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Tumor bacterial markers diagnose the initiation and four stages of colorectal cancer

Increasing evidence has supported dysbiosis in the faecal microbiome along control-adenoma-carcinoma sequence. In contrast, the data is lacking for in situ tumor bacterial community over colorectal cancer (CRC) progression, resulting in the uncertainties of identifying CRC-associated taxa and diagno...

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Autores principales: Cai, Ping, Xiong, Jinbo, Sha, Haonan, Dai, Xiaoyu, Lu, Jiaqi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10040638/
https://www.ncbi.nlm.nih.gov/pubmed/36992683
http://dx.doi.org/10.3389/fcimb.2023.1123544
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author Cai, Ping
Xiong, Jinbo
Sha, Haonan
Dai, Xiaoyu
Lu, Jiaqi
author_facet Cai, Ping
Xiong, Jinbo
Sha, Haonan
Dai, Xiaoyu
Lu, Jiaqi
author_sort Cai, Ping
collection PubMed
description Increasing evidence has supported dysbiosis in the faecal microbiome along control-adenoma-carcinoma sequence. In contrast, the data is lacking for in situ tumor bacterial community over colorectal cancer (CRC) progression, resulting in the uncertainties of identifying CRC-associated taxa and diagnosing the sequential CRC stages. Through comprehensive collection of benign polyps (BP, N = 45) and the tumors (N = 50) over the four CRC stages, we explored the dynamics of bacterial communities over CRC progression using amplicons sequencing. Canceration was the primarily factor governing the bacterial community, followed by the CRC stages. Besides confirming known CRC-associated taxa using differential abundance, we identified new CRC driver species based on their keystone features in NetShift, including Porphyromonas endodontalis, Ruminococcus torques and Odoribacter splanchnicus. Tumor environments were less selective for stable core community, resulting in heterogeneity in bacterial communities over CRC progression, as supported by higher average variation degree, lower occupancy and specificity compared with BP. Intriguingly, tumors could recruit beneficial taxa antagonizing CRC-associated pathogens at CRC initiation, a pattern known as “cry-for-help”. By distinguishing age- from CRC stage-associated taxa, the top 15 CRC stage-discriminatory taxa contributed an overall 87.4% accuracy in diagnosing BP and each CRC stage, in which no CRC patients were falsely diagnosed as BP. The accuracy of diagnosis model was unbiased by human age and gender. Collectively, our findings provide new CRC-associated taxa and updated interpretations for CRC carcinogenesis from an ecological perspective. Moving beyond stratifying case-control, the CRC-stage discriminatory taxa could add the diagnosis of BP and the four CRC stages, especially the patients with poor pathological feature and un-reproducibility between two observers.
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spelling pubmed-100406382023-03-28 Tumor bacterial markers diagnose the initiation and four stages of colorectal cancer Cai, Ping Xiong, Jinbo Sha, Haonan Dai, Xiaoyu Lu, Jiaqi Front Cell Infect Microbiol Cellular and Infection Microbiology Increasing evidence has supported dysbiosis in the faecal microbiome along control-adenoma-carcinoma sequence. In contrast, the data is lacking for in situ tumor bacterial community over colorectal cancer (CRC) progression, resulting in the uncertainties of identifying CRC-associated taxa and diagnosing the sequential CRC stages. Through comprehensive collection of benign polyps (BP, N = 45) and the tumors (N = 50) over the four CRC stages, we explored the dynamics of bacterial communities over CRC progression using amplicons sequencing. Canceration was the primarily factor governing the bacterial community, followed by the CRC stages. Besides confirming known CRC-associated taxa using differential abundance, we identified new CRC driver species based on their keystone features in NetShift, including Porphyromonas endodontalis, Ruminococcus torques and Odoribacter splanchnicus. Tumor environments were less selective for stable core community, resulting in heterogeneity in bacterial communities over CRC progression, as supported by higher average variation degree, lower occupancy and specificity compared with BP. Intriguingly, tumors could recruit beneficial taxa antagonizing CRC-associated pathogens at CRC initiation, a pattern known as “cry-for-help”. By distinguishing age- from CRC stage-associated taxa, the top 15 CRC stage-discriminatory taxa contributed an overall 87.4% accuracy in diagnosing BP and each CRC stage, in which no CRC patients were falsely diagnosed as BP. The accuracy of diagnosis model was unbiased by human age and gender. Collectively, our findings provide new CRC-associated taxa and updated interpretations for CRC carcinogenesis from an ecological perspective. Moving beyond stratifying case-control, the CRC-stage discriminatory taxa could add the diagnosis of BP and the four CRC stages, especially the patients with poor pathological feature and un-reproducibility between two observers. Frontiers Media S.A. 2023-03-13 /pmc/articles/PMC10040638/ /pubmed/36992683 http://dx.doi.org/10.3389/fcimb.2023.1123544 Text en Copyright © 2023 Cai, Xiong, Sha, Dai and Lu https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cellular and Infection Microbiology
Cai, Ping
Xiong, Jinbo
Sha, Haonan
Dai, Xiaoyu
Lu, Jiaqi
Tumor bacterial markers diagnose the initiation and four stages of colorectal cancer
title Tumor bacterial markers diagnose the initiation and four stages of colorectal cancer
title_full Tumor bacterial markers diagnose the initiation and four stages of colorectal cancer
title_fullStr Tumor bacterial markers diagnose the initiation and four stages of colorectal cancer
title_full_unstemmed Tumor bacterial markers diagnose the initiation and four stages of colorectal cancer
title_short Tumor bacterial markers diagnose the initiation and four stages of colorectal cancer
title_sort tumor bacterial markers diagnose the initiation and four stages of colorectal cancer
topic Cellular and Infection Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10040638/
https://www.ncbi.nlm.nih.gov/pubmed/36992683
http://dx.doi.org/10.3389/fcimb.2023.1123544
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