1. Puddu A., Sanguineti R., Montecucco F., Viviani G.L. Evidence for the gut microbiota short-chain fatty acids as key pathophysiological molecules improving diabetes. Mediators Inflamm. 2014;2014:162021. doi: 10.1155/2014/162021.
    1. Esgalhado M., Kemp J.A., Damasceno N.R., Fouque D., Mafra D. Short-chain fatty acids: A link between prebiotics and microbiota in chronic kidney disease. Future Microbiol. 2017;12:1413–1425. doi: 10.2217/fmb-2017-0059.
    1. Maslowski K.M., Vieira A.T., Ng A., Kranich J., Sierro F., Yu D., Schilter H.C., Rolph M.S., Mackay F., Artis D. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature. 2009;461:1282–1286. doi: 10.1038/nature08530.
    1. Zhu L., Baker R.D., Baker S.S. Gut microbiome and nonalcoholic fatty liver diseases. Pediatric. Res. 2015;77:245. doi: 10.1038/pr.2014.157.
    1. Tappenden K.A., McBurney M.I. Systemic short-chain fatty acids rapidly alter gastrointestinal structure, function, and expression of early response genes. Dig. Dis. Sci. 1998;43:1526–1536. doi: 10.1023/A:1018819032620.
    1. Chávez-Carbajal A., Nirmalkar K., Pérez-Lizaur A., Hernández-Quiroz F., Ramírez-del-Alto S., García-Mena J., Hernández-Guerrero C. Gut Microbiota and Predicted Metabolic Pathways in a Sample of Mexican Women Affected by Obesity and Obesity Plus Metabolic Syndrome. Int. J. Mol. Sci. 2019;20:438. doi: 10.3390/ijms20020438.
    1. Den Besten G., Bleeker A., Gerding A., van Eunen K., Havinga R., van Dijk T.H., Oosterveer M.H., Jonker J.W., Groen A.K., Reijngoud D.J. Short-Chain Fatty Acids protect against High-Fat Diet- Induced Obesity via a PPARgamma-dependent switch from lipogenesis to fat oxidation. Diabetes. 2015;65:2398–2408. doi: 10.2337/db14-1213.
    1. Misztak P., Pańczyszyn-Trzewik P., Sowa-Kućma M. Histone deacetylases (HDACs) as therapeutic target for depressive disorders. Pharmacol. Rep. 2018;70:398–408. doi: 10.1016/j.pharep.2017.08.001.
    1. Faraco G., Cavone L., Chiarugi A. The therapeutic potential of HDAC inhibitors in the treatment of multiple sclerosis. Mol. Med. 2011;17:442–447. doi: 10.2119/molmed.2011.00077.
    1. Gonzalez A., Krieg R., Massey H.D., Carl D., Ghosh S., Gehr T.W., Ghosh S.S. Sodium butyrate ameliorates insulin resistance and renal failure in CKD rats by modulating intestinal permeability and mucin expression. Nephrol. Dial. Transpl. 2019;34:783–794. doi: 10.1093/ndt/gfy238.
    1. Chen G., Ran X., Li B., Li Y., He D., Huang B., Wang W. Sodium butyrate inhibits inflammation and maintains epithelium barrier integrity in a TNBS-induced inflammatory bowel disease mice model. EBioMedicine. 2018;30:317–325. doi: 10.1016/j.ebiom.2018.03.030.
    1. Melbye P., Olsson A., Hansen T.H., Søndergaard H.B., Bang Oturai A. Short-chain fatty acids and gut microbiota in multiple sclerosis. Acta Neurol. Scand. 2019;139:208–219. doi: 10.1111/ane.13045.
    1. Braniste V., Al-Asmakh M., Kowal C., Anuar F., Abbaspour A., Tóth M., Korecka A., Bakocevic N., Guan N.L., Kundu P., et al. The gut microbiota influences blood-brain barrier permeability in mice. Sci. Transl. Med. 2014;6:263ra158. doi: 10.1126/scitranslmed.3009759.
    1. Soty M., Penhoat A., Amigo-Correig M., Vinera J., Sardella A., Vullin-Bouilloux F., Zitoun C., Houberdon I., Mithieux G. A gut-brain neural circuit controlled by intestinal gluconeogenesis is crucial in metabolic health. Mol. Metab. 2015;4:106–117. doi: 10.1016/j.molmet.2014.12.009.
    1. Frye R.E., Rose S., Chacko J., Wynne R., Bennuri S.C., Slattery J.C., Tippett M., Delhey L., Melnyk S., Kahler S.G., et al. Modulation of mitochondrial function by the microbiome metabolite propionic acid in autism and control cell lines. Transl. Psychiat. 2016;6:e927. doi: 10.1038/tp.2016.189.
    1. Sanna S., van Zuydam N.R., Mahajan A., Kurilshikov A., Vila A.V., Võsa U., Mujagic Z., Masclee A.A.M., Jonkers D.M.A.E., Oosting M., et al. Causal relationships among the gut microbiome, short-chain fatty acids and metabolic diseases. Nat. Genet. 2019;51:600–605. doi: 10.1038/s41588-019-0350-x.
    1. Png C.W., Lindén S.K., Gilshenan K.S., Zoetendal E.G., McSweeney C.S., Sly L.I., McGuckin M.A., Florin T.H. Mucolytic Bacteria With Increased Prevalence in IBD Mucosa AugmentIn VitroUtilization of Mucin by Other Bacteria. Am. J. Gastroenterol. 2010;105:2420–2428. doi: 10.1038/ajg.2010.281.
