Enteric fungal microbiota dysbiosis and ecological alterations in colorectal cancer
Open accessAbstract
OBJECTIVES: Bacteriome and virome alterations are associated with colorectal cancer (CRC). Nevertheless, the gut fungal microbiota in CRC remains largely unexplored. We aimed to characterise enteric mycobiome in CRC. DESIGN: Faecal shotgun metagenomic sequences of 184 patients with CRC, 197 patients with adenoma and 204 control subjects from Hong Kong were analysed (discovery cohort: 73 patients with CRC and 92 control subjects; validation cohort: 111 patients with CRC, 197 patients with adenoma and 112 controls from Hong Kong). CRC-associated fungal markers and ecological changes were also validated in additional independent cohorts of 90 patients with CRC, 42 patients with adenoma and 66 control subjects of published repository sequences from Germany and France. Assignment of taxonomies was performed by exact k-mer alignment against an integrated microbial reference genome database. RESULTS: Principal component analysis revealed separate clusters for CRC and control (p<0.0001), with distinct mycobiomes in early-stage and late-stage CRC (p=0.0048). Basidiomycota:Ascomycota ratio was higher in CRC (p=0.0042), with increase in Malasseziomycetes (p<0.0001) and decrease in Saccharomycetes (p<0.0001) and Pneumocystidomycetes (p=0.0017). Abundances of 14 fungal biomarkers distinguished CRC from controls with an area under the receiver-operating characteristic curve (AUC) of 0.93 and validated AUCs of 0.82 and 0.74 in independent Chinese cohort V1 and European cohort V2, respectively. Further ecological analysis revealed higher numbers of co-occurring fungal intrakingdom and co-exclusive bacterial-fungal correlations in CRC (p<0.0001). Moreover, co-occurrence interactions between fungi and bacteria, mostly contributed by fungal Ascomycota and bacterial Proteobacteria in control, were reverted to co-exclusive interplay in CRC (p=0.00045). CONCLUSIONS: This study revealed CRC-associated mycobiome dysbiosis characterised by altered fungal composition and ecology, signifying that the gut mycobiome might play a role in CRC.
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The enteric virome and mycobiome have been linked with colorectal cancer.
“The enteric virome and mycobiome (fungal microbiome) have also been linked with CRC.72–74”
From Influence of the Gut Microbiome, Diet, and Environment on Risk of Colorectal Cancer (2020) · cites this paper as [73]
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1 retracted
RETRACTED: Eukaryote Culturomics of the Gut Reveals New Species
Gouba, N., Raoult, D., & Drancourt, M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0106994 · Cited by 90 · see citing works
RetractedTrimmomatic: a flexible trimmer for Illumina sequence data
Bolger, A. M., Lohse, M., & Usadel, B. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btu170 · Cited by 65,548 · see citing works
Cancer incidence and mortality worldwide: Sources, methods and major patterns in GLOBOCAN 2012
Ferlay, J., Soerjomataram, I., Dikshit, R., Eser, S., Mathers, C., Rebelo, M., Parkin, D. M., Forman, D., & Bray, F. (2015) · International Journal of Cancer · doi:10.1002/ijc.29210 · Cited by 28,766 · see citing works
Diet rapidly and reproducibly alters the human gut microbiome
