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.

来自红海北部和亚喀巴湾的珊瑚表现出极高的耐热性。为了检查潜在的基因表达动态，我们将来自亚喀巴湾的Stylophora pistillata暴露于短期（数小时）和长期（数周）热应激，峰值海水温度范围从最高月平均值 27 °C（基线）至 29.5°C、32°C 和 34.5°C。在热应激结束时以及基线温度恢复期后对珊瑚进行取样。通过 RNA 测序 (RNA-Seq) 确定珊瑚宿主和共生藻类基因表达的变化。通过基于互补 DNA (cDNA) 的 16S 核糖体 RNA (rRNA) 基因测序检测珊瑚微生物组组成的变化。在高达 32 °C 的所有实验中，RNA-Seq 显示基因表达发生快速而普遍的变化，主要是在珊瑚宿主中，随后大多数珊瑚 (>94%) 和藻类 (>71) 的基因表达恢复到基线%) 恢复期间的基因。在 34.5 °C 时，观察到基因表达存在巨大差异，恢复率极低，珊瑚死亡率较高，微生物组以机会性细菌（包括弧菌物种）为主，这表明已超过致命温度阈值。我们的结果表明， S. pistillata holobiont 可以根据热应激的幅度和持续时间产生快速而普遍的基因表达反应。我们认为，观察到的转录组恢复力和转录组适应能力是这种全生物体以及由此推断的其他红海北部珊瑚全生物体非凡耐热性的关键，最高海水温度至少为 32 °C，即 5 °C高于当前最大月平均值。