Composition of the colon microbiota in the individuals with inflammatory bowel disease and colon cancer
Language English Country United States Media print-electronic
Document type Journal Article
Grant support
FCD-2020-2065
Inönü Üniversitesi
PubMed
37344611
DOI
10.1007/s12223-023-01072-w
PII: 10.1007/s12223-023-01072-w
Knihovny.cz E-resources
- Keywords
- 16SrRNA, 18SrRNA, Crohn’s disease, Metabarcoding, Mycobiome, Ulcerative colitis,
- MeSH
- Basidiomycota * MeSH
- Crohn Disease * microbiology MeSH
- Inflammatory Bowel Diseases * microbiology MeSH
- Humans MeSH
- Microbiota * MeSH
- Colonic Neoplasms * MeSH
- Intestinal Mucosa microbiology MeSH
- Check Tag
- Humans MeSH
- Publication type
- Journal Article MeSH
The human intestine is a habitat for microorganisms and, recently, the composition of the intestinal microbiota has been correlated with the etiology of diseases such as inflammations, sores, and tumors. Although many studies have been conducted to understand the composition of that microbiota, expanding these studies to more samples and different backgrounds will improve our knowledge. In this work, we showed the colon microbiota composition and diversity of healthy subjects, patients with inflammatory bowel disease (IBD), and colon cancer by metagenomic sequencing. Our results indicated that the relative abundance of prokaryotic and eukaryotic microbes differs between the healthy vs. tumor biopsies, tumor vs. IBD biopsies, and fresh vs. paraffin-embedded tumor biopsies. Fusobacterium, Escherichia-Shigella, and Streptococcus genera were relatively abundant in fresh tumor biopsies, while Pseudomonas was significantly elevated in IBD biopsies. Additionally, another opportunist pathogen Malasseziales was revealed as the most abundant fungal clade in IBD biopsies, especially in ulcerative colitis. We also found that, while the Basidiomycota:Ascomycota ratio was slightly lower in tumor biopsies compared to biopsies from healthy subjects, there was a significant increase in IBD biopsies. Our work will contribute to the known diversity of prokaryotic and eukaryotic microbes in the colon biopsies in patients with IBD and colon cancer.
Faculty of Medicine Department of Medical Pathology Inonu University Malatya 44000 Turkey
Faculty of Science Department of Biology Hacettepe University Ankara 06800 Turkey
See more in PubMed
Alhinai EA, Walton GE, Commane DM (2019) The role of the gut microbiota in colorectal cancer causation. Int J Mol Sci 20:5295. https://doi.org/10.3390/ijms20215295 DOI
Amaral-Zettler LA, McCliment EA, Ducklow HW, Huse SM (2009) A method for studying protistan diversity using massively parallel sequencing of V9 hypervariable regions of small-subunit ribosomal RNA genes. PLOS One 4:e6372. https://doi.org/10.1371/journal.pone.0006372
Antonopoulos DA, Huse SM, Morrison HG, Schmidt TM, Sogin ML, Young VB (2009) Reproducible community dynamics of the gastrointestinal microbiota following antibiotic perturbation. Infect Immun 77:2367–2375. https://doi.org/10.1128/iai.01520-08 DOI
Arthur JC et al (2012) Intestinal inflammation targets cancer-inducing activity of the microbiota. Science 338:120–123. https://doi.org/10.1126/science.1224820 DOI
Bisht V, Nash K, Xu Y, Agarwal P, Bosch S, Gkoutos GV, Acharjee A (2021) Integration of the Microbiome, Metabolome and Transcriptomics Data Identified Novel Metabolic Pathway Regulation in Colorectal Cancer. Int J Mol Sci 22:5763. https://doi.org/10.3390/ijms22115763 DOI
