Metacaspases contribute to the cellular response to heat stress in a marine diatom

Climate-driven marine heatwaves (HW) are extreme, large-scale events characterized by elevated ocean temperatures lasting from days to months. Despite their importance, little is known about the molecular mechanisms of algal response to marine HW. Recent studies suggest that metacaspases play an important role in thermotolerance. Metacaspases are cysteine proteases structurally similar to caspases that are best known for their role in programmed cell death. In order to study the role of metacaspases in diatoms' thermotolerance, we exposed the model diatom Phaeodactylum tricornutum and mutants in the metacaspase genes to a 72-h HW followed by a recovery phase that enables capturing the mechanisms underpinning acclimation. PtMCA-III triple mutants exhibited increased sensitivity to the HW treatment, including induction of cell death that peaked days after returning to initial temperatures. We revealed that HW treatment led to accumulation of H₂O₂ and PtMCA-III mutants were hypersensitive to oxidative stress. Application of antioxidants before exposure to elevated temperature led to significantly higher survival. We propose that although metacaspases are classically considered part of the cell death machinery in algae, they have a pivotal role in diatom's acclimation to elevated temperatures, a trait vital for algal survival considering climate change.