    1. Slavin J. Fiber and prebiotics: Mechanisms and health benefits. Nutrients. 2013;5:1417–1435. doi: 10.3390/nu5041417.
    1. Ríos-Covián D., Ruas-Madiedo P., Margolles A., Gueimonde M., de los Reyes-Gavilán C.G., Salazar N. Intestinal short chain fatty acids and their link with diet and human health. Front. Microbiol. 2016;7:185. doi: 10.3389/fmicb.2016.00185.
    1. Vernocchi P., Del Chierico F., Putignani L. Gut microbiota profiling: Metabolomics based approach to unravel compounds affecting human health. Front. Microbiol. 2016;7:1144. doi: 10.3389/fmicb.2016.01144.
    1. Perry R.J., Peng L., Barry N.A., Cline G.W., Zhang D., Cardone R.L., Petersen K.F., Kibbey R.G., Goodman A.L., Shulman G.I. Acetate mediates a microbiome–brain–β-cell axis to promote metabolic syndrome. Nature. 2016;534:213–217. doi: 10.1038/nature18309.
    1. Murugesan S., Nirmalkar K., Hoyo-Vadillo C., García-Espitia M., Ramírez-Sánchez D., García-Mena J. Gut microbiome production of short-chain fatty acids and obesity in children. Eur. J. Clin. Microbiol. 2018;37:621–625. doi: 10.1007/s10096-017-3143-0.
    1. Morrison D.J., Preston T. Formation of short chain fatty acids by the gut microbiota and their impact on human metabolism. Gut Microbes. 2016;7:189–200. doi: 10.1080/19490976.2015.1134082.
    1. Yamashita H., Fujisawa K., Ito E., Idei S., Kawaguchi N., Kimoto M., Hiemori M., Tsuji H. Improvement of obesity and glucose tolerance by acetate in type 2 diabetic otsuka long-evans tokushima fatty (OLETF) rats. Biosci. Biotechnol. Biochem. 2007;71:1236–1243. doi: 10.1271/bbb.60668.
    1. 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. doi: 10.1016/j.immuni.2013.08.003.
    1. Huć T., Nowinski A., Drapala A., Konopelski P., Ufnal M. Indole and indoxyl sulfate, gut bacteria metabolites of tryptophan, change arterial blood pressure via peripheral and central mechanisms in rats. Pharmacol. Res. 2018;130:172–179. doi: 10.1016/j.phrs.2017.12.025.
    1. Venkatesh M., Mukherjee S., Wang H., Li H., Sun K., Benechet A.P., Qiu Z., Maher L., Redinbo M.R., Phillips R.S., et al. Symbiotic bacterial metabolites regulate gastrointestinal barrier function via the xenobiotic sensor PXR and Toll-like receptor 4. Immunity. 2014;41:296–310. doi: 10.1016/j.immuni.2014.06.014.
    1. Chyan Y.J., Poeggeler B., Omar R.A., Chain D.G., Frangione B., Ghiso J., Pappolla M.A. Potent neuroprotective properties against the Alzheimer β-amyloid by an endogenous melatonin-related indole structure, indole-3-propionic acid. J. Biol. Chem. 1999;274:21937–21942. doi: 10.1074/jbc.274.31.21937.
    1. 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. doi: 10.1038/nature08821.
    1. Walker A.W., Ince J., Duncan S.H., Webster L.M., Holtrop G., Ze X., Brown D., Stares M.D., Scott P., Bergerat A., et al. Dominant and diet-responsive groups of bacteria within the human colonic microbiota. ISME J. 2011;5:220. doi: 10.1038/ismej.2010.118.
    1. Koh A., De Vadder F., Kovatcheva-Datchary P., Bäckhed F. From dietary fiber to host physiology: Short-chain fatty acids as key bacterial metabolites. Cell. 2016;165:1332–1345. doi: 10.1016/j.cell.2016.05.041.
    1. La Rosa S.L., Leth M.L., Michalak L., Hansen M.E., Pudlo N.A., Glowacki R., Gabriel Pereira G., Christopher T., Workman C.T., Arntzen M.Ø., et al. The human gut Firmicute Roseburia intestinalis is a primary degrader of dietary β-mannans. Nat. Commun. 2019;10:905. doi: 10.1038/s41467-019-08812-y.
    1. Murugesan S., Ulloa-Martínez M., Martínez-Rojano H., Galván-Rodríguez F.M., Miranda-Brito C., Romano M.C., Pina-Escobedo A., Pizano-Zárate M.L., Hoyo-Vadillo C., García-Mena J. Study of the diversity and short-chain fatty acids production by the bacterial community in overweight and obese Mexican children. Eur. J. Clin. Microbiol. Infect. Dis. 2015;34:1337–1346. doi: 10.1007/s10096-015-2355-4.
    1. Park S.K., Kim M.S., Roh S.W., Bae J.W. Blautia stercoris sp. nov., isolated from human faeces. Int. J. Syst. Evol. Microbiol. 2012;62:776–779. doi: 10.1099/ijs.0.031625-0.
    1. Sun M., Wu W., Liu Z., Cong Y. Microbiota metabolite short chain fatty acids, GPCR, and inflammatory bowel diseases. J. Gastroenterol. 2017;52:1–8. doi: 10.1007/s00535-016-1242-9.
