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Microbes from Mum: symbiont transmission in the tropical reef sponge Ianthella basta

Most marine sponge species harbour distinct communities of microorganisms which contribute to various aspects of their host’s health and physiology. In addition to their key roles in nutrient transformations and chemical defence, these symbiotic microbes can shape sponge phenotype by mediating impor...

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Autores principales: Engelberts, J. Pamela, Abdul Wahab, Muhammad A., Maldonado, Manuel, Rix, Laura, Marangon, Emma, Robbins, Steven J., Wagner, Michael, Webster, Nicole S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9723589/
https://www.ncbi.nlm.nih.gov/pubmed/37938734
http://dx.doi.org/10.1038/s43705-022-00173-w
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author Engelberts, J. Pamela
Abdul Wahab, Muhammad A.
Maldonado, Manuel
Rix, Laura
Marangon, Emma
Robbins, Steven J.
Wagner, Michael
Webster, Nicole S.
author_facet Engelberts, J. Pamela
Abdul Wahab, Muhammad A.
Maldonado, Manuel
Rix, Laura
Marangon, Emma
Robbins, Steven J.
Wagner, Michael
Webster, Nicole S.
author_sort Engelberts, J. Pamela
collection PubMed
description Most marine sponge species harbour distinct communities of microorganisms which contribute to various aspects of their host’s health and physiology. In addition to their key roles in nutrient transformations and chemical defence, these symbiotic microbes can shape sponge phenotype by mediating important developmental stages and influencing the environmental tolerance of the host. However, the characterisation of each microbial taxon throughout a sponge’s life cycle remains challenging, with several sponge species hosting up to 3000 distinct microbial species. Ianthella basta, an abundant broadcast spawning species in the Indo-Pacific, is an emerging model for sponge symbiosis research as it harbours only three dominant symbionts: a Thaumarchaeotum, a Gammaproteobacterium, and an Alphaproteobacterium. Here, we successfully spawned Ianthella basta, characterised its mode of reproduction, and used 16S rRNA gene amplicon sequencing, fluorescence in situ hybridisation, and transmission electron microscopy to characterise the microbial community throughout its life cycle. We confirmed I. basta as being gonochoric and showed that the three dominant symbionts, which together make up >90% of the microbiome according to 16S rRNA gene abundance, are vertically transmitted from mother to offspring by a unique method involving encapsulation in the peri-oocytic space, suggesting an obligate relationship between these microbes and their host.
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spelling pubmed-97235892023-01-04 Microbes from Mum: symbiont transmission in the tropical reef sponge Ianthella basta Engelberts, J. Pamela Abdul Wahab, Muhammad A. Maldonado, Manuel Rix, Laura Marangon, Emma Robbins, Steven J. Wagner, Michael Webster, Nicole S. ISME Commun Article Most marine sponge species harbour distinct communities of microorganisms which contribute to various aspects of their host’s health and physiology. In addition to their key roles in nutrient transformations and chemical defence, these symbiotic microbes can shape sponge phenotype by mediating important developmental stages and influencing the environmental tolerance of the host. However, the characterisation of each microbial taxon throughout a sponge’s life cycle remains challenging, with several sponge species hosting up to 3000 distinct microbial species. Ianthella basta, an abundant broadcast spawning species in the Indo-Pacific, is an emerging model for sponge symbiosis research as it harbours only three dominant symbionts: a Thaumarchaeotum, a Gammaproteobacterium, and an Alphaproteobacterium. Here, we successfully spawned Ianthella basta, characterised its mode of reproduction, and used 16S rRNA gene amplicon sequencing, fluorescence in situ hybridisation, and transmission electron microscopy to characterise the microbial community throughout its life cycle. We confirmed I. basta as being gonochoric and showed that the three dominant symbionts, which together make up >90% of the microbiome according to 16S rRNA gene abundance, are vertically transmitted from mother to offspring by a unique method involving encapsulation in the peri-oocytic space, suggesting an obligate relationship between these microbes and their host. Nature Publishing Group UK 2022-09-27 /pmc/articles/PMC9723589/ /pubmed/37938734 http://dx.doi.org/10.1038/s43705-022-00173-w Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Engelberts, J. Pamela
Abdul Wahab, Muhammad A.
Maldonado, Manuel
Rix, Laura
Marangon, Emma
Robbins, Steven J.
Wagner, Michael
Webster, Nicole S.
Microbes from Mum: symbiont transmission in the tropical reef sponge Ianthella basta
title Microbes from Mum: symbiont transmission in the tropical reef sponge Ianthella basta
title_full Microbes from Mum: symbiont transmission in the tropical reef sponge Ianthella basta
title_fullStr Microbes from Mum: symbiont transmission in the tropical reef sponge Ianthella basta
title_full_unstemmed Microbes from Mum: symbiont transmission in the tropical reef sponge Ianthella basta
title_short Microbes from Mum: symbiont transmission in the tropical reef sponge Ianthella basta
title_sort microbes from mum: symbiont transmission in the tropical reef sponge ianthella basta
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9723589/
https://www.ncbi.nlm.nih.gov/pubmed/37938734
http://dx.doi.org/10.1038/s43705-022-00173-w
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