Gut microbiome changes in mouse, Mongolian gerbil, and hamster models following Clostridioides difficile challenge
IntroductionClostridioides difficile infection (CDI), as well as its etiology and pathogenesis, have been extensively investigated. However, the absence of suitable CDI animal models that reflect CDI symptoms and the associated gut microbiome changes in humans has limited research progress in this f...
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| Format: | Article |
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Frontiers Media S.A.
2024-04-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2024.1368194/full |
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| author | Shuangshuang Wan Shuangshuang Wan Peijun You Qikai Shi Hui Hu Hui Hu Lu Zhang Leyang Chen Ziyi Wu Shan Lin Shan Lin Xiaojun Song Yongneng Luo Yongneng Luo Yaxuan Wang Feng Ju Dazhi Jin Dazhi Jin Yu Chen Yu Chen |
| author_facet | Shuangshuang Wan Shuangshuang Wan Peijun You Qikai Shi Hui Hu Hui Hu Lu Zhang Leyang Chen Ziyi Wu Shan Lin Shan Lin Xiaojun Song Yongneng Luo Yongneng Luo Yaxuan Wang Feng Ju Dazhi Jin Dazhi Jin Yu Chen Yu Chen |
| author_sort | Shuangshuang Wan |
| collection | DOAJ |
| description | IntroductionClostridioides difficile infection (CDI), as well as its etiology and pathogenesis, have been extensively investigated. However, the absence of suitable CDI animal models that reflect CDI symptoms and the associated gut microbiome changes in humans has limited research progress in this field. Thus, we aimed to investigate whether Mongolian gerbils, which present a range of human pathological conditions, can been used in studies on CDI. Methods: In this study, we infected Mongolian gerbils and two existing CDI model animals, mice and hamsters, with the hypervirulent ribotype 027 C. difficile strain, and comparatively analyzed changes in their gut microbiome composition via 16S rRNA gene sequencing.MethodsIn this study, we infected Mongolian gerbils and two existing CDI model animals, mice and hamsters, with the hypervirulent ribotype 027 C. difficile strain, and comparatively analyzed changes in their gut microbiome composition via 16S rRNA gene sequencing.ResultsThe results obtained showed that C. difficile colonized the gastrointestinal tracts of the three rodents, and after the C. difficile challenge, C57BL/6J mice did not manifest CDI symptoms and their intestines showed no significant pathological changes. However, the hamsters showed explosive intestinal bleeding and inflammation and the Mongolian gerbils presented diarrhea as well as increased infiltration of inflammatory cells, mucus secretion, and epithelial cell shedding in their intestinal tissue. Further, intestinal microbiome analysis revealed significant differences with respect to intestinal flora abundance and diversity. Specifically, after C. difficile challenge, the Firmicutes/Bacteroidetes ratio decreased for C57BL/6J mice, but increased significantly for Mongolian gerbils and hamsters. Furthermore, the abundance of Proteobacteria increased in all three models, especially in hamsters, while that of Verrucomicrobia only increased significantly in C57BL/6J mice and Mongolian gerbils. Our results also indicated that differences in the relative abundances of Lactobacillaceae and Akkermansia were primarily responsible for the observed differences in response to C. difficile challenge.ConclusionBased on the observed responses to C. difficile challenge, we concluded for the first time that the Mongolian gerbil could be used as an animal model for CDI. Additionally, the taxa identified in this study may be used as biomarkers for further studies on CDI and to improve understanding regarding changes in gut microbiome in CDI-related diseases. |
| first_indexed | 2024-04-24T13:46:45Z |
| format | Article |
| id | doaj.art-038729933b754b708b34838bc30d78a7 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-04-24T13:46:45Z |
| publishDate | 2024-04-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Microbiology |
| spelling | doaj.art-038729933b754b708b34838bc30d78a72024-04-04T05:09:17ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2024-04-011510.3389/fmicb.2024.13681941368194Gut microbiome changes in mouse, Mongolian gerbil, and hamster models following Clostridioides difficile challengeShuangshuang Wan0Shuangshuang Wan1Peijun You2Qikai Shi3Hui Hu4Hui Hu5Lu Zhang6Leyang Chen7Ziyi Wu8Shan Lin9Shan Lin10Xiaojun Song11Yongneng Luo12Yongneng Luo13Yaxuan Wang14Feng Ju15Dazhi Jin16Dazhi Jin17Yu Chen18Yu Chen19School of Laboratory Medicine, Hangzhou Medical College, Hangzhou, ChinaKey Laboratory of Biomarkers and In Vitro Diagnosis Translation of Zhejiang Province, Hangzhou, ChinaSchool of Laboratory Medicine, Hangzhou Medical College, Hangzhou, ChinaSchool of Laboratory Medicine, Hangzhou Medical College, Hangzhou, ChinaSchool of Laboratory Medicine, Hangzhou Medical College, Hangzhou, ChinaKey Laboratory of Biomarkers and In Vitro Diagnosis Translation of Zhejiang Province, Hangzhou, ChinaEnvironmental Microbiome and Biotechnology Laboratory, School of Engineering, Westlake University, Hangzhou, ChinaSchool of Clinical Medicine, Hangzhou Medical College, Hangzhou, ChinaSchool of Clinical Medicine, Hangzhou Medical College, Hangzhou, ChinaSchool of Laboratory