    1. Kasahara K., Krautkramer K.A., Org E., Romano K.A., Kerby R.L., Vivas E.I., Mehrabian M., Denu J.M., Bäckhed F., Lusis A.J., et al. Interactions between Roseburia intestinalis and diet modulate atherogenesis in a murine model. Nat. Microbiol. 2018;3:1461. doi: 10.1038/s41564-018-0272-x.
    1. Atarashi K., Tanoue T., Shima T., Imaoka A., Kuwahara T., Momose Y., Cheng G., Yamasaki S., Saito T., Ohba Y., et al. Induction of colonic regulatory T cells by indigenous Clostridium species. Science. 2011;331:337–341. doi: 10.1126/science.1198469.
    1. Goverse G., Molenaar R., Macia L., Tan J., Erkelens M.N., Konijn T., Knippenberg M., Cook E.C.L., Hanekamp D., Veldhoen M., et al. Diet-derived short chain fatty acids stimulate intestinal epithelial cells to induce mucosal tolerogenic dendritic cells. J. Immunol. 2017;198:2172–2181. doi: 10.4049/jimmunol.1600165.
    1. Geirnaert A., Calatayud M., Grootaert C., Laukens D., Devriese S., Smagghe G., De Vos M., Boon N., Van de Wiele T. Butyrate-producing bacteria supplemented in vitro to Crohn’s disease patient microbiota increased butyrate production and enhanced intestinal epithelial barrier integrity. Sci. Rep. 2017;7:11450. doi: 10.1038/s41598-017-11734-8.
    1. Nielsen D.S.G., Jensen B.B., Theil P.K., Nielsen T.S., Knudsen K.E.B., Purup S. Effect of butyrate and fermentation products on epithelial integrity in a mucus-secreting human colon cell line. J. Funct. Food. 2018;40:9–17. doi: 10.1016/j.jff.2017.10.023.
    1. Steinmeyer S., Lee K., Jayaraman A., Alaniz R.C. Microbiota metabolite regulation of host immune homeostasis: A mechanistic missing link. Curr. Allergy Asthma. Rep. 2015;15:24. doi: 10.1007/s11882-015-0524-2.
    1. Furusawa Y., Obata Y., Fukuda S., Endo T.A., Nakato G., Takahashi D., Nakanishi Y., Uetake C., Kato K., Kato T., et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature. 2013;504:446. doi: 10.1038/nature12721.
    1. Smith P.M., Howitt M.R., Panikov N., Michaud M., Gallini C.A., Bohlooly Y.M., Glickman J.N., Garrett W.S. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science. 2013;341:569–573. doi: 10.1126/science.1241165.
    1. Arpaia N., Campbell C., Fan X., Dikiy S., van der Veeken J., Deroos P., Liu H., Cross J.R., Pfeffer K., Coffer P.J., et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature. 2013;504:451. doi: 10.1038/nature12726.
    1. Jenq R.R., Taur Y., Devlin S.M., Ponce D.M., Goldberg J.D., Ahr K.F., Littmann E.R., Ling L., Gobourne A.C., Miller L.C., et al. Intestinal Blautia is associated with reduced death from graft-versus-host disease. Biol. Blood Marrow. Transpl. 2015;21:1373–1383. doi: 10.1016/j.bbmt.2015.04.016.
    1. Gong J., Chehrazi-Raffle A., Placencio-Hickok V., Guan M., Hendifar A., Salgia R. The gut microbiome and response to immune checkpoint inhibitors: Preclinical and clinical strategies. Clin. Trans. Med. 2019;8:9. doi: 10.1186/s40169-019-0225-x.
    1. Cong J., Zhang X. Roles of intestinal microbiota in response to cancer immunotherapy. Eur. J. Clin. Microbiol. Infect. Dis. 2018;37:2235–2240. doi: 10.1007/s10096-018-3374-8.
    1. Chen W., Liu F., Ling Z., Tong X., Xiang C. Human intestinal lumen and mucosa-associated microbiota in patients with colorectal cancer. PLoS ONE. 2012;7:e39743. doi: 10.1371/journal.pone.0039743.
    1. Bajaj J.S., Hylemon P.B., Ridlon J.M., Heuman D.M., Daita K., White M.B., Monteith P., Noble N.A., Sikaroodi M., Gillevet P.M. Colonic mucosal microbiome differs from stool microbiome in cirrhosis and hepatic encephalopathy and is linked to cognition and inflammation. Am. J. Physiol. Gastroint. Liver Physiol. 2012;303:G675–G685. doi: 10.1152/ajpgi.00152.2012.
    1. Deering K.E., Devine A., O’Sullivan T.A., Lo J., Boyce M.C., Christophersen C.T. Characterizing the Composition of the Pediatric Gut Microbiome: A Systematic Review. Nutrients. 2020;12:16. doi: 10.3390/nu12010016.
    1. Haidar Y.M., Cosman B.C. Obesity epidemiology. Clin. Colon Rectal. Surg. 2011;24:205–210. doi: 10.1055/s-0031-1295684.
    1. Festi D., Schiumerini R., Eusebi L.H., Marasco G., Taddia M., Colecchia A. Gut microbiota and metabolic syndrome. World J. Gastroenterol. 2014;20:16079. doi: 10.3748/wjg.v20.i43.16079.
    1. Kachur S., Morera R., De Schutter A., Lavie C.J. Cardiovascular risk in patients with prehypertension and the metabolic syndrome. Curr. Hypertens Rep. 2018;20:15. doi: 10.1007/s11906-018-0801-2.
