Comparison of microbial communities and the profile of sulfate-reducing bacteria in patients with ulcerative colitis and their association with bowel diseases: a pilot study

. 2024 ; 11 () : 79-89. [epub] 20240314

Status PubMed-not-MEDLINE Jazyk angličtina Země Rakousko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid38486888

Considerable evidence has accumulated regarding the molecular relationship between gut microbiota (GM) composition and the onset (clinical presentation and prognosis of ulcerative colitis (UC)). In addition, it is well documented that short-chain fatty acid (SCFA)-producing bacteria may play a fundamental role in maintaining an anti-inflammatory intestinal homeostasis, but sulfate- and sulfite reducing bacteria may be responsible for the production of toxic metabolites, such as hydrogen sulfide and acetate. Hence, the present study aimed to assess the GM composition - focusing on sulfate-reducing bacteria (SRB) - in patients with severe, severe-active and moderate UC. Each one of the six enrolled patients provided two stool samples in the following way: one sample was cultivated in a modified SRB-medium before 16S rRNA sequencing and the other was not cultivated. Comparative phylogenetic analysis was conducted on each sample. Percentage of detected gut microbial genera showed considerable variation based on the patients' disease severity and cultivation in the SRB medium. In detail, samples without cultivation from patients with moderate UC showed a high abundance of the genera Bacteroides, Bifidobacterium and Ruminococcus, but after SRB cultivation, the dominant genera were Bacteroides, Klebsiella and Bilophila. On the other hand, before SRB cultivation, the main represented genera in patients with severe UC were Escherichia-Shigella, Proteus, Methanothermobacter and Methanobacterium. However, after incubation in the SRB medium Bacteroides, Proteus, Alistipes and Lachnoclostridium were predominant. Information regarding GM compositional changes in UC patients may aid the development of novel therapeutic strategies (e.g., probiotic preparations containing specific bacterial strains) to counteract the mechanisms of virulence of harmful bacteria and the subsequent inflammatory response that is closely related to the pathogenesis of inflammatory bowel diseases.

Zobrazit více v PubMed

Boirivant M, Cossu A. Inflammatory bowel disease: Inflammatory bowel disease. Oral Dis. 2012;18(1):1–15. doi: 10.1111/j.1601-0825.2011.01811.x. PubMed DOI

Head K, Jurenka JS. Inflammatory bowel disease. Part II: Crohn's disease--pathophysiology and conventional and alternative treatment options. Altern Med Rev J Clin Ther. 2004;9(4):360–401. PubMed

Rubin DC, Shaker A, Levin MS. Chronic intestinal inflammation: inflammatory bowel disease and colitis-associated colon cancer. Front Immunol. 2012;3:107. doi: 10.3389/fimmu.2012.00107. PubMed DOI PMC

Vilela EG. Evaluation of inflammatory activity in Crohn's disease and ulcerative colitis. World J Gastroenterol. 2012;18(9):872. doi: 10.3748/wjg.v18.i9.872. PubMed DOI PMC

Kushkevych I, Dordević D, Vítězová M. Possible synergy effect of hydrogen sulfide and acetate produced by sulfate-reducing bacteria on inflammatory bowel disease development. J Adv Res. 2020;27:71–78. doi: 10.1016/j.jare.2020.03.007. PubMed DOI PMC

Ungaro R, Mehandru S, Allen PB, Peyrin-Biroulet L, Colombel J-F. Ulcerative colitis. The Lancet. 2017;389(10080):1756–1770. doi: 10.1016/S0140-6736(16)32126-2. PubMed DOI PMC

Kushkevych I, Dordević D, Vítězová M. Toxicity of hydrogen sulfide toward sulfate-reducing bacteria Desulfovibrio piger Vib-7. Arch Microbiol. 2019;201(3):389–397. doi: 10.1007/s00203-019-01625-z. PubMed DOI

