Alterations of gut microbiota and short-chain fatty acids induced by Balantidium polyvacuolum in the hindgut of Xenocyprinae fishes providing new insights into the relationship among protozoa, gut microbiota and host
IntroductionParasitic ciliates are protozoans with a global distribution. Along with the gut microbiota, they have formed a micro-ecosystem that affects the host’s nutrition, metabolism, and immunity. The interactions and relationships among the three components of this microecosystem (protozoa, gut...
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2023-11-01
|
| Series: | Frontiers in Microbiology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1295456/full |
| _version_ | 1797490441291038720 |
|---|---|
| author | Xialian Bu Xialian Bu Zhongyang Li Zhongyang Li Weishan Zhao Qingwen Zeng Qingwen Zeng Yushun Chen Wenxiang Li Hong Zou Ming Li Guitang Wang |
| author_facet | Xialian Bu Xialian Bu Zhongyang Li Zhongyang Li Weishan Zhao Qingwen Zeng Qingwen Zeng Yushun Chen Wenxiang Li Hong Zou Ming Li Guitang Wang |
| author_sort | Xialian Bu |
| collection | DOAJ |
| description | IntroductionParasitic ciliates are protozoans with a global distribution. Along with the gut microbiota, they have formed a micro-ecosystem that affects the host’s nutrition, metabolism, and immunity. The interactions and relationships among the three components of this microecosystem (protozoa, gut microbiota, and host) remain only partially understood. Xenocypris fish and the unique ciliate Balantidium polyvacuolum in its hindgut are good materials to study the interplay.MethodsIn this study, 16S rRNA gene amplicon sequencing and short-chain fatty acids (SCFAs) identification were used. Network was also constructed to understand their relationships.ResultsWe found that the gut microbiota of B. polyvacuolum-infected X. davidi and X. argentea had higher diversity, richness, and evenness than uninfected ones. B. polyvacuolum could lead to an increase of Fusobacterium and Chloroflexi in both X. davidi and X. argentea, while significantly increase the abundance of genera Romboutsia and Clostridium in X. argentea. Besides, B. polyvacuolum could significantly increase the content of total SCFAs and acetic acid in X. davidi and increase the concentrations of propionic, isobutyric and butanoic acids in X. argentea. Furthermore, correlation analyses showed that B. polyvacuolum may alter SCFAs by affecting key SCFAs-producing bacteria such as Clostridium and Cetobacterium.DiscussionThis study greatly expands our understanding of relationships among B. polyvacuolum, gut microbiota and host Xenocypris fish, which sheds new insights into the mechanism of interaction among protozoa, gut microbiota and host. |
| first_indexed | 2024-03-10T00:33:02Z |
| format | Article |
| id | doaj.art-f6017d6f49494ab1afe6794e7135d91f |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-03-10T00:33:02Z |
| publishDate | 2023-11-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-f6017d6f49494ab1afe6794e7135d91f2023-11-23T15:22:55ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-11-011410.3389/fmicb.2023.12954561295456Alterations of gut microbiota and short-chain fatty acids induced by Balantidium polyvacuolum in the hindgut of Xenocyprinae fishes providing new insights into the relationship among protozoa, gut microbiota and hostXialian Bu0Xialian Bu1Zhongyang Li2Zhongyang Li3Weishan Zhao4Qingwen Zeng5Qingwen Zeng6Yushun Chen7Wenxiang Li8Hong Zou9Ming Li10Guitang Wang11Key Laboratory of Breeding Biotechnology and Sustainable Aquaculture, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, Hubei, ChinaCollege of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing, ChinaKey Laboratory of Breeding Biotechnology and Sustainable Aquaculture, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, Hubei, ChinaCollege of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing, ChinaKey Laboratory of Breeding Biotechnology and Sustainable Aquaculture, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, Hubei, ChinaKey Laboratory of Breeding Biotechnology and Sustainable Aquaculture, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, Hubei, ChinaCollege of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing, ChinaKey Laboratory of Breeding Biotechnology and Sustainable Aquaculture, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, Hubei, ChinaKey Laboratory of Breeding Biotechnology and Sustainable Aquaculture, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, Hubei, ChinaKey Laboratory of Breeding Biotechnology and Sustainable Aquaculture, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, Hubei, ChinaKey Laboratory of Breeding Biotechnology and Sustainable Aquaculture, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, Hubei, ChinaKey Laboratory of Breeding Biotechnology and Sustainable Aquaculture, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, Hubei, ChinaIntroductionParasitic ciliates are protozoans with a global distribution. Along with the gut microbiota, they have formed a micro-ecosystem that affects the host’s nutrition, metabolism, and immunity. The interactions and relationships among the three components of this microecosystem (protozoa, gut microbiota, and host) remain only partially understood. Xenocypris fish and the unique ciliate Balantidium polyvacuolum in its hindgut are good materials to study the interplay.MethodsIn this study, 16S rRNA gene amplicon sequencing and short-chain fatty acids (SCFAs) identification were used. Network was also constructed to understand their relationships.ResultsWe found that