    1. Molina-Molina E., Krawczyk M., Stachowska E., Lammert F., Portincasa P. Non-alcoholic fatty liver disease in non-obese individuals: Prevalence, pathogenesis and treatment. Clin. Res. Hepatol. Gastroenterol. 2019;43:638–645. doi: 10.1016/j.clinre.2019.04.005.
    1. Eslam M., Sanyal A.J., George J. MAFLD: A consensus-driven proposed nomenclature for metabolic associated fatty liver disease. Gastroenterology. 2020 doi: 10.1053/j.gastro.2019.11.312.
    1. Chassaing B., Gewirtz A.T. Gut microbiota, low-grade inflammation, and metabolic syndrome. Toxicol. Pathol. 2014;42:49–53. doi: 10.1177/0192623313508481.
    1. D’Aversa F., Tortora A., Ianiro G., Ponziani F.R., Annicchiarico B.E., Gasbarrini A. Gut microbiota and metabolic syndrome. Intern. Emerg. Med. 2013;8:11–15. doi: 10.1007/s11739-013-0916-z.
    1. Natividad J.M., Agus A., Planchais J., Lamas B., Jarry A.C., Martin R., Michel M.L., Chong-Nguyen C., Roussel R., Straube S., et al. Impaired aryl hydrocarbon receptor ligand production by the gut microbiota is a key factor in metabolic syndrome. Cell Metab. 2018;28:737–749. doi: 10.1016/j.cmet.2018.07.001.
    1. Ley R.E., Turnbaugh P.J., Klein S., Gordon J.I. Microbial ecology: Human gut microbes associated with obesity. Nature. 2006;444:1022. doi: 10.1038/4441022a.
    1. Lippert K., Kedenko L., Antonielli L., Kedenko I., Gemeier C., Leitner M., Kautzky-Willer A., Paulweber B., Hackl E. Gut microbiota dysbiosis associated with glucose metabolism disorders and the metabolic syndrome in older adults. Benef. Microbes. 2017;8:545–556. doi: 10.3920/BM2016.0184.
    1. Salonen A., Lahti L., Salojärvi J., Holtrop G., Korpela K., Duncan S.H., Date P., Farquharson F., Johnstone A.M., Lobley G.E., et al. Impact of diet and individual variation on intestinal microbiota composition and fermentation products in obese men. ISME J. 2014;8:2218. doi: 10.1038/ismej.2014.63.
    1. Zeng H., Ishaq S.L., Zhao F.Q., Wright A.D.G. Colonic inflammation accompanies an increase of β-catenin signaling and Lachnospiraceae/Streptococcaceae bacteria in the hind gut of high-fat diet-fed mice. J. Nutr. Biochem. 2016;35:30–36. doi: 10.1016/j.jnutbio.2016.05.015.
    1. Kostic A.D., Gevers D., Siljander H., Vatanen T., Hyötyläinen T., Hämäläinen A.M., Peet A., Tillmann V., Pöhö P., Mattila I., et al. The dynamics of the human infant gut microbiome in development and in progression toward type 1 diabetes. Cell Host Microbe. 2015;17:260–273. doi: 10.1016/j.chom.2015.01.001.
    1. Qin J., Li Y., Cai Z., Li S., Zhu J., Zhang F., Liang S., Zhang W., Guan Y., Shen D., et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature. 2012;490:55. doi: 10.1038/nature11450.
    1. Kameyama K., Itoh K. Intestinal colonization by a Lachnospiraceae bacterium contributes to the development of diabetes in obese mice. Microbes Environ. 2014;29:427–430. doi: 10.1264/jsme2.ME14054.
    1. Zhai B., Zhang C., Sheng Y., Zhao C., He X., Xu W., Huang K., Luo Y. Hypoglycemic and hypolipidemic effect of S-allyl-cysteine sulfoxide (alliin) in DIO mice. Sci. Rep. 2018;8:1–7. doi: 10.1038/s41598-018-21421-x.
    1. Schwiertz A., Taras D., Schafer K., Beijer S., Bos N.A., Donus C., Hardt P.D. Microbiota and SCFA in lean and overweight healthy subjects. Obesity. 2010;18:190–195. doi: 10.1038/oby.2009.167.
    1. Patil D.P., Dhotre D.P., Chavan S.G., Sultan A., Jain D.S., Lanjekar V.B., Gangawani J., Shah P.S., Todkar J.S., Shah S. Molecular analysis of gut microbiota in obesity among Indian individuals. J. Biosci. 2012;37:647–657. doi: 10.1007/s12038-012-9244-0.
    1. Shen F., Zheng R.D., Sun X.Q., Ding W.J., Wang X.Y., Fan J.G. Gut microbiota dysbiosis in patients with non-alcoholic fatty liver disease. Hepatob. Pancreatic Dis. Int. 2017;16:375–381. doi: 10.1016/S1499-3872(17)60019-5.
    1. Compare D., Coccoli P., Rocco A., Nardone O.M., De Maria S., Cartenì M., Nardone G. Gut–liver axis: The impact of gut microbiota on non alcoholic fatty liver disease. Nutr. Metab. Carbiovasc. Dis. 2012;22:471–476. doi: 10.1016/j.numecd.2012.02.007.
