Multi-kingdom microbial signatures in excess body weight colorectal cancer based on global metagenomic analysis

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Abstract

Excess body weight (EBW) increases the risk of colorectal cancer (CRC) and is linked to lower colonoscopy compliance. Here, we extensively analyzed 981 metagenome samples from multiple cohorts to pinpoint the specific microbial signatures and their potential capability distinguishing EBW patients with CRC. The gut microbiome displayed considerable variations between EBW and lean CRC. We identify 44 and 37 distinct multi-kingdom microbial species differentiating CRC and controls in EBW and lean populations, respectively. Unique bacterial-fungal associations are also observed between EBW-CRC and lean-CRC. Our analysis revealed specific microbial functions in EBW-CRC, including D-Arginine and D-ornithine metabolism, and lipopolysaccharide biosynthesis. The best-performing classifier for EBW-CRC, comprising 12 bacterial and three fungal species, achieved an AUROC of 0.90, which was robustly validated across three independent cohorts (AUROC = 0.96, 0.94, and 0.80). Pathogenic microbial species, Anaerobutyricum hallii, Clostridioides difficile and Fusobacterium nucleatum, are EBW-CRC specific signatures. This work unearths the specific multi-kingdom microbial signatures for EBW-CRC and lean CRC, which may contribute to precision diagnosis and treatment of CRC.

Abstract

Metagenomic analysis reveals distinctive multi-kingdom species, functional signatures and bacteria-fungi interactions pattern between excess body weight CRC and lean CRC in gut microbiome, which contribute to precision medicine of CRC.

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Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries

Hyuna Sung, Jacques Ferlay, Rebecca Siegel … (2021)

This article provides an update on the global cancer burden using the GLOBOCAN 2020 estimates of cancer incidence and mortality produced by the International Agency for Research on Cancer. Worldwide, an estimated 19.3 million new cancer cases (18.1 million excluding nonmelanoma skin cancer) and almost 10.0 million cancer deaths (9.9 million excluding nonmelanoma skin cancer) occurred in 2020. Female breast cancer has surpassed lung cancer as the most commonly diagnosed cancer, with an estimated 2.3 million new cases (11.7%), followed by lung (11.4%), colorectal (10.0 %), prostate (7.3%), and stomach (5.6%) cancers. Lung cancer remained the leading cause of cancer death, with an estimated 1.8 million deaths (18%), followed by colorectal (9.4%), liver (8.3%), stomach (7.7%), and female breast (6.9%) cancers. Overall incidence was from 2-fold to 3-fold higher in transitioned versus transitioning countries for both sexes, whereas mortality varied <2-fold for men and little for women. Death rates for female breast and cervical cancers, however, were considerably higher in transitioning versus transitioned countries (15.0 vs 12.8 per 100,000 and 12.4 vs 5.2 per 100,000, respectively). The global cancer burden is expected to be 28.4 million cases in 2040, a 47% rise from 2020, with a larger increase in transitioning (64% to 95%) versus transitioned (32% to 56%) countries due to demographic changes, although this may be further exacerbated by increasing risk factors associated with globalization and a growing economy. Efforts to build a sustainable infrastructure for the dissemination of cancer prevention measures and provision of cancer care in transitioning countries is critical for global cancer control.

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Multi-omics of the gut microbial ecosystem in inflammatory bowel diseases

Jason Lloyd-Price, Cesar Arze, Ashwin Ananthakrishnan … (2019)

Inflammatory bowel diseases, which include Crohn’s disease and ulcerative colitis, affect several million individuals worldwide. Crohn’s disease and ulcerative colitis are complex diseases that are heterogeneous at the clinical, immunological, molecular, genetic, and microbial levels. Individual contributing factors have been the focus of extensive research. As part of the Integrative Human Microbiome Project (HMP2 or iHMP), we followed 132 subjects for one year each to generate integrated longitudinal molecular profiles of host and microbial activity during disease (up to 24 time points each; in total 2,965 stool, biopsy, and blood specimens). Here we present the results, which provide a comprehensive view of functional dysbiosis in the gut microbiome during inflammatory bowel disease activity. We demonstrate a characteristic increase in facultative anaerobes at the expense of obligate anaerobes, as well as molecular disruptions in microbial transcription (for example, among clostridia), metabolite pools (acylcarnitines, bile acids, and short-chain fatty acids), and levels of antibodies in host serum. Periods of disease activity were also marked by increases in temporal variability, with characteristic taxonomic, functional, and biochemical shifts. Finally, integrative analysis identified microbial, biochemical, and host factors central to this dysregulation. The study’s infrastructure resources, results, and data, which are available through the Inflammatory Bowel Disease Multi’omics Database (http://ibdmdb.org), provide the most comprehensive description to date of host and microbial activities in inflammatory bowel diseases.

