Document Type

Article

Publication Date

2021

DOI

10.1073/pnas.2023298118

Publication Title

Proceedings of the National Academy of Sciences of the United States of America

Volume

118

Issue

19

Pages

e2023298118 (1-9)

Abstract

Corals from the northern Red Sea and Gulf of Aqaba exhibit extreme thermal tolerance. To examine the underlying gene expression dynamics, we exposed Stylophora pistillata from the Gulf of Aqaba to short-term (hours) and long-term (weeks) heat stress with peak seawater temperatures ranging from their maximum monthly mean of 27 °C (baseline) to 29.5 °C, 32 °C, and 34.5 °C. Corals were sampled at the end of the heat stress as well as after a recovery period at baseline temperature. Changes in coral host and symbiotic algal gene expression were determined via RNA-sequencing (RNA-Seq). Shifts in coral microbiome composition were detected by complementary DNA (cDNA)-based 16S ribosomal RNA (rRNA) gene sequencing. In all experiments up to 32 °C, RNA-Seq revealed fast and pervasive changes in gene expression, primarily in the coral host, followed by a return to baseline gene expression for the majority of coral (>94%) and algal (>71%) genes during recovery. At 34.5 °C, large differences in gene expression were observed with minimal recovery, high coral mortality, and a microbiome dominated by opportunistic bacteria (including Vibrio species), indicating that a lethal temperature threshold had been crossed. Our results show that the S. pistillata holobiont can mount a rapid and pervasive gene expression response contingent on the amplitude and duration of the thermal stress. We propose that the transcriptomic resilience and transcriptomic acclimation observed are key to the extraordinary thermal tolerance of this holobiont and, by inference, of other northern Red Sea coral holobionts, up to seawater temperatures of at least 32 °C, that is, 5 °C above their current maximum monthly mean.

Rights

This open access article is distributed under a Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

Data Availability

Article states: "The raw RNA-Seq and bacterial 16S rRNA amplicon sequencing data are available at the National Center for Biotechnology Information (NCBI) under BioProject PRJNA674053. Data (DEGs, GOs, ASVs) can be found in supplementary datasets (Datasets S2, S3, S5, and S6), and scripts for gene expression abundance and gene expression analysis can be accessed at GitHub, https://github.com/rsavary/Fast-and-pervasive-transcriptomic-resilience. Bacterial community scripts can be accessed at GitHub, https://github.com/ajcardenasb/RSS_CBASS_16S."

Original Publication Citation

Savary, R., Barshis, D. J., Voolstra, C. R., Cárdenas, A., Evensen, N. R., Banc-Prandi, G., Fine, M., & Meibom, A. (2021). Fast and pervasive transcriptomic resilience and acclimation of extremely heat-tolerant coral holobionts from the northern Red Sea. Proceedings of the National Academy of Sciences of the United States of America, 118(19), 1-9, Article e2023298118. https://doi.org/10.1073/pnas.2023298118

ORCID

0000-0003-1510-8375 (Barshis)

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