Changes of the Gastric Mucosal Microbiome Associated With Histological Stages of Gastric Carcinogenesis
The changes of gastric microbiome across stages of neoplastic progression remain poorly understood, especially for intraepithelial neoplasia (IN) which has been recognized as a phenotypic bridge between atrophic/intestinal metaplastic lesions and invasive cancer. The gastric microbiota was investiga...
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Frontiers Media S.A.
2020-05-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2020.00997/full |
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| author | Zikai Wang Xuefeng Gao Ranran Zeng Qiong Wu Huaibo Sun Wenming Wu Xiaomei Zhang Gang Sun Bin Yan Lili Wu Rongrong Ren Mingzhou Guo Lihua Peng Yunsheng Yang |
| author_facet | Zikai Wang Xuefeng Gao Ranran Zeng Qiong Wu Huaibo Sun Wenming Wu Xiaomei Zhang Gang Sun Bin Yan Lili Wu Rongrong Ren Mingzhou Guo Lihua Peng Yunsheng Yang |
| author_sort | Zikai Wang |
| collection | DOAJ |
| description | The changes of gastric microbiome across stages of neoplastic progression remain poorly understood, especially for intraepithelial neoplasia (IN) which has been recognized as a phenotypic bridge between atrophic/intestinal metaplastic lesions and invasive cancer. The gastric microbiota was investigated in 30 healthy controls (HC), 21 non-atrophic chronic gastritis (CG), 27 gastric intestinal metaplasia (IM), 25 IN, and 29 gastric cancer (GC) patients by 16S rRNA gene profiling. The bacterial diversity, and abundances of phyla Armatimonadetes, Chloroflexi, Elusimicrobia, Nitrospirae, Planctomycetes, Verrucomicrobia, and WS3 reduced progressively from CG, through IM, IN to GC. Actinobacteria, Bacteriodes, Firmicutes, Fusobacteria, SR1, and TM7 were enriched in the IN and GC. At the community level, the proportions of Gram-positive and anaerobic bacteria increased in the IN and GC compared to other histological types, whereas the aerobic and facultatively anaerobic bacteria taxa were significantly reduced in GC. Remarkable changes in the gastric microbiota functions were detected after the formation of IN. The reduced nitrite-oxidizing phylum Nitrospirae together with a decreased nitrate/nitrite reductase functions indicated nitrate accumulation during neoplastic progression. We constructed a random forest model, which had a very high accuracy (AUC > 0.95) in predicating the histological types with as low as five gastric bacterial taxa. In summary, the changing patterns of the gastric microbiota composition and function are highly indicative of stages of neoplastic progression. |
| first_indexed | 2024-12-13T09:15:02Z |
| format | Article |
| id | doaj.art-b22df89099bc4b9cacedb4e5a9077d63 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-13T09:15:02Z |
| publishDate | 2020-05-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-b22df89099bc4b9cacedb4e5a9077d632022-12-21T23:52:52ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-05-011110.3389/fmicb.2020.00997481295Changes of the Gastric Mucosal Microbiome Associated With Histological Stages of Gastric CarcinogenesisZikai Wang0Xuefeng Gao1Ranran Zeng2Qiong Wu3Huaibo Sun4Wenming Wu5Xiaomei Zhang6Gang Sun7Bin Yan8Lili Wu9Rongrong Ren10Mingzhou Guo11Lihua Peng12Yunsheng Yang13Department of Gastroenterology and Hepatology, The First Medical Centre, Chinese PLA General Hospital, Beijing, ChinaDepartment of Hematology-Oncology, International Cancer Center, Shenzhen University General Hospital, Shenzhen University Health Science Center, Shenzhen, ChinaDepartment of Gastroenterology and Hepatology, The First Medical Centre, Chinese PLA General Hospital, Beijing, ChinaDepartment of Gastroenterology and Hepatology, The First Medical Centre, Chinese PLA General Hospital, Beijing, ChinaInstitute of Soil Science, Chinese Academy of Sciences, Nanjing, ChinaDepartment of Gastroenterology and Hepatology, The First Medical Centre, Chinese PLA General Hospital, Beijing, ChinaDepartment of Gastroenterology and Hepatology, The