    1. De Minicis S., Rychlicki C., Agostinelli L., Saccomanno S., Candelaresi C., Trozzi L., Mingarelli E., Facinelli B., Magi G., Palmieri C., et al. Dysbiosis contributes to fibrogenesis in the course of chronic liver injury in mice. Hepatology. 2014;59:1738–1749. doi: 10.1002/hep.26695.
    1. Krawczyk M., Bonfrate L., Portincasa P. Nonalcoholic fatty liver disease. Best Pract Res. Clin. Gastroenterol. 2010;24:695–708. doi: 10.1016/j.bpg.2010.08.005.
    1. Zhu L., Baker S.S., Gill C., Liu W., Alkhouri R., Baker R.D., Gill S.R. Characterization of gut microbiomes in nonalcoholic steatohepatitis (NASH) patients: A connection between endogenous alcohol and NASH. Hepatology. 2013;57:601–609. doi: 10.1002/hep.26093.
    1. Quraishi M.N., Sergeant M., Kay G., Iqbal T., Chan J., Constantinidou C., Trivedi P., Ferguson J., Adams D.H., Pallen M., et al. The gut-adherent microbiota of PSC–IBD is distinct to that of IBD. Gut. 2017;66:386–388. doi: 10.1136/gutjnl-2016-311915.
    1. Torres J., Bao X., Goel A., Colombel J.F., Pekow J., Jabri B., Williams K.M., Castillo A., Odin J.A., Meckel K., et al. The features of mucosa-associated microbiota in primary sclerosing cholangitis. Aliment. Pharmacol. Ther. 2016;43:790–801. doi: 10.1111/apt.13552.
    1. Chaves L.D., McSkimming D.I., Bryniarski M.A., Honan A.M., Abyad S., Thomas S.A., Wells S., Buck M., Sun Y., Genco R.J., et al. Chronic kidney disease, uremic milieu, and its effects on gut bacterial microbiota dysbiosis. Am. J. Physiol. Renal. Physiol. 2018;315:F487–F502. doi: 10.1152/ajprenal.00092.2018.
    1. De Angelis M., Montemurno E., Piccolo M., Vannini L., Lauriero G., Maranzano V., Gozzi G., Serrazanetti D., Dalfino G., Gobbetti M., et al. Microbiota and metabolome associated with immunoglobulin A nephropathy (IgAN) PLoS ONE. 2014;9:e99006. doi: 10.1371/journal.pone.0099006.
    1. Al Khodor S., Shatat I.F. Gut microbiome and kidney disease: A bidirectional relationship. Pediatr. Nephrol. 2017;32:921–931. doi: 10.1007/s00467-016-3392-7.
    1. Yang J., Lim S.Y., Ko Y.S., Lee H.Y., Oh S.W., Kim M.G., Cho W.Y., Jo S.K. Intestinal barrier disruption and dysregulated mucosal immunity contribute to kidney fibrosis in chronic kidney disease. Nephrol. Dial. Transplant. 2018;34:419–428. doi: 10.1093/ndt/gfy172.
    1. Wang F., Zhang P., Jiang H., Cheng S. Gut bacterial translocation contributes to microinflammation in experimental uremia. Dig. Dis. Sci. 2012;57:2856–2862. doi: 10.1007/s10620-012-2242-0.
    1. Vaziri N.D., Wong J., Pahl M., Piceno Y.M., Yuan J., DeSantis T.Z., Ni Z., Nguyen T.H., Andersen G.L. Chronic kidney disease alters intestinal microbial flora. Kidney Int. 2013;83:308–315. doi: 10.1038/ki.2012.345.
    1. Barrios C., Beaumont M., Pallister T., Villar J., Goodrich J.K., Clark A., Pascual J., Ley R.E., Spector T.D., Bell J.T., et al. Gut-microbiota-metabolite axis in early renal function decline. PLoS ONE. 2015;10:e0134311. doi: 10.1371/journal.pone.0134311.
    1. Wang Z., Klipfell E., Bennett B.J., Koeth R., Levison B.S., DuGar B., Feldstein A.E., Britt E.B., Fu X., Chung Y.M., et al. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature. 2011;472:57. doi: 10.1038/nature09922.
    1. Karlsson F.H., Tremaroli V., Nookaew I., Bergström G., Behre C.J., Fagerberg B., Nielsen J., Bäckhed F. Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature. 2013;498:99. doi: 10.1038/nature12198.
    1. Tang W.W., Wang Z., Levison B.S., Koeth R.A., Britt E.B., Fu X., Yuping Wu M.S., Hazen S.L. Intestinal microbial metabolism of phosphatidylcholine and cardiovascular risk. N. Engl. J. Med. 2013;368:1575–1584. doi: 10.1056/NEJMoa1109400.
    1. Castillo-Rodriguez E., Fernandez-Prado R., Esteras R., Perez-Gomez M., Gracia-Iguacel C., Fernandez-Fernandez B., Kanbay M., Tejedor A., Lazaro A., Ruiz-Ortega M., et al. Impact of altered intestinal microbiota on chronic kidney disease progression. Toxins. 2018;10:300. doi: 10.3390/toxins10070300.
    1. Hill N.R., Fatoba S.T., Oke J.L., Hirst J.A., O’Callaghan C.A., Lasserson D.S., Hobbs F.R. Global prevalence of chronic kidney disease–a systematic review and meta-analysis. PLoS ONE. 2016;11:e0158765. doi: 10.1371/journal.pone.0158765.
