Metagenomic analysis of colorectal cancer datasets identifies cross-cohort microbial diagnostic signatures and a link with choline degradation
Open accessAbstract
Several studies have investigated links between the gut microbiome and colorectal cancer (CRC), but questions remain about the replicability of biomarkers across cohorts and populations. We performed a meta-analysis of five publicly available datasets and two new cohorts and validated the findings on two additional cohorts, considering in total 969 fecal metagenomes. Unlike microbiome shifts associated with gastrointestinal syndromes, the gut microbiome in CRC showed reproducibly higher richness than controls (P < 0.01), partially due to expansions of species typically derived from the oral cavity. Meta-analysis of the microbiome functional potential identified gluconeogenesis and the putrefaction and fermentation pathways as being associated with CRC, whereas the stachyose and starch degradation pathways were associated with controls. Predictive microbiome signatures for CRC trained on multiple datasets showed consistently high accuracy in datasets not considered for model training and independent validation cohorts (average area under the curve, 0.84). Pooled analysis of raw metagenomes showed that the choline trimethylamine-lyase gene was overabundant in CRC (P = 0.001), identifying a relationship between microbiome choline metabolism and CRC. The combined analysis of heterogeneous CRC cohorts thus identified reproducible microbiome biomarkers and accurate disease-predictive models that can form the basis for clinical prognostic tests and hypothesis-driven mechanistic studies. Multicohort analysis identifies microbial signatures of colorectal cancer in fecal microbiomes.
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Streptococcus gallolyticus is potentially associated with disease, including colorectal cancer (11% prevalence vs. 3% in healthy controls).
“Streptococcus gallolyticus is similarly potentially associated with disease, including colorectal cancer 112-114 (11% prevalence vs. 3% in healthy controls; Table S4), and was also prevalent in food.”
From Unexplored microbial diversity from 2,500 food metagenomes and links with the human microbiome. (2024) · cites this paper as [112]
The Results section ('A panel of microbial biomarkers for CRC is reproducible across cohorts'; page not provided) confirms Streptococcus gallolyticus as a relevant colorectal-cancer biomarker. Our copy does not report the claimed 11% prevalence in cases versus 3% in healthy controls, so it supports the association but not those figures. (LLM, conf=0.87)
Experimental — accuracy not yet measuredThe lack of solid cross-study reproducible microbial biomarkers of ICI response is not attributable to analytical choices, as applying the same meta-analysis methods in colorectal cancer confirmed strong and consistent biomarkers across cohorts.
“The lack of solid cross-study reproducible microbial biomarkers of ICI response is not attributable to analytical choices, as applying the same meta-analysis methods in the context of colorectal cancer confirmed the strong and consistent biomarkers across cohorts described elsewhere13,14.”
From Cross-cohort gut microbiome associations with immune checkpoint inhibitor response in advanced melanoma (2022) · cites this paper as [14]
Enrichment of bacterial species from oral cavity is characteristic of CRC GOMS, along with enrichment in invasive polymicrobial bacterial biofilms in patients with right-sided tumours.
“The enrichment of bacterial species from the oral cavity is characteristic of the CRC GOMS50,76–79, along with an enrichment in invasive polymicrobial bacterial biofilms in patients with right-sided tumours76,80,81.”
From Gut OncoMicrobiome Signatures (GOMS) as next-generation biomarkers for cancer immunotherapy (2023) · cites this paper as [50]
CRC gut microbiome signature identified using supervised machine learning and meta-analysis included Solobacterium moorei, Fusobacterium nucleatum, Parvimonas micra, Peptostreptococcus stomatis, Peptostreptococcus anaerobius, and Gemella morbillorum.
“This signature, identified using both supervised machine learning and a meta-analysis, included the bacterial species Solobacterium moorei, Fusobacterium nucleatum, Parvimonas micra, Peptostreptococcus stomatis, Peptostreptococcus anaerobius and Gemella morbillorum”
From Gut OncoMicrobiome Signatures (GOMS) as next-generation biomarkers for cancer immunotherapy (2023) · cites this paper as [50]
A meta-analysis of metagenomic data found higher richness in colorectal cancer microbiomes than controls, partly from expansions of species typically from the oral cavity.
“However, a meta-analysis of metagenomic data from different cohorts and populations found higher richness in microbiomes of CRC than controls, partly due to expansions of species typically derived from the oral cavity.16, 17”
From Influence of the Gut Microbiome, Diet, and Environment on Risk of Colorectal Cancer (2020) · cites this paper as [16]
Given metagenomic enrichment of choline-metabolizing pathways in colorectal cancer patients, these findings support benefits of physical activity in reducing trimethylamine N-oxide production and colorectal cancer risk.
