Document Type

Article

Publication Date

2021

DOI

10.1111/mec.16064

Publication Title

Molecular Ecology

Volume

00

Pages

1-15

Abstract

Corals from the northern Red Sea, in particular the Gulf of Aqaba (GoA), have exceptionally high bleaching thresholds approaching >5℃ above their maximum monthly mean (MMM) temperatures. These elevated thresholds are thought to be due to historical selection, as corals passed through the warmer Southern Red Sea during recolonization from the Arabian Sea. To test this hypothesis, we determined thermal tolerance thresholds of GoA versus central Red Sea (CRS) Stylophora pistillata corals using multi-temperature acute thermal stress assays to determine thermal thresholds. Relative thermal thresholds of GoA and CRS corals were indeed similar and exceptionally high (~7℃ above MMM). However, absolute thermal thresholds of CRS corals were on average 3℃ above those of GoA corals. To explore the molecular underpinnings, we determined gene expression and microbiome response of the coral holobiont. Transcriptomic responses differed markedly, with a strong response to the thermal stress in GoA corals and their symbiotic algae versus a remarkably muted response in CRS colonies. Concomitant to this, coral and algal genes showed temperature-induced expression in GoA corals, while exhibiting fixed high expression (front-loading) in CRS corals. Bacterial community composition of GoA corals changed dramatically under heat stress, whereas CRS corals displayed stable assemblages. We interpret the response of GoA corals as that of a resilient population approaching a tipping point in contrast to a pattern of consistently elevated thermal resistance in CRS corals that cannot further attune. Such response differences suggest distinct thermal tolerance mechanisms that may affect the response of coral populations to ocean warming.

Rights

© 2021 The Authors

Published under an Attribution-NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0) Creative Commons License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.

Data Availability

Article states: "RNA-Seq, ITS2, 16S fastq sequencing data files have been made available at NCBI under BioProject PRJNA681108 https://www.ncbi.nlm.nih.gov/bioproject/PRJNA681108. Scripts for PAM data analysis and plotting, coral host and microalgal gene expression analyses, Symbiodiniaceae and bacterial community analyses and plotting, and coral host SNP analyses can be accessed at https://github.com/reefgenomics/CBASS84. Pictures of colony fragments after short-term thermal stress are available as Supporting Information (Data S1). Gene expression estimates (TPM) for 49,109 Symbiodinium microadriaticum and 25,769 Stylophora pistillata genes, PERMANOVA statistics on pairwise comparisons between temperatures & sites, and differentially expressed genes (DESeq) for S. pistillata and S. microadriaticum are available as Supporting Information (Data S2). Overview of differentially expressed genes, front- and back-loaded genes, GO enrichments, and heat stress response genes for S. pistillata and S. microadriaticum are available as supplementary data (Data S3). Symbiodiniaceae ITS2 type profiles, ITS2 sequences abundance, and ITS2 sequences are available as Supporting Information (Data S4). Bacterial 16S sequence statistics, taxa (OTUs) abundance table, and statistical analyses are available as Supporting Information (Data S5)."

Supporting material is available online at: https://doi.org/10.1111/mec.16064

Original Publication Citation

Voolstra, C. R., Valenzuela, J. J., Turkarslan, S., ... Fine, M., Frias-Torres, S., & Barshis, D. J. (2021). Contrasting heat stress response patterns of coral holobionts across the Red Sea suggest distinct mechanisms of thermal tolerance. Molecular Ecology, 00, 1-15. https://doi.org/10.1111/mec.16064

ORCID

0000-0003-1510-8375 (Barshis)

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