Dysbiotic but nonpathogenic shift in the fecal mycobiota of patients with rheumatoid arthritis

References

• Epstein FH, Harris ,ED. Rheumatoid arthritis: pathophysiology and implications for therapy. New Engl J Med. 1990;322(18):1277–16. doi:10.1056/NEJM199005033221805.
   PubMed Web of Science ®Google Scholar
• Klareskog L, Catrina AI, Paget S. Rheumatoid arthritis. Lancet. 2009;373:659–672.
   PubMed Web of Science ®Google Scholar
• Smolen JS, Aletaha D, Barton A, Burmester GR, Emery P, Firestein GS, Kavanaugh A, McInnes IB, Solomon DH, Strand V, et al. Rheumatoid arthritis. Nat Rev Dis Primers. 2018;4:18001.
   PubMed Web of Science ®Google Scholar
• Tsuchiya Y, Takayanagi N, Sugiura H, Miyahara Y, Tokunaga D, Kawabata Y, Sugita Y. Lung diseases directly associated with rheumatoid arthritis and their relationship to outcome. Eur Respir J. 2011;37:1411–1417.
   PubMed Web of Science ®Google Scholar
• Solomon DH, Goodson NJ, Katz JN, Weinblatt ME, Avorn J, Setoguchi S, Canning C, Schneeweiss S. Patterns of cardiovascular risk in rheumatoid arthritis. Ann Rheum Dis. 2006;65:1608–1612.
   PubMed Web of Science ®Google Scholar
• He J, Ding Y, Feng M, Guo J, Sun X, Zhao J, Yu D, Li Z. Characteristics of Sjögren’s syndrome in rheumatoid arthritis. Rheumatology. 2013;52:1084–1089.
   PubMed Web of Science ®Google Scholar
• Haugeberg G, Uhlig T, Falch JA, Halse JI, Kvien TK. Bone mineral density and frequency of osteoporosis in female patients with rheumatoid arthritis: results from 394 patients in the Oslo county rheumatoid arthritis register. Arthritis Rheumatol. 2000;43:522–530.
   PubMed Web of Science ®Google Scholar
• McInnes IB, Schett G. The pathogenesis of rheumatoid arthritis. New Engl J Med. 2011;365:2205–2219.
   PubMed Web of Science ®Google Scholar
• Stahl EA, Raychaudhuri S, Remmers EF, Xie G, Eyre S, Thomson BP, Li Y, Kurreeman FA, Zhernakova A, Hinks A. Genome-wide association study meta-analysis identifies seven new rheumatoid arthritis risk loci. Nat Genet. 2010;42:508.
   PubMed Web of Science ®Google Scholar
• Bae S-C. Epidemiology and etiology of rheumatoid arthritis. J Korean Med Assoc. 2010;53:843–852.
   Web of Science ®Google Scholar
• Okada Y, Wu D, Trynka G, Raj T, Terao C, Ikari K, Kochi Y, Ohmura K, Suzuki A, Yoshida S. Genetics of rheumatoid arthritis contributes to biology and drug discovery. Nature. 2014;506:376–381.
   PubMed Web of Science ®Google Scholar
• Li S, Yu Y, Yue Y, Zhang Z, Su K. Microbial infection and rheumatoid arthritis. J Clin Cell Immunol. 2013;4(6):1–6.
   Google Scholar
• Zhang X, Zhang D, Jia H, Feng Q, Wang D, Liang D, Wu X, Li J, Tang L, Li Y. The oral and gut microbiomes are perturbed in rheumatoid arthritis and partly normalized after treatment. Nat Med. 2015;21:895–905.
   PubMed Web of Science ®Google Scholar
• H-J W, Ivanov II, Darce J, Hattori K, Shima T, Umesaki Y, DR L, Benoist C, Mathis D. Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity. 2010;32:815–827.
   PubMed Web of Science ®Google Scholar
• Maeda Y, Takeda K. Host–microbiota interactions in rheumatoid arthritis. Exp Mol Med. 2019;51:1–6.
