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Erschienen in: Journal of Gastroenterology 2/2019

26.11.2018 | Original Article—Alimentary Tract

Characterization of fungal dysbiosis in Japanese patients with inflammatory bowel disease

verfasst von: Takayuki Imai, Ryo Inoue, Yuki Kawada, Yasuhiro Morita, Osamu Inatomi, Atsushi Nishida, Shigeki Bamba, Masahiro Kawahara, Akira Andoh

Erschienen in: Journal of Gastroenterology | Ausgabe 2/2019

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Abstract

Background and aims

There are no previous reports describing the fecal fungal microbiome of a Japanese population using advanced molecular techniques. In this study, we performed a molecular analysis on the fungal microbial community of a healthy Japanese population and patients with inflammatory bowel diseases (IBDs).

Patients and methods

Fecal samples were obtained from 18 patients with inactive ulcerative colitis (UC, n = 18), Crohn’s disease (CD, n = 20) and healthy volunteers (n = 20). Bacterial and fungal microbiome was analyzed by sequencing of 16S rRNA and the internal transcribed spacer (ITS) region, respectively.

Results

16S rRNA sequencing of the bacterial microbiome revealed that the α-diversity indicated by the Chao-1 and Shannon indices was significantly lower in CD patients compared to healthy controls and/or UC patients. Principal coordinate (PCo) analysis of the bacterial community revealed significant structural differences in microbiome among healthy controls, UC and CD patients (PERMANOVA P = 0.0001). ITS sequencing of the fungal microbiome indicated no significant differences in α-diversity between healthy controls and IBD patients. However, the overall structure of the fungal microbial community of CD patients was significantly different from those of healthy controls and UC patients (PERMANOVA = 0.03). At the genus level, the genus Saccharomyces was dominant and this was followed by the genus Sarocladium in healthy controls. The abundance of the genus Candida was significantly higher in CD patients than healthy controls and/or UC patients.