David, L. A., Maurice, C. F., Carmody, R. N., Gootenberg, D. B., Button, J. E., Wolfe, B. E., Ling, A. V., Devlin, A. S., Varma, Y., Fischbach, M. A., et al. (2014) · Nature · doi:10.1038/nature12820 · Cited by 10,100 · see citing works
Kraken: ultrafast metagenomic sequence classification using exact alignments
Wood, D. E., & Salzberg, S. L. (2014) · Genome Biology · doi:10.1186/gb-2014-15-3-r46 · Cited by 4,521 · see citing works
Global diversity and geography of soil fungi
Tedersoo, L., Bahram, M., Põlme, S., Kõljalg, U., Yorou, N. S., Wijesundera, R., Villarreal‐Ruiz, L., Vasco‐Palacios, A. M., Thu, P. Q., Suija, A., et al. (2014) · Science · doi:10.1126/science.1256688 · Cited by 3,739 · see citing works
Inferring Correlation Networks from Genomic Survey Data
Friedman, J., & Alm, E. J. (2012) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002687 · Cited by 2,727 · see citing works
Differential abundance analysis for microbial marker-gene surveys
Paulson, J. N., Stine, O. C., Bravo, H. C., & Pop, M. (2013) · Nature Methods · doi:10.1038/nmeth.2658 · Cited by 2,437 · see citing works
Potential of fecal microbiota for early-stage detection of colorectal cancer
Zeller, G., Tap, J., Voigt, A. Y., Sunagawa, S., Kultima, J. R., Costea, P. I., Amiot, A., Böhm, J., Brunetti, F., Habermann, N., et al. (2014) · Molecular Systems Biology · doi:10.15252/msb.20145645 · Cited by 1,375 · see citing works
Fungal microbiota dysbiosis in IBD
Sokol, H., Leducq, V., Aschard, H., Pham, H., Jégou, S., Landman, C., Cohen, D., Liguori, G., Bourrier, A., Nion–Larmurier, I., et al. (2016) · Gut · doi:10.1136/gutjnl-2015-310746 · Cited by 1,321 · see citing works
Yu, J. Q., Feng, Q., Wong, S. H., Zhang, D., Liang, Q. Y., Qin, Y., Tang, L., Zhao, H., Stenvang, J., Li, Y., et al. (2015) · Gut · doi:10.1136/gutjnl-2015-309800 · Cited by 1,259 · see citing works
Self-citationBiogeography and individuality shape function in the human skin metagenome
Program, N. C. S., Oh, J., Byrd, A. L., Deming, C., Conlan, S., Kong, H. H., & Segre, J. A. (2014) · Nature · doi:10.1038/nature13786 · Cited by 1,148 · see citing works
Interactions between commensal fungi and the C-type lectin receptor Dectin-1 influence colitis
Iliev, I. D., Funari, V. A., Taylor, K. D., Nguyen, Q., Reyes, C. N., Strom, S. P., Brown, J., Becker, C. A., Fleshner, P. R., Dubinsky, M., et al. (2012) · Science · doi:10.1126/science.1221789 · Cited by 1,073 · see citing works
The UCSC Genome Browser database: 2015 update
Rosenbloom, K., Armstrong, J., Barber, G. P., Casper, J., Clawson, H., Diekhans, M., Dreszer, T. R., Fujita, P. A., Guruvadoo, L., Haeussler, M., et al. (2014) · Nucleic Acids Res. · doi:10.1093/nar/gku1177 · Cited by 1,011 · see citing works
Aspergillus flavus: human pathogen, allergen and mycotoxin producer
Hedayati, M. T., Pasqualotto, A. C., Warn, P. A., Bowyer, P., & Denning, D. W. (2007) · Microbiology · doi:10.1099/mic.0.2007/007641-0 · Cited by 966 · see citing works
Archaea and fungi of the human gut microbiome: correlations with diet and bacterial residents
Hoffmann, C., Dollive, S., Grunberg, S., Chen, J., Li, H., Wu, G. D., Lewis, J. D., & Bushman, F. D. (2013) · PLoS ONE · doi:10.1371/journal.pone.0066019 · Cited by 808 · see citing works
The mycobiota: interactions between commensal fungi and the host immune system
