Gradual ocean warming and marine heatwaves represent major threats for marine organisms already facing other anthropogenic-derived hazards, such as chemical contamination in coastal areas. In this study, the combined effects of thermal stress and exposure to gadolinium (Gd), a metal used as a contrasting agent in medical imaging which enters the aquatic environment, were investigated in the embryos and larvae of the sea urchin Paracentrotus lividus. Embryos were exposed to six treatments of three temperatures (18 °C, 21 °C, 24 °C) and two Gd concentrations (control: 0 μM; treated: 20 μM). With respect to developmental progression, increased temperature accelerated development and achievement of the larval stage, while Gd-exposed embryos at the control temperature (18 °C) showed a general delay in development at 24 h post-fertilization (hpf), and a stunting effect and impaired skeleton growth at 48 hpf. Elevated temperatures at near-future projections (+3 °C, 21 °C) reduced the negative effects of Gd on development with a lower percentage of abnormality and improved skeleton growth. Combined extreme warming at present-day marine heatwave conditions (+6 °C, 24 °C) and Gd treatment resulted in a lower proportion of embryos reaching the advanced larval stages compared to the 21 °C + Gd. At the molecular level, western blot analysis showed that Gd was the main driver for the induction of heat shock protein (HSP60, HSP70) expression. At 48 hpf, temperature increase was the main driver for activation of additional cellular stress response strategies such as autophagy and apoptosis. Combined treatments showed the induction of HSP60 at 24 hpf and autophagic and apoptotic processes at 48 hpf. Treatments having low levels of HSPs expression showed high levels of apoptosis, and vice versa, clearly demonstrating the antagonistic effects of HSPs expression and apoptosis. Detection of fragmented DNA in apoptotic nuclei showed selective apoptosis, likely in extremely damaged cells. Our results indicate that the negative effects of Gd-exposure on P. lividus larval development and biomineralization will be mitigated by a near-future ocean warming, up to a thermotolerance threshold when negative synergistic effects were evident. Our data highlight the use of biomarkers as sensitive tools to detect environmental impacts as well as the need for a better understanding of the interactions between the multiple stressors faced by marine species in coastal environments.

海洋逐渐变暖和海洋热浪对已经面临其他人为危害（例如沿海地区的化学污染）的海洋生物构成了主要威胁。在这项研究中，研究了热应激和钆（Gd）暴露的综合影响，钆（Gd）是一种进入水生环境的医学成像造影剂金属，在海胆Paracentrotus lividus的胚胎和幼虫中进行了研究。将胚胎暴露于三种温度（18°C、21°C、24°C）和两种 Gd 浓度（对照：0 μM；处理：20 μM）的六次处理。就发育进程而言，温度升高加速了幼虫阶段的发育和实现，而在对照温度（18°C）下暴露于钆的胚胎在受精后（hpf）24小时（hpf）时表现出普遍的发育延迟，并且发育迟缓48 hpf 时骨骼生长受损。近期预测的升高温度（+3°C、21°C）减少了 Gd 对发育的负面影响，降低了异常百分比并改善了骨骼生长。与 21 °C + Gd 相比，当今海洋热浪条件下的极端变暖（+6 °C、24 °C）和 Gd 处理导致达到晚期幼虫阶段的胚胎比例较低。在分子水平上，蛋白质印迹分析表明Gd是诱导热休克蛋白（HSP60、HSP70）表达的主要驱动力。 48 hpf 时，温度升高是激活其他细胞应激反应策略（例如自噬和凋亡）的主要驱动力。联合治疗显示在 24 hpf 时诱导 HSP60，并在 48 hpf 时诱导自噬和凋亡过程。 HSPs表达水平低的处理显示高水平的细胞凋亡，反之亦然，清楚地证明了HSPs表达和细胞凋亡的拮抗作用。对凋亡细胞核中 DNA 片段的检测显示选择性凋亡，很可能发生在极度受损的细胞中。我们的研究结果表明，暴露于钆对青紫虾幼体发育和生物矿化的负面影响将通过不久的将来海洋变暖而减轻，当负面协同效应明显时达到耐热阈值。我们的数据强调了使用生物标志物作为检测环境影响的敏感工具，以及需要更好地了解沿海环境中海洋物种面临的多种压力源之间的相互作用。