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Parental care contributes to vertical transmission of microbes in a skin-feeding and direct-developing caecilian

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...

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Autores principales: Kouete, Marcel T., Bletz, Molly C., LaBumbard, Brandon C., Woodhams, Douglas C., Blackburn, David C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10184399/
https://www.ncbi.nlm.nih.gov/pubmed/37189209
http://dx.doi.org/10.1186/s42523-023-00243-x
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author Kouete, Marcel T.
Bletz, Molly C.
LaBumbard, Brandon C.
Woodhams, Douglas C.
Blackburn, David C.
author_facet Kouete, Marcel T.
Bletz, Molly C.
LaBumbard, Brandon C.
Woodhams, Douglas C.
Blackburn, David C.
author_sort Kouete, Marcel T.
collection PubMed
description 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. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-023-00243-x.
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spelling pubmed-101843992023-05-16 Parental care contributes to vertical transmission of microbes in a skin-feeding and direct-developing caecilian Kouete, Marcel T. Bletz, Molly C. LaBumbard, Brandon C. Woodhams, Douglas C. Blackburn, David C. Anim Microbiome Research 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. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-023-00243-x. BioMed Central 2023-05-15 /pmc/articles/PMC10184399/ /pubmed/37189209 http://dx.doi.org/10.1186/s42523-023-00243-x Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research
Kouete, Marcel T.
Bletz, Molly C.
LaBumbard, Brandon C.
Woodhams, Douglas C.
Blackburn, David C.
Parental care contributes to vertical transmission of microbes in a skin-feeding and direct-developing caecilian
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 Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10184399/
https://www.ncbi.nlm.nih.gov/pubmed/37189209
http://dx.doi.org/10.1186/s42523-023-00243-x
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