“Give the finding of metagenomic enrichment of choline-metabolizing pathways in patients with CRC, 16 these findings support the benefits of physical activity in reducing production of TMAO and risk of CRC.”
From Influence of the Gut Microbiome, Diet, and Environment on Risk of Colorectal Cancer (2020) · cites this paper as [16]
Compared with controls, colorectal cancer patients had lower abundances of Bifidobacterium and Lactobacillus spp. and other short-chain fatty acid-producing bacteria such as Clostridium, Roseburia, Lachnospiraceae, and Faecalibacterium prausnitzii.
“several studies have shown that compared with controls, patients with CRC had lower abundances of Bifidobacterium and Lactobacillus spp,16, 18 and other SCFA-producing bacteria, such as the genera Clostridium and Roseburia, the family Lachnospiraceae, and Faecalibacterium prausnitzii.15, 35, 37, 45, 53, 129”
From Influence of the Gut Microbiome, Diet, and Environment on Risk of Colorectal Cancer (2020) · cites this paper as [16]
Stool microbiome testing detects adenomas with moderate accuracy, with validation AUCs between 0.55 and 0.67, which is below its accuracy for colorectal cancer.
“Fecal microbiome analysis identifies patients with adenomas with reasonable levels of accuracy (area under receiver operating curves ranging from 0.55 to 0.67 in validation studies), although this is a lower value than for detection of CRC.16, 18, 186–188”
From Influence of the Gut Microbiome, Diet, and Environment on Risk of Colorectal Cancer (2020) · cites this paper as [16]
Several Faecalibacterium prausnitzii SGBs are linked to favorable prognosis in multiple cancer types.
“Various F. prausnitzii SGBs are associated with favorable prognosis in patients diagnosed with several cancer types 23,24,56”
From Impact of the ONCOBIOME network in cancer microbiome research (2025) · cites this paper as [24]
Strains, species, or subspecies, rather than higher-level taxa such as genera or phyla, are the entities that gain clinical relevance as favorable or unfavorable.
“it appears that specific strains, species or subspecies, rather than higher-level classifications (for example, genera, phyla), acquire clinical relevance as favorable or unfavorable entities 19,23,24 .”
From Impact of the ONCOBIOME network in cancer microbiome research (2025) · cites this paper as [24]
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“Streptococcus gallolyticus is similarly potentially associated with disease, including colorectal cancer 112–114 (11% prevalence vs. 3% in healthy controls; Table S4), and was also prevalent in food.”
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“In contrast to colorectal cancer (Thomas et al., 2019), there remains a large gap in our knowledge detailing how the microbiome composition of cancer patients with non-GI indications compares to that of healthy donors.”
BackgroundFacts and Hopes for Gut Microbiota Interventions in Cancer Immunotherapy
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- Authors
- Thomas, A. M., Manghi, P., Asnicar, F., Pasolli, E., Armanini, F., Zolfo, M., Beghini, F., Manara, S., Karcher, N., Pozzi, C., Gandini, S., Serrano, D., Tarallo, S., Francavilla, A., Gallo, G., Trompetto, M., Ferrero, G., Mizutani, S., Shiroma, H., Shiba, S., Shibata, T., Yachida, S., Yamada, T., Wirbel, J., Schrotz-King, P., Ulrich, C. M., Brenner, H., Arumugam, M., Bork, P., Zeller, G., Cordero, F., Dias-Neto, E., Setubal, J. C., Tett, A., Pardini, B., Rescigno, M., Waldron, L., Naccarati, A., & Segata, N.
- Affiliations
- Universidade de São Paulo (BR)
- University of Trento (IT)
- European Institute of Oncology (IT)
- Italian institute for Genomic Medicine (IT)
- Magna Graecia University (IT)
- University of Turin (IT)
- Tokyo Institute of Technology (JP)
- National Cancer Center Research Institute (JP)
- Institute of Medical Science, The University of Tokyo (JP)
- European Molecular Biology Laboratory (DE)
- University of Utah (US)
- German Cancer Research Center (DE)
- University of Copenhagen (DK)
- City University of New York (US)
- Corresponding author
- Segata, Nicola
- ORCID
- Thomas, Andrew Maltez
- Manghi, Paolo
- Asnicar, Francesco
- Pasolli, Edoardo
- Armanini, Federica
- Zolfo, Moreno
- Beghini, Francesco
- Manara, Serena
- Karcher, Nicolai
- Pozzi, Chiara
- Gandini, Sara
- Serrano, Davide
- Tarallo, Sonia
- Francavilla, Antonio
- Gallo, Gaetano
- Trompetto, Mario
- Ferrero, Giulio
- Mizutani, Sayaka
- Shiroma, Hirotsugu
- Shiba, Satoshi
- Shibata, Tatsuhiro
- Yachida, Shinichi
- Yamada, Takuji
- Wirbel, Jakob
- Schrotz-King, Petra
- Ulrich, Cornelia M.
