Disruption of intestinal oxygen balance in acute colitis alters the gut microbiome

References

• Friedman ES, Bittinger K, Esipova TV, Hou L, Chau L, Jiang J, Mesaros C, Lund PJ, Liang X, FitzGerald GA, et al. Microbes vs. chemistry in the origin of the anaerobic gut lumen. Proc Natl Acad Sci USA. 2018;115(16):4170–14. doi:10.1073/pnas.1718635115.
   PubMed Web of Science ®Google Scholar
• Glover LE, Lee JS, Colgan SP. Oxygen metabolism and barrier regulation in the intestinal mucosa. J Clin Invest. 2016;126(10):3680–3688. doi:10.1172/JCI84429.
   PubMed Web of Science ®Google Scholar
• Marteyn B, West NP, Browning DF, Cole JA, Shaw JG, Palm F, Mounier J, Prévost M-C, Sansonetti P, Tang CM, et al. Modulation of Shigella virulence in response to available oxygen in vivo. Nature. 2010;465(7296):355–358. doi:10.1038/nature08970.
   PubMed Web of Science ®Google Scholar
• Albenberg L, Esipova TV, Judge CP, Bittinger K, Chen J, Laughlin A, Grunberg S, Baldassano RN, Lewis JD, Li H, et al. Correlation between intraluminal oxygen gradient and radial partitioning of intestinal microbiota in humans and mice. Gastroenterology. 2014;147(5):1055–1063.e8. doi:10.1053/j.gastro.2014.07.020.
   PubMed Web of Science ®Google Scholar
• Jones RB, Zhu X, Moan E, Murff HJ, Ness RM, Seidner DL, Sun S, Yu C, Dai Q, Fodor AA, et al. Inter-niche and inter-individual variation in gut microbial community assessment using stool, rectal swab, and mucosal samples. Sci Rep. 2018;8(1):4139. doi:10.1038/s41598-018-22408-4.
   PubMedGoogle Scholar
• Winter SE, Lopez CA, Baumler AJ. The dynamics of gut-associated microbial communities during inflammation. EMBO Rep. 2013;14(4):319–327. doi:10.1038/embor.2013.27.
   PubMed Web of Science ®Google Scholar
• Rivera-Chavez F, Zhang LF, Faber F, Lopez C, Byndloss M, Olsan E, Xu G, Velazquez E, Lebrilla C, Winter S, et al. Depletion of butyrate-producing clostridia from the gut microbiota drives an aerobic luminal expansion of Salmonella. Cell Host Microbe. 2016;19(4):443–454. doi:10.1016/j.chom.2016.03.004.
   PubMed Web of Science ®Google Scholar
• Ni J, Shen T-C, Chen EZ, Bittinger K, Bailey A, Roggiani M, Sirota-Madi A, Friedman ES, Chau L, Lin A, et al. A role for bacterial urease in gut dysbiosis and Crohn’s disease. Sci Transl Med. 2017;9(416). doi:10.1126/scitranslmed.aah6888.
   Web of Science ®Google Scholar
• Litvak Y, Byndloss MX, Tsolis RM, Bäumler AJ. Dysbiotic Proteobacteria expansion: a microbial signature of epithelial dysfunction. Curr Opin Microbiol. 2017;39:1–6. doi:10.1016/j.mib.2017.07.003.
   PubMed Web of Science ®Google Scholar
• Chong SH, Ong YH, El Khatib M, Allu SR, Parthasarathy AB, Greenberg JH, Yodh AG, Vinogradov SA. Real-time tracking of brain oxygen gradients and blood flow during functional activation. Neurophotonics. 2022;9(4):045006. doi:10.1117/1.NPh.9.4.045006.
   PubMed Web of Science ®Google Scholar
• Esipova TV, Karagodov A, Miller J, Wilson DF, Busch TM, Vinogradov SA. Two new “protected” oxyphors for biological oximetry: properties and application in tumor imaging. Anal Chem. 2011;83(22):8756–8765. doi:10.1021/ac2022234.
   PubMed Web of Science ®Google Scholar
• Jerkic M, Peter M, Ardelean D, Fine M, Konerding MA, Letarte M. Dextran sulfate sodium leads to chronic colitis and pathological angiogenesis in Endoglin heterozygous mice. Inflamm Bowel Dis. 2010;16(11):1859–1870. doi:10.1002/ibd.21288.