Stange EF. Inflammatory bowel diseases. Preface. Dig Dis. 2013;31(3–4):269–269. doi: 10.1159/000354674. PubMed DOI

Sanchez-Morate E, Gimeno-Mallench L, Stromsnes K, Sanz-Ros J, Román-Domínguez A, Parejo-Pedrajas S, Inglés M, Olaso G, Gambini J, Mas-Bargues C. Relationship between Diet, Microbiota, and Healthy Aging. Biomedicines. 2020;8(8):287. doi: 10.3390/biomedicines8080287. PubMed DOI PMC

Fontana A, Manchia M, Panebianco C, Paribello P, Arzedi C, Cossu E, Garzilli M, Montis MA, Mura A, Pisanu C, Congiu D, Copetti M, Pinna F, Carpiniello B, Squassina A, Pazienza V. Exploring the Role of Gut Microbiota in Major Depressive Disorder and in Treatment Resistance to Antidepressants. Biomedicines. 2020;8(9):311. doi: 10.3390/biomedicines8090311. PubMed DOI PMC

Macfarlane, Hopkins, Ma S. Bacterial Growth and Metabolism on Surfaces in the Large Intestine. Microb Ecol Health Dis. 2000;12(2):64–72. doi: 10.1080/089106000750060314. DOI

Cummings JH, Macfarlane GT. Colonic microflora: Nutrition and health. Nutrition. 1997;13(5):476–478. doi: 10.1016/S0899-9007(97)00114-7. PubMed DOI

Macfarlane S, Steed H, Macfarlane GT. Intestinal bacteria and inflammatory bowel disease. Crit Rev Clin Lab Sci. 2009;46(1):25–54. doi: 10.1080/10408360802485792. PubMed DOI

Kushkevych I, Dordević D, Kollár P. Analysis of physiological parameters of Desulfovibrio strains from individuals with colitis. Open Life Sci. 2019;13(1):481–488. doi: 10.1515/biol-2018-0057. PubMed DOI PMC

Kushkevych I, Dordević D, Vítězová M. Analysis of pH dose-dependent growth of sulfate-reducing bacteria. Open Med. 2019;14(1):66–74. doi: 10.1515/med-2019-0010. PubMed DOI PMC

Kushkevych I, Kollar P, Ferreira AL, Palma D, Duarte A, Lopes MM, Bartos M, Pauk K, Imramovsky A, Jampilek J. Antimicrobial effect of salicylamide derivatives against intestinal sulfate-reducing bacteria. J Appl Biomed. 2016;14(2):125–130. doi: 10.1016/j.jab.2016.01.005. DOI

Öhman F, Hassenstab J, Berron D, Schöll M, Papp KV. Current advances in digital cognitive assessment for preclinical Alzheimer's disease. Alzheimers Dement Diagn Assess Dis Monit. 2021;13(1):e12217. doi: 10.1002/dad2.12217. PubMed DOI PMC

Ahmed EA, Ahmed SM, Zakaria NH, Baddour NM, Header DA. Study of the gut microbiome in Egyptian patients with active ulcerative colitis. Rev Gastroenterol México Engl Ed. 2022;88(3):246–255. doi: 10.1016/j.rgmxen.2022.07.006. PubMed DOI

Barberio B, Facchin S, Patuzzi I, Ford AC, Massimi D, Valle G, Sattin E, Simionati B, Bertazzo E, Zingone F, Savarino EV. A specific microbiota signature is associated to various degrees of ulcerative colitis as assessed by a machine learning approach. Gut Microbes. 2022;14(1):2028366. doi: 10.1080/19490976.2022.2028366. PubMed DOI PMC

Carbonnel F, Jantchou P, Monnet E, Cosnes J. Environmental risk factors in Crohn's disease and ulcerative colitis: an update. Gastroentérologie Clin Biol. 2009;33:S145–S157. doi: 10.1016/S0399-8320(09)73150-1. PubMed DOI