First Medical Centre, Chinese PLA General Hospital, Beijing, ChinaDepartment of Gastroenterology and Hepatology, The First Medical Centre, Chinese PLA General Hospital, Beijing, ChinaDepartment of Gastroenterology and Hepatology, The First Medical Centre, Chinese PLA General Hospital, Beijing, ChinaDepartment of Gastroenterology and Hepatology, The First Medical Centre, Chinese PLA General Hospital, Beijing, ChinaDepartment of Gastroenterology and Hepatology, The First Medical Centre, Chinese PLA General Hospital, Beijing, ChinaDepartment of Gastroenterology and Hepatology, The First Medical Centre, Chinese PLA General Hospital, Beijing, ChinaDepartment of Gastroenterology and Hepatology, The First Medical Centre, Chinese PLA General Hospital, Beijing, ChinaDepartment of Gastroenterology and Hepatology, The First Medical Centre, Chinese PLA General Hospital, Beijing, ChinaThe changes of gastric microbiome across stages of neoplastic progression remain poorly understood, especially for intraepithelial neoplasia (IN) which has been recognized as a phenotypic bridge between atrophic/intestinal metaplastic lesions and invasive cancer. The gastric microbiota was investigated in 30 healthy controls (HC), 21 non-atrophic chronic gastritis (CG), 27 gastric intestinal metaplasia (IM), 25 IN, and 29 gastric cancer (GC) patients by 16S rRNA gene profiling. The bacterial diversity, and abundances of phyla Armatimonadetes, Chloroflexi, Elusimicrobia, Nitrospirae, Planctomycetes, Verrucomicrobia, and WS3 reduced progressively from CG, through IM, IN to GC. Actinobacteria, Bacteriodes, Firmicutes, Fusobacteria, SR1, and TM7 were enriched in the IN and GC. At the community level, the proportions of Gram-positive and anaerobic bacteria increased in the IN and GC compared to other histological types, whereas the aerobic and facultatively anaerobic bacteria taxa were significantly reduced in GC. Remarkable changes in the gastric microbiota functions were detected after the formation of IN. The reduced nitrite-oxidizing phylum Nitrospirae together with a decreased nitrate/nitrite reductase functions indicated nitrate accumulation during neoplastic progression. We constructed a random forest model, which had a very high accuracy (AUC > 0.95) in predicating the histological types with as low as five gastric bacterial taxa. In summary, the changing patterns of the gastric microbiota composition and function are highly indicative of stages of neoplastic progression.https://www.frontiersin.org/article/10.3389/fmicb.2020.00997/fullgastric microbiotagastric cancerintraepithelial neoplasiaintestinal metaplasiachronic gastritis |
| spellingShingle | Zikai Wang Xuefeng Gao Ranran Zeng Qiong Wu Huaibo Sun Wenming Wu Xiaomei Zhang Gang Sun Bin Yan Lili Wu Rongrong Ren Mingzhou Guo Lihua Peng Yunsheng Yang Changes of the Gastric Mucosal Microbiome Associated With Histological Stages of Gastric Carcinogenesis Frontiers in Microbiology gastric microbiota gastric cancer intraepithelial neoplasia intestinal metaplasia chronic gastritis |
| title | Changes of the Gastric Mucosal Microbiome Associated With Histological Stages of Gastric Carcinogenesis |
| title_full | Changes of the Gastric Mucosal Microbiome Associated With Histological Stages of Gastric Carcinogenesis |
| title_fullStr | Changes of the Gastric Mucosal Microbiome Associated With Histological Stages of Gastric Carcinogenesis |
| title_full_unstemmed | Changes of the Gastric Mucosal Microbiome Associated With Histological Stages of Gastric Carcinogenesis |
| title_short | Changes of the Gastric Mucosal Microbiome Associated With Histological Stages of Gastric Carcinogenesis |
| title_sort | changes of the gastric mucosal microbiome associated with histological stages of gastric carcinogenesis |
| topic | gastric microbiota gastric cancer intraepithelial neoplasia intestinal metaplasia chronic gastritis |
| url | https://www.frontiersin.org/article/10.3389/fmicb.2020.00997/full |
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