Blais Lecours P, Marsolais D, Cormier Y, Berberi M, Haché C, Bourdages R, Duchaine C (2014) Increased prevalence of Methanosphaera stadtmanae in inflammatory bowel diseases. PLoS One 9:e87734. https://doi.org/10.1371/journal.pone.0087734
Borgognone A et al (2021) Performance of 16S Metagenomic Profiling in Formalin-Fixed Paraffin-Embedded versus Fresh-Frozen Colorectal Cancer Tissues. Cancers (Basel) pp. 5421. https://doi.org/10.3390/cancers13215421
Bouter KE, van Raalte DH, Groen AK, Nieuwdorp M (2017) Role of the gut microbiome in the pathogenesis of obesity and obesity-related metabolic dysfunction. Gastroenterology 152:1671–1678. https://doi.org/10.1053/j.gastro.2016.12.048 DOI
Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68:394–424. https://doi.org/10.3322/caac.21492 DOI
Cao Y, Shen J, Ran ZH (2014) Association between Faecalibacterium prausnitzii reduction and inflammatory bowel disease: A meta-analysis and systematic review of the literature. Gastroenterol Res Pract 2014:872725. https://doi.org/10.1155/2014/872725
Castellarin M et al (2012) Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome Res 22:299–306. https://doi.org/10.1101/gr.126516.111 DOI
Chan SN, Low END, Raja Ali RA, Mokhtar NM (2018) Delineating inflammatory bowel disease through transcriptomic studies: current review of progress and evidence. Intest Res 16:374–383. https://doi.org/10.5217/ir.2018.16.3.374 DOI
Chaudhary PP, Conway PL, Schlundt J (2018) Methanogens in humans: potentially beneficial or harmful for health. Appl Microbiol Biotechnol 102:3095–3104. https://doi.org/10.1007/s00253-018-8871-2 DOI
Christl SU, Eisner HD, Dusel G, Kasper H, Scheppach W (1996) Antagonistic effects of sulfide and butyrate on proliferation of colonic mucosa: a potential role for these agents in the pathogenesis of ulcerative colitis. Dig Dis Sci 41:2477–2481. https://doi.org/10.1007/BF02100146 DOI
Coker OO, Wu WKK, Wong SH, Sung JJY, Yu J (2020) Altered gut archaea composition and interaction with bacteria are associated with colorectal cancer. Gastroenterology 159:1459-1470.e1455. https://doi.org/10.1053/j.gastro.2020.06.042 DOI
David LA et al (2014) Diet rapidly and reproducibly alters the human gut microbiome. Nature 505:559–563. https://doi.org/10.1038/nature12820 DOI
De Filippo C et al (2017) A preliminary investigation in children living in rural and urban Burkina Faso and Italy. Front Microbiol 8:1979. https://doi.org/10.3389/fmicb.2017.01979 DOI
Debesa-Tur G, Pérez-Brocal V, Ruiz-Ruiz S, Castillejo A, Latorre A, Soto JL, Moya A (2021) Metagenomic analysis of formalin-fixed paraffin-embedded tumor and normal mucosa reveals differences in the microbiome of colorectal cancer patients. Sci Rep 11:391. https://doi.org/10.1038/s41598-020-79874-y DOI
Di Paola M et al (2020) Comparative immunophenotyping of Saccharomyces cerevisiae and Candida spp. strains from Crohn's disease patients and their interactions with the gut microbiome. J Transl Autoimmun 3:100036. https://doi.org/10.1016/j.jtauto.2020.100036
Dzutsev A, Goldszmid RS, Viaud S, Zitvogel L, Trinchieri G (2015) The role of the microbiota in inflammation, carcinogenesis, and cancer therapy. Eur J Immunol 45:17–31. https://doi.org/10.1002/eji.201444972 DOI
Erdem B, Kucukyildirim S, Saglar E, Polat Z, Mergen H (2014) Promoter hypermethylation of p16 and APC in gastrointestinal cancer patients. Turk J Gastroenterol 25:512–517. https://doi.org/10.5152/tjg.2014.4791 DOI
