Pre-colonization with the commensal fungus Candida albicans reduces murine susceptibility to Clostridium difficile infection

References

• Lessa FC, Mu Y, Bamberg WM, Beldavs ZG, Dumyati GK, Dunn JR, Farley MM, Holzbauer SM, Meek JI, Phipps EC, et al. Burden of Clostridium difficile infection in the United States. N Engl J Med. 2015;372:825–34. doi:10.1056/NEJMoa1408913. PMID:25714160.
   PubMed Web of Science ®Google Scholar
• Schenck L P, Beck P L, MacDonald J A. Gastrointestinal dysbiosis and the use of fecal microbial transplantation in Clostridium difficile infection. World J Gastrointest Pathophysiol. 2015;6:169–80. doi:10.4291/wjgp.v6.i4.169. PMID:26600975.
   PubMedGoogle Scholar
• Solomon K. The host immune response to Clostridium difficile infection. Ther Adv Infect Dis. 2013;1:19–35. doi:10.1177/2049936112472173. PMID:25165542.
   PubMedGoogle Scholar
• Shields K, Araujo-Castillo RV, Theethira TG, Alonso CD, Kelly CP. Recurrent Clostridium difficile infection: From colonization to cure. Anaerobe. 2015;34:59–73. doi:10.1016/j.anaerobe.2015.04.012. PMID:25930686.
   PubMed Web of Science ®Google Scholar
• van Nood E, Vrieze A, Nieuwdorp M, Fuentes S, Zoetendal EG, de Vos WM, Visser CE, Kuijper EJ, Bartelsman JF, Tijssen JG, et al. Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med. 2013;368:407–15. doi:10.1056/NEJMoa1205037. PMID:23323867.
   PubMed Web of Science ®Google Scholar
• Youngster I, Russell GH, Pindar C, Ziv-Baran T, Sauk J, Hohmann EL. Oral, capsulized, frozen fecal microbiota transplantation for relapsing Clostridium difficile infection. JAMA. 2014;312:1772–8. doi:10.1001/jama.2014.13875. PMID:25322359.
   PubMed Web of Science ®Google Scholar
• Kassam Z, Lee CH, Yuan Y, Hunt RH. Fecal microbiota transplantation for Clostridium difficile infection: systematic review and meta-analysis. Am J Gastroenterol. 2013;108:500–8. doi:10.1038/ajg.2013.59. PMID:23511459.
   PubMed Web of Science ®Google Scholar
• Li YT, Cai HF, Wang ZH, Xu J, Fang JY. Systematic review with meta-analysis: long-term outcomes of faecal microbiota transplantation for Clostridium difficile infection. Aliment Pharmacol Ther. 2016;43:445–57. doi:10.1111/apt.13492.
   Web of Science ®Google Scholar
• De Leon LM, Watson JB, Kelly CR. Transient flare of ulcerative colitis after fecal microbiota transplantation for recurrent Clostridium difficile infection. Clin Gastroenterol Hepatol. 2013;11:1036–8. doi:10.1016/j.cgh.2013.04.045. PMID:23669309.
   PubMed Web of Science ®Google Scholar
• Alang N, Kelly CR. Weight gain after fecal microbiota transplantation. Open Forum Infect Dis. 2015;2:ofv004. doi:10.1093/ofid/ofv004. PMID:26034755.
   PubMed Web of Science ®Google Scholar
• Erb Downward JR, Falkowski NR, Mason KL, Muraglia R, Huffnagle GB. Modulation of post-antibiotic bacterial community reassembly and host response by Candida albicans. Sci Rep. 2013;3:2191. doi:10.1038/srep02191. PMID:23846617.
   PubMed Web of Science ®Google Scholar
• De Luca A, Montagnoli C, Zelante T, Bonifazi P, Bozza S, Moretti S, D'Angelo C, Vacca C, Boon L, Bistoni F, et al. Functional yet balanced reactivity to Candida albicans requires TRIF, MyD88, and IDO-dependent inhibition of Rorc. J Immunol. 2007;179:5999–6008. doi:10.4049/jimmunol.179.9.5999. PMID:17947673.