    1. Cosola C., Rocchetti M.T., Sabatino A., Fiaccadori E., Di Iorio B.R., Gesualdo L. Microbiota issue in CKD: How promising are gut-targeted approaches? J. Nephrol. 2019;32:27–37. doi: 10.1007/s40620-018-0516-0.
    1. Manichanh C., Borruel N., Casellas F., Guarner F. The gut microbiota in IBD. Nat. Rev. Gastroenterol. Hepatol. 2012;9:599–608. doi: 10.1038/nrgastro.2012.152.
    1. Bonfrate L., Tack J., Grattagliano I., Cuomo R., Portincasa P. Microbiota in health and irritable bowel syndrome: Current knowledge, perspectives and therapeutic options. Scand. J. Gastroentero. 2013;48:995–1009. doi: 10.3109/00365521.2013.799220.
    1. Gevers D., Kugathasan S., Denson L.A., Vázquez-Baeza Y., Van Treuren W., Ren B., Schwager E., Knights D., Song S.J., Yassour M., et al. The treatment-naive microbiome in new-onset Crohn’s disease. Cell Host Microbe. 2014;15:382–392. doi: 10.1016/j.chom.2014.02.005.
    1. Baumgart M., Dogan B., Rishniw M., Weitzman G., Bosworth B., Yantiss R., Orsi R.H., Wiedmann M., McDonough P., Kim S.G., et al. Culture independent analysis of ileal mucosa reveals a selective increase in invasive Escherichia coli of novel phylogeny relative to depletion of Clostridiales in Crohn’s disease involving the ileum. ISME J. 2007;1:403–418. doi: 10.1038/ismej.2007.52.
    1. Frank D.N., Amand A.L.S., Feldman R.A., Boedeker E.C., Harpaz N., Pace N.R. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc. Natl. Acad. Sci. USA. 2007;104:13780–13785. doi: 10.1073/pnas.0706625104.
    1. Sasaki K., Inoue J., Sasaki D., Hoshi N., Shirai T., Fukuda I., Osawa R. Construction of a model culture system of human colonic microbiota to detect decreased Lachnospiraceae abundance and butyrogenesis in the feces of ulcerative colitis patients. Biotechnol. J. 2019;14:1800555. doi: 10.1002/biot.201800555.
    1. Boltin D., Perets T.T., Vilkin A., Niv Y. Mucin function in inflammatory bowel disease: An update. J. Clin Gastroenterol. 2013;47:106–111. doi: 10.1097/MCG.0b013e3182688e73.
    1. Torres J., Mehandru S., Colombel J.F., Peyrin-Biroulet L. Crohn’s disease. Lancet. 2017;389:1741–1755. doi: 10.1016/S0140-6736(16)31711-1.
    1. Jellbauer S., Raffatellu M. An intestinal arsonist: Pathobiont ignites IBD and flees the scene. Gut. 2014;63:1034–1035. doi: 10.1136/gutjnl-2013-305589.
    1. Duck W.L., Walter M.R., Novak J., Kelly D., Tomasi M., Cong Y., Elson C.O. Isolation of flagellated bacteria implicated in Crohn’s disease. Inflamm. Bowel. Dis. 2007;13:1191–1201. doi: 10.1002/ibd.20237.
    1. Carabotti M., Scirocco A., Maselli M.A., Severi C. The gut-brain axis: Interactions between enteric microbiota, central and enteric nervous systems. Ann. Gastroenterol. 2015;28:203–209.
    1. Inserra A., Rogers G.B., Licinio J., Wong M.L. The Microbiota-Inflammasome Hypothesis of Major Depression. Bioessays. 2018;40:1800027. doi: 10.1002/bies.201800027.
    1. Zheng P., Zeng B., Zhou C., Liu M., Fang Z., Xu X., Wang W., Tang W., Tan Z., Shi J., et al. Gut microbiome remodeling induces depressive-like behaviors through a pathway mediated by the host’s metabolism. Mol. Psychiatr. 2016;21:786. doi: 10.1038/mp.2016.44.
    1. Bonaz B., Bazin T., Pellissier S. The vagus nerve at the interface of the microbiota-gut-brain axis. Front. Neurosci. 2018;12:49. doi: 10.3389/fnins.2018.00049.
    1. Osadchiy V., Martin C.R., Mayer E.A. The Gut–Brain Axis and the Microbiome: Mechanisms and Clinical Implications. Clin. Gastroenterol. Hepatol. 2019;17:322–332. doi: 10.1016/j.cgh.2018.10.002.
    1. Wong M.L. The inflammasome and the microbiota-gut-brain axis. Neurol. Psychiatr Brain Res. 2018;29:25. doi: 10.1016/j.npbr.2018.01.110.
    1. Quigley E.M. Microbiota-brain-gut axis and neurodegenerative diseases. Curr. Neurol. Neurosci. Rep. 2017;17:94. doi: 10.1007/s11910-017-0802-6.
    1. Wang X., Wang B.R., Zhang X.J., Xu Z., Ding Y.Q., Ju G. Evidences for vagus nerve in maintenance of immune balance and transmission of immune information from gut to brain in STM-infected rats. World J. Gastroenterol. 2002;8:540. doi: 10.3748/wjg.v8.i3.540.
    1. Mass M., Kubera M., Leunis J.C. The gut-brain barrier in major depression: Intestinal mucosal dysfunction with an increased translocation of LPS from gram negative enterobacteria (leaky gut) plays a role in the inflammatory pathophysiology of depression. Neuroendocrinol. Lett. 2008;29:117–124.
