Interactions between Balantidium ctenopharyngodoni and microbiota reveal its low pathogenicity in the hindgut of grass carp
Abstract Background Hosts, parasites, and microbiota interact with each other, forming a complex ecosystem. Alterations to the microbial structure have been observed in various enteric parasitic infections (e.g. parasitic protists and helminths). Interestingly, some parasites are associated with hea...
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| Format: | Article |
| Language: | English |
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BMC
2024-01-01
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| Series: | BMC Microbiology |
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| Online Access: | https://doi.org/10.1186/s12866-023-03154-8 |
| _version_ | 1797363592080654336 |
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| author | Weishan Zhao Xialian Bu Weitian Zhou Qingwen Zeng Tian Qin Shangong Wu Wenxiang Li Hong Zou Ming Li Guitang Wang |
| author_facet | Weishan Zhao Xialian Bu Weitian Zhou Qingwen Zeng Tian Qin Shangong Wu Wenxiang Li Hong Zou Ming Li Guitang Wang |
| author_sort | Weishan Zhao |
| collection | DOAJ |
| description | Abstract Background Hosts, parasites, and microbiota interact with each other, forming a complex ecosystem. Alterations to the microbial structure have been observed in various enteric parasitic infections (e.g. parasitic protists and helminths). Interestingly, some parasites are associated with healthy gut microbiota linked to the intestinal eubiosis state. So the changes in bacteria and metabolites induced by parasite infection may offer benefits to the host, including protection from other parasitesand promotion of intestinal health. The only ciliate known to inhabit the hindgut of grass carp, Balantidium ctenopharyngodoni, does not cause obvious damage to the intestinal mucosa. To date, its impact on intestinal microbiota composition remains unknown. In this study, we investigated the microbial composition in the hindgut of grass carp infected with B. ctenopharyngodoni, as well as the changes of metabolites in intestinal contents resulting from infection. Results Colonization by B. ctenopharyngodoni was associated with an increase in bacterial diversity, a higher relative abundance of Clostridium, and a lower abundance of Enterobacteriaceae. The family Aeromonadaceae and the genus Citrobacter had significantly lower relative abundance in infected fish. Additionally, grass carp infected with B. ctenopharyngodoni exhibited a significant increase in creatine content in the hindgut. This suggested that the presence of B. ctenopharyngodoni may improve intestinal health through changes in microbiota and metabolites. Conclusions We found that grass carp infected with B. ctenopharyngodoni exhibit a healthy microbiota with an increased bacterial diversity. The results suggested that B. ctenopharyngodoni reshaped the composition of hindgut microbiota similarly to other protists with low pathogenicity. The shifts in the microbiota and metabolites during the colonization and proliferation of B. ctenopharyngodoni indicated that it may provide positive effects in the hindgut of grass carp. |
| first_indexed | 2024-03-08T16:23:22Z |
| format | Article |
| id | doaj.art-6a6070d46b9c4b3885ad4f382771e95b |
| institution | Directory Open Access Journal |
| issn | 1471-2180 |
| language | English |
| last_indexed | 2024-03-08T16:23:22Z |
| publishDate | 2024-01-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Microbiology |
| spelling | doaj.art-6a6070d46b9c4b3885ad4f382771e95b2024-01-07T12:14:08ZengBMCBMC Microbiology1471-21802024-01-0124111010.1186/s12866-023-03154-8Interactions between Balantidium ctenopharyngodoni and microbiota reveal its low pathogenicity in the hindgut of grass carpWeishan Zhao0Xialian Bu1Weitian Zhou2Qingwen Zeng3Tian Qin4Shangong Wu5Wenxiang Li6Hong Zou7Ming Li8Guitang Wang9Institute of Hydrobiology, Chinese Academy of SciencesInstitute of Hydrobiology, Chinese Academy of SciencesInstitute of Hydrobiology, Chinese Academy of SciencesInstitute of Hydrobiology, Chinese Academy of SciencesInstitute of Hydrobiology, Chinese Academy of SciencesInstitute of Hydrobiology, Chinese Academy of SciencesInstitute of Hydrobiology, Chinese Academy of SciencesInstitute of Hydrobiology, Chinese Academy of SciencesInstitute of Hydrobiology, Chinese Academy of SciencesInstitute of Hydrobiology, Chinese Academy of SciencesAbstract Background Hosts, parasites, and microbiota interact with each other, forming a complex ecosystem. Alterations to the microbial structure have been observed in various enteric parasitic infections (e.g. parasitic protists and helminths). Interestingly, some parasites are associated with healthy gut microbiota linked to the intestinal eubiosis state. So the changes in bacteria and metabolites induced by parasite infection may offer benefits to the host, including protection from other parasitesand promotion of intestinal health. The only ciliate known to inhabit the hindgut of grass carp, Balantidium ctenopharyngodoni, does not cause obvious damage to the intestinal mucosa. To date, its impact on intestinal microbiota composition remains unknown. In this study, we investigated the microbial composition in the hindgut of grass carp infected with B. ctenopharyngodoni, as well as the changes of metabolites in intestinal contents resulting from infection. Results Colonization by B. ctenopharyngodoni was associated with an increase in bacterial diversity, a higher relative abundance of Clostridium, and a lower abundance of Enterobacteriaceae. The family Aeromonadaceae and the genus Citrobacter had significantly lower relative abundance in infected fish. Additionally, grass carp infected with B. ctenopharyngodoni exhibited a significant increase in creatine content in the hindgut. This suggested that the presence of B. ctenopharyngodoni may improve intestinal health through changes in microbiota and metabolites. Conclusions We found that grass carp infected with B. ctenopharyngodoni exhibit a healthy microbiota with an increased bacterial diversity. The results suggested that B. ctenopharyngodoni reshaped the composition of hindgut microbiota similarly to other protists with low pathogenicity. The shifts in the microbiota and metabolites during the colonization and proliferation of B. ctenopharyngodoni indicated that it may provide positive effects in the hindgut of grass carp.https://doi.org/10.1186/s12866-023-03154-8Balantidium ctenopharyngodoniGrass carpIntestinal microbiotaMetabolitesCiliate |
| spellingShingle | Weishan Zhao Xialian Bu Weitian Zhou Qingwen Zeng Tian Qin Shangong Wu Wenxiang Li Hong Zou Ming Li Guitang Wang Interactions between Balantidium ctenopharyngodoni and microbiota reveal its low pathogenicity in the hindgut of grass carp BMC Microbiology Balantidium ctenopharyngodoni Grass carp Intestinal microbiota Metabolites Ciliate |
| title | Interactions between Balantidium ctenopharyngodoni and microbiota reveal its low pathogenicity in the hindgut of grass carp |
| title_full | Interactions between Balantidium ctenopharyngodoni and microbiota reveal its low pathogenicity in the hindgut of grass carp |
| title_fullStr | Interactions between Balantidium ctenopharyngodoni and microbiota reveal its low pathogenicity in the hindgut of grass carp |
| title_full_unstemmed | Interactions between Balantidium ctenopharyngodoni and microbiota reveal its low pathogenicity in the hindgut of grass carp |
| title_short | Interactions between Balantidium ctenopharyngodoni and microbiota reveal its low pathogenicity in the hindgut of grass carp |
| title_sort | interactions between balantidium ctenopharyngodoni and microbiota reveal its low pathogenicity in the hindgut of grass carp |
| topic | Balantidium ctenopharyngodoni Grass carp Intestinal microbiota Metabolites Ciliate |
| url | https://doi.org/10.1186/s12866-023-03154-8 |
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