   PubMed Web of Science ®Google Scholar
• Maeda Y, Kurakawa T, Umemoto E, Motooka D, Ito Y, Gotoh K, Hirota K, Matsushita M, Furuta Y, Narazaki M. Dysbiosis contributes to arthritis development via activation of autoreactive T cells in the intestine. Arthritis Rheumatol. 2016;68:2646–2661.
   PubMed Web of Science ®Google Scholar
• Picchianti-Diamanti A, Panebianco C, Salemi S, Sorgi ML, Di Rosa R, Tropea A, Sgrulletti M, Salerno G, Terracciano F, D’amelio R. Analysis of gut microbiota in rheumatoid arthritis patients: disease-related dysbiosis and modifications induced by etanercept. Int J Mol Sci. 2018;19:2938.
   PubMed Web of Science ®Google Scholar
• Chen J, Wright K, Davis JM, Jeraldo P, Marietta EV, Murray J, Nelson H, Matteson EL, Taneja V. An expansion of rare lineage intestinal microbes characterizes rheumatoid arthritis. Genome Med. 2016;8:1–14.
   PubMed Web of Science ®Google Scholar
• Rooney CM, Mankia K, Mitra S, Moura IB, Emery P, Wilcox MH. Perturbations of the gut microbiome in anti-CCP positive individuals at risk of developing rheumatoid arthritis. Rheumatology. 2021;60:3380–3387.
   PubMed Web of Science ®Google Scholar
• Chiang H-I, J-R L, Liu -C-C, Liu P-Y, Chen -H-H, Chen Y-M, Lan J-L, Chen D-Y. An association of gut microbiota with different phenotypes in Chinese patients with rheumatoid arthritis. J Clin Med. 2019;8:1770.
   PubMed Web of Science ®Google Scholar
• Yoshitomi H, Sakaguchi N, Kobayashi K, Brown GD, Tagami T, Sakihama T, Hirota K, Tanaka S, Nomura T, Miki I. A role for fungal β-glucans and their receptor Dectin-1 in the induction of autoimmune arthritis in genetically susceptible mice. J Exp Med. 2005;201:949–960.
   PubMed Web of Science ®Google Scholar
• Sun X, Wang Y, Li X, Wang M, Dong J, Tang W, Lei Z, Guo Y, Li M, Li Y. Alterations of gut fungal microbiota in patients with rheumatoid arthritis. PeerJ. 2022;10:e13037.
   PubMed Web of Science ®Google Scholar
• Artacho A, Isaac S, Nayak R, Flor‐Duro A, Alexander M, Koo I, Manasson J, Smith PB, Rosenthal P, Homsi Y. The pretreatment gut microbiome is associated with lack of response to methotrexate in new‐onset rheumatoid arthritis. Arthritis Rheumatol. 2021;73:931–942.
   PubMed Web of Science ®Google Scholar
• Jeong Y, Kim J-W, You HJ, Park S-J, Lee J, Ju JH, Park MS, Jin H, Cho M-L, Kwon B. Gut microbial composition and function are altered in patients with early rheumatoid arthritis. J Clin Med. 2019;8:693.
   PubMed Web of Science ®Google Scholar
• Liu Z, Wu Y, Luo Y, Wei S, Lu C, Zhou Y, Wang J, Miao T, Lin H, Zhao Y. Self-balance of intestinal flora in spouses of patients with rheumatoid arthritis. Front Med. 2020;7:538–549.
   Web of Science ®Google Scholar
• Sam QH, Chang MW, Chai LYA. The fungal mycobiome and its interaction with gut bacteria in the host. Int J Mol Sci. 2017;18:330.
   PubMed Web of Science ®Google Scholar
• Deveau A, Bonito G, Uehling J, Paoletti M, Becker M, Bindschedler S, Hacquard S, Hervé V, Labbé J, Lastovetsky OA. Bacterial–fungal interactions: ecology, mechanisms and challenges. FEMS Microbiol Rev. 2018;42:335–352.
   PubMed Web of Science ®Google Scholar
• van Tilburg Bernardes E, Pettersen VK, Gutierrez MW, Laforest-Lapointe I, Jendzjowsky NG, Cavin J-B, Vicentini FA, Keenan CM, Ramay HR, Samara J. Intestinal fungi are causally implicated in microbiome assembly and immune development in mice. Nat Commun. 2020;11:1–16.
