Shan Gao

Increasing ocean temperatures threaten the productivity and species composition of marine diatoms. High temperature response and regulation is important for the acclimation of marine diatoms to such environments. However, the molecular mechanisms behind their acclimation to high temperature are still largely unknown. In this study, the abundance of PtCPF1 homologs (a member of the cryptochrome-photolyase family [CPF] in the model diatom Phaeodactylum tricornutum) transcripts in marine phytoplankton is shown to increase with rising temperature based on Tara Oceans datasets. Moreover, the expression of PtCPF1 in P. tricornutum at high temperature (26°C) was much higher than that at optimum temperature (20°C). Deletion of PtCPF1 in P. tricornutum disrupted the expression of genes encoding two phytotransferrins (ISIP2A and ISIP1) and two Na⁺/P co-transporters (PHATRDRAFT_47667 and PHATRDRAFT_40433) at 26°C. This further impacted the uptake of Fe and P, and eventually caused the arrest of cell division. Gene expression, Fe and P uptake, and cell division were restored by rescue with the native PtCPF1 gene. Furthermore, PtCPF1 interacts with two putative transcription factors (BolA and TF IIA) that potentially regulate the expression of genes encoding phytotransferrins and Na⁺/P co-transporters. To the best of our knowledge, this is the first study to reveal PtCPF1 as an essential regulator in the acclimation of marine diatoms to high temperature through the coordination of Fe and P uptake. Therefore, these findings help elucidate how marine diatoms acclimate to high temperature.

Unlike in terrestrial and freshwater ecosystems, light fields in oceans fluctuate due to both horizontal current and vertical mixing. Diatoms thrive and dominate the phytoplankton community in these fluctuating light fields. However, the molecular mechanisms that regulate diatom acclimation and adaptation to light fluctuations are poorly understood. Here, we performed transcriptome sequencing, metabolome profiling, and ¹³C-tracer labeling on the model diatom Phaeodactylum tricornutum. The diatom acclimated to constant light conditions was transferred to six different light conditions, including constant light (CL5d), short-term (1 h) high light (sHL1h), and short-term (1 h) and long-term (5 days) mild or severe light fluctuation conditions (mFL1h, sFL1h, mFL5d, and sFL5d) that mimicked land and ocean light levels. We identified 2,673 transcripts (25% of the total expressed genes) expressed differentially under different fluctuating light regimes. We also identified 497 transcription factors, 228 not reported previously, which exhibited higher expression under light fluctuations, including 7 with a light-sensitive PAS domain (Per-period circadian protein, Arnt-aryl hydrocarbon receptor nuclear translocator protein, Sim-single-minded protein) and 10 predicted to regulate genes related to light-harvesting complex proteins. Our data showed that prolonged preconditioning in severe light fluctuation enhanced photosynthesis in P. tricornutum under this condition, as evidenced by increased oxygen evolution accompanied by the upregulation of Rubisco and light-harvesting proteins. Furthermore, severe light fluctuation diverted the metabolic flux of assimilated carbon preferentially toward fatty acid storage over sugar and protein. Our results suggest that P. tricornutum use a series of complex and different responsive schemes in photosynthesis and carbon metabolism to optimize their growth under mild and severe light fluctuations. These insights underscore the importance of using more intense conditions when investigating the resilience of phytoplankton to light fluctuations.