   PubMed Web of Science ®Google Scholar
• Turhan A, Lin M, Lee GS, Miele LF, Tsuda A, Konerding MA, Mentzer SJ. Vascular microarchitecture of murine colitis-associated lymphoid angiogenesis. Anat Rec (Hoboken). 2009;292(5):621–632. doi:10.1002/ar.20902.
   PubMedGoogle Scholar
• Johansson ME. Mucus layers in inflammatory bowel disease. Inflamm Bowel Dis. 2014;20(11):2124–2131. doi:10.1097/MIB.0000000000000117.
   PubMed Web of Science ®Google Scholar
• Coskun M. Intestinal epithelium in inflammatory bowel disease. Front Med. 2014;1:24. doi:10.3389/fmed.2014.00024.
   PubMedGoogle Scholar
• Desai MS, Seekatz AM, Koropatkin NM, Kamada N, Hickey CA, Wolter M, Pudlo NA, Kitamoto S, Terrapon N, Muller A, et al. A dietary fiber-deprived gut microbiota degrades the colonic mucus barrier and enhances pathogen susceptibility. Cell. 2016;167(5):1339–1353.e21. doi:10.1016/j.cell.2016.10.043.
   PubMed Web of Science ®Google Scholar
• Glover JS, Ticer TD, Engevik MA. Characterizing the mucin-degrading capacity of the human gut microbiota. Sci Rep. 2022;12(1):8456. doi:10.1038/s41598-022-11819-z.
   PubMed Web of Science ®Google Scholar
• Martens EC, Neumann M, Desai MS. Interactions of commensal and pathogenic microorganisms with the intestinal mucosal barrier. Nat Rev Microbiol. 2018;16(8):457–470. doi:10.1038/s41579-018-0036-x.
   PubMed Web of Science ®Google Scholar
• Clemente AM, Castronovo G, Antonelli A, D’Andrea MM, Tanturli M, Perissi E, Paccosi S, Parenti A, Cozzolino F, Rossolini GM, et al. Differential Th17 response induced by the two clades of the pandemic ST258 Klebsiella pneumoniae clonal lineages producing KPC-type carbapenemase. PLOS ONE. 2017;12(6):e0178847. doi:10.1371/journal.pone.0178847.
   PubMed Web of Science ®Google Scholar
• Pandiyan P, Bhaskaran N, Zou M, Schneider E, Jayaraman S, Huehn J. Microbiome dependent regulation of T(regs) and Th17 cells in Mucosa. Front Immunol. 2019;10:426. doi:10.3389/fimmu.2019.00426.
   PubMed Web of Science ®Google Scholar
• Donohoe DR, Garge N, Zhang X, Sun W, O’Connell T, Bunger M, Bultman S. The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell Metab. 2011;13(5):517–526. doi:10.1016/j.cmet.2011.02.018.
   PubMed Web of Science ®Google Scholar
• Smith SA, Ogawa SA, Chau L, Whelan KA, Hamilton KE, Chen J, Tan L, Chen EZ, Keilbaugh S, Fogt F, et al. Mitochondrial dysfunction in inflammatory bowel disease alters intestinal epithelial metabolism of hepatic acylcarnitines. J Clin Invest. 2021;131(1):131. doi:10.1172/JCI133371.
   Web of Science ®Google Scholar
• Binion DG, Rafiee P. Is inflammatory bowel disease a vascular disease? Targeting angiogenesis improves chronic inflammation in inflammatory bowel disease. Gastroenterology. 2009;136(2):400–403. doi:10.1053/j.gastro.2008.12.029.
   PubMed Web of Science ®Google Scholar
• Chidlow JH Jr., Shukla D, Grisham MB, Kevil CG. Pathogenic angiogenesis in IBD and experimental colitis: new ideas and therapeutic avenues. Am J Physiol Gastrointestinal Liver Physiol. 2007;293(1):G5–G18. doi:10.1152/ajpgi.00107.2007.
   PubMed Web of Science ®Google Scholar
• Deban L, Correale C, Vetrano S, Malesci A, Danese S. Multiple pathogenic roles of microvasculature in inflammatory bowel disease: a Jack of all trades. Am J Pathol. 2008;172(6):1457–1466. doi:10.2353/ajpath.2008.070593.
