Multi-omics analysis of fecal microbiota transplantation’s impact on functional constipation and comorbid depression and anxiety
Abstract Background Depression and anxiety are common comorbid diseases of constipation. Fecal microbiota transplantation (FMT) significantly relieves gastrointestinal-related symptoms, but its impact on psychiatric symptoms remains uncharted. Methods We collected fecal and serum samples before and...
| Main Authors: | , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2023-12-01
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| Series: | BMC Microbiology |
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| Online Access: | https://doi.org/10.1186/s12866-023-03123-1 |
| _version_ | 1827590743428956160 |
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| author | Chuanli Yang Tianjiao Hu Xin Xue Xiaohu Su Xuan Zhang Yunhe Fan Xiaobing Shen Xiushan Dong |
| author_facet | Chuanli Yang Tianjiao Hu Xin Xue Xiaohu Su Xuan Zhang Yunhe Fan Xiaobing Shen Xiushan Dong |
| author_sort | Chuanli Yang |
| collection | DOAJ |
| description | Abstract Background Depression and anxiety are common comorbid diseases of constipation. Fecal microbiota transplantation (FMT) significantly relieves gastrointestinal-related symptoms, but its impact on psychiatric symptoms remains uncharted. Methods We collected fecal and serum samples before and after FMT from 4 functional constipation patients with psychiatric symptoms and corresponding donor stool samples. We categorized the samples into two groups: before FMT (Fb) and after FMT (Fa). Parameters associated with constipation, depression, and anxiety symptoms were evaluated. Metagenomics and targeted neurotransmitter metabolomics were performed to investigate the gut microbiota and metabolites. 5-hydroxytryptamine (5-HT) biosynthesis was detected in patients’ fecal supernatants exposed to the QGP-1 cell model in vitro. Results Our study demonstrated that patient’s constipation, depression, and anxiety were improved after FMT intervention. At the genus level, relative abundance of g_Bacteroides and g_Klebsiella decreased in the Fa group, while g_Lactobacillus, and g_Selenomonas content increased in the same group. These observations suggest a potential involvement of these genera in the pathogenesis of constipation with psychiatric symptoms. Metabolomics analysis showed that FMT intervention decreased serum 5-HT levels. Additionally, we found that species, including s_Klebsiella sp. 1_1_55, s_Odoribacter splanchnicus, and s_Ruminococcus gnavus CAG:126, were positively correlated with 5-HT levels. In contrast, s_Acetobacterium bakii, s_Enterococcus hermanniensis, s_Prevotella falsenii, s_Propionispira arboris, s_Schwartzia succinivorans, s_Selenomonas artemidis, and s_Selenomonas sp. FC4001 were negatively correlated with 5-HT levels. Furthermore, we observed that patients’ fecal supernatants increased 5-HT biosynthesis in QGP-1 cells. Conclusion FMT can relieve patients’ constipation, depression, and anxiety symptoms by reshaping gut microbiota. The 5-HT level was associated with an altered abundance of specific bacteria or metabolites. This study provides specific evidence for FMT intervention in constipation patients with psychiatric symptoms. |
| first_indexed | 2024-03-09T01:21:05Z |
| format | Article |
| id | doaj.art-fc5050bb914e44359f6f9bbf139d9235 |
| institution | Directory Open Access Journal |
| issn | 1471-2180 |
| language | English |
| last_indexed | 2024-03-09T01:21:05Z |
| publishDate | 2023-12-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Microbiology |
| spelling | doaj.art-fc5050bb914e44359f6f9bbf139d92352023-12-10T12:09:27ZengBMCBMC Microbiology1471-21802023-12-0123111310.1186/s12866-023-03123-1Multi-omics analysis of fecal microbiota transplantation’s impact on functional constipation and comorbid depression and anxietyChuanli Yang0Tianjiao Hu1Xin Xue2Xiaohu Su3Xuan Zhang4Yunhe Fan5Xiaobing Shen6Xiushan Dong7Key Laboratory of Environmental Medical Engineering and Education Ministry, School of Public Health, Southeast UniversityDepartment of General Surgery, Tongji Shanxi Hospital, Shanxi Bethune Hospital, Shanxi Academy of Medical Sciences, Third Hospital of Shanxi Medical UniversityDepartment of General Surgery, Tongji Shanxi Hospital, Shanxi Bethune Hospital, Shanxi Academy of Medical Sciences, Third Hospital of Shanxi Medical UniversityDepartment of General Surgery, Tongji Shanxi Hospital, Shanxi Bethune Hospital, Shanxi