Underhill, D. M., & Iliev, I. D. (2014) · Nature reviews. Immunology · doi:10.1038/nri3684 · Cited by 696 · see citing works
The Malassezia Genus in Skin and Systemic Diseases
Gaitanis, G., Magiatis, P., Hantschke, M., Bassukas, I. D., & Velegraki, A. (2012) · Clinical Microbiology Reviews · doi:10.1128/cmr.00021-11 · Cited by 642 · see citing works
Soil Fungal:Bacterial Ratios Are Linked to Altered Carbon Cycling
Malik, A. A., Chowdhury, S. P., Schlager, V., Oliver, A., Puissant, J., Mellado-Vázquez, P. G., Jehmlich, N., von Bergen�, M., Griffiths, R. I., & Gleixner, G. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.01247 · Cited by 457 · see citing works
Fungal dysbiosis: immunity and interactions at mucosal barriers
Iliev, I. D., & Leonardi, I. (2017) · Nature reviews. Immunology · doi:10.1038/nri.2017.55 · Cited by 392 · see citing works
Alterations in Enteric Virome Are Associated With Colorectal Cancer and Survival Outcomes
Nakatsu, G., Zhou, H., Wu, W. K. K., Wong, S. H., Coker, O. O., Dai, Z., Li, X., Szeto, C.-H., Sugimura, N., Lam, T. Y.-T., et al. (2018) · Gastroenterology · doi:10.1053/j.gastro.2018.04.018 · Cited by 386 · see citing works
Self-citationEpidemiology of Rhodotorula : An Emerging Pathogen
Wirth, F., & Goldani, L. Z. (2012) · Interdisciplinary Perspectives on Infectious Diseases · doi:10.1155/2012/465717 · Cited by 340 · see citing works
Scanlan, P. D., & Marchesi, J. R. (2008) · The ISME Journal · doi:10.1038/ismej.2008.76 · Cited by 315 · see citing works
Commensal Fungi Recapitulate the Protective Benefits of Intestinal Bacteria
Jiang, T. T., Shao, T., Ang, W. X. G., Kinder, J. M., Turner, L. H., Pham, G. H., Whitt, J., Alenghat, T., & Way, S. S. (2017) · Cell Host & Microbe · doi:10.1016/j.chom.2017.10.013 · Cited by 296 · see citing works
Dysbiosis of Gut Fungal Microbiota is Associated With Mucosal Inflammation in Crohn’s Disease
Li, Q., Wang, C., Tang, C. X., He, Q., Li, N., & Li, J. (2013) · Journal of Clinical Gastroenterology · doi:10.1097/mcg.0000000000000035 · Cited by 279 · see citing works
Arrieta, M., Arévalo‐Cortes, A., Stiemsma, L. T., Dimitriu, P. A., Chico, M. E., Loor, S., Vaca, M. G., Boutin, R. C. T., Morien, E., Jin, M., et al. (2017) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2017.08.041 · Cited by 277 · see citing works
Fungal Signature in the Gut Microbiota of Pediatric Patients With Inflammatory Bowel Disease
Chehoud, C., Albenberg, L. G., Judge-Golden, C. P., Hoffmann, C., Grunberg, S., Bittinger, K. L., Baldassano, R. N., Lewis, J. D., Bushman, F. D., & Wu, G. D. (2015) · Inflammatory Bowel Diseases · doi:10.1097/mib.0000000000000454 · Cited by 265 · see citing works
Microbial Eukaryotes in the Human Microbiome: Ecology, Evolution, and Future Directions
Parfrey, L. W., Walters, W. A., & Knight, R. D. (2011) · Frontiers in Microbiology · doi:10.3389/fmicb.2011.00153 · Cited by 243 · see citing works
Candida albicans Colonization and ASCA in Familial Crohn's Disease
Standaert‐Vitse, A., Sendid, B., Joossens, M., François, N., Khoury, P. V.-E., Branche, J., Kruiningen, H. J. V., Jouault, T., Rutgeerts, P. J., Gower‐Rousseau, C., et al. (2009) · The American Journal of Gastroenterology · doi:10.1038/ajg.2009.225 · Cited by 206 · see citing works
Gut microbiota and colorectal cancer
Gao, R., Gao, Z., Huang, L., & Qin, H. (2017) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s10096-016-2881-8 · Cited by 205 · see citing works