Conclusion

The fecal fungal microbiome of a Japanese population differed considerably from that of a Western population. We identified fungal dysbiosis in Japanese patients with IBD.
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Literatur
1.
Zurück zum Zitat Kaplan GG, Ng SC. Understanding and preventing the global increase of inflammatory bowel disease. Gastroenterology. 2017;152(2):313–21 (e2).CrossRefPubMed Kaplan GG, Ng SC. Understanding and preventing the global increase of inflammatory bowel disease. Gastroenterology. 2017;152(2):313–21 (e2).CrossRefPubMed
2.
Zurück zum Zitat Chan HC, Ng SC. Emerging biologics in inflammatory bowel disease. J Gastroenterol. 2017;52(2):141–50.CrossRefPubMed Chan HC, Ng SC. Emerging biologics in inflammatory bowel disease. J Gastroenterol. 2017;52(2):141–50.CrossRefPubMed
3.
Zurück zum Zitat Sartor RB, Wu GD. Roles for intestinal bacteria, viruses, and fungi in pathogenesis of inflammatory bowel diseases and therapeutic approaches. Gastroenterology. 2017;152(2):327–39 (e4).CrossRefPubMed Sartor RB, Wu GD. Roles for intestinal bacteria, viruses, and fungi in pathogenesis of inflammatory bowel diseases and therapeutic approaches. Gastroenterology. 2017;152(2):327–39 (e4).CrossRefPubMed
4.
Zurück zum Zitat Nishino K, Nishida A, Inoue R, Kawada Y, Ohno M, Sakai S, et al. Analysis of endoscopic brush samples identified mucosa-associated dysbiosis in inflammatory bowel disease. J Gastroenterol. 2018;53(1):95–106.CrossRefPubMed Nishino K, Nishida A, Inoue R, Kawada Y, Ohno M, Sakai S, et al. Analysis of endoscopic brush samples identified mucosa-associated dysbiosis in inflammatory bowel disease. J Gastroenterol. 2018;53(1):95–106.CrossRefPubMed
5.
Zurück zum Zitat Frank DN, Robertson CE, Hamm CM, Kpadeh Z, Zhang T, Chen H, et al. Disease phenotype and genotype are associated with shifts in intestinal-associated microbiota in inflammatory bowel diseases. Inflamm Bowel Dis. 2011;17(1):179–84.CrossRefPubMed Frank DN, Robertson CE, Hamm CM, Kpadeh Z, Zhang T, Chen H, et al. Disease phenotype and genotype are associated with shifts in intestinal-associated microbiota in inflammatory bowel diseases. Inflamm Bowel Dis. 2011;17(1):179–84.CrossRefPubMed
6.
Zurück zum Zitat Nagalingam NA, Lynch SV. Role of the microbiota in inflammatory bowel diseases. Inflamm Bowel Dis. 2012;18(5):968–84.CrossRefPubMed Nagalingam NA, Lynch SV. Role of the microbiota in inflammatory bowel diseases. Inflamm Bowel Dis. 2012;18(5):968–84.CrossRefPubMed
7.
Zurück zum Zitat Sartor RB. The intestinal microbiota in inflammatory bowel diseases. Nestle Nutr Inst Workshop Ser. 2014;79:29–39.CrossRefPubMed Sartor RB. The intestinal microbiota in inflammatory bowel diseases. Nestle Nutr Inst Workshop Ser. 2014;79:29–39.CrossRefPubMed
8.
Zurück zum Zitat Li J, Chen D, Yu B, He J, Zheng P, Mao X, et al. Fungi in gastrointestinal tracts of human and mice: from community to functions. Microb Ecol. 2018;75(4):821–9.CrossRefPubMed Li J, Chen D, Yu B, He J, Zheng P, Mao X, et al. Fungi in gastrointestinal tracts of human and mice: from community to functions. Microb Ecol. 2018;75(4):821–9.CrossRefPubMed
10.
Zurück zum Zitat Iliev ID, Funari VA, Taylor KD, Nguyen Q, Reyes CN, Strom SP, et al. Interactions between commensal fungi and the C-type lectin receptor Dectin-1 influence colitis. Science. 2012;336(6086):1314–7.CrossRefPubMedPubMedCentral Iliev ID, Funari VA, Taylor KD, Nguyen Q, Reyes CN, Strom SP, et al. Interactions between commensal fungi and the C-type lectin receptor Dectin-1 influence colitis. Science. 2012;336(6086):1314–7.CrossRefPubMedPubMedCentral
11.
Zurück zum Zitat Sokol H, Conway KL, Zhang M, Choi M, Morin B, Cao Z, et al. Card9 mediates intestinal epithelial cell restitution, T-helper 17 responses, and control of bacterial infection in mice. Gastroenterology. 2013;145(3):591–601 (e3).CrossRefPubMed Sokol H, Conway KL, Zhang M, Choi M, Morin B, Cao Z, et al. Card9 mediates intestinal epithelial cell restitution, T-helper 17 responses, and control of bacterial infection in mice. Gastroenterology. 2013;145(3):591–601 (e3).CrossRefPubMed
12.
Zurück zum Zitat Jawhara S, Thuru X, Standaert-Vitse A, Jouault T, Mordon S, Sendid B, et al. Colonization of mice by Candida albicans is promoted by chemically induced colitis and augments inflammatory responses through galectin-3. J Infect Dis. 2008;197(7):972–80.CrossRefPubMed Jawhara S, Thuru X, Standaert-Vitse A, Jouault T, Mordon S, Sendid B, et al. Colonization of mice by Candida albicans is promoted by chemically induced colitis and augments inflammatory responses through galectin-3. J Infect Dis. 2008;197(7):972–80.CrossRefPubMed
13.
Zurück zum Zitat Jawhara S, Poulain D. Saccharomyces boulardii decreases inflammation and intestinal colonization by Candida albicans in a mouse model of chemically-induced colitis. Med Mycol. 2007;45(8):691–700.CrossRefPubMed Jawhara S, Poulain D. Saccharomyces boulardii decreases inflammation and intestinal colonization by Candida albicans in a mouse model of chemically-induced colitis. Med Mycol. 2007;45(8):691–700.CrossRefPubMed
14.
Zurück zum Zitat Sokol H, Leducq V, Aschard H, Pham HP, Jegou S, Landman C, et al. Fungal microbiota dysbiosis in IBD. Gut. 2017;66(6):1039–48.CrossRefPubMed Sokol H, Leducq V, Aschard H, Pham HP, Jegou S, Landman C, et al. Fungal microbiota dysbiosis in IBD. Gut. 2017;66(6):1039–48.CrossRefPubMed
15.