Academy of Medical Sciences, Third Hospital of Shanxi Medical UniversityDepartment of General Surgery, Tongji Shanxi Hospital, Shanxi Bethune Hospital, Shanxi Academy of Medical Sciences, Third Hospital of Shanxi Medical UniversityDepartment of General Surgery, Tongji Shanxi Hospital, Shanxi Bethune Hospital, Shanxi Academy of Medical Sciences, Third Hospital of Shanxi Medical UniversityKey Laboratory of Environmental Medical Engineering and Education Ministry, School of Public Health, Southeast UniversityDepartment of General Surgery, Tongji Shanxi Hospital, Shanxi Bethune Hospital, Shanxi Academy of Medical Sciences, Third Hospital of Shanxi Medical UniversityAbstract Background Depression and anxiety are common comorbid diseases of constipation. Fecal microbiota transplantation (FMT) significantly relieves gastrointestinal-related symptoms, but its impact on psychiatric symptoms remains uncharted. Methods We collected fecal and serum samples before and after FMT from 4 functional constipation patients with psychiatric symptoms and corresponding donor stool samples. We categorized the samples into two groups: before FMT (Fb) and after FMT (Fa). Parameters associated with constipation, depression, and anxiety symptoms were evaluated. Metagenomics and targeted neurotransmitter metabolomics were performed to investigate the gut microbiota and metabolites. 5-hydroxytryptamine (5-HT) biosynthesis was detected in patients’ fecal supernatants exposed to the QGP-1 cell model in vitro. Results Our study demonstrated that patient’s constipation, depression, and anxiety were improved after FMT intervention. At the genus level, relative abundance of g_Bacteroides and g_Klebsiella decreased in the Fa group, while g_Lactobacillus, and g_Selenomonas content increased in the same group. These observations suggest a potential involvement of these genera in the pathogenesis of constipation with psychiatric symptoms. Metabolomics analysis showed that FMT intervention decreased serum 5-HT levels. Additionally, we found that species, including s_Klebsiella sp. 1_1_55, s_Odoribacter splanchnicus, and s_Ruminococcus gnavus CAG:126, were positively correlated with 5-HT levels. In contrast, s_Acetobacterium bakii, s_Enterococcus hermanniensis, s_Prevotella falsenii, s_Propionispira arboris, s_Schwartzia succinivorans, s_Selenomonas artemidis, and s_Selenomonas sp. FC4001 were negatively correlated with 5-HT levels. Furthermore, we observed that patients’ fecal supernatants increased 5-HT biosynthesis in QGP-1 cells. Conclusion FMT can relieve patients’ constipation, depression, and anxiety symptoms by reshaping gut microbiota. The 5-HT level was associated with an altered abundance of specific bacteria or metabolites. This study provides specific evidence for FMT intervention in constipation patients with psychiatric symptoms.https://doi.org/10.1186/s12866-023-03123-1ConstipationDepression and anxietyFecal microbiota transplantationMetagenomicsMetabolomics5-hydroxytryptamine |
| spellingShingle | Chuanli Yang Tianjiao Hu Xin Xue Xiaohu Su Xuan Zhang Yunhe Fan Xiaobing Shen Xiushan Dong Multi-omics analysis of fecal microbiota transplantation’s impact on functional constipation and comorbid depression and anxiety BMC Microbiology Constipation Depression and anxiety Fecal microbiota transplantation Metagenomics Metabolomics 5-hydroxytryptamine |
| title | Multi-omics analysis of fecal microbiota transplantation’s impact on functional constipation and comorbid depression and anxiety |
| title_full | Multi-omics analysis of fecal microbiota transplantation’s impact on functional constipation and comorbid depression and anxiety |
| title_fullStr | Multi-omics analysis of fecal microbiota transplantation’s impact on functional constipation and comorbid depression and anxiety |
| title_full_unstemmed | Multi-omics analysis of fecal microbiota transplantation’s impact on functional constipation and comorbid depression and anxiety |
| title_short | Multi-omics analysis of fecal microbiota transplantation’s impact on functional constipation and comorbid depression and anxiety |
| title_sort | multi omics analysis of fecal microbiota transplantation s impact on functional constipation and comorbid depression and anxiety |
| topic | Constipation Depression and anxiety Fecal microbiota transplantation Metagenomics Metabolomics 5-hydroxytryptamine |
| url | https://doi.org/10.1186/s12866-023-03123-1 |
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