   PubMed Web of Science ®Google Scholar
• Zelante T, De Luca A, Bonifazi P, Montagnoli C, Bozza S, Moretti S, Belladonna ML, Vacca C, Conte C, Mosci P, et al. IL-23 and the Th17 pathway promote inflammation and impair antifungal immune resistance. Eur J Immunol. 2007;37:2695–706. doi:10.1002/eji.200737409. PMID:17899546.
   PubMed Web of Science ®Google Scholar
• Zelante T, Iannitti RG, 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;39:372–85. doi:10.1016/j.immuni.2013.08.003. PMID:23973224.
   PubMed Web of Science ®Google Scholar
• Carvalho A, Giovannini G, De Luca A, D'Angelo C, Casagrande A, Iannitti R G, Ricci G, Cunha C, Romani L. Dectin-1 isoforms contribute to distinct Th1/Th17 cell activation in mucosal candidiasis. Cell Mol Immunol. 2012;9:276–86. doi:10.1038/cmi.2012.1. PMID:22543832.
   PubMed Web of Science ®Google Scholar
• De Luca A, Zelante T, D'Angelo C, Zagarella S, Fallarino F, Spreca A, Iannitti RG, Bonifazi P, Renauld J C, Bistoni F, et al. IL-22 defines a novel immune pathway of antifungal resistance. Mucosal Immunol. 2010;3:361–73. doi:10.1038/mi.2010.22. PMID:20445503.
   PubMed Web of Science ®Google Scholar
• Quintin J, Saeed S, Martens JH, Giamarellos-Bourboulis EJ, Ifrim DC, Logie C, Jacobs L, Jansen T, Kullberg BJ, Wijmenga C, et al. Candida albicans infection affords protection against reinfection via functional reprogramming of monocytes. Cell Host Microbe. 2012;12:223–32. doi:10.1016/j.chom.2012.06.006. PMID:22901542.
   PubMed Web of Science ®Google Scholar
• Reeves A E, Theriot CM, Bergin IL, Huffnagle GB, Schloss PD, Young VB. The interplay between microbiome dynamics and pathogen dynamics in a murine model of Clostridium difficile Infection. Gut Microbes. 2011;2:145–58. doi:10.4161/gmic.2.3.16333. PMID:21804357.
   PubMedGoogle Scholar
• Sorg J A, Sonenshein AL. Inhibiting the initiation of Clostridium difficile spore germination using analogs of chenodeoxycholic acid, a bile acid. J Bacteriol. 2010;192:4983–90. doi:10.1128/JB.00610-10. PMID:20675492.
   PubMed Web of Science ®Google Scholar
• Shen A. Clostridium difficile toxins: mediators of inflammation. J Innate Immun. 2012;4:149–58. doi:10.1159/000332946. PMID:22237401.
   PubMed Web of Science ®Google Scholar
• Yang G, Zhou B, Wang J, He X, Sun X, Nie W, Tzipori S, Feng H. Expression of recombinant Clostridium difficile toxin A and B in Bacillus megaterium. BMC Microbiol. 2008;8:192. doi:10.1186/1471-2180-8-192. PMID:18990232.
   PubMed Web of Science ®Google Scholar
• Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335–6. doi:10.1038/nmeth.f.303. PMID:20383131.
   PubMed Web of Science ®Google Scholar
• Schubert A M, Sinani H, Schloss PD. Antibiotic-Induced Alterations of the Murine Gut Microbiota and Subsequent Effects on Colonization Resistance against Clostridium difficile. MBio. 2015;6:e00974. doi:10.1128/mBio.00974-15.
   PubMed Web of Science ®Google Scholar
• Schubert AM, Rogers MA, Ring C, Mogle J, Petrosino JP, Young VB, Aronoff DM, Schloss PD. Microbiome data distinguish patients with Clostridium difficile infection and non-C. difficile-associated diarrhea from healthy controls. MBio. 2014;5:e01021–01014. doi:10.1128/mBio.01021-14. PMID:24803517.