   PubMed Web of Science ®Google Scholar
• Scaldaferri F, Vetrano S, Sans M, Arena V, Straface G, Stigliano E, Repici A, Sturm A, Malesci A, Panes J, et al. VEGF-A links angiogenesis and inflammation in inflammatory bowel disease pathogenesis. Gastroenterology. 2009;136(2):585–595.e5. doi:10.1053/j.gastro.2008.09.064.
   PubMed Web of Science ®Google Scholar
• Riedel TE, Berelson WM, Nealson KH, Finkel SE. Oxygen consumption rates of bacteria under nutrient-limited conditions. Appl Environ Microbiol. 2013;79(16):4921–4931. doi:10.1128/AEM.00756-13.
   PubMed Web of Science ®Google Scholar
• Nagalingam NA, Lynch SV. Role of the microbiota in inflammatory bowel diseases. Inflamm Bowel Dis. 2012;18(5):968–984. doi:10.1002/ibd.21866.
   PubMed Web of Science ®Google Scholar
• Velazquez EM, Nguyen H, Heasley KT, Saechao CH, Gil LM, Rogers AWL, Miller BM, Rolston MR, Lopez CA, Litvak Y, et al. Endogenous Enterobacteriaceae underlie variation in susceptibility to Salmonella infection. Nat Microbiol. 2019;4(6):1057–1064. doi:10.1038/s41564-019-0407-8.
   PubMed Web of Science ®Google Scholar
• Tanes C, Bittinger K, Gao Y, Friedman ES, Nessel L, Roy Paladhi U, Chau L, Panfen E, Fischbach MA, Braun J, et al. Role of dietary fiber in the recovery of the human gut microbiome and its metabolome. Cell Host Microbe. 2021;29(3):394–407. doi:10.1016/j.chom.2020.12.012.
   PubMed Web of Science ®Google Scholar
• Ouwerkerk JP, van der Ark KCH, Davids M, Claassens NJ, Finestra TR, de Vos WM, Belzer C. Adaptation of akkermansia muciniphila to the oxic-anoxic interface of the mucus layer. Appl Environ Microbiol. 2016;82(23):6983–6993. doi:10.1128/AEM.01641-16.
   PubMed Web of Science ®Google Scholar
• Zhang T, Li Q, Cheng L, Buch H, Zhang F. Akkermansia muciniphila is a promising probiotic. Microb Biotechnol. 2019;12(6):1109–1125. doi:10.1111/1751-7915.13410.
   PubMed Web of Science ®Google Scholar
• Machado D, Almeida D, Seabra CL, Andrade JC, Gomes AM, Freitas AC. Uncovering Akkermansia muciniphila resilience or susceptibility to different temperatures, atmospheres and gastrointestinal conditions. Anaerobe. 2020;61:102135. doi:10.1016/j.anaerobe.2019.102135.
   PubMed Web of Science ®Google Scholar
• Berry D, Schwab C, Milinovich G, Reichert J, Ben Mahfoudh K, Decker T, Engel M, Hai B, Hainzl E, Heider S, et al. Phylotype-level 16S rRNA analysis reveals new bacterial indicators of health state in acute murine colitis. Isme J. 2012;6(11):2091–2106. doi:10.1038/ismej.2012.39.
   PubMed Web of Science ®Google Scholar
• Ito T, Gallegos R, Matano LM, Butler NL, Hantman N, Kaili M, Coyne MJ, Comstock LE, Malamy MH, Barquera B, et al. Genetic and biochemical analysis of anaerobic respiration in bacteroides fragilis and its importance in vivo. mBio. 2020;11(1):11. doi:10.1128/mBio.03238-19.
   Web of Science ®Google Scholar
• Mishra S, Imlay JA. An anaerobic bacterium, bacteroides thetaiotaomicron, uses a consortium of enzymes to scavenge hydrogen peroxide. Mol Microbiol. 2013;90(6):1356–1371. doi:10.1111/mmi.12438.
   PubMed Web of Science ®Google Scholar
• Park H, Yeo S, Kang S, Huh CS. Longitudinal microbiome analysis in a dextran sulfate sodium-induced colitis mouse model. Microorganisms. 2021;9(2):370. doi:10.3390/microorganisms9020370.
