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...
Main Authors: | , , , , , , , |
---|---|
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 |