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Coral microbiome manipulation elicits metabolic and genetic restructuring to mitigate heat stress and evade mortality

Beneficial microorganisms for corals (BMCs) ameliorate environmental stress, but whether they can prevent mortality and the underlying host response mechanisms remains elusive. Here, we conducted omics analyses on the coral Mussismilia hispida exposed to bleaching conditions in a long-term mesocosm...

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Autores principales: Santoro, Erika P., Borges, Ricardo M., Espinoza, Josh L., Freire, Marcelo, Messias, Camila S. M. A., Villela, Helena D. M., Pereira, Leandro M., Vilela, Caren L. S., Rosado, João G., Cardoso, Pedro M., Rosado, Phillipe M., Assis, Juliana M., Duarte, Gustavo A. S., Perna, Gabriela, Rosado, Alexandre S., Macrae, Andrew, Dupont, Christopher L., Nelson, Karen E., Sweet, Michael J., Voolstra, Christian R., Peixoto, Raquel S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Association for the Advancement of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8363143/
https://www.ncbi.nlm.nih.gov/pubmed/34389536
http://dx.doi.org/10.1126/sciadv.abg3088
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author Santoro, Erika P.
Borges, Ricardo M.
Espinoza, Josh L.
Freire, Marcelo
Messias, Camila S. M. A.
Villela, Helena D. M.
Pereira, Leandro M.
Vilela, Caren L. S.
Rosado, João G.
Cardoso, Pedro M.
Rosado, Phillipe M.
Assis, Juliana M.
Duarte, Gustavo A. S.
Perna, Gabriela
Rosado, Alexandre S.
Macrae, Andrew
Dupont, Christopher L.
Nelson, Karen E.
Sweet, Michael J.
Voolstra, Christian R.
Peixoto, Raquel S.
author_facet Santoro, Erika P.
Borges, Ricardo M.
Espinoza, Josh L.
Freire, Marcelo
Messias, Camila S. M. A.
Villela, Helena D. M.
Pereira, Leandro M.
Vilela, Caren L. S.
Rosado, João G.
Cardoso, Pedro M.
Rosado, Phillipe M.
Assis, Juliana M.
Duarte, Gustavo A. S.
Perna, Gabriela
Rosado, Alexandre S.
Macrae, Andrew
Dupont, Christopher L.
Nelson, Karen E.
Sweet, Michael J.
Voolstra, Christian R.
Peixoto, Raquel S.
author_sort Santoro, Erika P.
collection PubMed
description Beneficial microorganisms for corals (BMCs) ameliorate environmental stress, but whether they can prevent mortality and the underlying host response mechanisms remains elusive. Here, we conducted omics analyses on the coral Mussismilia hispida exposed to bleaching conditions in a long-term mesocosm experiment and inoculated with a selected BMC consortium or a saline solution placebo. All corals were affected by heat stress, but the observed “post-heat stress disorder” was mitigated by BMCs, signified by patterns of dimethylsulfoniopropionate degradation, lipid maintenance, and coral host transcriptional reprogramming of cellular restructuration, repair, stress protection, and immune genes, concomitant with a 40% survival rate increase and stable photosynthetic performance by the endosymbiotic algae. This study provides insights into the responses that underlie probiotic host manipulation. We demonstrate that BMCs trigger a dynamic microbiome restructuring process that instigates genetic and metabolic alterations in the coral host that eventually mitigate coral bleaching and mortality.
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spelling pubmed-83631432021-08-20 Coral microbiome manipulation elicits metabolic and genetic restructuring to mitigate heat stress and evade mortality Santoro, Erika P. Borges, Ricardo M. Espinoza, Josh L. Freire, Marcelo Messias, Camila S. M. A. Villela, Helena D. M. Pereira, Leandro M. Vilela, Caren L. S. Rosado, João G. Cardoso, Pedro M. Rosado, Phillipe M. Assis, Juliana M. Duarte, Gustavo A. S. Perna, Gabriela Rosado, Alexandre S. Macrae, Andrew Dupont, Christopher L. Nelson, Karen E. Sweet, Michael J. Voolstra, Christian R. Peixoto, Raquel S. Sci Adv Research Articles Beneficial microorganisms for corals (BMCs) ameliorate environmental stress, but whether they can prevent mortality and the underlying host response mechanisms remains elusive. Here, we conducted omics analyses on the coral Mussismilia hispida exposed to bleaching conditions in a long-term mesocosm experiment and inoculated with a selected BMC consortium or a saline solution placebo. All corals were affected by heat stress, but the observed “post-heat stress disorder” was mitigated by BMCs, signified by patterns of dimethylsulfoniopropionate degradation, lipid maintenance, and coral host transcriptional reprogramming of cellular restructuration, repair, stress protection, and immune genes, concomitant with a 40% survival rate increase and stable photosynthetic performance by the endosymbiotic algae. This study provides insights into the responses that underlie probiotic host manipulation. We demonstrate that BMCs trigger a dynamic microbiome restructuring process that instigates genetic and metabolic alterations in the coral host that eventually mitigate coral bleaching and mortality. American Association for the Advancement of Science 2021-08-13 /pmc/articles/PMC8363143/ /pubmed/34389536 http://dx.doi.org/10.1126/sciadv.abg3088 Text en Copyright © 2021 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC). https://creativecommons.org/licenses/by-nc/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license (https://creativecommons.org/licenses/by-nc/4.0/) , which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.
spellingShingle Research Articles
Santoro, Erika P.
Borges, Ricardo M.
Espinoza, Josh L.
Freire, Marcelo
Messias, Camila S. M. A.
Villela, Helena D. M.
Pereira, Leandro M.
Vilela, Caren L. S.
Rosado, João G.
Cardoso, Pedro M.
Rosado, Phillipe M.
Assis, Juliana M.
Duarte, Gustavo A. S.
Perna, Gabriela
Rosado, Alexandre S.
Macrae, Andrew
Dupont, Christopher L.
Nelson, Karen E.
Sweet, Michael J.
Voolstra, Christian R.
Peixoto, Raquel S.
Coral microbiome manipulation elicits metabolic and genetic restructuring to mitigate heat stress and evade mortality
title Coral microbiome manipulation elicits metabolic and genetic restructuring to mitigate heat stress and evade mortality
title_full Coral microbiome manipulation elicits metabolic and genetic restructuring to mitigate heat stress and evade mortality
title_fullStr Coral microbiome manipulation elicits metabolic and genetic restructuring to mitigate heat stress and evade mortality
title_full_unstemmed Coral microbiome manipulation elicits metabolic and genetic restructuring to mitigate heat stress and evade mortality
title_short Coral microbiome manipulation elicits metabolic and genetic restructuring to mitigate heat stress and evade mortality
title_sort coral microbiome manipulation elicits metabolic and genetic restructuring to mitigate heat stress and evade mortality
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8363143/
https://www.ncbi.nlm.nih.gov/pubmed/34389536
http://dx.doi.org/10.1126/sciadv.abg3088
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