Convergent dysbiosis of gastric mucosa and fluid microbiome during stomach carcinogenesis
Abstract Background A complex microbiota in the gastric mucosa (GM) has been unveiled recently and its dysbiosis is identified to be associated with gastric cancer (GC). However, the microbial composition in gastric fluid (GF) and its correlation wit...
| Main Authors: | , , , , , , , , , , , , |
|---|---|
| Other Authors: | |
| Format: | Article |
| Language: | English |
| Published: |
Springer Nature Singapore
2022
|
| Online Access: | https://hdl.handle.net/1721.1/144306 |
| _version_ | 1826193735352844288 |
|---|---|
| author | He, Cong Peng, Chao Shu, Xu Wang, Huan Zhu, Zhenhua Ouyang, Yaobin Yang, Xiaoyu Xie, Chuan Hu, Yi Li, Nianshuang Ge, Zhongming Zhu, Yin Lu, Nonghua |
| author2 | Massachusetts Institute of Technology. Division of Comparative Medicine |
| author_facet | Massachusetts Institute of Technology. Division of Comparative Medicine He, Cong Peng, Chao Shu, Xu Wang, Huan Zhu, Zhenhua Ouyang, Yaobin Yang, Xiaoyu Xie, Chuan Hu, Yi Li, Nianshuang Ge, Zhongming Zhu, Yin Lu, Nonghua |
| author_sort | He, Cong |
| collection | MIT |
| description | Abstract
Background
A complex microbiota in the gastric mucosa (GM) has been unveiled recently and its dysbiosis is identified to be associated with gastric cancer (GC). However, the microbial composition in gastric fluid (GF) and its correlation with GM during gastric carcinogenesis are unclear.
Methods
We obtained GM and GF samples from 180 patients, including 61 superficial gastritis (SG), 55 intestinal metaplasia (IM) and 64 GC and performed 16S rRNA gene sequencing analysis. The concentration of gastric acid and metabolite nitrite has been measured.
Results
Overall, the composition of microbiome in GM was distinct from GF with less diversity, and both were influenced by H. pylori infection. The structure of microbiota changed differentially in GM and GF across histological stages of GC, accompanied with decreased gastric acid and increased carcinogenic nitrite. The classifiers of GC based on microbial markers were identified in both GM and GF, including Lactobacillus, Veillonella, Gemella, and were further validated in an independent cohort with good performance. Interestingly, paired comparison between GM and GF showed that their compositional distinction remarkably dwindled from SG to GC, with some GF-enriched bacteria significantly increased in GM. Moreover, stronger interaction network between microbes of GM and GF was observed in GC compared to SG.
Conclusion
Our results, for the first time, revealed a comprehensive profile of both GM and GF microbiomes during the development of GC. The convergent microbial characteristics between GM and GF in GC suggest that the colonization of carcinogenic microbes in GM might derive from GF. |
| first_indexed | 2024-09-23T09:44:06Z |
| format | Article |
| id | mit-1721.1/144306 |
| institution | Massachusetts Institute of Technology |
| language | English |
| last_indexed | 2024-09-23T09:44:06Z |
| publishDate | 2022 |
| publisher | Springer Nature Singapore |
| record_format | dspace |
| spelling | mit-1721.1/1443062023-07-03T05:33:14Z Convergent dysbiosis of gastric mucosa and fluid microbiome during stomach carcinogenesis He, Cong Peng, Chao Shu, Xu Wang, Huan Zhu, Zhenhua Ouyang, Yaobin Yang, Xiaoyu Xie, Chuan Hu, Yi Li, Nianshuang Ge, Zhongming Zhu, Yin Lu, Nonghua Massachusetts Institute of Technology. Division of Comparative Medicine Abstract Background A complex microbiota in the gastric mucosa (GM) has been unveiled recently and its dysbiosis is identified to be associated with gastric cancer (GC). However, the microbial composition in gastric fluid (GF) and its correlation with GM during gastric carcinogenesis are unclear. Methods We obtained GM and GF samples from 180 patients, including 61 superficial gastritis (SG), 55 intestinal metaplasia (IM) and 64 GC and performed 16S rRNA gene sequencing analysis. The