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Surface Topography, Bacterial Carrying Capacity, and the Prospect of Microbiome Manipulation in the Sea Anemone Coral Model Aiptasia

Aiptasia is an emerging model organism to study cnidarian symbioses due to its taxonomic relatedness to other anthozoans such as stony corals and similarities of its microalgal and bacterial partners, complementing the existing Hydra (Hydrozoa) and Nematostella (Anthozoa) model systems. Despite the...

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Autores principales: Costa, Rúben M., Cárdenas, Anny, Loussert-Fonta, Céline, Toullec, Gaëlle, Meibom, Anders, Voolstra, Christian R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8060496/
https://www.ncbi.nlm.nih.gov/pubmed/33897642
http://dx.doi.org/10.3389/fmicb.2021.637834
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author Costa, Rúben M.
Cárdenas, Anny
Loussert-Fonta, Céline
Toullec, Gaëlle
Meibom, Anders
Voolstra, Christian R.
author_facet Costa, Rúben M.
Cárdenas, Anny
Loussert-Fonta, Céline
Toullec, Gaëlle
Meibom, Anders
Voolstra, Christian R.
author_sort Costa, Rúben M.
collection PubMed
description Aiptasia is an emerging model organism to study cnidarian symbioses due to its taxonomic relatedness to other anthozoans such as stony corals and similarities of its microalgal and bacterial partners, complementing the existing Hydra (Hydrozoa) and Nematostella (Anthozoa) model systems. Despite the availability of studies characterizing the microbiomes of several natural Aiptasia populations and laboratory strains, knowledge on basic information, such as surface topography, bacterial carrying capacity, or the prospect of microbiome manipulation is lacking. Here we address these knowledge gaps. Our results show that the surface topographies of the model hydrozoan Hydra and anthozoans differ substantially, whereas the ultrastructural surface architecture of Aiptasia and stony corals is highly similar. Further, we determined a bacterial carrying capacity of ∼10(4) and ∼10(5) bacteria (i.e., colony forming units, CFUs) per polyp for aposymbiotic and symbiotic Aiptasia anemones, respectively, suggesting that the symbiotic status changes bacterial association/density. Microbiome transplants from Acropora humilis and Porites sp. to gnotobiotic Aiptasia showed that only a few foreign bacterial taxa were effective colonizers. Our results shed light on the putative difficulties of transplanting microbiomes between cnidarians in a manner that consistently changes microbial host association at large. At the same time, our study provides an avenue to identify bacterial taxa that exhibit broad ability to colonize different hosts as a starting point for cross-species microbiome manipulation. Our work is relevant in the context of microbial therapy (probiotics) and microbiome manipulation in corals and answers to the need of having cnidarian model systems to test the function of bacteria and their effect on holobiont biology. Taken together, we provide important foundation data to extend Aiptasia as a coral model for bacterial functional studies.
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spelling pubmed-80604962021-04-23 Surface Topography, Bacterial Carrying Capacity, and the Prospect of Microbiome Manipulation in the Sea Anemone Coral Model Aiptasia Costa, Rúben M. Cárdenas, Anny Loussert-Fonta, Céline Toullec, Gaëlle Meibom, Anders Voolstra, Christian R. Front Microbiol Microbiology Aiptasia is an emerging model organism to study cnidarian symbioses due to its taxonomic relatedness to other anthozoans such as stony corals and similarities of its microalgal and bacterial partners, complementing the existing Hydra (Hydrozoa) and Nematostella (Anthozoa) model systems. Despite the availability of studies characterizing the microbiomes of several natural Aiptasia populations and laboratory strains, knowledge on basic information, such as surface topography, bacterial carrying capacity, or the prospect of microbiome manipulation is lacking. Here we address these knowledge gaps. Our results show that the surface topographies of the model hydrozoan Hydra and anthozoans differ substantially, whereas the ultrastructural surface architecture of Aiptasia and stony corals is highly similar. Further, we determined a bacterial carrying capacity of ∼10(4) and ∼10(5) bacteria (i.e., colony forming units, CFUs) per polyp for aposymbiotic and symbiotic Aiptasia anemones, respectively, suggesting that the symbiotic status changes bacterial association/density. Microbiome transplants from Acropora humilis and Porites sp. to gnotobiotic Aiptasia showed that only a few foreign bacterial taxa were effective colonizers. Our results shed light on the putative difficulties of transplanting microbiomes between cnidarians in a manner that consistently changes microbial host association at large. At the same time, our study provides an avenue to identify bacterial taxa that exhibit broad ability to colonize different hosts as a starting point for cross-species microbiome manipulation. Our work is relevant in the context of microbial therapy (probiotics) and microbiome manipulation in corals and answers to the need of having cnidarian model systems to test the function of bacteria and their effect on holobiont biology. Taken together, we provide important foundation data to extend Aiptasia as a coral model for bacterial functional studies. Frontiers Media S.A. 2021-04-08 /pmc/articles/PMC8060496/ /pubmed/33897642 http://dx.doi.org/10.3389/fmicb.2021.637834 Text en Copyright © 2021 Costa, Cárdenas, Loussert-Fonta, Toullec, Meibom and Voolstra. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Costa, Rúben M.
Cárdenas, Anny
Loussert-Fonta, Céline
Toullec, Gaëlle
Meibom, Anders
Voolstra, Christian R.
Surface Topography, Bacterial Carrying Capacity, and the Prospect of Microbiome Manipulation in the Sea Anemone Coral Model Aiptasia
title Surface Topography, Bacterial Carrying Capacity, and the Prospect of Microbiome Manipulation in the Sea Anemone Coral Model Aiptasia
title_full Surface Topography, Bacterial Carrying Capacity, and the Prospect of Microbiome Manipulation in the Sea Anemone Coral Model Aiptasia
title_fullStr Surface Topography, Bacterial Carrying Capacity, and the Prospect of Microbiome Manipulation in the Sea Anemone Coral Model Aiptasia
title_full_unstemmed Surface Topography, Bacterial Carrying Capacity, and the Prospect of Microbiome Manipulation in the Sea Anemone Coral Model Aiptasia
title_short Surface Topography, Bacterial Carrying Capacity, and the Prospect of Microbiome Manipulation in the Sea Anemone Coral Model Aiptasia
title_sort surface topography, bacterial carrying capacity, and the prospect of microbiome manipulation in the sea anemone coral model aiptasia
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8060496/
https://www.ncbi.nlm.nih.gov/pubmed/33897642
http://dx.doi.org/10.3389/fmicb.2021.637834
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