Multi-omics analysis reveals associations between gut microbiota and host transcriptome in colon cancer patients

Study information

Reviewed Marked as Reviewed by Svetlana up on 2025-3-26

study design

case-control

Citation

PMID PubMed identifier for scientific articles.

40013792

DOI Digital object identifier for electronic documents.

10.1128/msystems.00805-24

URI Uniform resource identifier for web resources.

Authors

Qin Y, Wang Q, Lin Q, Liu F, Pan X, Wei C, Chen J, Huang T, Fang M, Yang W, Pan L

Journal

mSystems

Year

2025

Keywords:

bile secretion, colon cancer, correlation, immune, mucosal microbiota, multi-omics, survival value

UNLABELLED: Colon cancer (CC) is one of the most common cancers globally, which is associated with the gut microbiota intimately. In current research, exploring the complex interaction between microbiomes and CC is a hotspot. However, the information on microbiomes in most previous studies is based on fecal, which does not fully display the microbial environment of CC. Herein, we collected mucosal and tissue samples from both the tumor and normal regions of 19 CC patients and clarified the composition of mucosal microbiota by 16S rRNA and metagenomic sequencing. Additionally, RNA-Seq was also conducted to identify the different expression genes between tumor and normal tissue samples. We revealed significantly different microbial community structures and expression profiles to CC. Depending on correlation analysis, we demonstrated that 1,472 genes were significantly correlated with CC tumor microbiota. Our study reveals a significant enrichment of Campylobacter jejuni in the mucosa of CC, which correlates with bile secretion. Additionally, we observe a negative correlation between C. jejuni and immune cells CD4+ Tem and mast cells. Finally, we discovered that metabolic bacterial endosymbiont of Bathymodiolus sp., Bacillus wiedmannii, and Mycobacterium tuberculosis had a significant survival value for CC, which was ignored by previous research. Overall, our study expands the understanding of the complex interplay between microbiota and CC and provides new targets for the treatment of CC. IMPORTANCE: This study contributes to our understanding of the interaction between microbiota and colon cancer (CC). By examining mucosal and tissue samples rather than solely relying on fecal samples, we have uncovered previously unknown aspects of CC-associated microbiota. Our findings reveal distinct microbial community structures and gene expression profiles correlated with CC progression. Notably, the enrichment of Campylobacter jejuni in CC mucosa, linked to bile secretion, underscores potential mechanisms in CC pathogenesis. Additionally, observed correlations between microbial taxa and immune cell populations offer new avenues for immunotherapy research in CC. Importantly, this study introduces CC-associated microbiota with survival implications for CC, expanding therapeutic targets beyond conventional strategies. By elucidating these correlations, our study not only contributes to uncovering the potential role of gut microbiota in colon cancer but also establishes a foundation for mechanistic studies of gut microbiota in colon cancer, emphasizing the broader impact of microbiota research on cancer biology.

Experiment 1

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Reviewed Marked as Reviewed by Svetlana up on 2025-3-26

Curated date: 2025/03/21

Curator: Victoria

Revision editor(s): Victoria

Subjects

Location of subjects: China

Host species Species from which microbiome was sampled. Contact us to have more species added.: Homo sapiens

Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology: Mucosa Mucosa of organ,Mucosa of organ part,Mucosal region,Mucous membrane,Organ mucosa,Region of mucosa,Tunica mucosa,Mucosa,mucosa

Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology: Colon carcinoma carcinoma of colon,carcinoma of the colon,colon cancer,colon carcinoma,colonic carcinoma,Colon carcinoma

Group 0 name Corresponds to the control (unexposed) group for case-control studies: Normal group

Group 1 name Corresponds to the case (exposed) group for case-control studies: Tumor group

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group: Patients in this group had radical resection of colon cancer tumors and were diagnosed with colon cancer for the first time, confirmed by colonoscopy pathology.

Group 0 sample size Number of subjects in the control (unexposed) group: 19

Group 1 sample size Number of subjects in the case (exposed) group: 19

Antibiotics exclusion Number of days without antibiotics usage (if applicable) and other antibiotics-related criteria used to exclude participants (if any): 1 month

Lab analysis

Sequencing type: 16S

16S variable region One or more hypervariable region(s) of the bacterial 16S gene: V3-V5

Sequencing platform Manufacturer and experimental platform used for quantifying microbial abundance: Illumina

Statistical Analysis

Data transformation Data transformation applied to microbial abundance measurements prior to differential abundance testing (if any).: relative abundances

Statistical test: LEfSe

Significance threshold p-value or FDR threshold used for differential abundance testing (if any): 0.05

MHT correction Have statistical tests be corrected for multiple hypothesis testing (MHT)?: No

LDA Score above Threshold for the linear discriminant analysis (LDA) score for studies using the popular LEfSe tool: 3

Alpha Diversity

Richness Number of species: decreased

Signature 1

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Reviewed Marked as Reviewed by Svetlana up on 2025-3-26

Curated date: 2025/03/22

Curator: Victoria

Revision editor(s): Victoria

Source: Figure 2f

Description: Distribution histogram of LDA values of different species (LDA > 3).

Abundance in Group 1: increased abundance in Tumor group

NCBI	Quality Control	Links
Salmonella enterica
Klebsiella aerogenes
Bacillus cereus
Bacillus pseudomycoides
Staphylococcus aureus
Chlamydia trachomatis
Streptococcus pneumoniae
Bacillus wiedmannii
Mycobacterium tuberculosis
Streptococcus dysgalactiae
Human endogenous retrovirus
Pseudomonas aeruginosa
Campylobacter jejuni
Mycobacterium sp. 1100029.7
methanotrophic bacterial endosymbiont of Bathymodiolus sp.