Thermal tolerance and cellular plasticity in marine phytoplankton diatoms modulated by epigenetic mechanisms for environmental adaptation

Abstract Diatoms are a crucial component of marine ecosystems, known for their broad environmental adaptability and wide temperature tolerance. However, the molecular mechanisms underlying their adaptability to diverse temperatures are unknown. In this study, we discovered that heat shock transcription factors (HSFs) are potentially important for thermal tolerance in diatoms. Our study focused on PtHSF2, which was annotated as HSF2 in Phaeodactylum tricornutum’s genome and was ubiquitous in diatoms. Overexpression of PtHSF2 markedly enhanced diatom's thermal tolerance and influenced cell size; caused significant differential expression of many genes such as cell division cycle protein 45 like (Cdc45-like, named PtCdc45-like), light harvesting complex protein 2 (Lhcx2), and fatty acid desaturase (FAD). Cleavage Under Targets and Tagmentation (CUT&Tag) and CUT&Tag-qPCR analyses demonstrated that PtHSF2 targeted and up-regulated Cdc45-like and Lhcx2, down-regulated ATP-binding cassette (ABC) transporter. Functional validation analysis of PtCdc45-like showed that its overexpression induced a larger cell size, enhanced antioxidant capacity, and therefore improved cell survival rate at high temperatures. Collectively, our results elucidated the molecular mechanism of PtHSF2 mediating high-temperature tolerance of diatoms and validated the functions of its target gene PtCdc45-like. These findings emphasize the importance of heat shock transcription factors in the temperature adaptation of diatoms and provide new insights for temperature acclimation studies in microalgae.