Multi-omic characterization of the thermal stress phenome in the stony coral Montipora capitata

Background Corals, which form the foundation of biodiverse reef ecosystems, are under threat from warming oceans. Reefs provide essential ecological services, including food, income from tourism, nutrient cycling, waste removal, and the absorption of wave energy to mitigate erosion. Here, we studied...

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Autores principales:	Amanda Williams, Jananan S. Pathmanathan, Timothy G. Stephens, Xiaoyang Su, Eric N. Chiles, Dennis Conetta, Hollie M. Putnam, Debashish Bhattacharya
Formato:	article
Lenguaje:	EN
Publicado:	PeerJ Inc. 2021
Materias:	Montipora capitata Metabolomics Stress biology Stony coral Hawaii Multi-omics analysis Medicine R
Acceso en línea:	https://doaj.org/article/eb14df68adf94171b5849f4cb3c2d6cc
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spelling	oai:doaj.org-article:eb14df68adf94171b5849f4cb3c2d6cc2021-11-12T15:05:10ZMulti-omic characterization of the thermal stress phenome in the stony coral Montipora capitata10.7717/peerj.123352167-8359https://doaj.org/article/eb14df68adf94171b5849f4cb3c2d6cc2021-11-01T00:00:00Zhttps://peerj.com/articles/12335.pdfhttps://peerj.com/articles/12335/https://doaj.org/toc/2167-8359Background Corals, which form the foundation of biodiverse reef ecosystems, are under threat from warming oceans. Reefs provide essential ecological services, including food, income from tourism, nutrient cycling, waste removal, and the absorption of wave energy to mitigate erosion. Here, we studied the coral thermal stress response using network methods to analyze transcriptomic and polar metabolomic data generated from the Hawaiian rice coral Montipora capitata. Coral nubbins were exposed to ambient or thermal stress conditions over a 5-week period, coinciding with a mass spawning event of this species. The major goal of our study was to expand the inventory of thermal stress-related genes and metabolites present in M. capitata and to study gene-metabolite interactions. These interactions provide the foundation for functional or genetic analysis of key coral genes as well as provide potentially diagnostic markers of pre-bleaching stress. A secondary goal of our study was to analyze the accumulation of sex hormones prior to and during mass spawning to understand how thermal stress may impact reproductive success in M. capitata. Methods M. capitata was exposed to thermal stress during its spawning cycle over the course of 5 weeks, during which time transcriptomic and polar metabolomic data were collected. We analyzed these data streams individually, and then integrated both data sets using MAGI (Metabolite Annotation and Gene Integration) to investigate molecular transitions and biochemical reactions. Results Our results reveal the complexity of the thermal stress phenome in M. capitata, which includes many genes involved in redox regulation, biomineralization, and reproduction. The size and number of modules in the gene co-expression networks expanded from the initial stress response to the onset of bleaching. The later stages involved the suppression of metabolite transport by the coral host, including a variety of sodium-coupled transporters and a putative ammonium transporter, possibly as a response to reduction in algal productivity. The gene-metabolite integration data suggest that thermal treatment results in the activation of animal redox stress pathways involved in quenching molecular oxygen to prevent an overabundance of reactive oxygen species. Lastly, evidence that thermal stress affects reproductive activity was provided by the downregulation of CYP-like genes and the irregular production of sex hormones during the mass spawning cycle. Overall, redox regulation and metabolite transport are key components of the coral animal thermal stress phenome. Mass spawning was highly attenuated under thermal stress, suggesting that global climate change may negatively impact reproductive behavior in this species.Amanda WilliamsJananan S. PathmanathanTimothy G. StephensXiaoyang SuEric N. ChilesDennis ConettaHollie M. PutnamDebashish BhattacharyaPeerJ Inc.articleMontipora capitataMetabolomicsStress biologyStony coralHawaiiMulti-omics analysisMedicineRENPeerJ, Vol 9, p e12335 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Montipora capitata Metabolomics Stress biology Stony coral Hawaii Multi-omics analysis Medicine R
