Gallbladder microbial species and host bile acids biosynthesis linked to cholesterol gallstone comparing to pigment individuals

Gallstones are crystalline deposits in the gallbladder that are traditionally classified as cholesterol, pigment, or mixed stones based on their composition. Microbiota and host metabolism variances among the different types of gallstones remain largely unclear. Here, the bile and gallstone microbia...

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Main Authors: Xinpeng Zhang, Junqing Hu, Yi Li, Jichao Tang, Kaijin Yang, Ayan Zhong, Yanjun Liu, Tongtong Zhang
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-03-01
Series:Frontiers in Cellular and Infection Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcimb.2024.1283737/full
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author Xinpeng Zhang
Junqing Hu
Junqing Hu
Junqing Hu
Yi Li
Jichao Tang
Kaijin Yang
Ayan Zhong
Yanjun Liu
Yanjun Liu
Tongtong Zhang
Tongtong Zhang
Tongtong Zhang
author_facet Xinpeng Zhang
Junqing Hu
Junqing Hu
Junqing Hu
Yi Li
Jichao Tang
Kaijin Yang
Ayan Zhong
Yanjun Liu
Yanjun Liu
Tongtong Zhang
Tongtong Zhang
Tongtong Zhang
author_sort Xinpeng Zhang
collection DOAJ
description Gallstones are crystalline deposits in the gallbladder that are traditionally classified as cholesterol, pigment, or mixed stones based on their composition. Microbiota and host metabolism variances among the different types of gallstones remain largely unclear. Here, the bile and gallstone microbial species spectra of 29 subjects with gallstone disease (GSD, 24 cholesterol and 5 pigment) were revealed by type IIB restriction site-associated DNA microbiome sequencing (2bRAD-M). Among them (21 subjects: 18 cholesterol and 3 pigment), plasma samples were subjected to liquid chromatography–mass spectrometry (LC-MS) untargeted metabolomics. The microbiome yielded 896 species comprising 882 bacteria, 13 fungi, and 1 archaeon. Microbial profiling revealed significant enrichment of Cutibacterium acnes and Microbacterium sp005774735 in gallstone and Agrobacterium pusense and Enterovirga sp013044135 in the bile of cholesterol GSD subjects. The metabolome revealed 2296 metabolites, in which malvidin 3-(6’’-malonylglucoside), 2-Methylpropyl glucosinolate, and ergothioneine were markedly enriched in cholesterol GSD subjects. Metabolite set enrichment analysis (MSEA) demonstrated enriched bile acids biosynthesis in individuals with cholesterol GSD. Overall, the multi-omics analysis revealed that microbiota and host metabolism interaction perturbations differ depending on the disease type. Perturbed gallstone type-related microbiota may contribute to unbalanced bile acids metabolism in the gallbladder and host, representing a potential early diagnostic marker and therapeutic target for GSD.
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spelling doaj.art-3b375c80e2d343d58410f160cf72b6d92024-03-11T15:49:11ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882024-03-011410.3389/fcimb.2024.12837371283737Gallbladder microbial species and host bile acids biosynthesis linked to cholesterol gallstone comparing to pigment individualsXinpeng Zhang0Junqing Hu1Junqing Hu2Junqing Hu3Yi Li4Jichao Tang5Kaijin Yang6Ayan Zhong7Yanjun Liu8Yanjun Liu9Tongtong Zhang10Tongtong Zhang11Tongtong Zhang12General Surgery Day Ward, Department of General Surgery, The Third People’s Hospital of Chengdu, Affiliated Hospital of Southwest Jiaotong University & The Second Affiliated Hospital of Chengdu, Chongqing Medical University, Chengdu, ChinaCenter of Gastrointestinal and Minimally Invasive Surgery, Department of General Surgery, The Third People’s Hospital of Chengdu, Affiliated Hospital of Southwest Jiaotong University & The Second Affiliated Hospital of Chengdu, Chongqing Medical University, Chengdu, ChinaThe Center of Obesity and Metabolic Diseases, Department of General Surgery, The Third People’s Hospital of Chengdu, Affiliated Hospital of Southwest Jiaotong University & The Second Affiliated Hospital of Chengdu, Chongqing Medical University, Chengdu, ChinaMedical Research Center, The Third People’s Hospital of Chengdu, Affiliated Hospital of Southwest Jiaotong University & The Second Affiliated Hospital of Chengdu, Chongqing Medical University, Chengdu, ChinaGeneral Surgery Day Ward, Department of General Surgery, The Third People’s Hospital of Chengdu, Affiliated Hospital of Southwest Jiaotong University & The Second Affiliated Hospital of Chengdu, Chongqing Medical University, Chengdu, ChinaGeneral Surgery Day Ward, Department of General Surgery, The Third People’s Hospital of Chengdu, Affiliated Hospital of Southwest Jiaotong University & The Second Affiliated Hospital of Chengdu, Chongqing Medical University, Chengdu, ChinaGeneral Surgery Day Ward, Department of General Surgery, The Third People’s Hospital of Chengdu, Affiliated Hospital of Southwest Jiaotong