Fast and pervasive transcriptomic resilience and acclimation of extremely heat-tolerant coral holobionts from the northern Red Sea

Romain Savary, Daniel J. Barshis, Christian R. Voolstra, Anny Cárdenas, Nicolas R. Evensen, Guilhem Banc-Prandi, Maoz Fine, Anders Meibom

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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.

Original languageEnglish
Article numbere2023298118
JournalProceedings of the National Academy of Sciences of the United States of America
Volume118
Issue number19
DOIs
StatePublished - 11 May 2021

Bibliographical note

Publisher Copyright:
© 2021 National Academy of Sciences. All rights reserved.

Funding

R.S. was supported by a fellowship from the AXA foundation for "Ocean, marine biodiversity and conflict prevention" and funding provided by Ecole Polytechnique Fédérale de Lausanne. Experimental work was supported by US-Israeli Bi-National Science Foundation Grant #2016403 (D.J.B. and M.F.) and US National Science Foundation Grant #1833201 (D.J.B.). C.R.V. was supported through the Deutsche Forschungsgemeinschaft (German Research Foundation) Project Number 433042944. A.M. was supported by Swiss National Science Foundation through Grant Number 200021-179092. Corals used in this study were collected under permit 2019/42143 from Israel's Nature and Parks Authority. ACKNOWLEDGMENTS. R.S. was supported by a fellowship from the AXA foundation for “Ocean, marine biodiversity and conflict prevention” and funding provided by Ecole Polytechnique Fédérale de Lausanne. Experimental work was supported by US-Israeli Bi-National Science Foundation Grant #2016403 (D.J.B. and M.F.) and US National Science Foundation Grant #1833201 (D.J.B.). C.R.V. was supported through the Deutsche Forschungsgemeinschaft (German Research Foundation) Project Number 433042944. A.M. was supported by Swiss National Science Foundation through Grant Number 200021_179092. Corals used in this study were collected under permit 2019/42143 from Israel’s Nature and Parks Authority.

FundersFunder number
AXA foundation for "Ocean, marine biodiversity and conflict prevention
AXA foundation for “Ocean, marine biodiversity and conflict prevention
Israel's Nature and Parks Authority
US-Israeli Bi-National Science Foundation2016403
National Science Foundation1833201
Deutsche Forschungsgemeinschaft433042944
École Polytechnique Fédérale de Lausanne
Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung200021_179092

    Keywords

    • Coral bleaching
    • Gene expression profiling
    • Heat stress
    • Metaorganism
    • Microbiome

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