Botschuijver, S., Roeselers, G., Levin, E., Jonkers, D. M., Welting, O., Heinsbroek, S. E. M., de Weerd, H. H., Boekhout, T., Fornai, M., Masclee, A. A., et al. (2017) · Gastroenterology · doi:10.1053/j.gastro.2017.06.004 · Cited by 202 · see citing works
Dysbiosis of Fungal Microbiota in the Intestinal Mucosa of Patients with Colorectal Adenomas
Luan, C., Xie, L., Yang, X., Miao, H., Lv, N., Zhang, R., Xiao, X., Hu, Y., Liu, Y., Wu, N., et al. (2015) · Scientific Reports · doi:10.1038/srep07980 · Cited by 190 · see citing works
Enterobacteriaceae are essential for the modulation of colitis severity by fungi
Sovran, B., Planchais, J., Jégou, S., Straube, M., Lamas, B., Natividad, J. M., Agus, A., Dupraz, L., Glodt, J., Costa, G. D., et al. (2018) · Microbiome · doi:10.1186/s40168-018-0538-9 · Cited by 181 · see citing works
Bajaj, J. S., Liu, E., Kheradman, R., Fagan, A., Heuman, D. M., White, M. B., Gavis, E. A., Hylemon, P. B., Sikaroodi, M., & Gillevet, P. M. (2017) · Gut · doi:10.1136/gutjnl-2016-313170 · Cited by 167 · see citing works
Ukhanova, M., Wang, X., Baer, D. J., Novotny, J. A., Fredborg, M., & Mai, V. (2014) · British Journal Of Nutrition · doi:10.1017/s0007114514000385 · Cited by 153 · see citing works
Buentke, E., Heffler, L. C., Scheynius, A., Wilson, J. L., Wallin, R. P. A., Löfman, C. O., Chambers, B. J., & Ljunggren, H. (2002) · Journal of Investigative Dermatology · doi:10.1046/j.1523-1747.2002.00132.x · Cited by 152 · see citing works
Spectrum of Clinically Relevant Acremonium Species in the United States
Perdomo, H., Sutton, D. A., García, D., et al. (2010) · Journal of Clinical Microbiology · doi:10.1128/jcm.00793-10 · Cited by 146 · see citing works
Sequence-based methods for detecting and evaluating the human gut mycobiome
Haute, M. J. S. V., Banjara, N., & Hallen‐Adams, H. E. (2015) · Letters in Applied Microbiology · doi:10.1111/lam.12539 · Cited by 127 · see citing works
Jawhara, S., Habib, K. A., Maggiotto, F., Pignède, G., Vandekerckove, P., Maes, E., Dubuquoy, L., Fontaine, T., Guérardel, Y., & Poulain, D. (2012) · PLoS ONE · doi:10.1371/journal.pone.0040648 · Cited by 113 · see citing works
Richard, M. L., Lamas, B., Liguori, G., Hoffmann, T. W., & Sokol, H. (2015) · Inflammatory Bowel Diseases · doi:10.1097/mib.0000000000000261 · Cited by 113 · see citing works
Sivignon, A., de Vallée, A., Barnich, N., Denizot, J., Darcha, C., Pignède, G., Vandekerckove, P., & Darfeuille–Michaud, A. (2015) · Inflammatory Bowel Diseases · doi:10.1097/mib.0000000000000280 · Cited by 99 · see citing works
Angebault, C., Djossou, F., Abélanet, S., Permal, E., Soltana, M. B., Diancourt, L., Bouchier, C., Woerther, P., Catzeflis, F. M., Andremont, A., et al. (2013) · The Journal of Infectious Diseases · doi:10.1093/infdis/jit389 · Cited by 99 · see citing works
Host–microbe interactions: commensal fungi in the gut
Paterson, M. J., Oh, S., & Underhill, D. M. (2017) · Current Opinion in Microbiology · doi:10.1016/j.mib.2017.11.012 · Cited by 80 · see citing works
Kuramae, E. E., Hillekens, R., de Hollander, M., van der Heijden, M. G. A., van den Berg, M., van Straalen, N. M., & Kowalchuk, G. A. (2013) · FEMS Microbiology Ecology · doi:10.1111/1574-6941.12080 · Cited by 76 · see citing works