   PubMed Web of Science ®Google Scholar
• Shahinas D, Silverman M, Sittler T, Chiu C, Kim P, Allen-Vercoe E, Weese S, Wong A, Low DE, Pillai DR. Toward an understanding of changes in diversity associated with fecal microbiome transplantation based on 16S rRNA gene deep sequencing. MBio. 2012;3:e00338–12. doi:10.1128/mBio.00338-12. PMID:23093385.
   PubMed Web of Science ®Google Scholar
• Buffie CG, Bucci V, Stein RR, McKenney PT, Ling L, Gobourne A, No D, Liu H, Kinnebrew M, Viale A, et al. Precision microbiome reconstitution restores bile acid mediated resistance to Clostridium difficile. Nature. 2015;517:205–8. doi:10.1038/nature13828. PMID:25337874.
   PubMed Web of Science ®Google Scholar
• Reeves AE, Koenigsknecht MJ, Bergin IL, Young VB. Suppression of Clostridium difficile in the gastrointestinal tracts of germfree mice inoculated with a murine isolate from the family Lachnospiraceae. Infect Immun. 2012;80:3786–94. doi:10.1128/IAI.00647-12. PMID:22890996.
   PubMed Web of Science ®Google Scholar
• Manian FA, Bryant A. Does Candida species overgrowth protect against Clostridium difficile infection?. Clin Infect Dis. 2013;56:464–5. doi:10.1093/cid/cis854. PMID:23042967.
   PubMed Web of Science ®Google Scholar
• Nerandzic MM, Mullane K, Miller MA, Babakhani F, Donskey CJ. Reduced acquisition and overgrowth of vancomycin-resistant enterococci and Candida species in patients treated with fidaxomicin versus vancomycin for Clostridium difficile infection. Clin Infect Dis. 2012;55(2):S121–126. doi:10.1093/cid/cis440. PMID:22752860.
   PubMedGoogle Scholar
• Blanco N, Walk S, Malani AN, Rickard A, Benn M, Eisenberg M, Zhang M, Foxman B. Clostridium difficile shows no trade-off between toxin and spore production within the human host. J Med Microbiol. 2018;67:631–640. doi:10.1099/jmm.0.000719. PMID:29533173.
   PubMed Web of Science ®Google Scholar
• Kumamoto CA. Inflammation and gastrointestinal Candida colonization. Curr Opin Microbiol. 2011;14:386–91. doi:10.1016/j.mib.2011.07.015. PMID:21802979.
   PubMed Web of Science ®Google Scholar
• Hsu MS, Wang JT, Huang WK, Liu YC, Chang SC. Prevalence and clinical features of Clostridium difficile-associated diarrhea in a tertiary hospital in northern Taiwan. J Microbiol Immunol Infect. 2006;39:242–8. PMID:
   PubMedGoogle Scholar
• McFarland LV. Deciphering meta-analytic results: a mini-review of probiotics for the prevention of paediatric antibiotic-associated diarrhoea and Clostridium difficile infections. Benef Microbes. 2015;6:189–94. doi:10.3920/BM2014.0034. PMID:24889895.
   PubMed Web of Science ®Google Scholar
• Johnson S, Maziade PJ, McFarland LV, Trick W, Donskey C, Currie B, Low DE, Goldstein EJ. Is primary prevention of Clostridium difficile infection possible with specific probiotics?. Int J Infect Dis. 2012;16:e786–792. doi:10.1016/j.ijid.2012.06.005. PMID:22863358.
   PubMed Web of Science ®Google Scholar
• O'Horo JC, Jindai K, Kunzer B, Safdar N. Treatment of recurrent Clostridium difficile infection: a systematic review. Infection. 2014;42:43–59. doi:10.1007/s15010-013-0496-x. PMID:23839210.
