Microbiome and metabolic features of tissues and feces reveal diagnostic biomarkers for colorectal cancer

Microbiome and their metabolites are increasingly being recognized for their role in colorectal cancer (CRC) carcinogenesis. Towards revealing new CRC biomarkers, we compared 16S rRNA gene sequencing and liquid chromatography-mass spectrometry (LC–MS) metabolite analyses in 10 CRC (TCRC) and normal...

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Main Authors: Jiahui Feng, Zhizhong Gong, Zhangran Sun, Juan Li, Na Xu, Rick F. Thorne, Xu Dong Zhang, Xiaoying Liu, Gang Liu
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-01-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1034325/full
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author Jiahui Feng
Zhizhong Gong
Zhangran Sun
Zhangran Sun
Juan Li
Na Xu
Rick F. Thorne
Rick F. Thorne
Xu Dong Zhang
Xu Dong Zhang
Xiaoying Liu
Xiaoying Liu
Gang Liu
author_facet Jiahui Feng
Zhizhong Gong
Zhangran Sun
Zhangran Sun
Juan Li
Na Xu
Rick F. Thorne
Rick F. Thorne
Xu Dong Zhang
Xu Dong Zhang
Xiaoying Liu
Xiaoying Liu
Gang Liu
author_sort Jiahui Feng
collection DOAJ
description Microbiome and their metabolites are increasingly being recognized for their role in colorectal cancer (CRC) carcinogenesis. Towards revealing new CRC biomarkers, we compared 16S rRNA gene sequencing and liquid chromatography-mass spectrometry (LC–MS) metabolite analyses in 10 CRC (TCRC) and normal paired tissues (THC) along with 10 matched fecal samples (FCRC) and 10 healthy controls (FHC). The highest microbial phyla abundance from THC and TCRC were Firmicutes, while the dominant phyla from FHC and FCRC were Bacteroidetes, with 72 different microbial genera identified among four groups. No changes in Chao1 indices were detected between tissues or between fecal samples whereas non-metric multidimensional scaling (NMDS) analysis showed distinctive clusters among fecal samples but not tissues. LEfSe analyses indicated Caulobacterales and Brevundimonas were higher in THC than in TCRC, while Burkholderialese, Sutterellaceaed, Tannerellaceaea, and Bacteroidaceae were higher in FHC than in FCRC. Microbial association networks indicated some genera had substantially different correlations. Tissue and fecal analyses indicated lipids and lipid-like molecules were the most abundant metabolites detected in fecal samples. Moreover, partial least squares discriminant analysis (PLS-DA) based on metabolic profiles showed distinct clusters for CRC and normal samples with a total of 102 differential metabolites between THC and TCRC groups and 700 metabolites different between FHC and FCRC groups. However, only Myristic acid was detected amongst all four groups. Highly significant positive correlations were recorded between genus-level microbiome and metabolomics data in tissue and feces. And several metabolites were associated with paired microbes, suggesting a strong microbiota-metabolome coupling, indicating also that part of the CRC metabolomic signature was attributable to microbes. Suggesting utility as potential biomarkers, most such microbiome and metabolites showed directionally consistent changes in CRC patients. Nevertheless, further studies are needed to increase sample sizes towards verifying these findings.
