Meta-analysis reveals Helicobacter pylori mutual exclusivity and reproducible gastric microbiome alterations during gastric carcinoma progression

ABSTRACTAccumulating evidence shows that the gastric bacterial community may contribute to the development of gastric cancer (GC). However, the reported alterations of gastric microbiota were not always consistent among the literature. To assess reproducible signals in gastric microbiota during the...

Full description

Bibliographic Details
Main Authors: Yan Li, Yichen Hu, Xiang Zhan, Ying Song, Meng Xu, Shijie Wang, Xiaochang Huang, Zhenjiang Zech Xu
Format: Article
Language:English
Published: Taylor & Francis Group 2023-12-01
Series:Gut Microbes
Subjects:
Online Access:https://www.tandfonline.com/doi/10.1080/19490976.2023.2197835
_version_ 1827303830771990528
author Yan Li
Yichen Hu
Xiang Zhan
Ying Song
Meng Xu
Shijie Wang
Xiaochang Huang
Zhenjiang Zech Xu
author_facet Yan Li
Yichen Hu
Xiang Zhan
Ying Song
Meng Xu
Shijie Wang
Xiaochang Huang
Zhenjiang Zech Xu
author_sort Yan Li
collection DOAJ
description ABSTRACTAccumulating evidence shows that the gastric bacterial community may contribute to the development of gastric cancer (GC). However, the reported alterations of gastric microbiota were not always consistent among the literature. To assess reproducible signals in gastric microbiota during the progression of GC across studies, we performed a meta-analysis of nine publicly available 16S datasets with standard tools of the state-of-the-art. Despite study-specific batch effect, significant changes in the composition of the gastric microbiome were found during the progression of gastric carcinogenesis, especially when the Helicobacter pylori (HP) reads were removed from analyses to mitigate its compositional effect as they accounted for extremely large proportions of sequencing depths in many gastric samples. Differential microbes, including Fusobacterium, Leptotrichia, and several lactic acid bacteria such as Bifidobacterium, Lactobacillus, and Streptococcus anginosus, which were frequently and significantly enriched in GC patients compared with gastritis across studies, had good discriminatory capacity to distinguish GC samples from gastritis. Oral microbes were significantly enriched in GC compared to precancerous stages. Intriguingly, we observed mutual exclusivity of different HP species across studies. In addition, the comparison between gastric fluid and mucosal microbiome suggested their convergent dysbiosis during gastric disease progression. Taken together, our systematic analysis identified novel and consistent microbial patterns in gastric carcinogenesis.
first_indexed 2024-03-11T14:20:51Z
format Article
id doaj.art-eccb9e7ff48b475e8a5e47bacd3b5cb5
institution Directory Open Access Journal
issn 1949-0976
1949-0984
language English
last_indexed 2024-04-24T17:07:49Z
publishDate 2023-12-01
publisher Taylor & Francis Group
record_format Article
series Gut Microbes
spelling doaj.art-eccb9e7ff48b475e8a5e47bacd3b5cb52024-03-28T22:38:19ZengTaylor & Francis GroupGut Microbes1949-09761949-09842023-12-0115110.1080/19490976.2023.2197835Meta-analysis reveals Helicobacter pylori mutual exclusivity and reproducible gastric microbiome alterations during gastric carcinoma progressionYan Li0Yichen Hu1Xiang Zhan2Ying Song3Meng Xu4Shijie Wang5Xiaochang Huang6Zhenjiang Zech Xu7State Key Laboratory of Food Science and Technology, Nanchang University, Nanchang, ChinaState Key Laboratory of Food Science and Technology, Nanchang University, Nanchang, ChinaSchool of Public Health and Beijing International Center for Mathematical Research, Peking University, Beijing, ChinaState Key Laboratory of Food Science and Technology, Nanchang University, Nanchang, ChinaState Key Laboratory of Food Science and Technology, Nanchang University, Nanchang, ChinaState Key Laboratory of Food Science and Technology, Nanchang University, Nanchang, ChinaState Key Laboratory of Food Science and Technology, Nanchang University, Nanchang, ChinaState Key Laboratory of Food Science and Technology, Nanchang University, Nanchang, ChinaABSTRACTAccumulating evidence shows that the gastric bacterial community may contribute to the development of gastric cancer (GC). However, the reported