spellingShingle	Montipora capitata Metabolomics Stress biology Stony coral Hawaii Multi-omics analysis Medicine R Amanda Williams Jananan S. Pathmanathan Timothy G. Stephens Xiaoyang Su Eric N. Chiles Dennis Conetta Hollie M. Putnam Debashish Bhattacharya Multi-omic characterization of the thermal stress phenome in the stony coral Montipora capitata
description	Background Corals, which form the foundation of biodiverse reef ecosystems, are under threat from warming oceans. Reefs provide essential ecological services, including food, income from tourism, nutrient cycling, waste removal, and the absorption of wave energy to mitigate erosion. Here, we studied the coral thermal stress response using network methods to analyze transcriptomic and polar metabolomic data generated from the Hawaiian rice coral Montipora capitata. Coral nubbins were exposed to ambient or thermal stress conditions over a 5-week period, coinciding with a mass spawning event of this species. The major goal of our study was to expand the inventory of thermal stress-related genes and metabolites present in M. capitata and to study gene-metabolite interactions. These interactions provide the foundation for functional or genetic analysis of key coral genes as well as provide potentially diagnostic markers of pre-bleaching stress. A secondary goal of our study was to analyze the accumulation of sex hormones prior to and during mass spawning to understand how thermal stress may impact reproductive success in M. capitata. Methods M. capitata was exposed to thermal stress during its spawning cycle over the course of 5 weeks, during which time transcriptomic and polar metabolomic data were collected. We analyzed these data streams individually, and then integrated both data sets using MAGI (Metabolite Annotation and Gene Integration) to investigate molecular transitions and biochemical reactions. Results Our results reveal the complexity of the thermal stress phenome in M. capitata, which includes many genes involved in redox regulation, biomineralization, and reproduction. The size and number of modules in the gene co-expression networks expanded from the initial stress response to the onset of bleaching. The later stages involved the suppression of metabolite transport by the coral host, including a variety of sodium-coupled transporters and a putative ammonium transporter, possibly as a response to reduction in algal productivity. The gene-metabolite integration data suggest that thermal treatment results in the activation of animal redox stress pathways involved in quenching molecular oxygen to prevent an overabundance of reactive oxygen species. Lastly, evidence that thermal stress affects reproductive activity was provided by the downregulation of CYP-like genes and the irregular production of sex hormones during the mass spawning cycle. Overall, redox regulation and metabolite transport are key components of the coral animal thermal stress phenome. Mass spawning was highly attenuated under thermal stress, suggesting that global climate change may negatively impact reproductive behavior in this species.
format	article
author	Amanda Williams Jananan S. Pathmanathan Timothy G. Stephens Xiaoyang Su Eric N. Chiles Dennis Conetta Hollie M. Putnam Debashish Bhattacharya
author_facet	Amanda Williams Jananan S. Pathmanathan Timothy G. Stephens Xiaoyang Su Eric N. Chiles Dennis Conetta Hollie M. Putnam Debashish Bhattacharya
author_sort	Amanda Williams
title	Multi-omic characterization of the thermal stress phenome in the stony coral Montipora capitata
title_short	Multi-omic characterization of the thermal stress phenome in the stony coral Montipora capitata
title_full	Multi-omic characterization of the thermal stress phenome in the stony coral Montipora capitata
title_fullStr	Multi-omic characterization of the thermal stress phenome in the stony coral Montipora capitata
title_full_unstemmed	Multi-omic characterization of the thermal stress phenome in the stony coral Montipora capitata
title_sort	multi-omic characterization of the thermal stress phenome in the stony coral montipora capitata
publisher	PeerJ Inc.
publishDate	2021
url	https://doaj.org/article/eb14df68adf94171b5849f4cb3c2d6cc
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Multi-omic characterization of the thermal stress phenome in the stony coral Montipora capitata

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