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spelling doaj.art-4d718631b83c477abeeeb80100f23bca2023-01-13T05:11:56ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-01-011410.3389/fmicb.2023.10343251034325Microbiome and metabolic features of tissues and feces reveal diagnostic biomarkers for colorectal cancerJiahui Feng0Zhizhong Gong1Zhangran Sun2Zhangran Sun3Juan Li4Na Xu5Rick F. Thorne6Rick F. Thorne7Xu Dong Zhang8Xu Dong Zhang9Xiaoying Liu10Xiaoying Liu11Gang Liu12School of Life Sciences, Anhui Medical University, Hefei, ChinaSchool of Life Sciences, Anhui Medical University, Hefei, ChinaSchool of Life Sciences, Anhui Medical University, Hefei, ChinaHenan International Joint Laboratory of Non-coding RNA and Metabolism in Cancer, Henan Provincial Key Laboratory of Long Non-coding RNA and Cancer Metabolism, Translational Research Institute of Henan Provincial People’s Hospital and People’s Hospital of Zhengzhou University, Zhengzhou, Henan, ChinaDepartment of Oncology, BinHu Hospital of Hefei, Hefei, ChinaSchool of Life Sciences, Anhui Medical University, Hefei, ChinaHenan International Joint Laboratory of Non-coding RNA and Metabolism in Cancer, Henan Provincial Key Laboratory of Long Non-coding RNA and Cancer Metabolism, Translational Research Institute of Henan Provincial People’s Hospital and People’s Hospital of Zhengzhou University, Zhengzhou, Henan, ChinaSchool of Biomedical Sciences and Pharmacy, The University of Newcastle, Callaghan, NSW, AustraliaHenan International Joint Laboratory of Non-coding RNA and Metabolism in Cancer, Henan Provincial Key Laboratory of Long Non-coding RNA and Cancer Metabolism, Translational Research Institute of Henan Provincial People’s Hospital and People’s Hospital of Zhengzhou University, Zhengzhou, Henan, ChinaSchool of Biomedical Sciences and Pharmacy, The University of Newcastle, Callaghan, NSW, AustraliaSchool of Life Sciences, Anhui Medical University, Hefei, ChinaHenan International Joint Laboratory of Non-coding RNA and Metabolism in Cancer, Henan Provincial Key Laboratory of Long Non-coding RNA and Cancer Metabolism, Translational Research Institute of Henan Provincial People’s Hospital and People’s Hospital of Zhengzhou University, Zhengzhou, Henan, ChinaSchool of Life Sciences, Anhui Medical University, Hefei, ChinaMicrobiome and their metabolites are increasingly being recognized for their role in colorectal cancer (CRC) carcinogenesis. Towards revealing new CRC biomarkers, we compared 16S rRNA gene sequencing and liquid chromatography-mass spectrometry (LC–MS) metabolite analyses in 10 CRC (TCRC) and normal paired tissues (THC) along with 10 matched fecal samples (FCRC) and 10 healthy controls (FHC). The highest microbial phyla abundance from THC and TCRC were Firmicutes, while the dominant phyla from FHC and FCRC were Bacteroidetes, with 72 different microbial genera identified among four groups. No changes in Chao1 indices were detected between tissues or between fecal samples whereas non-metric multidimensional scaling (NMDS) analysis showed distinctive clusters among fecal samples but not tissues. LEfSe analyses indicated Caulobacterales and Brevundimonas were higher in THC than in TCRC, while Burkholderialese, Sutterellaceaed, Tannerellaceaea, and Bacteroidaceae were higher in FHC than in FCRC. Microbial association networks indicated some genera had substantially different correlations. Tissue and fecal analyses indicated lipids and lipid-like molecules were the most abundant metabolites detected in fecal samples. Moreover, partial least squares discriminant analysis (PLS-DA) based on metabolic profiles showed distinct clusters for CRC and normal samples with a total of 102 differential metabolites between THC and TCRC groups and 700 metabolites different between FHC and FCRC groups. However, only Myristic acid was detected amongst all four groups. Highly significant positive correlations were recorded between genus-level microbiome and metabolomics data in tissue and feces. And several metabolites were associated with paired microbes, suggesting a strong microbiota-metabolome coupling, indicating also that part of the CRC metabolomic signature was attributable to microbes. Suggesting utility as potential biomarkers, most such microbiome and metabolites showed directionally consistent changes in CRC patients. Nevertheless, further studies are needed to increase sample sizes towards verifying these findings.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1034325/fullcolorectal cancergut microbiomemetabolomicsbiomarkerstissuefeces
spellingShingle Jiahui Feng
Zhizhong Gong
Zhangran Sun
Zhangran Sun
Juan Li
Na Xu
Rick F. Thorne
Rick F. Thorne
Xu Dong Zhang
Xu Dong Zhang
Xiaoying Liu
Xiaoying Liu
Gang Liu
Microbiome and metabolic features of tissues and feces reveal diagnostic biomarkers for colorectal cancer
Frontiers in Microbiology
colorectal cancer
gut microbiome
metabolomics
biomarkers
tissue
feces
title Microbiome and metabolic features of tissues and feces reveal diagnostic biomarkers for colorectal cancer
title_full Microbiome and metabolic features of tissues and feces reveal diagnostic biomarkers for colorectal cancer
title_fullStr Microbiome and metabolic features of tissues and feces reveal diagnostic biomarkers for colorectal cancer
title_full_unstemmed Microbiome and metabolic features of tissues and feces reveal diagnostic biomarkers for colorectal cancer
title_short Microbiome and metabolic features of tissues and feces reveal diagnostic biomarkers for colorectal cancer
title_sort microbiome and metabolic features of tissues and feces reveal diagnostic biomarkers for colorectal cancer
topic colorectal cancer
gut microbiome
metabolomics
biomarkers
tissue
feces
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1034325/full
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