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Unveiling microbiome changes in Mediterranean octocorals during the 2022 marine heatwaves: quantifying key bacterial symbionts and potential pathogens

BACKGROUND: Climate change has accelerated the occurrence and severity of heatwaves in the Mediterranean Sea and poses a significant threat to the octocoral species that form the foundation of marine animal forests (MAFs). As coral health intricately relies on the symbiotic relationships established...

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Autores principales: Prioux, Camille, Tignat-Perrier, Romie, Gervais, Ophélie, Estaque, Tristan, Schull, Quentin, Reynaud, Stéphanie, Béraud, Eric, Mérigot, Bastien, Beauvieux, Anaïs, Marcus, Maria-Isabelle, Richaume, Justine, Bianchimani, Olivier, Cheminée, Adrien, Allemand, Denis, Ferrier-Pagès, Christine
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10696765/
http://dx.doi.org/10.1186/s40168-023-01711-x
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author Prioux, Camille
Tignat-Perrier, Romie
Gervais, Ophélie
Estaque, Tristan
Schull, Quentin
Reynaud, Stéphanie
Béraud, Eric
Mérigot, Bastien
Beauvieux, Anaïs
Marcus, Maria-Isabelle
Richaume, Justine
Bianchimani, Olivier
Cheminée, Adrien
Allemand, Denis
Ferrier-Pagès, Christine
author_facet Prioux, Camille
Tignat-Perrier, Romie
Gervais, Ophélie
Estaque, Tristan
Schull, Quentin
Reynaud, Stéphanie
Béraud, Eric
Mérigot, Bastien
Beauvieux, Anaïs
Marcus, Maria-Isabelle
Richaume, Justine
Bianchimani, Olivier
Cheminée, Adrien
Allemand, Denis
Ferrier-Pagès, Christine
author_sort Prioux, Camille
collection PubMed
description BACKGROUND: Climate change has accelerated the occurrence and severity of heatwaves in the Mediterranean Sea and poses a significant threat to the octocoral species that form the foundation of marine animal forests (MAFs). As coral health intricately relies on the symbiotic relationships established between corals and microbial communities, our goal was to gain a deeper understanding of the role of bacteria in the observed tissue loss of key octocoral species following the unprecedented heatwaves in 2022. RESULTS: Using amplicon sequencing and taxon-specific qPCR analyses, we unexpectedly found that the absolute abundance of the major bacterial symbionts, Spirochaetaceae (C. rubrum) and Endozoicomonas (P. clavata), remained, in most cases, unchanged between colonies with 0% and 90% tissue loss. These results suggest that the impairment of coral health was not due to the loss of the main bacterial symbionts. However, we observed a significant increase in the total abundance of bacterial opportunists, including putative pathogens such as Vibrio, which was not evident when only their relative abundance was considered. In addition, there was no clear relation between bacterial symbiont loss and the intensity of thermal stress, suggesting that factors other than temperature may have influenced the differential response of octocoral microbiomes at different sampling sites. CONCLUSIONS: Our results indicate that tissue loss in octocorals is not directly caused by the decline of the main bacterial symbionts but by the proliferation of opportunistic and pathogenic bacteria. Our findings thus underscore the significance of considering both relative and absolute quantification approaches when evaluating the impact of stressors on coral microbiome as the relative quantification does not accurately depict the actual changes in the microbiome. Consequently, this research enhances our comprehension of the intricate interplay between host organisms, their microbiomes, and environmental stressors, while offering valuable insights into the ecological implications of heatwaves on marine animal forests. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-023-01711-x.
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spelling pubmed-106967652023-12-06 Unveiling microbiome changes in Mediterranean octocorals during the 2022 marine heatwaves: quantifying key bacterial symbionts and potential pathogens Prioux, Camille Tignat-Perrier, Romie Gervais, Ophélie Estaque, Tristan Schull, Quentin Reynaud, Stéphanie Béraud, Eric Mérigot, Bastien Beauvieux, Anaïs Marcus, Maria-Isabelle Richaume, Justine Bianchimani, Olivier Cheminée, Adrien Allemand, Denis Ferrier-Pagès, Christine Microbiome Research BACKGROUND: Climate change has accelerated the occurrence and severity of heatwaves in the Mediterranean Sea and poses a significant threat to the octocoral species that form the foundation of marine animal forests (MAFs). As coral health intricately relies on the symbiotic relationships established between corals and microbial communities, our goal was to gain a deeper understanding of the role of bacteria in the observed tissue loss of key octocoral species following the unprecedented heatwaves in 2022. RESULTS: Using amplicon sequencing and taxon-specific qPCR analyses, we unexpectedly found that the absolute abundance of the major bacterial symbionts, Spirochaetaceae (C. rubrum) and Endozoicomonas (P. clavata), remained, in most cases, unchanged between colonies with 0% and 90% tissue loss. These results suggest that the impairment of coral health was not due to the loss of the main bacterial symbionts. However, we observed a significant increase in the total abundance of bacterial opportunists, including putative pathogens such as Vibrio, which was not evident when only their relative abundance was considered. In addition, there was no clear relation between bacterial symbiont loss and the intensity of thermal stress, suggesting that factors other than temperature may have influenced the differential response of octocoral microbiomes at different sampling sites. CONCLUSIONS: Our results indicate that tissue loss in octocorals is not directly caused by the decline of the main bacterial symbionts but by the proliferation of opportunistic and pathogenic bacteria. Our findings thus underscore the significance of considering both relative and absolute quantification approaches when evaluating the impact of stressors on coral microbiome as the relative quantification does not accurately depict the actual changes in the microbiome. Consequently, this research enhances our comprehension of the intricate interplay between host organisms, their microbiomes, and environmental stressors, while offering valuable insights into the ecological implications of heatwaves on marine animal forests. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-023-01711-x. BioMed Central 2023-12-05 /pmc/articles/PMC10696765/ http://dx.doi.org/10.1186/s40168-023-01711-x Text en © The Author(s) 2023 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 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/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Prioux, Camille
Tignat-Perrier, Romie
Gervais, Ophélie
Estaque, Tristan
Schull, Quentin
Reynaud, Stéphanie
Béraud, Eric
Mérigot, Bastien
Beauvieux, Anaïs
Marcus, Maria-Isabelle
Richaume, Justine
Bianchimani, Olivier
Cheminée, Adrien
Allemand, Denis
Ferrier-Pagès, Christine
Unveiling microbiome changes in Mediterranean octocorals during the 2022 marine heatwaves: quantifying key bacterial symbionts and potential pathogens
title Unveiling microbiome changes in Mediterranean octocorals during the 2022 marine heatwaves: quantifying key bacterial symbionts and potential pathogens
title_full Unveiling microbiome changes in Mediterranean octocorals during the 2022 marine heatwaves: quantifying key bacterial symbionts and potential pathogens
title_fullStr Unveiling microbiome changes in Mediterranean octocorals during the 2022 marine heatwaves: quantifying key bacterial symbionts and potential pathogens
title_full_unstemmed Unveiling microbiome changes in Mediterranean octocorals during the 2022 marine heatwaves: quantifying key bacterial symbionts and potential pathogens
title_short Unveiling microbiome changes in Mediterranean octocorals during the 2022 marine heatwaves: quantifying key bacterial symbionts and potential pathogens
title_sort unveiling microbiome changes in mediterranean octocorals during the 2022 marine heatwaves: quantifying key bacterial symbionts and potential pathogens
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10696765/
http://dx.doi.org/10.1186/s40168-023-01711-x
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