A CSN5-dependent protein degradation pathway underlies diatom resilience to high temperature

Global warming causes a serious threat to the productivity and species composition of marine diatoms which dominate marine ecosystems and possess immense ecological significance. However, the molecular basis of their high-temperature adaptation remains enigmatic. Here, we focused on the Constitutive Photomorphogenesis 9 (COP9), and identified the COP9 signalosome (CSN) complex as a potential regulator of high-temperature acclimation in diatoms. Meta-transcriptomic data from the Tara Oceans project revealed that CSN5, the catalytic subunit of CSN, showed increased transcript abundance with rising temperature. In the model marine diatom Phaeodactylum tricornutum, CSN5 expression was induced at high temperature, and CSN5 knockout mutants displayed growth defects and altered morphotypes at 28°C. These phenotypes were rescued by CSN5 complementation, while overexpression enhances growth and biomass at high temperature. Proteomic analysis indicated that CSN5 mediates high-temperature acclimation by modulating chloroplast, cytoplasmic, and nuclear processes including photosynthesis and energy metabolism. These findings not only help us to elucidate how marine diatoms acclimate to high temperature, but also provide a molecular target for developing high-temperature-tolerant P. tricornutum.