Feng Q et al (2015) Gut microbiome development along the colorectal adenoma-carcinoma sequence. Nat Commun 6:6528. https://doi.org/10.1038/ncomms7528 DOI
Flemer B et al (2017) Tumour-associated and non-tumour-associated microbiota in colorectal cancer. Gut 66:633–643. https://doi.org/10.1136/gutjnl-2015-309595 DOI
Franzosa EA et al (2014) Relating the metatranscriptome and metagenome of the human gut. Proc Nat Acad Sci USA 111:E2329–E2338. https://doi.org/10.1073/pnas.1319284111 DOI
Fulbright LE, Ellermann M, Arthur JC (2017) The microbiome and the hallmarks of cancer. PLoS Pathog 13:e1006480. https://doi.org/10.1371/journal.ppat.1006480
Gaci N, Borrel G, Tottey W, O’Toole PW, Brugère JF (2014) Archaea and the human gut: new beginning of an old story. World J Gastroenterol 20:16062–16078. https://doi.org/10.3748/wjg.v20.i43.16062 DOI
Gao R, Kong C, Li H, Huang L, Qu X, Qin N, Qin H (2017) Dysbiosis signature of mycobiota in colon polyp and colorectal cancer. Eur J Clin Microbiol Infect Dis 36:2457–2468. https://doi.org/10.1007/s10096-017-3085-6 DOI
Gao Z, Guo B, Gao R, Zhu Q, Wu W, Qin H (2015) Probiotics modify human intestinal mucosa-associated microbiota in patients with colorectal cancer. Mol Med Rep 12:6119–6127. https://doi.org/10.3892/mmr.2015.4124 DOI
Gaulke CA, Sharpton TJ (2018) The influence of ethnicity and geography on human gut microbiome composition. Nat Med 24:1495–1496. https://doi.org/10.1038/s41591-018-0210-8 DOI
Gibson GR, MacFarlane GT, Cummings JH (1988) Ocurrence of sulphate-reducing bacteria in human faeces and the relationship of dissimilatory sulphate reduction to methanogenesis in the large gut. J Appl Bacteriol 65:103–111 DOI
Gill SR et al (2006) Metagenomic analysis of the human distal gut microbiome. Science 312:1355–1359. https://doi.org/10.1126/science.1124234 DOI
Gillen CD, Walmsley RS, Prior P, Andrews HA, Allan RN (1994) Ulcerative colitis and Crohn’s disease: a comparison of the colorectal cancer risk in extensive colitis. Gut 35:1590–1592. https://doi.org/10.1136/gut.35.11.1590 DOI
Gomaa EZ (2020) Human gut microbiota/microbiome in health and diseases: a review. Antonie Van Leewenhoek 113:2019–2040. https://doi.org/10.1007/s10482-020-01474-7 DOI
Goodrich JK et al (2014) Human genetics shape the gut microbiome. Cell 159:789–799. https://doi.org/10.1016/j.cell.2014.09.053 DOI
Gupta VK, Paul S, Dutta C (2017) Geography, ethnicity or subsistence-specific variations in human microbiome composition and diversity. Front Microbiol 8:1162. https://doi.org/10.3389/fmicb.2017.01162 DOI
Han S, Zhuang J, Pan Y, Wu W, Ding K (2022) Different characteristics in gut microbiome between advanced adenoma patients and colorectal cancer patients by metagenomic analysis. Microbiol Spectr 10:e0159322. https://doi.org/10.1128/spectrum.01593-22
Hoegenauer C, Hammer HF, Mahnert A, Moissl-Eichinger C (2022) Methanogenic archaea in the human gastrointestinal tract. Nat Rev Gastroenterol Hepatol 19:805–813. https://doi.org/10.1038/s41575-022-00673-z DOI
Hoffmann C et al (2013) Archaea and fungi of the human gut microbiome: correlations with diet and bacterial residents. PLoS One 8:e66019. https://doi.org/10.1371/journal.pone.0066019
Hong SN et al (2017) RNA-seq reveals transcriptomic differences in inflamed and noninflamed intestinal mucosa of Crohn’s disease patients compared with normal mucosa of healthy controls. Inflamm Bowel Dis 23:1098–1108. https://doi.org/10.1097/MIB.0000000000001066 DOI
