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Different disease inoculations cause common responses of the host immune system and prokaryotic component of the microbiome in Acropora palmata

Reef-building corals contain a complex consortium of organisms, a holobiont, which responds dynamically to disease, making pathogen identification difficult. While coral transcriptomics and microbiome communities have previously been characterized, similarities and differences in their responses to...

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Autores principales: Young, Benjamin D., Rosales, Stephanie M., Enochs, Ian C., Kolodziej, Graham, Formel, Nathan, Moura, Amelia, D’Alonso, Gabrielle L., Traylor-Knowles, Nikki
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10212133/
https://www.ncbi.nlm.nih.gov/pubmed/37228141
http://dx.doi.org/10.1371/journal.pone.0286293
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author Young, Benjamin D.
Rosales, Stephanie M.
Enochs, Ian C.
Kolodziej, Graham
Formel, Nathan
Moura, Amelia
D’Alonso, Gabrielle L.
Traylor-Knowles, Nikki
author_facet Young, Benjamin D.
Rosales, Stephanie M.
Enochs, Ian C.
Kolodziej, Graham
Formel, Nathan
Moura, Amelia
D’Alonso, Gabrielle L.
Traylor-Knowles, Nikki
author_sort Young, Benjamin D.
collection PubMed
description Reef-building corals contain a complex consortium of organisms, a holobiont, which responds dynamically to disease, making pathogen identification difficult. While coral transcriptomics and microbiome communities have previously been characterized, similarities and differences in their responses to different pathogenic sources has not yet been assessed. In this study, we inoculated four genets of the Caribbean branching coral Acropora palmata with a known coral pathogen (Serratia marcescens) and white band disease. We then characterized the coral’s transcriptomic and prokaryotic microbiomes’ (prokaryiome) responses to the disease inoculations, as well as how these responses were affected by a short-term heat stress prior to disease inoculation. We found strong commonality in both the transcriptomic and prokaryiomes responses, regardless of disease inoculation. Differences, however, were observed between inoculated corals that either remained healthy or developed active disease signs. Transcriptomic co-expression analysis identified that corals inoculated with disease increased gene expression of immune, wound healing, and fatty acid metabolic processes. Co-abundance analysis of the prokaryiome identified sets of both healthy-and-disease-state bacteria, while co-expression analysis of the prokaryiomes’ inferred metagenomic function revealed infected corals’ prokaryiomes shifted from free-living to biofilm states, as well as increasing metabolic processes. The short-term heat stress did not increase disease susceptibility for any of the four genets with any of the disease inoculations, and there was only a weak effect captured in the coral hosts’ transcriptomic and prokaryiomes response. Genet identity, however, was a major driver of the transcriptomic variance, primarily due to differences in baseline immune gene expression. Despite genotypic differences in baseline gene expression, we have identified a common response for components of the coral holobiont to different disease inoculations. This work has identified genes and prokaryiome members that can be focused on for future coral disease work, specifically, putative disease diagnostic tools.
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spelling pubmed-102121332023-05-26 Different disease inoculations cause common responses of the host immune system and prokaryotic component of the microbiome in Acropora palmata Young, Benjamin D. Rosales, Stephanie M. Enochs, Ian C. Kolodziej, Graham Formel, Nathan Moura, Amelia D’Alonso, Gabrielle L. Traylor-Knowles, Nikki PLoS One Research Article Reef-building corals contain a complex consortium of organisms, a holobiont, which responds dynamically to disease, making pathogen identification difficult. While coral transcriptomics and microbiome communities have previously been characterized, similarities and differences in their responses to different pathogenic sources has not yet been assessed. In this study, we inoculated four genets of the Caribbean branching coral Acropora palmata with a known coral pathogen (Serratia marcescens) and white band disease. We then characterized the coral’s transcriptomic and prokaryotic microbiomes’ (prokaryiome) responses to the disease inoculations, as well as how these responses were affected by a short-term heat stress prior to disease inoculation. We found strong commonality in both the transcriptomic and prokaryiomes responses, regardless of disease inoculation. Differences, however, were observed between inoculated corals that either remained healthy or developed active disease signs. Transcriptomic co-expression analysis identified that corals inoculated with disease increased gene expression of immune, wound healing, and fatty acid metabolic processes. Co-abundance analysis of the prokaryiome identified sets of both healthy-and-disease-state bacteria, while co-expression analysis of the prokaryiomes’ inferred metagenomic function revealed infected corals’ prokaryiomes shifted from free-living to biofilm states, as well as increasing metabolic processes. The short-term heat stress did not increase disease susceptibility for any of the four genets with any of the disease inoculations, and there was only a weak effect captured in the coral hosts’ transcriptomic and prokaryiomes response. Genet identity, however, was a major driver of the transcriptomic variance, primarily due to differences in baseline immune gene expression. Despite genotypic differences in baseline gene expression, we have identified a common response for components of the coral holobiont to different disease inoculations. This work has identified genes and prokaryiome members that can be focused on for future coral disease work, specifically, putative disease diagnostic tools. Public Library of Science 2023-05-25 /pmc/articles/PMC10212133/ /pubmed/37228141 http://dx.doi.org/10.1371/journal.pone.0286293 Text en https://creativecommons.org/publicdomain/zero/1.0/This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 (https://creativecommons.org/publicdomain/zero/1.0/) public domain dedication.
spellingShingle Research Article
Young, Benjamin D.
Rosales, Stephanie M.
Enochs, Ian C.
Kolodziej, Graham
Formel, Nathan
Moura, Amelia
D’Alonso, Gabrielle L.
Traylor-Knowles, Nikki
Different disease inoculations cause common responses of the host immune system and prokaryotic component of the microbiome in Acropora palmata
title Different disease inoculations cause common responses of the host immune system and prokaryotic component of the microbiome in Acropora palmata
title_full Different disease inoculations cause common responses of the host immune system and prokaryotic component of the microbiome in Acropora palmata
title_fullStr Different disease inoculations cause common responses of the host immune system and prokaryotic component of the microbiome in Acropora palmata
title_full_unstemmed Different disease inoculations cause common responses of the host immune system and prokaryotic component of the microbiome in Acropora palmata
title_short Different disease inoculations cause common responses of the host immune system and prokaryotic component of the microbiome in Acropora palmata
title_sort different disease inoculations cause common responses of the host immune system and prokaryotic component of the microbiome in acropora palmata
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10212133/
https://www.ncbi.nlm.nih.gov/pubmed/37228141
http://dx.doi.org/10.1371/journal.pone.0286293
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