   PubMed Web of Science ®Google Scholar
• Munyaka PM, Rabbi MF, Khafipour E, Ghia J-E. Acute dextran sulfate sodium (DSS)-induced colitis promotes gut microbial dysbiosis in mice. J Basic Microbiol. 2016;56(9):986–998. doi:10.1002/jobm.201500726.
   PubMed Web of Science ®Google Scholar
• Hughes ER, Winter MG, Duerkop BA, Spiga L, Furtado de Carvalho T, Zhu W, Gillis CC, Büttner L, Smoot MP, Behrendt CL, et al. Microbial respiration and formate oxidation as metabolic signatures of inflammation-associated dysbiosis. Cell Host Microbe. 2017;21(2):208–219. doi:10.1016/j.chom.2017.01.005.
   PubMed Web of Science ®Google Scholar
• Zhang Q, Wu Y, Wang J, Wu G, Long W, Xue Z, Wang L, Zhang X, Pang X, Zhao Y, et al. Accelerated dysbiosis of gut microbiota during aggravation of DSS-induced colitis by a butyrate-producing bacterium. Sci Rep. 2016;6(1):27572. doi:10.1038/srep27572.
   PubMedGoogle Scholar
• van der Post S, Jabbar KS, Birchenough G, Arike L, Akhtar N, Sjovall H, Johansson MEV, Hansson GC. Structural weakening of the colonic mucus barrier is an early event in ulcerative colitis pathogenesis. Gut. 2019;68(12):2142–2151. doi:10.1136/gutjnl-2018-317571.
   PubMed Web of Science ®Google Scholar
• Cooper HS, Murthy SN, Shah RS, Sedergran DJ. Clinicopathologic study of dextran sulfate sodium experimental murine colitis. Lab Invest. 1993;69(2):238–249.
   PubMed Web of Science ®Google Scholar
• Lebedev AY, Cheprakov AV, Sakadzic S, Boas DA, Wilson DF, Vinogradov SA. Dendritic phosphorescent probes for oxygen imaging in biological systems. ACS Appl Mater Interfaces. 2009;1(6):1292–1304. doi:10.1021/am9001698.
   PubMed Web of Science ®Google Scholar
• Lewis JD, Chen EZ, Baldassano RN, Otley A, Griffiths A, Lee D, Bittinger K, Bailey A, Friedman E, Hoffmann C, et al. Inflammation, antibiotics, and diet as environmental stressors of the gut microbiome in pediatric Crohn’s disease. Cell Host Microbe. 2015;18(4):489–500. doi:10.1016/j.chom.2015.09.008.
   PubMed Web of Science ®Google Scholar
• Friedman ES, Li Y, Shen TCD, Jiang J, Chau L, Adorini L, Babakhani F, Edwards J, Shapiro D, Zhao C, et al. FXR-Dependent modulation of the human small intestinal microbiome by the bile acid derivative obeticholic acid. Gastroenterology. 2018;155(6):1741–1752. doi:10.1053/j.gastro.2018.08.022.
   PubMed Web of Science ®Google Scholar
• Ramsteijn AS, Jašarević E, Houwing DJ, Bale TL, Olivier JD. Antidepressant treatment with fluoxetine during pregnancy and lactation modulates the gut microbiome and metabolome in a rat model relevant to depression. Gut Microbes. 2020;11(4):1–19. doi:10.1080/19490976.2019.1705728.
   PubMed Web of Science ®Google Scholar
• Velázquez-Hernández ML, Baizabal-Aguirre VM, Bravo-Patiño A, Cajero-Juárez M, Chávez-Moctezuma MP, Valdez-Alarcón JJ. Microbial fructosyltransferases and the role of fructans. J Appl Microbiol. 2009;106(6):1763–1778. doi:10.1111/j.1365-2672.2008.04120.x.
   PubMed Web of Science ®Google Scholar
• Tailford LE, Crost EH, Kavanaugh D, Juge N. Mucin glycan foraging in the human gut microbiome. Front Genet. 2015;6:81. doi:10.3389/fgene.2015.00081.