Dai Z, Ramesh V, Locasale JW. The evolving metabolic landscape of chromatin biology and epigenetics. Nat Rev Genet. 2020;21(12):737–753. doi: 10.1038/s41576-020-0270-8. PubMed DOI PMC

Kushkevych I, Castro Sangrador J, Dordević D, Rozehnalová M, Černý M, Fafula R, Vítězová M, Rittmann SK-MR. Evaluation of Physiological Parameters of Intestinal Sulfate-Reducing Bacteria Isolated from Patients Suffering from IBD and Healthy People. J Clin Med. 2020;9(6):1920. doi: 10.3390/jcm9061920. PubMed DOI PMC

Kushkevych I, Dordević D, Kollar P, Vítězová M, Drago L. Hydrogen Sulfide as a Toxic Product in the Small–Large Intestine Axis and its Role in IBD Development. J Clin Med. 2019;8(7):1054. doi: 10.3390/jcm8071054. PubMed DOI PMC

Kushkevych I, Kotrsová V, Dordević D, Buňková L, Vítězová M, Amedei A. Hydrogen Sulfide Effects on the Survival of Lactobacilli with Emphasis on the Development of Inflammatory Bowel Diseases. Biomolecules. 2019;9(12):752. doi: 10.3390/biom9120752. PubMed DOI PMC

Kováč J, Vítězová M, Kushkevych I. Metabolic activity of sulfate-reducing bacteria from rodents with colitis. Open Med. 2018;13(1):344–349. doi: 10.1515/med-2018-0052. PubMed DOI PMC

Kushkevych I, Cejnar J, Treml J, Dordević D, Kollar P, Vítězová M. Recent Advances in Metabolic Pathways of Sulfate Reduction in Intestinal Bacteria. Cells. 2020;9(3):698. doi: 10.3390/cells9030698. PubMed DOI PMC

Parada Venegas D, De la Fuente MK, Landskron G, González MJ, Quera R, Dijkstra G, Harmsen HJM, Faber KN, Hermoso MA. Short Chain Fatty Acids (SCFAs)-Mediated Gut Epithelial and Immune Regulation and Its Relevance for Inflammatory Bowel Diseases. Front Immunol. 2019;10:277. doi: 10.3389/fimmu.2019.00277. PubMed DOI PMC

LeBlanc JG, Chain F, Martín R, Bermúdez-Humarán LG, Courau S, Langella P. Beneficial effects on host energy metabolism of short-chain fatty acids and vitamins produced by commensal and probiotic bacteria. Microb Cell Factories. 2017;16(1):79. doi: 10.1186/s12934-017-0691-z. PubMed DOI PMC

Deleu S, Machiels K, Raes J, Verbeke K, Vermeire S. Short chain fatty acids and its producing organisms: An overlooked therapy for IBD? EBioMedicine. 2021;66:103293. doi: 10.1016/j.ebiom.2021.103293. PubMed DOI PMC

Massier L, Blüher M, Kovacs P, Chakaroun RM. Impaired Intestinal Barrier and Tissue Bacteria: Pathomechanisms for Metabolic Diseases. Front Endocrinol. 2021;12:616506. doi: 10.3389/fendo.2021.616506. PubMed DOI PMC

Abdulina D, Kováč J, Iutynska G, Kushkevych I. ATP sulfurylase activity of sulfate-reducing bacteria from various ecotopes. 3 Biotech. 2020;10(2):55. doi: 10.1007/s13205-019-2041-9. PubMed DOI PMC

Kushkevych I, Fafula R, Parák T, Bartoš M. Activity of Na+/K+-activated Mg2+-dependent ATP-hydrolase in the cell-free extracts of the sulfate-reducing bacteria Desulfovibrio piger Vib-7 and Desulfomicrobium sp. Rod-9. Acta Vet Brno. 2015;84(1):3–12. doi: 10.2754/avb201585010003. DOI

