Elevated Temperature As the Dominant Stressor on the Harmful Algal Bloom-Causing Dinoflagellate Prorocentrum Obtusidens in a Future Ocean Scenario

Marine dinoflagellates are increasingly affected by ongoing global climate changes. While understanding of their physiological and molecular responses to individual stressors anticipated in the future ocean has improved, their responses to multiple concurrent stressors remain poorly understood. Here, we investigated the individual and combined effects of elevated temperature (26 °C relative to 22 °C), increased pCO2 (1000 μatm relative to 400 μatm), and high nitrogen: phosphorus ratio (180:1 relative to 40:1) on a harmful algal bloom-causing dinoflagellate Prorocentrum obtusidens under short-term (28 days) exposure. Elevated temperature was the most dominant stressor affecting P. obtusidens at physiological and transcriptomic levels. It significantly increased cell growth rate and maximum photosynthetic efficiency (Fv/Fm), but reduced chlorophyll a, particulate organic carbon, particulate organic nitrogen, and particulate organic phosphorus. Elevated temperature also interacted with other stressors to produce synergistic positive effects on cell growth and Fv/Fm. Transcriptomic analysis indicated that elevated temperature promoted energy production by enhancing glycolysis, tricarboxylic acid cycle, and nitrogen and carbon assimilation, which supported rapid cell growth but reduced material storage. Increased pCO2 enhanced the expression of genes involved in ionic acid-base regulation and oxidative stress resistance, whereas a high N:P ratio inhibited photosynthesis, compromising cell viability, although the effect was alleviated by elevated temperature. The combined effect of these multiple stressors resulted in increased energy metabolism and up-regulation of material-synthesis pathways compared to the effect caused by elevated temperature alone. Our results underscore ocean warming as the predominant stressor for dinoflagellates and highlight the complex, synergistic effects of multi-stressors on dinoflagellates.