   PubMed Web of Science ®Google Scholar
• Kumar A, Asthana M, Gupta A, Nigam D, Mahajan S. 2018. Secondary metabolism and antimicrobial metabolites of Penicillium. In: Gupta V, editor. New and future developments in microbial biotechnology and bioengineering. Amsterdam, The Netherlands: Elsevier; p. 47–68.
   Google Scholar
• Mangalea MR, Paez-Espino D, Kieft K, Chatterjee A, Chriswell ME, Seifert JA, Feser ML, Demoruelle MK, Sakatos A, Anantharaman K. Individuals at risk for rheumatoid arthritis harbor differential intestinal bacteriophage communities with distinct metabolic potential. Cell Host Microbe. 2021;29:726–739. e725.
   PubMed Web of Science ®Google Scholar
• Nash AK, Auchtung TA, Wong MC, Smith DP, Gesell JR, Ross MC, Stewart CJ, Metcalf GA, Muzny DM, Gibbs RA. The gut mycobiome of the human microbiome project healthy cohort. Microbiome. 2017;5:1–13.
   PubMed Web of Science ®Google Scholar
• Wu X, Xia Y, He F, Zhu C, Ren W. Intestinal mycobiota in health and diseases: from a disrupted equilibrium to clinical opportunities. Microbiome. 2021;9:1–18.
   PubMed Web of Science ®Google Scholar
• Hallen-Adams HE, Suhr MJ. Fungi in the healthy human gastrointestinal tract. Virulence. 2017;8:352–358.
   PubMed Web of Science ®Google Scholar
• Suhr MJ, Banjara N, Hallen‐Adams HE. Sequence‐based methods for detecting and evaluating the human gut mycobiome. Lett Appl Microbiol. 2016;62:209–215.
   PubMed Web of Science ®Google Scholar
• Motooka D, Fujimoto K, Tanaka R, Yaguchi T, Gotoh K, Maeda Y, Furuta Y, Kurakawa T, Goto N, Yasunaga T. Fungal ITS1 deep-sequencing strategies to reconstruct the composition of a 26-species community and evaluation of the gut mycobiota of healthy Japanese individuals. Front Microbiol. 2017;8:238.
   PubMed Web of Science ®Google Scholar
• Qiu X, Zhao X, Cui X, Mao X, Tang N, Jiao C, Wang D, Zhang Y, Ye Z, Zhang H. Characterization of fungal and bacterial dysbiosis in young adult Chinese patients with Crohn’s disease. Therap Adv Gastroenterol. 2020;13:1756284820971202.
   Web of Science ®Google Scholar
• Gurleen K, Savio R. Prevalence of candida in diarrhoeal stools. IOSR J Dent and Med Sci. 2016;15:47–49.
   Google Scholar
• Limon JJ, Skalski JH, Underhill DM. Commensal fungi in health and disease. Cell Host Microbe. 2017;22:156–165.
   PubMed Web of Science ®Google Scholar
• Li Q, Wang C, Tang C, He Q, Li N, Li J. Dysbiosis of gut fungal microbiota is associated with mucosal inflammation in Crohn’s disease. J Clin Gastroenterol. 2014;48:513.
   PubMed Web of Science ®Google Scholar
• Sokol H, Leducq V, Aschard H, Pham H-P, Jegou S, Landman C, Cohen D, Liguori G, Bourrier A, Nion-Larmurier I. Fungal microbiota dysbiosis in IBD. Gut. 2017;66:1039–1048.
   PubMed Web of Science ®Google Scholar
• Imai T, Inoue R, Kawada Y, Morita Y, Inatomi O, Nishida A, Bamba S, Kawahara M, Andoh A. Characterization of fungal dysbiosis in Japanese patients with inflammatory bowel disease. J Gastroenterol. 2019;54:149–159.
   PubMed Web of Science ®Google Scholar
• Bishu S, Su EW, Wilkerson ER, Reckley KA, Jones DM, McGeachy MJ, Gaffen SL, Levesque MC. Rheumatoid arthritis patients exhibit impaired Candida albicans-specific Th17 responses. Arthrit Res Ther. 2014;16:1–9.
