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

Autor: Nicolas R. Evensen, Romain Savary, Anny Cárdenas, Guilhem Banc-Prandi, Anders Meibom, Daniel J. Barshis, Maoz Fine, Christian R. Voolstra
Jazyk: angličtina
Rok vydání: 2021
Předmět:
0301 basic medicine
Hot Temperature
Time Factors
Acclimatization
Coral
microbiome
Stylophora pistillata
heat stress
RNA
Ribosomal
16S

RNA-Seq
Indian Ocean
Multidisciplinary
Ecology
biology
Coral Reefs
Microbiota
coral bleaching
Biological Sciences
Anthozoa
reveal
Holobiont
climate-change
ecosystems
metaorganism
geographic locations
Coral bleaching
030106 microbiology
Zoology
thermal-stress
diversity
03 medical and health sciences
Algae
ddc:570
gene expression profiling
Animals
bacterial
natural sciences
coral bleaching
microbiome
heat stress
gene expression profiling
metaorganism

14. Life underwater
Microbiome
Symbiosis
stylophora-pistillata
Bacteria
fungi
biology.organism_classification
gene-expression
030104 developmental biology
13. Climate action
Seawater
genomes
Transcriptome
Heat-Shock Response
Zdroj: Proceedings of the National Academy of Sciences of the United States of America
Popis: Significance Coral reefs are in catastrophic decline worldwide, in part due to increasingly warm surface waters that cause mass coral bleaching and mortality. However, corals in the northern Red Sea and Gulf of Aqaba have shown no sign of bleaching, despite local seawater temperature rising faster than the global average. We show that the exceptional heat tolerance of the common symbiotic reef-building coral Stylophora pistillata from the Gulf of Aqaba is based on a rapid gene expression response and recovery pattern when exposed to heat stress up to 32 °C. Such temperatures are not anticipated to occur in the region within this century, giving real hope for the preservation of at least one major coral reef ecosystem for future generations.
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.
Databáze: OpenAIRE