Kushkevych I, Dordević D, Vítězová M, Rittmann SK-MR. Environmental Impact of Sulfate-Reducing Bacteria, Their Role in Intestinal Bowel Diseases, and Possible Control by Bacteriophages. Appl Sci. 2021;11(2):735. doi: 10.3390/app11020735. DOI

Dordević D, Jančíková S, Vítězová M, Kushkevych I. Hydrogen sulfide toxicity in the gut environment: Meta–analysis of sulfate-reducing and lactic acid bacteria in inflammatory processes. J Adv Res. 2020;27:55–69. doi: 10.1016/j.jare.2020.03.003. PubMed DOI PMC

Kushkevych I, Vítězová M, Fedrová P, Vochyanová Z, Paráková L, Hošek J. Kinetic properties of growth of intestinal sulphate-reducing bacteria isolated from healthy mice and mice with ulcerative colitis. Acta Vet Brno. 2017;86(4):405–411. doi: 10.2754/avb201786040405. DOI

Kushkevych I, Dordević D, Vítězová M, Kollár P. Cross-correlation analysis of the Desulfovibrio growth parameters of intestinal species isolated from people with colitis. Biologia. 2018;73(11):1137–1143. doi: 10.2478/s11756-018-0118-2. DOI

Kushkevych I, Vítězová M, Kos J, Kollár P, Jampílek J. Effect of selected 8-hydroxyquinoline-2-carboxanilides on viability and sulfate metabolism of Desulfovibrio piger. J Appl Biomed. 2018;16(3):241–246. doi: 10.1016/j.jab.2018.01.004. DOI

Earley H, Lennon G, Coffey JC, Winter DC, O'Connell PR. Colonisation of the colonic mucus gel layer with butyrogenic and hydrogenotropic bacteria in health and ulcerative colitis. Sci Rep. 2021;11(1):7262. doi: 10.1038/s41598-021-86166-6. PubMed DOI PMC

Chaudhary PP, Conway PL, Schlundt J. Methanogens in humans: potentially beneficial or harmful for health. Appl Microbiol Biotechnol. 2018;102(7):3095–3104. doi: 10.1007/s00253-018-8871-2. PubMed DOI

Akar M, Aydin F, Yurci MA, Abay S, Ateş İ, Deniz K. The possible relationship between Campylobacter spp./Arcobacter spp. and patients with ulcerative colitis. Eur J Gastroenterol Hepatol. 2018;30(5):531–538. doi: 10.1097/MEG.0000000000001095. PubMed DOI

Kanareykina SK, Misautova AA, Zlatkina AR, Levina EN. Proteus dysbioses in patients with ulcerative colitis. Food Nahr. 1987;31(5–6):557–561. doi: 10.1002/food.19870310570. PubMed DOI

Kushkevych I. Etiological Role of Sulfate-Reducing Bacteria in the Development of Inflammatory Bowel Diseases and Ulcerative Colitis. Am J Infect Dis Microbiol. 2014;2(3):63–73. doi: 10.12691/ajidm-2-3-5. DOI

Seishima J, Iida N, Kitamura K, Yutani M, Wang Z, Seki A, Yamashita T, Sakai Y, Honda M, Yamashita T, Kagaya T, Shirota Y, Fujinaga Y, Mizukoshi E, Kaneko S. Gut-derived Enterococcus faecium from ulcerative colitis patients promotes colitis in a genetically susceptible mouse host. Genome Biol. 2019;20(1):252. doi: 10.1186/s13059-019-1879-9. PubMed DOI PMC

Leccese G, Bibi A, Mazza S, Facciotti F, Caprioli F, Landini P, Paroni M. Probiotic Lactobacillus and Bifidobacterium Strains Counteract Adherent-Invasive Escherichia coli (AIEC) Virulence and Hamper IL-23/Th17 Axis in Ulcerative Colitis, but Not in Crohn's Disease. Cells. 2020;9(8):1824. doi: 10.3390/cells9081824. PubMed DOI PMC