   Google Scholar
• Aletaha D, Neogi T, Silman AJ, Funovits J, Felson DT, Bingham IIICO, Birnbaum NS, Burmester GR, Bykerk VP, Cohen MD. rheumatoid arthritis classification criteria: an American college of rheumatology/European league against rheumatism collaborative initiative. Arthritis Rheum. 2010;62:2569–2581.
   PubMed Web of Science ®Google Scholar
• Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–583.
   PubMed Web of Science ®Google Scholar
• Rognes T, Flouri T, Nichols B, Quince C, Mahé F. VSEARCH: a versatile open source tool for metagenomics. PeerJ. 2016;4:e2584.
   PubMed Web of Science ®Google Scholar
• 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:D590–596.
   PubMed Web of Science ®Google Scholar
• Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 2011;27:2194–2200.
   PubMed Web of Science ®Google Scholar
• Nilsson RH, Tedersoo L, Ryberg M, Kristiansson E, Hartmann M, Unterseher M, Porter TM, Bengtsson-Palme J, Walker DM, De Sousa F. A comprehensive, automatically updated fungal ITS sequence dataset for reference-based chimera control in environmental sequencing efforts. Microbes Environ. 2015;30:145–150.
   PubMed Web of Science ®Google Scholar
• Bokulich NA, Kaehler BD, Rideout JR, Dillon M, Bolyen E, Knight R, Huttley GA, Caporaso JG. Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2ʹs q2-feature-classifier plugin. Microbiome. 2018;6:1–17.
   PubMed Web of Science ®Google Scholar
• Abarenkov K, Henrik Nilsson R, Larsson KH, Alexander IJ, Eberhardt U, Erland S, Høiland K, Kjøller R, Larsson E, Pennanen T. The UNITE database for molecular identification of fungi–recent updates and future perspectives. New Phytol. 2010;186:281–285.
   PubMed Web of Science ®Google Scholar
• McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One. 2013;8:e61217.
   PubMed Web of Science ®Google Scholar
• R-Core-Team. R: a Language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2017.
   Google Scholar
• Paulson JN, Stine OC, Bravo HC, Pop M. Differential abundance analysis for microbial marker-gene surveys. Nat Methods. 2013;10:1200–1202.
   PubMed Web of Science ®Google Scholar
• Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H. vegan: community ecology package. R package version 2.5-3. 2018.
   Google Scholar
• Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12:R60.
   PubMed Web of Science ®Google Scholar
• Friedman J, Alm EJ. Inferring correlation networks from genomic survey data. PLoS Comput Biol. 2012;8:e1002687.
   PubMed Web of Science ®Google Scholar
• Kurtz ZD, Müller CL, Miraldi ER, Littman DR, Blaser MJ, Bonneau RA. Sparse and compositionally robust inference of microbial ecological networks. PLoS Comput Biol. 2015;11:e1004226.
   PubMed Web of Science ®Google Scholar
• Bastian M, Heymann S, Jacomy M. 2009. Gephi: an open source software for exploring and manipulating networks. Proceedings of the international AAAI conference on web and social media; San Jose, California. 361–362.
   Google Scholar
• Durán P, Thiergart T, Garrido-Oter R, Agler M, Kemen E, Schulze-Lefert P, Hacquard S. Microbial interkingdom interactions in roots promote Arabidopsis survival. Cell. 2018;175:973–983. e914.
   PubMed Web of Science ®Google Scholar
• Csardi G, Nepusz T. The igraph software package for complex network research. Int J Complex Syst. 2006;1695:1–9.
   Google Scholar
• Frykman PK, Nordenskjöld A, Kawaguchi A, Hui TT, Granström AL, Cheng Z, Tang J, Underhill DM, Iliev I, Funari VA, et al. Characterization of bacterial and fungal microbiome in children with Hirschsprung disease with and without a history of enterocolitis: a multicenter study. PLoS One. 2015;10:e0124172–e0124172.
   PubMed Web of Science ®Google Scholar