concentration of gastric acid and metabolite nitrite has been measured. Results Overall, the composition of microbiome in GM was distinct from GF with less diversity, and both were influenced by H. pylori infection. The structure of microbiota changed differentially in GM and GF across histological stages of GC, accompanied with decreased gastric acid and increased carcinogenic nitrite. The classifiers of GC based on microbial markers were identified in both GM and GF, including Lactobacillus, Veillonella, Gemella, and were further validated in an independent cohort with good performance. Interestingly, paired comparison between GM and GF showed that their compositional distinction remarkably dwindled from SG to GC, with some GF-enriched bacteria significantly increased in GM. Moreover, stronger interaction network between microbes of GM and GF was observed in GC compared to SG. Conclusion Our results, for the first time, revealed a comprehensive profile of both GM and GF microbiomes during the development of GC. The convergent microbial characteristics between GM and GF in GC suggest that the colonization of carcinogenic microbes in GM might derive from GF. 2022-08-11T12:11:36Z 2022-08-11T12:11:36Z 2022-06-04 2022-08-11T03:15:31Z Article http://purl.org/eprint/type/JournalArticle https://hdl.handle.net/1721.1/144306 He, Cong, Peng, Chao, Shu, Xu, Wang, Huan, Zhu, Zhenhua et al. 2022. "Convergent dysbiosis of gastric mucosa and fluid microbiome during stomach carcinogenesis." en https://doi.org/10.1007/s10120-022-01302-z Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use. The Author(s) under exclusive licence to The International Gastric Cancer Association and The Japanese Gastric Cancer Association application/pdf Springer Nature Singapore Springer Nature Singapore |
| spellingShingle | He, Cong Peng, Chao Shu, Xu Wang, Huan Zhu, Zhenhua Ouyang, Yaobin Yang, Xiaoyu Xie, Chuan Hu, Yi Li, Nianshuang Ge, Zhongming Zhu, Yin Lu, Nonghua Convergent dysbiosis of gastric mucosa and fluid microbiome during stomach carcinogenesis |
| title | Convergent dysbiosis of gastric mucosa and fluid microbiome during stomach carcinogenesis |
| title_full | Convergent dysbiosis of gastric mucosa and fluid microbiome during stomach carcinogenesis |
| title_fullStr | Convergent dysbiosis of gastric mucosa and fluid microbiome during stomach carcinogenesis |
| title_full_unstemmed | Convergent dysbiosis of gastric mucosa and fluid microbiome during stomach carcinogenesis |
| title_short | Convergent dysbiosis of gastric mucosa and fluid microbiome during stomach carcinogenesis |
| title_sort | convergent dysbiosis of gastric mucosa and fluid microbiome during stomach carcinogenesis |
| url | https://hdl.handle.net/1721.1/144306 |
| work_keys_str_mv | AT hecong convergentdysbiosisofgastricmucosaandfluidmicrobiomeduringstomachcarcinogenesis AT pengchao convergentdysbiosisofgastricmucosaandfluidmicrobiomeduringstomachcarcinogenesis AT shuxu convergentdysbiosisofgastricmucosaandfluidmicrobiomeduringstomachcarcinogenesis AT wanghuan convergentdysbiosisofgastricmucosaandfluidmicrobiomeduringstomachcarcinogenesis AT zhuzhenhua convergentdysbiosisofgastricmucosaandfluidmicrobiomeduringstomachcarcinogenesis AT ouyangyaobin convergentdysbiosisofgastricmucosaandfluidmicrobiomeduringstomachcarcinogenesis AT yangxiaoyu convergentdysbiosisofgastricmucosaandfluidmicrobiomeduringstomachcarcinogenesis AT xiechuan convergentdysbiosisofgastricmucosaandfluidmicrobiomeduringstomachcarcinogenesis AT huyi convergentdysbiosisofgastricmucosaandfluidmicrobiomeduringstomachcarcinogenesis AT linianshuang convergentdysbiosisofgastricmucosaandfluidmicrobiomeduringstomachcarcinogenesis AT gezhongming convergentdysbiosisofgastricmucosaandfluidmicrobiomeduringstomachcarcinogenesis AT zhuyin convergentdysbiosisofgastricmucosaandfluidmicrobiomeduringstomachcarcinogenesis AT lunonghua convergentdysbiosisofgastricmucosaandfluidmicrobiomeduringstomachcarcinogenesis |