Multi-omics profiling reveals resource allocation and acclimation strategies to temperature changes in a marine dinoflagellate

Temperature is a critical environmental factor that affects the cell growth of dinoflagellates and bloom formation. To date, the molecular mechanisms underlying the physiological responses to temperature variations are poorly understood. Here, we applied quantitative proteomic and untargeted metabolomic approaches to investigate protein and metabolite expression profiles of a bloom-forming dinoflagellate Prorocentrum shikokuense at different temperatures. Of the four temperatures (19, 22, 25, and 28°C) investigated, P. shikokuense at 25°C exhibited the maximal cell growth rate and maximum quantum efficiency of photosystem II (Fv/Fm) value. The levels of particulate organic carbon (POC) and nitrogen (PON) decreased with increasing temperature, while the POC/PON ratio increased and peaked at 25°C. Proteomic analysis showed proteins related to photoreaction, light harvesting, and protein homeostasis were highly expressed at 28°C when cells were under moderate heat stress. Metabolomic analysis further confirmed reallocated amino acids and soluble sugars at this temperature. Both omic analyses showed glutathione metabolism that scavenges the excess reactive oxygen species, and transcription and lipid biosynthesis that compensate for the low translation efficiency and plasma membrane fluidity were largely upregulated at suboptimal temperature. Higher accumulations of glutathione, glutarate semialdehyde, and 5-KETE at 19°C implied their important roles in low-temperature acclimation. The strikingly active nitrate reduction and nitrogen flux into asparagine, glutamine, and aspartic acid at 19°C indicated these three amino acids may serve as nitrogen storage pools and help cells cope with low temperature. Our study provides insights into the effects of temperature on dinoflagellate resource allocation and advances our knowledge of dinoflagellate bloom formation in marine environments.