Effects of temperature on physiology, transcription, and toxin production of the harmful benthic dinoflagellate Gambierdiscus belizeanus

Benthic dinoflagellates constitute a group of microalgae that inhabit the ocean floor, adhering to substrates such as coral, seagrasses, and sand. Certain species within this group have the potential to produce toxins. Ocean warming could increase the occurrence of harmful benthic dinoflagellate blooms, which pose a significant threat to coastal ecosystems in tropical and subtropical regions. However, the impact of water temperatures on the growth and toxicity of these harmful algal species remains uncertain. In this study, we investigated the physiological and transcriptional responses, as well as toxin production, of Gambierdiscus belizeanus, a common dinoflagellate responsible for increasing ciguatera risk, when exposed to temperatures ranging from 18 °C to 28 °C. Based on 70-day growth curves, G. belizeanus grew fastest at 26 °C, with a maximum specific growth rate of 0.088 ± 0.018 div·d^-1. At stationary phase of algal cultures, the photosynthetic efficiency (Fv/Fm) of algal cells at 26 °C was the highest (0.56 ± 0.02) among all treatments; significant decreases in pigment contents, including chlorophyll a, chlorophyll c, and carotenoids, were observed in algal cells exposed to 18 °C. However, during the exponential phase, only algal cultures exposed to 22 °C exhibited significantly lower levels of chlorophyll a and photosynthetic efficiency. The levels of algal toxins (44-methylgambierone and gambierone) in the 18 °C and 22 °C groups were significantly higher than those in groups exposed to higher temperatures (26 °C and 28 °C). Transcriptomic analysis showed that improved growth and photosynthesis at higher temperatures (26 °C and 28 °C) corresponded with the increased activity of crucial genes in carbon metabolism and photosynthesis. These genes, essential for energy and growth, could potentially facilitate the spread of G. belizeanus blooms. Lower temperatures led to molecular adaptations in G. belizeanus, such as modulated cell cycle genes and suppressed photosynthesis, explaining the physiological changes observed. Furthermore, the activation of toxin production-related genes under lower temperatures suggests a potential risk to ecosystems due to bioaccumulation of toxins. This study elucidates the distinct cellular and molecular responses of harmful dinoflagellates to variations in seawater temperature. These findings enhance our understanding of the emerging threats that toxin-producing benthic dinoflagellates pose to coastal ecosystems. This concern is especially significant as ocean warming has enabled some benthic toxic dinoflagellates to extend their range into higher-latitude regions.