Multi-Omics Analysis Reveals Adaptation Strategies of Marine Diatom to Long-Term Ocean Warming: Resource Allocation Trade-Offs and Epigenetic Regulation.

High CO emissions originating from anthropogenic sources have resulted in ocean warming (OW), posing a severe threat to marine organisms and ecosystems. Recent evidence has shown that marine phytoplankton may acclimate and adapt to long-term OW. Whether and how marine diatoms-a functional group of phytoplankton that contributes to 40% of marine primary production-can adapt to long-term OW remains virtually unknown. The model marine diatom Phaeodactylum tricornutum was subjected to thermal stress (25°C, compared to the Control at 20°C) for 400 days (~400 generations), and physiological, transcriptomic, genetic and epigenetic analyses were performed to reveal the adaptation mechanisms under long-term OW. During the adaptation, regulation of resource allocation (e.g., photosynthesis, nitrogen metabolism, ribosomal synthesis and translation, carbon metabolism and heat shock response) at the genetic and transcriptional levels was linked to accumulated proteins, carbohydrates and particulate organic carbon, reduced lipid content, and enlarged cell size. Integrated analyses of histone modification (H3K27me3) and transcriptome data sets revealed the potential role of transposable elements and epigenetic regulation of transposable elements via histone modification in the adaptation of P. tricornutum to long-term thermal stress. These mechanistic insights may facilitate the modelling and prediction of OW-induced impacts on marine phytoplankton in the future.