IARC Working Gorup on the Evaluation of Carcinogenic Risks to Humans (2012) Biological agents. vol 100 B. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans
Iljazovic A, Roy U, Gálvez EJC et al (2021) Perturbation of the gut microbiome by Prevotella spp. enhances host susceptibility to mucosal inflammation. Mucosal Immunol 14:113–124. https://doi.org/10.1038/s41385-020-0296-4
Johnson CH, Spilker ME, Goetz L, Peterson SN, Siuzdak G (2016) Metabolite and microbiome interplay in cancer immunotherapy. Cancer Res 76:6146–6152. https://doi.org/10.1158/0008-5472.CAN-16-0309 DOI
Kim G et al (2012) Methanobrevibacter smithii is the predominant methanogen in patients with constipation-predominant IBS and methane on breath. Dig Dis Sci 57:3213–3218. https://doi.org/10.1007/s10620-012-2197-1 DOI
Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, Glöckner FO (2013) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res 41:e1. https://doi.org/10.1093/nar/gks808
Koskinen K et al (2017) First insights into the diverse human archaeome: Specific detection of archaea in the gastrointestinal tract, lung, and nose and on skin. mBio 8:e00824–00817. https://doi.org/10.1128/mBio.00824-17
Kostic AD et al (2012) Genomic analysis identifies association of Fusobacterium with colorectal carcinoma. Genome Res 22:292–298. https://doi.org/10.1101/gr.126573.111 DOI
Kourkoumpetis T et al (2021) Colonic mucosa-associated mycobiota in individuals with normal colons. Research Square:Preprint. https://doi.org/10.21203/rs.3.rs-1147234/v1
Kucukyildirim S, Erdem B, Saglar E, Polat Z, Mergen H (2014) Evaluation of MUC1, CK20 and hTERT expression in preipheral blood of gastrointestinal cancer patients in search of diagnostic criteria. Turkish J Biol 38:848–858. https://doi.org/10.3906/biy-1403-73 DOI
Lam SY et al (2021) Technical challenges regarding the use of formalin-fixed paraffin embedded (FFPE) tissue specimens for the detection of bacterial alterations in colorectal cancer. BMC Microbiol 21:297. https://doi.org/10.1186/s12866-021-02359-z DOI
Ley RE (2016) Prevotella in the gut: choose carefully. Nat Rev Gastroenterol Hepatol 13:69–70. https://doi.org/10.1038/nrgastro.2016.4 DOI
Ley RE, Bäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI (2005) Obesity alters gut microbial ecology. Proc Nat Acad Sci USA 102:11070–11075. https://doi.org/10.1073/pnas.0504978102 DOI
Li R, Shen J, Xu Y (2022) Fusobacterium nucleatum and colorectal cancer. Infect Drug Resist 15:1115–1120. https://doi.org/10.2147/IDR.S357922 DOI
Liu H, Xu X, Liang J, Wang J, Li Y (2022) The relationship between Clostridium butyricum and colorectal cancer. J Cancer Res Ther 18:1855–1859. https://doi.org/10.4103/jcrt.jcrt_1565_21 DOI
Lloyd-Price J, Abu-Ali G, Huttenhower C (2016) The healthy human microbiome. Genome Med 8:51. https://doi.org/10.1186/s13073-016-0307-y DOI
Lopez-Siles M et al (2016) Changes in the abundance of Faecalibacterium prausnitzii phylogroups I and II in the intestinal mucosa of inflammatory bowel disease and patients with colorectal cancer. Inflammation Bowel Dis 22:28–41. https://doi.org/10.1097/MIB.0000000000000590 DOI
Louca S, Parfrey LW, Doebeli M (2016) Decoupling function and taxonomy in the global ocean microbiome. Science 353:1272–1277. https://doi.org/10.1126/science.aaf4507 DOI
