Parental care contributes to vertical transmission of microbes in a skin-feeding and direct-developing caecilian
Abstract Background Our current understanding of vertebrate skin and gut microbiomes, and their vertical transmission, remains incomplete as major lineages and varied forms of parental care remain unexplored. The diverse and elaborate forms of parental care exhibited by amphibians constitute an idea...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2023-05-01
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| Series: | Animal Microbiome |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s42523-023-00243-x |
| _version_ | 1827943203720921088 |
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| author | Marcel T. Kouete Molly C. Bletz Brandon C. LaBumbard Douglas C. Woodhams David C. Blackburn |
| author_facet | Marcel T. Kouete Molly C. Bletz Brandon C. LaBumbard Douglas C. Woodhams David C. Blackburn |
| author_sort | Marcel T. Kouete |
| collection | DOAJ |
| description | Abstract Background Our current understanding of vertebrate skin and gut microbiomes, and their vertical transmission, remains incomplete as major lineages and varied forms of parental care remain unexplored. The diverse and elaborate forms of parental care exhibited by amphibians constitute an ideal system to study microbe transmission, yet investigations of vertical transmission among frogs and salamanders have been inconclusive. In this study, we assess bacteria transmission in Herpele squalostoma, an oviparous direct-developing caecilian in which females obligately attend juveniles that feed on their mother’s skin (dermatophagy). Results We used 16S rRNA amplicon-sequencing of the skin and gut of wild caught H. squalostoma individuals (males, females, including those attending juveniles) as well as environmental samples. Sourcetracker analyses revealed that juveniles obtain an important portion of their skin and gut bacteria communities from their mother. The contribution of a mother’s skin to the skin and gut of her respective juveniles was much larger than that of any other bacteria source. In contrast to males and females not attending juveniles, only the skins of juveniles and their mothers were colonized by bacteria taxa Verrucomicrobiaceae, Nocardioidaceae, and Erysipelotrichaceae. In addition to providing indirect evidence for microbiome transmission linked to parental care among amphibians, our study also points to noticeable differences between the skin and gut communities of H. squalostoma and that of many frogs and salamanders, which warrants further investigation. Conclusion Our study is the first to find strong support for vertical bacteria transmission attributed to parental care in a direct-developing amphibian species. This suggests that obligate parental care may promote microbiome transmission in caecilians. |
| first_indexed | 2024-03-13T10:11:56Z |
| format | Article |
| id | doaj.art-d00d343b9fa3491a9b2382409fff60c1 |
| institution | Directory Open Access Journal |
| issn | 2524-4671 |
| language | English |
| last_indexed | 2024-03-13T10:11:56Z |
| publishDate | 2023-05-01 |
| publisher | BMC |
| record_format | Article |
| series | Animal Microbiome |
| spelling | doaj.art-d00d343b9fa3491a9b2382409fff60c12023-05-21T11:28:20ZengBMCAnimal Microbiome2524-46712023-05-015111510.1186/s42523-023-00243-xParental care contributes to vertical transmission of microbes in a skin-feeding and direct-developing caecilianMarcel T. Kouete0Molly C. Bletz1Brandon C. LaBumbard2Douglas C. Woodhams3David C. Blackburn4School of Natural Resources and Environment, University of FloridaDepartment of Biology, University of MassachusettsDepartment of Biology, University of MassachusettsDepartment of Biology, University of MassachusettsDepartment of Natural History, Florida Museum of Natural History, University of FloridaAbstract Background Our current understanding of vertebrate skin and gut microbiomes, and their vertical transmission, remains incomplete as major lineages and varied forms of parental care remain unexplored. The diverse and elaborate forms of parental care exhibited by amphibians constitute an ideal system to study microbe transmission, yet investigations of vertical transmission among frogs and salamanders have been inconclusive. In this study, we assess bacteria transmission in Herpele squalostoma, an oviparous direct-developing caecilian in which females obligately attend juveniles that feed on their mother’s skin (dermatophagy). Results We used 16S rRNA amplicon-sequencing of the skin and gut of wild caught H. squalostoma individuals (males, females, including those attending juveniles) as well as environmental samples. Sourcetracker analyses revealed that juveniles obtain an important portion of their skin and gut bacteria communities from their mother. The contribution of a mother’s skin to the skin and gut of her respective juveniles was much larger than that of any other bacteria source. In contrast to males and females not attending juveniles, only the skins of juveniles and their mothers were colonized by bacteria taxa Verrucomicrobiaceae, Nocardioidaceae, and Erysipelotrichaceae. In addition to providing indirect evidence for microbiome transmission linked to parental care among amphibians, our study also points to noticeable differences between the skin and gut communities of H. squalostoma and that of many frogs and salamanders, which warrants further investigation. Conclusion Our study is the first to find strong support for vertical bacteria transmission attributed to parental care in a direct-developing amphibian species. This suggests that obligate parental care may promote microbiome transmission in caecilians.https://doi.org/10.1186/s42523-023-00243-x16S rRNAAmphibiaDermatophagyHorizontal transmissionSkin and gut microbiomesVertical transmission |
| spellingShingle | Marcel T. Kouete Molly C. Bletz Brandon C. LaBumbard Douglas C. Woodhams David C. Blackburn Parental care contributes to vertical transmission of microbes in a skin-feeding and direct-developing caecilian Animal Microbiome 16S rRNA Amphibia Dermatophagy Horizontal transmission Skin and gut microbiomes Vertical transmission |
| title | Parental care contributes to vertical transmission of microbes in a skin-feeding and direct-developing caecilian |
| title_full | Parental care contributes to vertical transmission of microbes in a skin-feeding and direct-developing caecilian |
| title_fullStr | Parental care contributes to vertical transmission of microbes in a skin-feeding and direct-developing caecilian |
| title_full_unstemmed | Parental care contributes to vertical transmission of microbes in a skin-feeding and direct-developing caecilian |
| title_short | Parental care contributes to vertical transmission of microbes in a skin-feeding and direct-developing caecilian |
| title_sort | parental care contributes to vertical transmission of microbes in a skin feeding and direct developing caecilian |
| topic | 16S rRNA Amphibia Dermatophagy Horizontal transmission Skin and gut microbiomes Vertical transmission |
| url | https://doi.org/10.1186/s42523-023-00243-x |
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