alterations of gastric microbiota were not always consistent among the literature. To assess reproducible signals in gastric microbiota during the progression of GC across studies, we performed a meta-analysis of nine publicly available 16S datasets with standard tools of the state-of-the-art. Despite study-specific batch effect, significant changes in the composition of the gastric microbiome were found during the progression of gastric carcinogenesis, especially when the Helicobacter pylori (HP) reads were removed from analyses to mitigate its compositional effect as they accounted for extremely large proportions of sequencing depths in many gastric samples. Differential microbes, including Fusobacterium, Leptotrichia, and several lactic acid bacteria such as Bifidobacterium, Lactobacillus, and Streptococcus anginosus, which were frequently and significantly enriched in GC patients compared with gastritis across studies, had good discriminatory capacity to distinguish GC samples from gastritis. Oral microbes were significantly enriched in GC compared to precancerous stages. Intriguingly, we observed mutual exclusivity of different HP species across studies. In addition, the comparison between gastric fluid and mucosal microbiome suggested their convergent dysbiosis during gastric disease progression. Taken together, our systematic analysis identified novel and consistent microbial patterns in gastric carcinogenesis.https://www.tandfonline.com/doi/10.1080/19490976.2023.2197835Meta-analysisgastric cancergastric microbiomeHelicobacter pylorioral microbescompositional effect
spellingShingle Yan Li
Yichen Hu
Xiang Zhan
Ying Song
Meng Xu
Shijie Wang
Xiaochang Huang
Zhenjiang Zech Xu
Meta-analysis reveals Helicobacter pylori mutual exclusivity and reproducible gastric microbiome alterations during gastric carcinoma progression
Gut Microbes
Meta-analysis
gastric cancer
gastric microbiome
Helicobacter pylori
oral microbes
compositional effect
title Meta-analysis reveals Helicobacter pylori mutual exclusivity and reproducible gastric microbiome alterations during gastric carcinoma progression
title_full Meta-analysis reveals Helicobacter pylori mutual exclusivity and reproducible gastric microbiome alterations during gastric carcinoma progression
title_fullStr Meta-analysis reveals Helicobacter pylori mutual exclusivity and reproducible gastric microbiome alterations during gastric carcinoma progression
title_full_unstemmed Meta-analysis reveals Helicobacter pylori mutual exclusivity and reproducible gastric microbiome alterations during gastric carcinoma progression
title_short Meta-analysis reveals Helicobacter pylori mutual exclusivity and reproducible gastric microbiome alterations during gastric carcinoma progression
title_sort meta analysis reveals helicobacter pylori mutual exclusivity and reproducible gastric microbiome alterations during gastric carcinoma progression
topic Meta-analysis
gastric cancer
gastric microbiome
Helicobacter pylori
oral microbes
compositional effect
url https://www.tandfonline.com/doi/10.1080/19490976.2023.2197835
work_keys_str_mv AT yanli metaanalysisrevealshelicobacterpylorimutualexclusivityandreproduciblegastricmicrobiomealterationsduringgastriccarcinomaprogression
AT yichenhu metaanalysisrevealshelicobacterpylorimutualexclusivityandreproduciblegastricmicrobiomealterationsduringgastriccarcinomaprogression
AT xiangzhan metaanalysisrevealshelicobacterpylorimutualexclusivityandreproduciblegastricmicrobiomealterationsduringgastriccarcinomaprogression
AT yingsong metaanalysisrevealshelicobacterpylorimutualexclusivityandreproduciblegastricmicrobiomealterationsduringgastriccarcinomaprogression
AT mengxu metaanalysisrevealshelicobacterpylorimutualexclusivityandreproduciblegastricmicrobiomealterationsduringgastriccarcinomaprogression
AT shijiewang metaanalysisrevealshelicobacterpylorimutualexclusivityandreproduciblegastricmicrobiomealterationsduringgastriccarcinomaprogression
AT xiaochanghuang metaanalysisrevealshelicobacterpylorimutualexclusivityandreproduciblegastricmicrobiomealterationsduringgastriccarcinomaprogression
AT zhenjiangzechxu metaanalysisrevealshelicobacterpylorimutualexclusivityandreproduciblegastricmicrobiomealterationsduringgastriccarcinomaprogression