Lu K et al (2014) Arsenic exposure perturbs the gut microbiome and its metabolic profile in mice: an integrated metagenomics and metabolomics analysis. Envrion Health Perspect 122:284–291. https://doi.org/10.1289/ehp.1307429 DOI
Lynch SV, Pedersen O (2016) The human intestinal microbiome in health and disease. N Eng J Med 375:2369–2379. https://doi.org/10.1056/NEJMra1600266 DOI
Machiels K et al (2014) A decrease of the butyrate-producing species Roseburia hominis and Faecalibacterium prausnitzii defines dysbiosis in patients with ulcerative colitis. Gut 63:1275–1283. https://doi.org/10.1136/gutjnl-2013-304833 DOI
Manichanh C et al (2006) Reduced diversity of faecal microbiota in Crohn’s disease revealed by a metagenomic approach. Gut 55:205–211. https://doi.org/10.1136/gut.2005.073817 DOI
Mbakwa CA, Penders J, Savelkoul PH, Thijs C, Dagnelie PC, Mommers M, Arts IC (2015) Gut colonization with Methanobrevibacter smithii is associated with childhood weight development. Obesity 23:2508–2516. https://doi.org/10.1002/oby.21266 DOI
McLean MH et al (2011) The inflammatory microenvironment in colorectal neoplasia. PLOS One 6:e15366. https://doi.org/10.1371/journal.pone.0015366
McMurdie PJ, Holmes S (2013) phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8:e61217. https://doi.org/10.1371/journal.pone.0061217
Mima K et al (2016) Fusobacterium nucleatum in colorectal carcinoma tissue and patient prognosis. Gut 65:1973–1980. https://doi.org/10.1136/gutjnl-2015-310101 DOI
Mutignani M et al (2021) Blood bacterial DNA load and profiling differ in colorectal cancer patients compared to tumor-free controls. Cancers (basel) 13:6363. https://doi.org/10.3390/cancers13246363 DOI
Nardelli C et al (2021) 16S rRNA of mucosal colon microbiome and CCL2 circulating levels are potential biomarkers in colorectal cancer. Int J Mol Sci 22:10747. https://doi.org/10.3390/ijms221910747 DOI
Narunsky-Haziza L et al (2022) Pan-cancer analyses reveal cancer-type-specific fungal ecologies and bacteriome interactions. Cell 185:3789–3806. https://doi.org/10.1016/j.cell.2022.09.005 DOI
Ni J, Wu GD, Albenberg L, Tomov VT (2017) Gut microbiota and IBD: causation or correlation? Nat Rev Gastroenterol Hepatol 14:573–584. https://doi.org/10.1038/nrgastro.2017.88 DOI
Nishida A, Inoue R, Inatomi O, Bamba S, Naito Y, Andoh A (2018) Gut microbiota in the pathogenesis of inflammatory bowel disease. Clin J Gastroenterol 11:1–10. https://doi.org/10.1007/s12328-017-0813-5 DOI
Oh HJ, Kim JH, Bae JM, Kim HJ, Cho NY, Kang GH (2019) Prognostic impact of Fusobacterium nucleatum depends on combined tumor location and microsatellite instability status in stage II/III colorectal cancers treated with adjuvant chemotherapy. J Pathol Transl Med 53:40–49. https://doi.org/10.4132/jptm.2018.11.29 DOI
Oksanen J et al (2013) vegan: Community ecology package. R package version 2.0–10. http://CRAN.Rproject.org/package=vegan
Panebianco C, Andriulli A, Pazienza V (2018) Pharmacomicrobiomics: exploiting the drug-microbiota interactions in anticancer therapies. Microbiome 6:92. https://doi.org/10.1186/s40168-018-0483-7 DOI
Park CH, Eun CS, Han DS (2018) Intestinal microbiota, chronic inflammation, and colorectal cancer. Intest Res 16:338–345. https://doi.org/10.5217/ir.2018.16.3.338 DOI
Pascal V et al (2017) A microbial signature for Crohn’s disease. Gut 66:813–822. https://doi.org/10.1136/gutjnl-2016-313235 DOI
Peterson DA, Frank DN, Pace NR, Gordon JI (2008) Metagenomic approaches for defining the pathogenesis of inflammatory bowel diseases. Cell Host Microbe 3:417–427. https://doi.org/10.1016/j.chom.2008.05.001 DOI