Zurück zum Zitat Liguori G, Lamas B, Richard ML, Brandi G, da Costa G, Hoffmann TW, et al. Fungal dysbiosis in mucosa-associated microbiota of Crohn’s disease patients. J Crohns Colitis. 2016;10(3):296–305.CrossRefPubMed Liguori G, Lamas B, Richard ML, Brandi G, da Costa G, Hoffmann TW, et al. Fungal dysbiosis in mucosa-associated microbiota of Crohn’s disease patients. J Crohns Colitis. 2016;10(3):296–305.CrossRefPubMed
16.
Zurück zum Zitat Nishijima S, Suda W, Oshima K, Kim SW, Hirose Y, Morita H, et al. The gut microbiome of healthy Japanese and its microbial and functional uniqueness. DNA Res. 2016;23(2):125–33.CrossRefPubMedPubMedCentral Nishijima S, Suda W, Oshima K, Kim SW, Hirose Y, Morita H, et al. The gut microbiome of healthy Japanese and its microbial and functional uniqueness. DNA Res. 2016;23(2):125–33.CrossRefPubMedPubMedCentral
17.
Zurück zum Zitat Rutgeerts P, Sandborn WJ, Feagan BG, Reinisch W, Olson A, Johanns J, et al. Infliximab for induction and maintenance therapy for ulcerative colitis. N Engl J Med. 2005;353(23):2462–76.CrossRefPubMed Rutgeerts P, Sandborn WJ, Feagan BG, Reinisch W, Olson A, Johanns J, et al. Infliximab for induction and maintenance therapy for ulcerative colitis. N Engl J Med. 2005;353(23):2462–76.CrossRefPubMed
18.
Zurück zum Zitat Best WR, Becktel JM, Singleton JW, Kern F Jr. Development of a Crohn’s disease activity index. National Cooperative Crohn’s Disease Study. Gastroenterology. 1976;70(3):439–44.CrossRefPubMed Best WR, Becktel JM, Singleton JW, Kern F Jr. Development of a Crohn’s disease activity index. National Cooperative Crohn’s Disease Study. Gastroenterology. 1976;70(3):439–44.CrossRefPubMed
19.
Zurück zum Zitat Matsumoto M, Inoue R, Tsuruta T, Hara H, Yajima T. Long-term oral administration of cows’ milk improves insulin sensitivity in rats fed a high-sucrose diet. Br J Nutr. 2009;102(9):1324–33.CrossRefPubMed Matsumoto M, Inoue R, Tsuruta T, Hara H, Yajima T. Long-term oral administration of cows’ milk improves insulin sensitivity in rats fed a high-sucrose diet. Br J Nutr. 2009;102(9):1324–33.CrossRefPubMed
20.
Zurück zum Zitat Inoue R, Sakaue Y, Sawai C, Sawai T, Ozeki M, Romero-Perez GA, et al. A preliminary investigation on the relationship between gut microbiota and gene expressions in peripheral mononuclear cells of infants with autism spectrum disorders. Biosci Biotechnol Biochem. 2016;80(12):2450–8.CrossRefPubMed Inoue R, Sakaue Y, Sawai C, Sawai T, Ozeki M, Romero-Perez GA, et al. A preliminary investigation on the relationship between gut microbiota and gene expressions in peripheral mononuclear cells of infants with autism spectrum disorders. Biosci Biotechnol Biochem. 2016;80(12):2450–8.CrossRefPubMed
21.
Zurück zum Zitat Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7(5):335–6.CrossRefPubMedPubMedCentral Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7(5):335–6.CrossRefPubMedPubMedCentral
22.
Zurück zum Zitat Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26(19):2460–1.CrossRefPubMed Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26(19):2460–1.CrossRefPubMed
24.
Zurück zum Zitat DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol. 2006;72(7):5069–72.CrossRefPubMedPubMedCentral DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol. 2006;72(7):5069–72.CrossRefPubMedPubMedCentral
25.
Zurück zum Zitat Gardes M, Bruns TD. ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol. 1993;2(2):113–8.CrossRefPubMed Gardes M, Bruns TD. ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol. 1993;2(2):113–8.CrossRefPubMed
26.
Zurück zum Zitat Abarenkov K, Henrik Nilsson R, Larsson KH, Alexander IJ, Eberhardt U, Erland S, et al. The UNITE database for molecular identification of fungi—recent updates and future perspectives. New Phytol. 2010;186(2):281–5.CrossRefPubMed Abarenkov K, Henrik Nilsson R, Larsson KH, Alexander IJ, Eberhardt U, Erland S, et al. The UNITE database for molecular identification of fungi—recent updates and future perspectives. New Phytol. 2010;186(2):281–5.CrossRefPubMed
27.
Zurück zum Zitat McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One. 2013;8(4):e61217.CrossRefPubMedPubMedCentral McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One. 2013;8(4):e61217.CrossRefPubMedPubMedCentral
28.
Zurück zum Zitat Parks DH, Tyson GW, Hugenholtz P, Beiko RG. STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics. 2014;30(21):3123–4.CrossRefPubMedPubMedCentral Parks DH, Tyson GW, Hugenholtz P, Beiko RG. STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics. 2014;30(21):3123–4.CrossRefPubMedPubMedCentral
29.
Zurück zum Zitat Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, et al. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12(6):R60.CrossRefPubMedPubMedCentral Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, et al. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12(6):R60.CrossRefPubMedPubMedCentral
31.
Zurück zum Zitat Willing BP, Dicksved J, Halfvarson J, Andersson AF, Lucio M, Zheng Z, et al. A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes. Gastroenterology. 2010;139(6):1844–54 (e1).CrossRefPubMed Willing BP, Dicksved J, Halfvarson J, Andersson AF, Lucio M, Zheng Z, et al. A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes. Gastroenterology. 2010;139(6):1844–54 (e1).CrossRefPubMed
Metadaten
Titel
Characterization of fungal dysbiosis in Japanese patients with inflammatory bowel disease
verfasst von
Takayuki Imai
Ryo Inoue
Yuki Kawada
Yasuhiro Morita
Osamu Inatomi
Atsushi Nishida
Shigeki Bamba
Masahiro Kawahara
Akira Andoh
Publikationsdatum
26.11.2018
Verlag
Springer Japan
Erschienen in
Journal of Gastroenterology / Ausgabe 2/2019
Print ISSN: 0944-1174
Elektronische ISSN: 1435-5922
DOI
https://doi.org/10.1007/s00535-018-1530-7

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