- Brenner, Hermann
- Arumugam, Manimozhiyan
- Bork, Peer
- Zeller, Georg
- Cordero, Francesca
- Dias-Neto, Emmanuel
- Tett, Adrian
- Pardini, Barbara
- Waldron, Levi
- Naccarati, Alessio
- Segata, Nicola
- Venue
- Nature Medicine
- Published
- 2019-04
- Volume
- 25
- Issue
- 4
- Pages
- 667-678
- ISSN
- 1078-8956 (ISSN-L)
- 1546-170X
- PMC
- PMC9533319
- OpenAlex
- W2932049125
- Semantic Scholar
- 53a7e9051e837d1fbfd8bc55900c4e388c562d6c
- Cited by
- 1,030
- References
- 84
- Citations by year
- 2026: 153 · 2025: 138 · 2024: 177 · 2023: 143 · 2022: 129 · 2021: 139 · 2020: 110 · 2019: 37 · 2017: 1 · 2016: 1
- FWCI
- 34.34
- Type
- journal article
- Language
- en
- Update notices
- correction (2019-10-29)
- Open access
- Licence
- other-oa
- www.springer.com/tdm (tdm)
- Locations
- Nature Medicine (publishedVersion)
- PubMed (publishedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (publishedVersion, other-oa)
- PubMed Central (acceptedVersion)
- Iris (University of Trento) (submittedVersion, public-domain)
- Institutional Research Information System University of Turin (University of Turin) (submittedVersion, public-domain)
- University of Southern Denmark Research Portal (University of Southern Denmark) (submittedVersion, public-domain)
- MDC Repository (Max-Delbrueck-Center for Molecular Medicine) (submittedVersion)
- IRIS Research product catalog (Sapienza University of Rome) (submittedVersion)
- Archivio Istituzionale della Ricerca - Università Vita-Salute San Raffaele (submittedVersion)
- Funders
- Compagnia di San Paolo
- Suzuken Memorial Foundation
- Deutsches Krebsforschungszentrum
- Japan Agency for Medical Research and Development (221S0002, 18ek0109187h0003)
- Huntsman Cancer Foundation (R01 CA189184, P30CA042014, U01CA206110, 01KT1503)
- European Commission (707345, H2020, 669830)
- Fundação de Amparo à Pesquisa do Estado de São Paulo (14/26897-0)
- Grantová Agentura České Republiky (GA17-16857S)
- Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
- Bundesministerium für Bildung und Forschung (01KT1503, R01 CA189184, R01 CA207371, U01 CA206110, 031A537B)
- Eidgenössische Technische Hochschule Zürich
- Ministero dell’Istruzione, dell’Università e della Ricerca (H2020, RBFR13EWWI_001, year 2018)
- Conselho Nacional de Desenvolvimento Científico e Tecnológico
- Università degli Studi di Trento
- Novo Nordisk (NNF10CC1016515)
- Fondazione Umberto Veronesi
- University of Tokyo
- Novo Nordisk Fonden (NNF10CC1016515)
- Helmut Horten Stiftung
- German Network for Bioinformatics Infrastructure (031 A537B)
- National Institutes of Health (ERC-2010-AdG_20100317, 221S0002, H2020)
- Horizon 2020 Framework Programme (707345)
- Japan Society for the Promotion of Science (16J10135, 16H06279, 18K15800, 221S0002)
- Japan Science and Technology Agency (JPMJPR1507)
- Strategic Research Council
- Institute of Medical Science, University of Tokyo
- National Cancer Institute (R01CA189184, U24CA180996, R01CA207371, CA042014, CA189184, P30CA042014, R01CA230551, U01CA206110)
- National Institute of Allergy and Infectious Diseases (R21AI121784)
- Precursory Research for Embryonic Science and Technology (JPMJPR1507)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
- Health Sciences › Medicine › Oncology › Colorectal Cancer Treatments and Studies
- Keywords
- colorectal cancer, gut microbiota, microbiome biomarkers, cross-cohort validation, choline metabolism, trimethylamine N-oxide, gut microbiota diversity, gluconeogenesis, metagenomics
- MeSH terms
- Gastrointestinal Microbiome, Choline, Humans, Lyases, Species Specificity, Biomarkers, Tumor, Colorectal Neoplasms, Cohort Studies, Databases, Genetic, Metagenomics
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