University & The Second Affiliated Hospital of Chengdu, Chongqing Medical University, Chengdu, ChinaGeneral Surgery Day Ward, Department of General Surgery, The Third People’s Hospital of Chengdu, Affiliated Hospital of Southwest Jiaotong University & The Second Affiliated Hospital of Chengdu, Chongqing Medical University, Chengdu, ChinaCenter of Gastrointestinal and Minimally Invasive Surgery, Department of General Surgery, The Third People’s Hospital of Chengdu, Affiliated Hospital of Southwest Jiaotong University & The Second Affiliated Hospital of Chengdu, Chongqing Medical University, Chengdu, ChinaThe Center of Obesity and Metabolic Diseases, Department of General Surgery, The Third People’s Hospital of Chengdu, Affiliated Hospital of Southwest Jiaotong University & The Second Affiliated Hospital of Chengdu, Chongqing Medical University, Chengdu, ChinaCenter of Gastrointestinal and Minimally Invasive Surgery, Department of General Surgery, The Third People’s Hospital of Chengdu, Affiliated Hospital of Southwest Jiaotong University & The Second Affiliated Hospital of Chengdu, Chongqing Medical University, Chengdu, ChinaThe Center of Obesity and Metabolic Diseases, Department of General Surgery, The Third People’s Hospital of Chengdu, Affiliated Hospital of Southwest Jiaotong University & The Second Affiliated Hospital of Chengdu, Chongqing Medical University, Chengdu, ChinaMedical Research Center, The Third People’s Hospital of Chengdu, Affiliated Hospital of Southwest Jiaotong University & The Second Affiliated Hospital of Chengdu, Chongqing Medical University, Chengdu, ChinaGallstones are crystalline deposits in the gallbladder that are traditionally classified as cholesterol, pigment, or mixed stones based on their composition. Microbiota and host metabolism variances among the different types of gallstones remain largely unclear. Here, the bile and gallstone microbial species spectra of 29 subjects with gallstone disease (GSD, 24 cholesterol and 5 pigment) were revealed by type IIB restriction site-associated DNA microbiome sequencing (2bRAD-M). Among them (21 subjects: 18 cholesterol and 3 pigment), plasma samples were subjected to liquid chromatography–mass spectrometry (LC-MS) untargeted metabolomics. The microbiome yielded 896 species comprising 882 bacteria, 13 fungi, and 1 archaeon. Microbial profiling revealed significant enrichment of Cutibacterium acnes and Microbacterium sp005774735 in gallstone and Agrobacterium pusense and Enterovirga sp013044135 in the bile of cholesterol GSD subjects. The metabolome revealed 2296 metabolites, in which malvidin 3-(6’’-malonylglucoside), 2-Methylpropyl glucosinolate, and ergothioneine were markedly enriched in cholesterol GSD subjects. Metabolite set enrichment analysis (MSEA) demonstrated enriched bile acids biosynthesis in individuals with cholesterol GSD. Overall, the multi-omics analysis revealed that microbiota and host metabolism interaction perturbations differ depending on the disease type. Perturbed gallstone type-related microbiota may contribute to unbalanced bile acids metabolism in the gallbladder and host, representing a potential early diagnostic marker and therapeutic target for GSD.https://www.frontiersin.org/articles/10.3389/fcimb.2024.1283737/fullcholesterol gallstonegallbladder microbiota2bRAD-Mbile acids metabolismLC-MS metabolomicsmultiomics
spellingShingle Xinpeng Zhang
Junqing Hu
Junqing Hu
Junqing Hu
Yi Li
Jichao Tang
Kaijin Yang
Ayan Zhong
Yanjun Liu
Yanjun Liu
Tongtong Zhang
Tongtong Zhang
Tongtong Zhang
Gallbladder microbial species and host bile acids biosynthesis linked to cholesterol gallstone comparing to pigment individuals
Frontiers in Cellular and Infection Microbiology
cholesterol gallstone
gallbladder microbiota
2bRAD-M
bile acids metabolism
LC-MS metabolomics
multiomics
title Gallbladder microbial species and host bile acids biosynthesis linked to cholesterol gallstone comparing to pigment individuals
title_full Gallbladder microbial species and host bile acids biosynthesis linked to cholesterol gallstone comparing to pigment individuals
title_fullStr Gallbladder microbial species and host bile acids biosynthesis linked to cholesterol gallstone comparing to pigment individuals
title_full_unstemmed Gallbladder microbial species and host bile acids biosynthesis linked to cholesterol gallstone comparing to pigment individuals
title_short Gallbladder microbial species and host bile acids biosynthesis linked to cholesterol gallstone comparing to pigment individuals
title_sort gallbladder microbial species and host bile acids biosynthesis linked to cholesterol gallstone comparing to pigment individuals
topic cholesterol gallstone
gallbladder microbiota
2bRAD-M
bile acids metabolism
LC-MS metabolomics
multiomics
url https://www.frontiersin.org/articles/10.3389/fcimb.2024.1283737/full
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