    1. Cheung S., Goldenthal A.R., Uhlemann A.C., Mann J.J., Miller J.M., Sublette M.E. Systematic Review of Gut Microbiota and Major Depression. Front. Psychiatry. 2019;10:34. doi: 10.3389/fpsyt.2019.00034.
    1. Jiang H., Ling Z., Zhang Y., Mao H., Ma Z., Yin Y., Wang W., Tang W., Tan Z., Shi J., et al. Altered fecal microbiota composition in patients with major depressive disorder. Brain Behav. Immun. 2015;48:186–194. doi: 10.1016/j.bbi.2015.03.016.
    1. Berer K., Gerdes L.A., Cekanaviciute E., Jia X., Xiao L., Xia Z., Liu C., Klotz L., Stauffer U., Baranzini S.E., et al. Gut microbiota from multiple sclerosis patients enables spontaneous autoimmune encephalomyelitis in mice. Proc. Natl. Acad. Sci. USA. 2017;114:10719–10724. doi: 10.1073/pnas.1711233114.
    1. Cree B.A., Spencer C.M., Varrin-Doyer M., Baranzini S.E., Zamvil S.S. Gut microbiome analysis in neuromyelitis optica reveals overabundance of Clostridium perfringens. Ann. Neurol. 2016;80:443–447. doi: 10.1002/ana.24718.
    1. Cekanaviciute E., Yoo B.B., Runia T.F., Debelius J.W., Singh S., Nelson C.A., Kanner R., Bencosme Y., Kyung Lee Y., Hauser S.L., et al. Gut bacteria from multiple sclerosis patients modulate human T cells and exacerbate symptoms in mouse models. Proc. Natl. Acad. Sci. USA. 2017;114:10713–10718. doi: 10.1073/pnas.1711235114.
    1. Chen J., Chia N., Kalari K.R., Yao J.Z., Novotna M., Soldan M.M.P., Luckey D.H., Marietta E.V., Jeraldo P.R., Chen X., et al. Multiple sclerosis patients have a distinct gut microbiota compared to healthy controls. Sci. Rep. 2016;6:28484. doi: 10.1038/srep28484.
    1. Schirmer M., Smeekens S.P., Vlamakis H., Jaeger M., Oosting M., Franzosa E.A., Horst R.T., Jansen T., Jacobs L., Bonder M.J., et al. Linking the Human Gut Microbiome to Inflammatory Cytokine Production Capacity. Cell. 2016;167:1897. doi: 10.1016/j.cell.2016.11.046.
    1. Shahi S.K., Freedman S.N., Mangalam A.K. Gut microbiome in multiple sclerosis: The players involved and the roles they play. Gut Microbes. 2017;8:607–615. doi: 10.1080/19490976.2017.1349041.
    1. Cekanaviciute E., Debelius J.W., Singh S., Runia T., Nelson C., Yoo B. Gut dysbiosis is a feature of MS and it is characterized by bacteria able to regulate lymphocyte differentiation in vitro; Proceedings of the 2016 European Committee for Treatment and Research in Multiple Sclerosis; London, UK. 14 September 2016.
    1. Jangi S., Gandhi R., Cox L.M., Li N., von Glehn F., Yan R., Patel B., Mazzola M.A., Liu S., Glanz B.L., et al. Alterations of the human gut microbiome in multiple sclerosis. Nat. Commun. 2016;7:12015. doi: 10.1038/ncomms12015.
    1. Bibbò S., Ianiro G., Giorgio V., Scaldaferri F., Masucci L., Gasbarrini A., Cammarota G. The role of diet on gut microbiota composition. Eur. Rev. Med. Pharmacol. Sci. 2016;20:4742–4749.
    1. Flint H.J., Duncan S.H., Scott K.P., Louis P. Links between diet, gut microbiota composition and gut metabolism. Proc. Nutr. Soc. 2015;74:13–22. doi: 10.1017/S0029665114001463.
    1. Scott K.P., Gratz S.W., Sheridan P.O., Flint H.J., Duncan S.H. The influence of diet on the gut microbiota. Pharmacol. Res. 2013;69:52–60. doi: 10.1016/j.phrs.2012.10.020.
    1. Wu G.D., Chen J., Hoffmann C., Bittinger K., Chen Y.Y., Keilbaugh S.A., Bewtra M., Knights D., Walters W.A., Knight R., et al. Linking long-term dietary patterns with gut microbial enterotypes. Science. 2011;334:105–108. doi: 10.1126/science.1208344.
    1. De Angelis M., Ferrocino I., Calabrese F.M., De Filippis F., Cavallo N., Siragusa S., Rampelli S., Di Cagno R., Rantsiou K., Vannini L., et al. Diet influences the functions of the human intestinal microbiome. Sci. Rep. 2020;10:1–15. doi: 10.1038/s41598-020-61192-y.
    1. Rinninella E., Cintoni M., Raoul P., Lopetuso L.R., Scaldaferri F., Pulcini G., Miggiano G.A.D., Gasbarrini A., Mele M.C. Food components and dietary habits: Keys for a healthy gut microbiota composition. Nutrients. 2019;11:2393. doi: 10.3390/nu11102393.
    1. Flint H.J., Scott K.P., Louis P., Duncan S.H. The role of the gut microbiota in nutrition and health. Nat. Rev. Gastroenterol. Hepatol. 2012;9:577. doi: 10.1038/nrgastro.2012.156.