Harris KG, Chang EB. The intestinal microbiota in the pathogenesis of inflammatory bowel diseases: new insights into complex disease. Clin Sci. 2018;132(18):2013–2028. doi: 10.1042/CS20171110. PubMed DOI PMC

Forbes JD, Van Domselaar G, Bernstein CN. Microbiome Survey of the Inflamed and Noninflamed Gut at Different Compartments Within the Gastrointestinal Tract of Inflammatory Bowel Disease Patients. Inflamm Bowel Dis. 2016;22(4):817–825. doi: 10.1097/MIB.0000000000000684. PubMed DOI

Russo E, Cinci L, Di Gloria L, Baldi S, D'Ambrosio M, Nannini G, Bigagli E, Curini L, Pallecchi M, Andrea Arcese D, Scaringi S, Malentacchi C, Bartolucci G, Ramazzotti M, Luceri C, Amedei A, Giudici F. Crohn's disease recurrence updates: first surgery vs. surgical relapse patients display different profiles of ileal microbiota and systemic microbial-associated inflammatory factors. Front Immunol. 2022;13:886468. doi: 10.3389/fimmu.2022.886468. PubMed DOI PMC

Borrel G, Brugère J-F, Gribaldo S, Schmitz RA, Moissl-Eichinger C. The host-associated archaeome. Nat Rev Microbiol. 2020;18(11):622–636. doi: 10.1038/s41579-020-0407-y. PubMed DOI

Houshyar Y, Massimino L, Lamparelli LA, Danese S, Ungaro F. Going Beyond Bacteria: Uncovering the Role of Archaeome and Mycobiome in Inflammatory Bowel Disease. Front Physiol. 2021;12:783295. doi: 10.3389/fphys.2021.783295. PubMed DOI PMC

Campieri M. Bacteria as the cause of ulcerative colitis. Gut. 2001;48(1):132–135. doi: 10.1136/gut.48.1.132. PubMed DOI PMC

Onderdonk AB, Bronson R, Cisneros R. Comparison of Bacteroides vulgatus strains in the enhancement of experimental ulcerative colitis. Infect Immun. 1987;55(3):835–836. doi: 10.1128/iai.55.3.835-836.1987. PubMed DOI PMC

Rath HC, Ikeda JS, Linde HJ, Schölmerich J, Wilson KH, Sartor RB. Varying cecal bacterial loads influences colitis and gastritis in HLA-B27 transgenic rats. Gastroenterology. 1999;116(2):310–319. doi: 10.1016/S0016-5085(99)70127-7. PubMed DOI

Ehrhardt RO, Lúdvíksson BR, Gray B, Neurath M, Strober W. Induction and prevention of colonic inflammation in IL-2-deficient mice. J Immunol Baltim Md 1950. 1997;158(2):566–573. PubMed

Kühn R, Löhler J, Rennick D, Rajewsky K, Müller W. Interleukin-10-deficient mice develop chronic enterocolitis. Cell. 1993;75(2):263–274. doi: 10.1016/0092-8674(93)80068-P. PubMed DOI

LeBlanc J-F, Segal JP, de Campos Braz LM, Hart AL. The Microbiome as a Therapy in Pouchitis and Ulcerative Colitis. Nutrients. 2021;13(6):1780. doi: 10.3390/nu13061780. PubMed DOI PMC

Sankarasubramanian J, Ahmad R, Avuthu N, Singh AB, Guda C. Gut Microbiota and Metabolic Specificity in Ulcerative Colitis and Crohn's Disease. Front Med. 2020;7:606298. doi: 10.3389/fmed.2020.606298. PubMed DOI PMC

Kuever J, Rainey FA, Widdel F. In: Bergey's Manual® Syst. Bacteriol. Brenner DJ, Krieg NR, Staley JT, editors. Springer US; Boston, MA: 2005. Class IV. Deltaproteobacteria class nov. pp. 922–1144.