   PubMed Web of Science ®Google Scholar
• Raponi G, Visconti V, Brunetti G, Ghezzi M C. Clostridium difficile infection and Candida colonization of the gut: is there a correlation?. Clin Infect Dis. 2014;59:1648–9. doi:10.1093/cid/ciu637. PMID:25091308.
   PubMed Web of Science ®Google Scholar
• Nakagawa T, Mori N, Kajiwara C, Kimura S, Akasaka Y, Ishii Y, Saji T, Tateda K. Endogenous IL-17 as a factor determining the severity of Clostridium difficile infection in mice. J Med Microbiol. 2016;65:821–7. doi:10.1099/jmm.0.000273. PMID:27166143.
   PubMed Web of Science ®Google Scholar
• Hasegawa M, Yada S, Liu MZ, Kamada N, Munoz-Planillo R, Do N, Nunez G, Inohara N. Interleukin-22 regulates the complement system to promote resistance against pathobionts after pathogen-induced intestinal damage. Immunity. 2014;41:620–32. doi:10.1016/j.immuni.2014.09.010. PMID:25367575.
   PubMed Web of Science ®Google Scholar
• Wang L, Cao J, Li C, Zhang L. IL-27/IL-27receptor signaling provides protection in Clostridium difficile-induced colitis. J Infect Dis. 2018;217:198–207. doi:10.1093/infdis/jix581.
   Web of Science ®Google Scholar
• Buonomo EL, Cowardin CA, Wilson MG, Saleh MM, Pramoonjago P, Petri WA, Jr. Microbiota-Regulated IL-25 Increases Eosinophil Number to Provide Protection during Clostridium difficile Infection. Cell Rep. 2016;16:432–43. doi:10.1016/j.celrep.2016.06.007. PMID:27346351.
   PubMed Web of Science ®Google Scholar
• Rubino SJ, Geddes K, Girardin SE. Innate IL-17 and IL-22 responses to enteric bacterial pathogens. Trends Immunol. 2012;33:112–8. doi:10.1016/j.it.2012.01.003. PMID:22342740.
   PubMed Web of Science ®Google Scholar
• Lee JS, Tato CM, Joyce-Shaikh B, Gulan F, Cayatte C, Chen Y, Blumenschein WM, Judo M, Ayanoglu G, McClanahan TK, et al. Interleukin-23-Independent IL-17 Production Regulates Intestinal Epithelial Permeability. Immunity. 2015;43:727–38. doi:10.1016/j.immuni.2015.09.003. PMID:26431948.
   PubMed Web of Science ®Google Scholar
• Caplan MS, Miller-Catchpole R, Kaup S, Russell T, Lickerman M, Amer M, Xiao Y, Thomson R, Jr. Bifidobacterial supplementation reduces the incidence of necrotizing enterocolitis in a neonatal rat model. Gastroenterology. 1999;117:577–83. doi:10.1016/S0016-5085(99)70450-6. PMID:10464133.
   PubMed Web of Science ®Google Scholar
• Fanning S, Hall LJ, Cronin M, Zomer A, MacSharry J, Goulding D, Motherway MO, Shanahan F, Nally K, Dougan G, et al. Bifidobacterial surface-exopolysaccharide facilitates commensal-host interaction through immune modulation and pathogen protection. Proc Natl Acad Sci U S A. 2012;109:2108–13. doi:10.1073/pnas.1115621109. PMID:22308390.
   PubMed Web of Science ®Google Scholar
• O'Hara A M, O'Regan P, Fanning A, O'Mahony C, Macsharry J, Lyons A, Bienenstock J, O'Mahony L, Shanahan F. Functional modulation of human intestinal epithelial cell responses by Bifidobacterium infantis and Lactobacillus salivarius. Immunology. 2006;118:202–15. doi:10.1111/j.1365-2567.2006.02358.x. PMID:16771855.