    1. Wilson M. In: Bacteriology of Humans: An Ecological Perspective. Nibali L., Henderson B., editors. John Wiley & Sons; Hoboken, NJ, USA: 2009.
    1. Tottey W., Feria-Gervasio D., Gaci N., Laillet B., Pujos E., Martin J.F., Sebedio J.L., Sion B., Jarrige J.F., Alric M., et al. Colonic transit time is a driven force of the gut microbiota composition and metabolism: In vitro evidence. J. Neurogastroenterol. Motil. 2017;23:124. doi: 10.5056/jnm16042.
    1. Flint H.J., Duncan S.H., Scott K.P., Louis P. Interactions and competition within the microbial community of the human colon: Links between diet and health. Environ. Microbiol. 2007;9:1101–1111. doi: 10.1111/j.1462-2920.2007.01281.x.
    1. Belenguer A., Duncan S.H., Calder A.G., Holtrop G., Louis P., Lobley G.E., Flint H.J. Two routes of metabolic cross-feeding between Bifidobacterium adolescentis and butyrate-producing anaerobes from the human gut. Appl. Environ. Microbiol. 2006;72:3593–3599. doi: 10.1128/AEM.72.5.3593-3599.2006.
    1. Aminov R.I., Walker A.W., Duncan S.H., Harmsen H.J.M., Welling G.W., Flint H.J. Molecular diversity, cultivation and improved detection by fluorescent in situ hybridization of a dominant group of human gut bacteria related to Roseburia spp. or Eubacterium rectale. Appl. Environ. Microbiol. 2006;72:6371–6376. doi: 10.1128/AEM.00701-06.
    1. Martínez I., Lattimer J.M., Hubach K.L., Case J.A., Yang J., Weber C.G., Louk J.A., Rose D.J., Kyureghian G., Peterson D.A., et al. Gut microbiome composition is linked to whole grain-induced immunological improvements. ISME J. 2013;7:269. doi: 10.1038/ismej.2012.104.
    1. Di Iorio B.R., Rocchetti M.T., De Angelis M., Cosola C., Marzocco S., Di Micco L., di Bari I., Accetturo M., Vacca M., Gobbetti M., et al. Nutritional Therapy Modulates Intestinal Microbiota and Reduces Serum Levels of Total and Free Indoxyl Sulfate and P-Cresyl Sulfate in Chronic Kidney Disease (Medika Study) J. Clin. Med. 2019;8:1424. doi: 10.3390/jcm8091424.
    1. De Filippis F., Pellegrini N., Vannini L., Jeffery I.B., La Storia A., Laghi L., Serrazanetti D.I., Di Cagno R., Ferrocino I., Lazzi C., et al. High-level adherence to a Mediterranean diet beneficially impacts the gut microbiota and associated metabolome. Gut. 2016;65:1812–1821. doi: 10.1136/gutjnl-2015-309957.
    1. Daniel H., Gholami A.M., Berry D., Desmarchelier C., Hahne H., Loh G., Mondot S., Lepage P., Rothballer M., Walker A., et al. High-fat diet alters gut microbiota physiology in mice. ISME J. 2014;8:295. doi: 10.1038/ismej.2013.155.
    1. Ortega J.F., Morales-Palomo F., Fernandez-Elias V., Hamouti N., Bernardo F.J., Martin-Doimeadios R.C., Nelson R.K., Horowitz J.F., Mora-Rodriguez R. Dietary supplementation with omega-3 fatty acids and oleate enhances exercise training effects in patients with metabolic syndrome. Obesity. 2016;24:1704–1711. doi: 10.1002/oby.21552.
    1. Marik P.E., Varon J. Omega-3 dietary supplements and the risk of cardiovascular events: A systematic review. Clin. Cardiol. 2009;32:365–372. doi: 10.1002/clc.20604.
    1. Liu J., Ma D.W. The role of n-3 polyunsaturated fatty acids in the prevention and treatment of breast cancer. Nutrients. 2014;6:5184–5223. doi: 10.3390/nu6115184.
    1. Noriega B.S., Sanchez-Gonzalez M.A., Salyakina D., Coffman J. Understanding the impact of omega-3 rich diet on the gut microbiota. Case Rep. Med. 2016 doi: 10.1155/2016/3089303.
    1. Menni C., Zierer J., Pallister T., Jackson M.A., Long T., Mohney R.P., Steves C.J., Spector T.D., Valdes A.M. Omega-3 fatty acids correlate with gut microbiome diversity and production of N-carbamylglutamate in middle aged and elderly women. Sci. Rep. 2017;7:1–11. doi: 10.1038/s41598-017-10382-2.
    1. Howe P., Buckley J. Metabolic health benefits of long-chain omega-3 polyunsaturated fatty acids. Mil. Med. 2014;179:138–143. doi: 10.7205/MILMED-D-14-00154.
    1. Horrocks L.A., Yeo Y.K. Health benefits of docosahexaenoic acid (DHA) Pharmacol. Res. 1999;40:211–225. doi: 10.1006/phrs.1999.0495.
    1. Kim E., Kim D.B., Park J.Y. Changes of mouse gut microbiota diversity and composition by modulating dietary protein and carbohydrate contents: A pilot study. Prev. Nutr. Food Sci. 2016;21:57. doi: 10.3746/pnf.2016.21.1.57.

Source: PubMed

3
구독하다