Medicine, Hangzhou Medical College, Hangzhou, ChinaTEDA Institute of Biological Sciences and Biotechnology, Nankai University, Tianjin, ChinaLaboratory Medicine Center, Department of Clinical Laboratory, Zhejiang Provincial People’s Hospital, Hangzhou Medical College, Hangzhou, ChinaSchool of Laboratory Medicine, Hangzhou Medical College, Hangzhou, ChinaKey Laboratory of Biomarkers and In Vitro Diagnosis Translation of Zhejiang Province, Hangzhou, ChinaNational Center for Clinical Laboratories, Institute of Geriatric Medicine, Chinese Academy of Medical Sciences, Beijing Hospital/National Center of Gerontology, Beijing, ChinaEnvironmental Microbiome and Biotechnology Laboratory, School of Engineering, Westlake University, Hangzhou, ChinaSchool of Laboratory Medicine, Hangzhou Medical College, Hangzhou, ChinaKey Laboratory of Biomarkers and In Vitro Diagnosis Translation of Zhejiang Province, Hangzhou, ChinaSchool of Laboratory Medicine, Hangzhou Medical College, Hangzhou, ChinaKey Laboratory of Biomarkers and In Vitro Diagnosis Translation of Zhejiang Province, Hangzhou, ChinaIntroductionClostridioides difficile infection (CDI), as well as its etiology and pathogenesis, have been extensively investigated. However, the absence of suitable CDI animal models that reflect CDI symptoms and the associated gut microbiome changes in humans has limited research progress in this field. Thus, we aimed to investigate whether Mongolian gerbils, which present a range of human pathological conditions, can been used in studies on CDI. Methods: In this study, we infected Mongolian gerbils and two existing CDI model animals, mice and hamsters, with the hypervirulent ribotype 027 C. difficile strain, and comparatively analyzed changes in their gut microbiome composition via 16S rRNA gene sequencing.MethodsIn this study, we infected Mongolian gerbils and two existing CDI model animals, mice and hamsters, with the hypervirulent ribotype 027 C. difficile strain, and comparatively analyzed changes in their gut microbiome composition via 16S rRNA gene sequencing.ResultsThe results obtained showed that C. difficile colonized the gastrointestinal tracts of the three rodents, and after the C. difficile challenge, C57BL/6J mice did not manifest CDI symptoms and their intestines showed no significant pathological changes. However, the hamsters showed explosive intestinal bleeding and inflammation and the Mongolian gerbils presented diarrhea as well as increased infiltration of inflammatory cells, mucus secretion, and epithelial cell shedding in their intestinal tissue. Further, intestinal microbiome analysis revealed significant differences with respect to intestinal flora abundance and diversity. Specifically, after C. difficile challenge, the Firmicutes/Bacteroidetes ratio decreased for C57BL/6J mice, but increased significantly for Mongolian gerbils and hamsters. Furthermore, the abundance of Proteobacteria increased in all three models, especially in hamsters, while that of Verrucomicrobia only increased significantly in C57BL/6J mice and Mongolian gerbils. Our results also indicated that differences in the relative abundances of Lactobacillaceae and Akkermansia were primarily responsible for the observed differences in response to C. difficile challenge.ConclusionBased on the observed responses to C. difficile challenge, we concluded for the first time that the Mongolian gerbil could be used as an animal model for CDI. Additionally, the taxa identified in this study may be used as biomarkers for further studies on CDI and to improve understanding regarding changes in gut microbiome in CDI-related diseases.https://www.frontiersin.org/articles/10.3389/fmicb.2024.1368194/fullClostridioides difficilerodent modelsMongolian gerbilsgut microbiomeLactobacillaceaeAkkermansia |
| spellingShingle | Shuangshuang Wan Shuangshuang Wan Peijun You Qikai Shi Hui Hu Hui Hu Lu Zhang Leyang Chen Ziyi Wu Shan Lin Shan Lin Xiaojun Song Yongneng Luo Yongneng Luo Yaxuan Wang Feng Ju Dazhi Jin Dazhi Jin Yu Chen Yu Chen Gut microbiome changes in mouse, Mongolian gerbil, and hamster models following Clostridioides difficile challenge Frontiers in Microbiology Clostridioides difficile rodent models Mongolian gerbils gut microbiome Lactobacillaceae Akkermansia |
| title | Gut microbiome changes in mouse, Mongolian gerbil, and hamster models following Clostridioides difficile challenge |
| title_full | Gut microbiome changes in mouse, Mongolian gerbil, and hamster models following Clostridioides difficile challenge |
| title_fullStr | Gut microbiome changes in mouse, Mongolian gerbil, and hamster models following Clostridioides difficile challenge |
| title_full_unstemmed | Gut microbiome changes in mouse, Mongolian gerbil, and hamster models following Clostridioides difficile challenge |
| title_short | Gut microbiome changes in mouse, Mongolian gerbil, and hamster models following Clostridioides difficile challenge |
| title_sort | gut microbiome changes in mouse mongolian gerbil and hamster models following clostridioides difficile challenge |
| topic | Clostridioides difficile rodent models Mongolian gerbils gut microbiome Lactobacillaceae Akkermansia |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2024.1368194/full |
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