Comparative Metabolomics Approach Detects Stress-Specific Responses during Coral Bleaching in Soft Corals

Chronic exposure to ocean acidification and elevated sea-surface temperatures pose significant stress to marine ecosystems. This in turn necessitates costly acclimation responses in corals in both the symbiont and host, with a reorganization of cell metabolism and structure. A large-scale untargeted metabolomics approach comprising gas chromatography mass spectrometry (GC–MS) and ultraperformance liquid chromatography coupled to high resolution mass spectrometry (UPLC–MS) was applied to profile the metabolite composition of the soft coral Sarcophyton ehrenbergi and its dinoflagellate symbiont. Metabolite profiling compared ambient conditions with response to simulated climate change stressors and with the sister species, S. glaucum. Among ∼300 monitored metabolites, 13 metabolites were modulated. Incubation experiments providing four selected upregulated metabolites (alanine, GABA, nicotinic acid, and proline) in the culturing water failed to subside the bleaching response at temperature-induced stress, despite their known ability to mitigate heat stress in plants or animals. Thus, the results hint to metabolite accumulation (marker) during heat stress. This study provides the first detailed map of metabolic pathways transition in corals in response to different environmental stresses, accounting for the superior thermal tolerance of S. ehrenbergi versus S. glaucum, which can ultimately help maintain a viable symbiosis and mitigate against coral bleaching.

长期暴露于海洋酸化与海表温度升高会对海洋生态系统造成显著胁迫。这进而促使珊瑚在共生体与宿主中产生高成本的适应响应，伴随细胞代谢与结构的重组。本研究采用涵盖气相色谱-质谱联用（gas chromatography mass spectrometry, GC-MS）与超高效液相色谱-高分辨质谱联用（ultraperformance liquid chromatography coupled to high resolution mass spectrometry, UPLC-MS）的大规模非靶向代谢组学（untargeted metabolomics）方法，对软珊瑚埃伦贝格肉芝软珊瑚（Sarcophyton ehrenbergi）及其共生的甲藻共生体的代谢物组成进行表征。代谢物表征实验将环境对照条件、模拟气候变化胁迫下的响应，以及姊妹物种灰肉芝软珊瑚（S. glaucum）的情况进行了对比。在约300种被监测的代谢物中，有13种发生了显著调控。尽管已知四种筛选出的上调代谢物——丙氨酸（alanine）、γ-氨基丁酸（GABA）、烟酸（nicotinic acid）与脯氨酸（proline）——能够缓解动植物的热胁迫，但在培养液中添加这四种代谢物的培养实验并未缓解温度胁迫诱导的珊瑚白化响应。因此，研究结果提示热胁迫期间存在代谢物积累（可作为胁迫标记物）。本研究首次详细绘制了珊瑚响应不同环境胁迫时的代谢通路转变图谱，解释了埃伦贝格肉芝软珊瑚相较于灰肉芝软珊瑚具有更强耐热性的原因，该成果最终可助力维持健康的珊瑚共生关系并缓解珊瑚白化现象。