Feng Z, Long W, Hao B, Ding D, Ma X, Zhao L, Pang X. A human stool-derived Bilophila wadsworthia strain caused systemic inflammation in specific-pathogen-free mice. Gut Pathog. 2017;9(1):59. doi: 10.1186/s13099-017-0208-7. PubMed DOI PMC

Laue H, Denger K, Cook AM. Taurine reduction in anaerobic respiration of Bilophila wadsworthia RZATAU. Appl Environ Microbiol. 1997;63(5):2016–2021. doi: 10.1128/aem.63.5.2016-2021.1997. PubMed DOI PMC

Laue H, Smits THM, Schumacher UK, Claros MC, Hartemink R, Cook AM. Identification of Bilophila wadsworthia by specific PCR which targets the taurine:pyruvate aminotransferase gene. FEMS Microbiol Lett. 2006;261(1):74–79. doi: 10.1111/j.1574-6968.2006.00335.x. PubMed DOI

Burrichter AG, Dörr S, Bergmann P, Haiβ S, Keller A, Fournier C, Franchini P, Isono E, Schleheck D. Bacterial microcompartments for isethionate desulfonation in the taurine-degrading human-gut bacterium Bilophila wadsworthia. BMC Microbiol. 2021;21(1):340. doi: 10.1186/s12866-021-02386-w. PubMed DOI PMC

Hanson BT, Dimitri Kits K, Löffler J, Burrichter AG, Fiedler A, Denger K, Frommeyer B, Herbold CW, Rattei T, Karcher N, Segata N, Schleheck D, Loy A. Sulfoquinovose is a select nutrient of prominent bacteria and a source of hydrogen sulfide in the human gut. ISME J. 2021;15(9):2779–2791. doi: 10.1038/s41396-021-00968-0. PubMed DOI PMC

Kovac J, Kushkevych I. MendelNet 2017. Mendel Univ Brno, Fac AgriSciences; Brno, Brno: 2019. New modification of cultivation medium for isolation and growth of intestinal sulfate-reducing bacteria. pp. 702–707.

Pichler M, Coskun ÖK, Ortega-Arbulú A, Conci N, Wörheide G, Vargas S, Orsi WD. A 16S rRNA gene sequencing and analysis protocol for the Illumina MiniSeq platform. MicrobiologyOpen. 2018;7(6):e00611. doi: 10.1002/mbo3.611. PubMed DOI PMC

Nossa CW. Design of 16S rRNA gene primers for 454 pyrosequencing of the human foregut microbiome. World J Gastroenterol. 2010;16(33):4135. doi: 10.3748/wjg.v16.i33.4135. PubMed DOI PMC

Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: High–resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13(7):581–583. doi: 10.1038/nmeth.3869. PubMed DOI PMC

Callahan BJ, Sankaran K, Fukuyama JA, McMurdie PJ, Holmes SP. Bioconductor Workflow for Microbiome Data Analysis: from raw reads to community analyses. F1000Research. 2016;5:1492. doi: 10.12688/f1000research.8986.2. PubMed DOI PMC

Wang Q, Garrity GM, Tiedje JM, Cole JR. Naïve Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy. Appl Environ Microbiol. 2007;73(16):5261–5267. doi: 10.1128/AEM.00062-07. PubMed DOI PMC

Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2012;41(D1):D590–D596. doi: 10.1093/nar/gks1219. PubMed DOI PMC

Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. PubMed DOI

Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol. 2016;33(7):1870–1874. doi: 10.1093/molbev/msw054. PubMed DOI PMC

Kushkevych I, Vítězová M, Vítěz T, Bartoš M. Production of biogas: relationship between methanogenic and sulfate-reducing microorganisms. Open Life Sci. 2017;12(1):82–91. doi: 10.1515/biol-2017-0009. DOI

Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. Clustal W and Clustal X version 2.0. Bioinformatics. 2007;23(21):2947–2948. doi: 10.1093/bioinformatics/btm404. PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...