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Bacterial community dynamics during embryonic development of the little skate (Leucoraja erinacea)

BACKGROUND: Microbial transmission from parent to offspring is hypothesized to be widespread in vertebrates. However, evidence for this is limited as many evolutionarily important clades remain unexamined. There is currently no data on the microbiota associated with any Chondrichthyan species during...

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Autores principales: Mika, Katelyn, Okamoto, Alexander S., Shubin, Neil H., Mark Welch, David B.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8513177/
https://www.ncbi.nlm.nih.gov/pubmed/34645528
http://dx.doi.org/10.1186/s42523-021-00136-x
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author Mika, Katelyn
Okamoto, Alexander S.
Shubin, Neil H.
Mark Welch, David B.
author_facet Mika, Katelyn
Okamoto, Alexander S.
Shubin, Neil H.
Mark Welch, David B.
author_sort Mika, Katelyn
collection PubMed
description BACKGROUND: Microbial transmission from parent to offspring is hypothesized to be widespread in vertebrates. However, evidence for this is limited as many evolutionarily important clades remain unexamined. There is currently no data on the microbiota associated with any Chondrichthyan species during embryonic development, despite the global distribution, ecological importance, and phylogenetic position of this clade. In this study, we take the first steps towards filling this gap by investigating the microbiota associated with embryonic development in the little skate, Leucoraja erinacea, a common North Atlantic species and popular system for chondrichthyan biology. METHODS: To assess the potential for bacterial transmission in an oviparous chondrichthyan, we used 16S rRNA amplicon sequencing to characterize the microbial communities associated with the skin, gill, and egg capsule of the little skate, at six points during ontogeny. Community composition was analyzed using the QIIME2 pipeline and microbial continuity between stages was tracked using FEAST. RESULTS: We identify site-specific and stage-specific microbiota dominated by the bacterial phyla Proteobacteria and Bacteroidetes. This composition is similar to, but distinct from, that of previously published data on the adult microbiota of other chondrichthyan species. Our data reveal that the skate egg capsule harbors a highly diverse bacterial community–particularly on the internal surface of the capsule–and facilitates intergenerational microbial transfer to the offspring. Embryonic skin and external gill tissues host similar bacterial communities; the skin and gill communities later diverge as the internal gills and skin denticles develop. CONCLUSIONS: Our study is the first exploration of the chondrichthyan microbiota throughout ontogeny and provides the first evidence of vertical transmission in this group. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-021-00136-x.
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spelling pubmed-85131772021-10-20 Bacterial community dynamics during embryonic development of the little skate (Leucoraja erinacea) Mika, Katelyn Okamoto, Alexander S. Shubin, Neil H. Mark Welch, David B. Anim Microbiome Research Article BACKGROUND: Microbial transmission from parent to offspring is hypothesized to be widespread in vertebrates. However, evidence for this is limited as many evolutionarily important clades remain unexamined. There is currently no data on the microbiota associated with any Chondrichthyan species during embryonic development, despite the global distribution, ecological importance, and phylogenetic position of this clade. In this study, we take the first steps towards filling this gap by investigating the microbiota associated with embryonic development in the little skate, Leucoraja erinacea, a common North Atlantic species and popular system for chondrichthyan biology. METHODS: To assess the potential for bacterial transmission in an oviparous chondrichthyan, we used 16S rRNA amplicon sequencing to characterize the microbial communities associated with the skin, gill, and egg capsule of the little skate, at six points during ontogeny. Community composition was analyzed using the QIIME2 pipeline and microbial continuity between stages was tracked using FEAST. RESULTS: We identify site-specific and stage-specific microbiota dominated by the bacterial phyla Proteobacteria and Bacteroidetes. This composition is similar to, but distinct from, that of previously published data on the adult microbiota of other chondrichthyan species. Our data reveal that the skate egg capsule harbors a highly diverse bacterial community–particularly on the internal surface of the capsule–and facilitates intergenerational microbial transfer to the offspring. Embryonic skin and external gill tissues host similar bacterial communities; the skin and gill communities later diverge as the internal gills and skin denticles develop. CONCLUSIONS: Our study is the first exploration of the chondrichthyan microbiota throughout ontogeny and provides the first evidence of vertical transmission in this group. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-021-00136-x. BioMed Central 2021-10-13 /pmc/articles/PMC8513177/ /pubmed/34645528 http://dx.doi.org/10.1186/s42523-021-00136-x Text en © The Author(s) 2021 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 Article
Mika, Katelyn
Okamoto, Alexander S.
Shubin, Neil H.
Mark Welch, David B.
Bacterial community dynamics during embryonic development of the little skate (Leucoraja erinacea)
title Bacterial community dynamics during embryonic development of the little skate (Leucoraja erinacea)
title_full Bacterial community dynamics during embryonic development of the little skate (Leucoraja erinacea)
title_fullStr Bacterial community dynamics during embryonic development of the little skate (Leucoraja erinacea)
title_full_unstemmed Bacterial community dynamics during embryonic development of the little skate (Leucoraja erinacea)
title_short Bacterial community dynamics during embryonic development of the little skate (Leucoraja erinacea)
title_sort bacterial community dynamics during embryonic development of the little skate (leucoraja erinacea)
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8513177/
https://www.ncbi.nlm.nih.gov/pubmed/34645528
http://dx.doi.org/10.1186/s42523-021-00136-x
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