Thermal Shock Induces Host Proteostasis Disruption and Endoplasmic Reticulum Stress in the Model Symbiotic Cnidarian Aiptasia

Coral bleaching has devastating effects on coral survival and reef ecosystem function, but many of the fundamental cellular effects of thermal stress on cnidarian physiology are unclear. We used label-free liquid chromatography–tandem mass spectrometry to compare the effects of rapidly (33.5 °C, 24 h) and gradually (30 and 33.5 °C, 12 days) elevated temperatures on the proteome of the model symbiotic anemone Aiptasia. We identified 2133 proteins in Aiptasia, 136 of which were differentially abundant between treatments. Thermal shock, but not acclimation, resulted in significant abundance changes in 104 proteins, including those involved in protein folding and synthesis, redox homeostasis, and central metabolism. Nineteen abundant structural proteins showed particularly reduced abundance, demonstrating proteostasis disruption and potential protein synthesis inhibition. Heat shock induced antioxidant mechanisms and proteins involved in stabilizing nascent proteins, preventing protein aggregation and degrading damaged proteins, which is indicative of endoplasmic reticulum stress. Host proteostasis disruption occurred before either bleaching or symbiont photoinhibition was detected, suggesting host-derived reactive oxygen species production as the proximate cause of thermal damage. The pronounced abundance changes in endoplasmic reticulum proteins associated with proteostasis and protein turnover indicate that these processes are essential in the cellular response of symbiotic cnidarians to severe thermal stress.

珊瑚白化对珊瑚存活与珊瑚礁生态系统功能具有毁灭性影响，但目前学界对于热胁迫对刺胞动物（Cnidarian）生理的核心细胞效应仍不甚明晰。本研究采用无标记液相色谱-串联质谱（label-free liquid chromatography–tandem mass spectrometry）技术，对比了快速升温（33.5℃，持续24小时）与渐进式升温（30℃、33.5℃，持续12天）两种温度胁迫模式对模式共生海葵艾氏海葵（Aiptasia）蛋白质组的影响。本研究在艾氏海葵中共鉴定出2133种蛋白质，其中136种在不同处理组间存在丰度差异。热休克处理（而非温度驯化）可导致104种蛋白质的丰度发生显著变化，这些蛋白质涉及蛋白质折叠与合成、氧化还原稳态以及中枢代谢等生物学过程。19种高丰度结构蛋白的丰度出现显著下调，这表明蛋白质稳态（proteostasis）遭到破坏，且蛋白质合成过程可能受到抑制。热休克会诱导抗氧化机制以及参与稳定新生蛋白质、防止蛋白质聚集并降解受损蛋白质的相关蛋白表达，该现象提示存在内质网应激（endoplasmic reticulum stress）。宿主蛋白质稳态破坏发生在珊瑚白化或共生体光抑制被检测到之前，这表明宿主来源的活性氧（reactive oxygen species）生成是热损伤的直接诱因。与蛋白质稳态及蛋白质周转相关的内质网蛋白质丰度发生显著变化，这表明上述过程在共生刺胞动物应对剧烈热胁迫的细胞应答中发挥着不可或缺的作用。