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Global burden of colorectal cancer: emerging trends, risk factors and prevention strategies

NaNa Keum, Edward Luciano Giovannucci (2019)

Globally, colorectal cancer (CRC) is the third most commonly diagnosed malignancy and the second leading cause of cancer death. Arising through three major pathways, including adenoma-carcinoma sequence, serrated pathway and inflammatory pathway, CRC represents an aetiologically heterogeneous disease according to subtyping by tumour anatomical location or global molecular alterations. Genetic factors such as germline MLH1 and APC mutations have an aetiologic role, predisposing individuals to CRC. Yet, the majority of CRC is sporadic and largely attributable to the constellation of modifiable environmental risk factors characterizing westernization (for example, obesity, physical inactivity, poor diets, alcohol drinking and smoking). As such, the burden of CRC is shifting towards low-income and middle-income countries as they become westernized. Furthermore, the rising incidence of CRC at younger ages (before age 50 years) is an emerging trend. This Review provides a comprehensive summary of CRC epidemiology, with emphasis on modifiable lifestyle and nutritional factors, chemoprevention and screening. Overall, the optimal reduction of CRC incidence and mortality will require concerted efforts to reduce modifiable risk factors, to leverage chemoprevention research and to promote population-wide and targeted screening.

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Author and article information

Contributors

Ruixin Zhu:

ORCID: http://orcid.org/0000-0002-5070-6453

rxzhu@tongji.edu.cn

Lixin Zhu:

ORCID: http://orcid.org/0000-0001-7904-1769

zhulx6@mail.sysu.edu.cn

Na Jiao:

ORCID: http://orcid.org/0000-0003-3976-6313

jiaona@zju.edu.cn

Journal

Journal ID (nlm-ta): Commun Biol

Journal ID (iso-abbrev): Commun Biol

Title: Communications Biology

Publisher: Nature Publishing Group UK (London )

ISSN (Electronic): 2399-3642

Publication date (Electronic): 5 January 2024

Publication date PMC-release: 5 January 2024

Publication date Collection: 2024

Volume: 7

Electronic Location Identifier: 24

Affiliations

[1 ]Putuo People’s Hospital, School of Life Sciences and Technology, Tongji University, ( https://ror.org/03rc6as71) Shanghai, PR China

[2 ]GRID grid.8547.e, ISNI 0000 0001 0125 2443, Department of Colorectal Surgery, Zhongshan Hospital, , Fudan University, ; Shanghai, PR China

[3 ]Guangdong Institute of Gastroenterology; Guangdong Provincial Key Laboratory of Colorectal and Pelvic Floor Diseases; Biomedical Innovation Center, Sun Yat-Sen University, ( https://ror.org/0064kty71) Guangzhou, PR China

[4 ]Department of General Surgery, The Sixth Affiliated Hospital of Sun Yat-Sen University, ( https://ror.org/005pe1772) Guangzhou, PR China

[5 ]National Clinical Research Center for Child Health, the Children’s Hospital, Zhejiang University School of Medicine, ( https://ror.org/025fyfd20) Hangzhou, Zhejiang PR China

Author information

Xinyue Zhu http://orcid.org/0009-0009-4168-6196

Ruixin Zhu http://orcid.org/0000-0002-5070-6453

Wenxing Gao http://orcid.org/0000-0002-1740-8227

Ping Lan http://orcid.org/0000-0002-8901-8498

Lixin Zhu http://orcid.org/0000-0001-7904-1769

Na Jiao http://orcid.org/0000-0003-3976-6313

Article

Publisher ID: 5714

DOI: 10.1038/s42003-023-05714-0

PMC ID: 10770074

PubMed ID: 38182885

SO-VID: 080b1128-cb79-4686-8659-111f44f37ac3

License:

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

History

Date received : 9 October 2023

Date accepted : 15 December 2023

Funding

Funded by: FundRef https://doi.org/10.13039/501100001809, National Natural Science Foundation of China (National Science Foundation of China);

Award ID: 82000536

Award Recipient : Na Jiao

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Keywords: cancer screening,clinical microbiology

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Keywords: cancer screening, clinical microbiology

Multi-kingdom microbial signatures in excess body weight colorectal cancer based on global metagenomic analysis

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Most cited references 59

Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries

Multi-omics of the gut microbial ecosystem in inflammatory bowel diseases

Global burden of colorectal cancer: emerging trends, risk factors and prevention strategies

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