Cary, J. W., Ehrlich, K., Beltz, S. B., Harris-Coward, P. Y., & Klich, M. A. (2009) · Mycologia · doi:10.3852/08-173 · Cited by 61 · see citing works
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Song, M., Chan, A. T., & Sun, J. (2020) · Gastroenterology · doi:10.1053/j.gastro.2019.06.048 · Cited by 752 · see citing works
Gut microbiome, liver immunology, and liver diseases
Wang, R., Tang, R., Li, B., Ma, X., Schnabl, B., & Tilg, H. (2021) · Cellular & Molecular Immunology · doi:10.1038/s41423-020-00592-6 · Cited by 466 · see citing works
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Janney, A., Powrie, F., & Mann, E. H. (2020) · Nature · doi:10.1038/s41586-020-2729-3 · Cited by 445 · see citing works
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Cheng, W. Y., Wu, C.-Y., & Yu, J. (2020) · Gut · doi:10.1136/gutjnl-2020-321153 · Cited by 384 · see citing works
Self-citationModulating the microbiome to improve therapeutic response in cancer
McQuade, J. L., Daniel, C. R., Helmink, B. A., & Wargo, J. A. (2019) · The Lancet Oncology · doi:10.1016/s1470-2045(18)30952-5 · Cited by 376 · see citing works
Liu, N.-N., Jiao, N., Tan, J.-C., Wang, Z., Wu, D., Wang, A.-J., Chen, J., Tao, L., Zhou, C., Fang, W., et al. (2022) · Nature Microbiology · doi:10.1038/s41564-021-01030-7 · Cited by 306 · see citing works
The microbiome and the hallmarks of cancer
Fulbright, L. E., Ellermann, M., & Arthur, J. C. (2017) · PLOS Pathogens · doi:10.1371/journal.ppat.1006480 · Cited by 164 · see citing works
Lin, Y., Lau, H. C.-H., Liu, Y., Kang, X., Wang, Y., Ting, N. L.-N., Kwong, T. N.-Y., Han, J., Liu, W., Liu, C., et al. (2022) · Gastroenterology · doi:10.1053/j.gastro.2022.06.038 · Cited by 142 · see citing works
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- Authors
- Coker, O. O., Nakatsu, G., Dai, R. Z., Wu, W. K. K., Wong, S. H., Ng, S. C., Chan, F. K. L., Sung, J. J. Y., & Yu, J.
- Affiliations
- Chinese University of Hong Kong (HK)
- Corresponding author
- Yu, Jun
- ORCID
- Venue
- Gut
- Publisher
- BMJ
- Published
- 2018-11-24
- Volume
- 68
- Issue
- 4
- Pages
- 654-662
- ISSN
- 0017-5749 (ISSN-L)
- 1468-3288
- PMC
- PMC6580778
- OpenAlex
- W2903428492
- Cited by
- 511
- References
- 45
- Citations by year
- 2026: 49 · 2025: 54 · 2024: 84 · 2023: 108 · 2022: 77 · 2021: 70 · 2020: 44 · 2019: 23 · 2017: 1
- FWCI
- 12.18
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc
- Locations
- Gut (publishedVersion, cc-by-nc)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- HighWire Press Open Archive (submittedVersion)
- Funders
- HMRF Hong Kong
- Shenzhen Virtual University Park Support Scheme to CUHK Shenzhen Research Institute
- Grant from Faculty of Medicine CUHK on Microbiota Research, RGC-GRF Hong Kong
- Vice-Chancellor’s Discretionary Fund CUHK
- Vice-Chancellor’s Discretionary Fund CUHK and CUHK direct grant
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Mycorrhizal Fungi and Plant Interactions
- Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
- Keywords
- colorectal cancer, gut mycobiome, fungal dysbiosis, colorectal adenoma, fungal biomarkers, Basidiomycota, Ascomycota, Proteobacteria
- MeSH terms
- Gastrointestinal Microbiome, Mycobiome, Aged, Female, Hong Kong, Humans, Male, Middle Aged, Biomarkers, Tumor, Colorectal Neoplasms, Case-Control Studies, Principal Component Analysis, Dysbiosis
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