Planell N et al (2013) Transcriptional analysis of the intestinal mucosa of patients with ulcerative colitis in remission reveals lasting epithelial cell alterations. Gut 62:967–976. https://doi.org/10.1136/gutjnl-2012-303333 DOI
Pleguezuelos-Manzano C et al (2020) Mutational signature in colorectal cancer caused by genotoxic pks+ E. coli. Nature 580:269–273. https://doi.org/10.1038/s41586-020-2080-8 DOI
Qin J et al (2012) A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 490:55–60. https://doi.org/10.1038/nature11450 DOI
Qin X, Gu Y, Liu T, Wang C, Zhong W, Wang B, Cao H (2021) Gut mycobiome: A promising target for colorectal cancer. Biochim Biophys Acta Rev Cancer 1875:188489. https://doi.org/10.1016/j.bbcan.2020.188489
Quaglio AEV, Grillo TG, De Oliveira ECS, Di Stasi LC, Sassaki LY (2022) Gut microbiota, inflammatory bowel disease and colorectal cancer. World J Gastroenterol 28:4053–4060. https://doi.org/10.3748/wjg.v28.i30.4053 DOI
R Development Core Team (2015) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria
Rognes T, Flouri T, Nichols B, Quince C, Mahé F (2016) VSEARCH: a versatile open source tool for metagenomics. PeerJ 4:e2584. https://doi.org/10.7717/peerj.2584
Rothschild D et al (2018) Environment dominates over host genetics in shaping human gut microbiota. Nature 555:210–215. https://doi.org/10.1038/nature25973 DOI
Ryma T, Samer A, Soufli I, Rafa H, Touil-Boukoffa C (2021) Role of probiotics and their metabolites in inflammatory bowel diseases (IBDs). Gastroenterol Insights 12:56–66. https://doi.org/10.3390/gastroent12010006 DOI
Saad MJ, Santos A, Prada PO (2016) Linking gut microbiota and inflammation to obesity and insulin resistance. Physiology (bethesda) 31:283–293. https://doi.org/10.1152/physiol.00041.2015 DOI
Schroeder BO, Bäckhed F (2016) Signals from the gut microbiota to distant organs in physiology and disease. Nat Med 22:1079–1089. https://doi.org/10.1038/nm.4185 DOI
Schwabe RF, Jobin C (2013) The microbiome and cancer. Nat Rev Cancer 13:800–812. https://doi.org/10.1038/nrc3610 DOI
Shah MS, DeSantis T, Yamal JM, Weir T, Ryan EP, Cope JL, Hollister EB (2018) Re-purposing 16S rRNA gene sequence data from within case paired tumor biopsy and tumor-adjacent biopsy or fecal samples to identify microbial markers for colorectal cancer. PloS One 13:e0207002. https://doi.org/10.1371/journal.pone.0207002
Shen XJ et al (2010) Molecular characterization of mucosal adherent bacteria and associations with colorectal adenomas. Gut Microbes 1:138–147. https://doi.org/10.4161/gmic.1.3.12360 DOI
Sokol H et al (2009) Low counts of Faecalibacterium prausnitzii in colitis microbiota. Inflamm Bowel Dis 15:1183–1189. https://doi.org/10.1002/ibd.20903 DOI
Strauss J et al (2011) Invasive potential of gut mucosa-derived Fusobacterium nucleatum positively correlates with IBD status of the host. Inflamm Bowel Dis 17:1971–1978. https://doi.org/10.1002/ibd.21606 DOI
The Human Microbiome Project Consortium (2012a) A framework for human microbiome research. Nature 486:215–221. https://doi.org/10.1038/nature11209 DOI
The Human Microbiome Project Consortium (2012b) Structure, function and diversity of the healthy human microbiome. Nature 486:207–214. https://doi.org/10.1038/nature11234 DOI
Tilg H, Adolph TE, Gerner RR, Moschen AR (2018) The intestinal microbiota in colorectal cancer. Cancer Cell 33:954–964. https://doi.org/10.1016/j.ccell.2018.03.004 DOI