the gut microbiota of B. polyvacuolum-infected X. davidi and X. argentea had higher diversity, richness, and evenness than uninfected ones. B. polyvacuolum could lead to an increase of Fusobacterium and Chloroflexi in both X. davidi and X. argentea, while significantly increase the abundance of genera Romboutsia and Clostridium in X. argentea. Besides, B. polyvacuolum could significantly increase the content of total SCFAs and acetic acid in X. davidi and increase the concentrations of propionic, isobutyric and butanoic acids in X. argentea. Furthermore, correlation analyses showed that B. polyvacuolum may alter SCFAs by affecting key SCFAs-producing bacteria such as Clostridium and Cetobacterium.DiscussionThis study greatly expands our understanding of relationships among B. polyvacuolum, gut microbiota and host Xenocypris fish, which sheds new insights into the mechanism of interaction among protozoa, gut microbiota and host.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1295456/fullBalantidium polyvacuolumgut microbiotashort-chain fatty acids (SCFAs)protozoaco-occurrence network |
| spellingShingle | Xialian Bu Xialian Bu Zhongyang Li Zhongyang Li Weishan Zhao Qingwen Zeng Qingwen Zeng Yushun Chen Wenxiang Li Hong Zou Ming Li Guitang Wang Alterations of gut microbiota and short-chain fatty acids induced by Balantidium polyvacuolum in the hindgut of Xenocyprinae fishes providing new insights into the relationship among protozoa, gut microbiota and host Frontiers in Microbiology Balantidium polyvacuolum gut microbiota short-chain fatty acids (SCFAs) protozoa co-occurrence network |
| title | Alterations of gut microbiota and short-chain fatty acids induced by Balantidium polyvacuolum in the hindgut of Xenocyprinae fishes providing new insights into the relationship among protozoa, gut microbiota and host |
| title_full | Alterations of gut microbiota and short-chain fatty acids induced by Balantidium polyvacuolum in the hindgut of Xenocyprinae fishes providing new insights into the relationship among protozoa, gut microbiota and host |
| title_fullStr | Alterations of gut microbiota and short-chain fatty acids induced by Balantidium polyvacuolum in the hindgut of Xenocyprinae fishes providing new insights into the relationship among protozoa, gut microbiota and host |
| title_full_unstemmed | Alterations of gut microbiota and short-chain fatty acids induced by Balantidium polyvacuolum in the hindgut of Xenocyprinae fishes providing new insights into the relationship among protozoa, gut microbiota and host |
| title_short | Alterations of gut microbiota and short-chain fatty acids induced by Balantidium polyvacuolum in the hindgut of Xenocyprinae fishes providing new insights into the relationship among protozoa, gut microbiota and host |
| title_sort | alterations of gut microbiota and short chain fatty acids induced by balantidium polyvacuolum in the hindgut of xenocyprinae fishes providing new insights into the relationship among protozoa gut microbiota and host |
| topic | Balantidium polyvacuolum gut microbiota short-chain fatty acids (SCFAs) protozoa co-occurrence network |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1295456/full |
| work_keys_str_mv | AT xialianbu alterationsofgutmicrobiotaandshortchainfattyacidsinducedbybalantidiumpolyvacuoluminthehindgutofxenocyprinaefishesprovidingnewinsightsintotherelationshipamongprotozoagutmicrobiotaandhost AT xialianbu alterationsofgutmicrobiotaandshortchainfattyacidsinducedbybalantidiumpolyvacuoluminthehindgutofxenocyprinaefishesprovidingnewinsightsintotherelationshipamongprotozoagutmicrobiotaandhost AT zhongyangli alterationsofgutmicrobiotaandshortchainfattyacidsinducedbybalantidiumpolyvacuoluminthehindgutofxenocyprinaefishesprovidingnewinsightsintotherelationshipamongprotozoagutmicrobiotaandhost AT zhongyangli alterationsofgutmicrobiotaandshortchainfattyacidsinducedbybalantidiumpolyvacuoluminthehindgutofxenocyprinaefishesprovidingnewinsightsintotherelationshipamongprotozoagutmicrobiotaandhost AT weishanzhao alterationsofgutmicrobiotaandshortchainfattyacidsinducedbybalantidiumpolyvacuoluminthehindgutofxenocyprinaefishesprovidingnewinsightsintotherelationshipamongprotozoagutmicrobiotaandhost AT qingwenzeng alterationsofgutmicrobiotaandshortchainfattyacidsinducedbybalantidiumpolyvacuoluminthehindgutofxenocyprinaefishesprovidingnewinsightsintotherelationshipamongprotozoagutmicrobiotaandhost AT qingwenzeng alterationsofgutmicrobiotaandshortchainfattyacidsinducedbybalantidiumpolyvacuoluminthehindgutofxenocyprinaefishesprovidingnewinsightsintotherelationshipamongprotozoagutmicrobiotaandhost AT yushunchen alterationsofgutmicrobiotaandshortchainfattyacidsinducedbybalantidiumpolyvacuoluminthehindgutofxenocyprinaefishesprovidingnewinsightsintotherelationshipamongprotozoagutmicrobiotaandhost AT wenxiangli alterationsofgutmicrobiotaandshortchainfattyacidsinducedbybalantidiumpolyvacuoluminthehindgutofxenocyprinaefishesprovidingnewinsightsintotherelationshipamongprotozoagutmicrobiotaandhost AT hongzou alterationsofgutmicrobiotaandshortchainfattyacidsinducedbybalantidiumpolyvacuoluminthehindgutofxenocyprinaefishesprovidingnewinsightsintotherelationshipamongprotozoagutmicrobiotaandhost AT mingli alterationsofgutmicrobiotaandshortchainfattyacidsinducedbybalantidiumpolyvacuoluminthehindgutofxenocyprinaefishesprovidingnewinsightsintotherelationshipamongprotozoagutmicrobiotaandhost AT guitangwang alterationsofgutmicrobiotaandshortchainfattyacidsinducedbybalantidiumpolyvacuoluminthehindgutofxenocyprinaefishesprovidingnewinsightsintotherelationshipamongprotozoagutmicrobiotaandhost |