   PubMed Web of Science ®Google Scholar
• Miwa M, Horimoto T, Kiyohara M, Katayama T, Kitaoka M, Ashida H, Yamamoto K. Cooperation of β-galactosidase and β-N-acetylhexosaminidase from bifidobacteria in assimilation of human milk oligosaccharides with type 2 structure. Glycobiology. 2010;20(11):1402–1409. doi:10.1093/glycob/cwq101.
   PubMed Web of Science ®Google Scholar
• Mariethoz J, Alocci D, Gastaldello A, Horlacher O, Gasteiger E, Rojas-Macias M, Karlsson NG, Packer NH, Lisacek F. Glycomics@ExPASy: Bridging the Gap. Mol Cell Proteomics: MCP. 2018;17(11):2164–2176. doi:10.1074/mcp.RA118.000799.
   PubMed Web of Science ®Google Scholar
• Little MS, Pellock SJ, Walton WG, Tripathy A, Redinbo MR. Structural basis for the regulation of β-glucuronidase expression by human gut Enterobacteriaceae. Proc Natl Acad Sci USA. 2018;115(2):E152–e161. doi:10.1073/pnas.1716241115.
   PubMed Web of Science ®Google Scholar
• Kuriki T, Imanaka T. Nucleotide sequence of the neopullulanase gene from Bacillus stearothermophilus. J Gen Microbiol. 1989;135(6):1521–1528. doi:10.1099/00221287-135-6-1521.
   PubMedGoogle Scholar
• Humblot C, Murkovic M, Rigottier-Gois L, Bensaada M, Bouclet A, Andrieux C, Anba J, Rabot S. Beta-glucuronidase in human intestinal microbiota is necessary for the colonic genotoxicity of the food-borne carcinogen 2-amino-3-methylimidazo[4,5-f]quinoline in rats. Carcinogenesis. 2007;28(11):2419–2425. doi:10.1093/carcin/bgm170.
   PubMed Web of Science ®Google Scholar
• Flint HJ, Scott KP, Duncan SH, Louis P, Forano E. Microbial degradation of complex carbohydrates in the gut. Gut Microbes. 2012;3(4):289–306. doi:10.4161/gmic.19897.
   PubMed Web of Science ®Google Scholar
• Dogsa I, Brloznik M, Stopar D, Mandic-Mulec I. Exopolymer diversity and the role of levan in Bacillus subtilis biofilms. PLOS ONE. 2013;8(4):e62044. doi:10.1371/journal.pone.0062044.
   PubMed Web of Science ®Google Scholar
• Derrien M, van Passel MW, van de Bovenkamp JH, Schipper R, de Vos W, Dekker J. Mucin-bacterial interactions in the human oral cavity and digestive tract. Gut Microbes. 2010;1(4):254–268. doi:10.4161/gmic.1.4.12778.
   PubMed Web of Science ®Google Scholar
• Dabek M, McCrae SI, Stevens VJ, Duncan SH, Louis P. Distribution of β-glucosidase and β-glucuronidase activity and of β-glucuronidase gene gus in human colonic bacteria. FEMS Microbiol Ecol. 2008;66(3):487–495. doi:10.1111/j.1574-6941.2008.00520.x.
   PubMed Web of Science ®Google Scholar
• Bøhle LA, Mathiesen G, Vaaje-Kolstad G, Eijsink VGH. An endo-β-N-acetylglucosaminidase from Enterococcus faecalis V583 responsible for the hydrolysis of high-mannose and hybrid-type N-linked glycans. FEMS Microbiol Lett. 2011;325(2):123–129. doi:10.1111/j.1574-6968.2011.02419.x.
   PubMed Web of Science ®Google Scholar
• Bairoch A. The ENZYME database in 2000. Nucleic Acids Res. 2000;28(1):304–305. doi:10.1093/nar/28.1.304.
   PubMed Web of Science ®Google Scholar
• Bonnett GD, Sims IM, Simpson RJ, Cairns AJ. Structural diversity of fructan in relation to the taxonomy of the Poaceae. New Phytol. 1997;136(1):11–17. doi:10.1111/j.1469-8137.1997.tb04726.x.
   Web of Science ®Google Scholar
• Benjamini Y, Hochberg Y. Controlling the false discovery rate - a practical and powerful approach to multiple testing. J R Stat Soc Ser B-Methodol. 1995;57(1):289–300. doi:10.1111/j.2517-6161.1995.tb02031.x.
   Google Scholar