Tiso M, Schechter AN (2015) Nitrate reduction to nitrite, nitric oxide and ammonia by gut bacteria under physiological conditions. PLOS One 10:e0119712. https://doi.org/10.1371/journal.pone.0119712
Tu P et al (2020) Gut microbiome toxicity: Connecting the environment and gut microbiome-associated diseases. Toxics 8:19. https://doi.org/10.3390/toxics8010019 DOI
Turnbaugh PJ, Ridaura VK, Faith JJ, Rey FE, Knight R, Gordon JI (2009) The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Trans Med 1:6ra14. https://doi.org/10.1126/scitranslmed.3000322
Tyakht AV et al (2013) Human gut microbiota community structures in urban and rural populations in Russia. Nat Commun 4:2469. https://doi.org/10.1038/ncomms3469 DOI
Vallianou N, Kounatidis D, Christodoulatos GS, Panagopoulos F, Karampela I, Dalamaga M (2021) Mycobiome and cancer: What is the evidence? Cancers (basel) 13:3149. https://doi.org/10.3390/cancers13133149 DOI
Volant S et al (2020) SHAMAN: a user-friendly website for metataxonomic analysis from raw reads to statistical analysis BMC Bioinformatics 21:345. https://doi.org/10.1186/s12859-020-03666-4
Walker AW et al (2011) High-throughput clone library analysis of the mucosa-associated microbiota reveals dysbiosis and differences between inflamed and non-inflamed regions of the intestine in inflammatory bowel disease. BMC Microbiol 11:7. https://doi.org/10.1186/1471-2180-11-7 DOI
Walujkar SA, Kumbhare SV, Marathe NP, Patangia DV, Lawate PS, Bharadwaj RS, Shouche YS (2018) Molecular profiling of mucosal tissue associated microbiota in patients manifesting acute exacerbations and remission stage of ulcerative colitis. World J Microbiol Biotechnol 34:76. https://doi.org/10.1007/s11274-018-2449-0 DOI
Wang T et al (2012) Structural segregation of gut microbiota between colorectal cancer patients and healthy volunteers. ISME J 6:320–329. https://doi.org/10.1038/ismej.2011.109 DOI
Wickham H (2016) ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag New York. https://ggplot2.tidyverse.org
Willing BP et al (2010) A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes. Gastroenterology 139:1844–1854. https://doi.org/10.1053/j.gastro.2010.08.049 DOI
Wirbel J et al (2019) Meta-analysis of fecal metagenomes reveals global microbial signatures that are specific for colorectal cancer. Nat Med 25:679–689. https://doi.org/10.1038/s41591-019-0406-6 DOI
Wu J, Li Q, Fu X (2019) Fusobacterium nucleatum contributes to the carcinogenesis of colorectal cancer by inducing inflammation and suppressing host immunity. Transl Oncol 12:846–851. https://doi.org/10.1016/j.tranon.2019.03.003 DOI
Wu N et al (2013) Dysbiosis signature of fecal microbiota in colorectal cancer patients. Microb Ecol 66:462–470. https://doi.org/10.1007/s00248-013-0245-9 DOI
Wu S et al (2009) A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses. Nat Med 15:1016–1022. https://doi.org/10.1038/nm.2015 DOI
Yang L et al (2019) Difference in pathomechanism between Crohn’s disease and ulcerative colitis revealed by colon transcriptome. Inflamm Bowel Dis 25:722–731. https://doi.org/10.1093/ibd/izy359 DOI
Zeller G et al (2014) Potential of fecal microbiota for early-stage detection of colorectal cancer. Mol Syst Biol 10:766. https://doi.org/10.15252/msb.20145645 .
Zhang X et al (2022) Salivary Fusobacterium nucleatum serves as a potential biomarker for colorectal cancer. iScience 25:104203. https://doi.org/10.1016/j.isci.2022.104203