   PubMed Web of Science ®Google Scholar
• Underwood MA, Arriola J, Gerber CW, Kaveti A, Kalanetra KM, Kananurak A, Bevins CL, Mills DA, Dvorak B. Bifidobacterium longum subsp. infantis in experimental necrotizing enterocolitis: alterations in inflammation, innate immune response, and the microbiota. Pediatr Res. 2014;76:326–33. doi:10.1038/pr.2014.102. PMID:25000347.
   PubMed Web of Science ®Google Scholar
• Wang H, Zhang W, Zuo L, Zhu W, Wang B, Li Q, Li J. Bifidobacteria may be beneficial to intestinal microbiota and reduction of bacterial translocation in mice following ischaemia and reperfusion injury. Br J Nutr. 2013;109:1990–8. doi:10.1017/S0007114512004308. PMID:23122253.
   PubMed Web of Science ®Google Scholar
• Derrien M, Vaughan E E, Plugge C M, de Vos W M. Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. Int J Syst Evol Microbiol. 2004;54:1469–76. doi:10.1099/ijs.0.02873-0. PMID:15388697.
   PubMed Web of Science ®Google Scholar
• Kang C S, Ban M, Choi EJ, Moon HG, Jeon JS, Kim DK, Park SK, Jeon SG, Roh TY, Myung SJ, et al. Extracellular vesicles derived from gut microbiota, especially Akkermansia muciniphila, protect the progression of dextran sulfate sodium-induced colitis. PLoS One. 2013;8:e76520. doi:10.1371/journal.pone.0076520. PMID:24204633.
   PubMed Web of Science ®Google Scholar
• Reunanen J, Kainulainen V, Huuskonen L, Ottman N, Belzer C, Huhtinen H, de Vos W M, Satokari R. Akkermansia muciniphila Adheres to Enterocytes and Strengthens the Integrity of the Epithelial Cell Layer. Appl Environ Microbiol. 2015;81:3655–62. doi:10.1128/AEM.04050-14. PMID:25795669.
   PubMed Web of Science ®Google Scholar
• Derrien M, Van Baarlen P, Hooiveld G, Norin E, Muller M, de Vos W M. Modulation of Mucosal Immune Response, Tolerance, and Proliferation in Mice Colonized by the Mucin-Degrader Akkermansia muciniphila. Front Microbiol. 2011;2:166. doi:10.3389/fmicb.2011.00166. PMID:21904534.
   PubMed Web of Science ®Google Scholar
• van Leeuwen PT, van der Peet JM, Bikker FJ, Hoogenkamp M, Oliveira Paiva AM, Kostidis S, Mayboroda OA, Smits WK, Krom BP. Interspecies Interactions between Clostridium difficile and Candida albicans. mSphere. 2016;1:e00187–00116. doi:10.1128/mSphere.00187-16. PMID:27840850.
   PubMed Web of Science ®Google Scholar
• Brown DH, Jr., Giusani AD, Chen X, Kumamoto CA. Filamentous growth of Candida albicans in response to physical environmental cues and its regulation by the unique CZF1 gene. Mol Microbiol. 1999;34:651–62. doi:10.1046/j.1365-2958.1999.01619.x. PMID:10564506.
   PubMed Web of Science ®Google Scholar
• Sherman F. Getting started with yeast. Methods Enzymol. 1991;194:3–21. doi:10.1016/0076-6879(91)94004-V. PMID:2005794.
   PubMed Web of Science ®Google Scholar
• Sorg JA, Sonenshein AL. Bile salts and glycine as cogerminants for Clostridium difficile spores. J Bacteriol. 2008;190:2505–12. doi:10.1128/JB.01765-07. PMID:18245298.
   PubMed Web of Science ®Google Scholar
• Wilson KH, Kennedy MJ, Fekety FR. Use of sodium taurocholate to enhance spore recovery on a medium selective for Clostridium difficile. J Clin Microbiol. 1982;15:443–6. PMID:
   PubMed Web of Science ®Google Scholar
• Caporaso JG, Lauber CL, WaltersWA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 2012;6:1621–4. doi:10.1038/ismej.2012.8. PMID:22402401.
   PubMed Web of Science ®Google Scholar