Widespread Presence of SPX and Its Potential Role as a Phosphorus Nutrient Regulator in Dinoflagellates

SPX domain-containing proteins (SPXc) are crucial for regulating phosphorus (P) homeostasis in plants. Recently, the SPX gene was identified in the diatom model Phaeodactylum tricornutum and shown to serve as a negative regulator of P acquisition. Whether SPXc occurs in dinoflagellates is unclear. Here, we report the presence and potential functions of genes encoding SPXc in dinoflagellates (dino-SPXc). Four classes of SPXc were identified in dinoflagellates, including the three known classes—the stand-alone SPX, SPX-EXS, and SPX-VTC—and SPX-other, with SPX and SPX-EXS being dominant. Using the TARA Oceans database, we investigated the taxonomic and geographic distributions of dino-SPXc and found variations in dino-SPXc expression among size classes of dinoflagellates. The harmful algal bloom-causative species Prorocentrum shikokuense possesses all four classes of SPXc proteins, showing a fluctuating expression pattern under different nutrient conditions and during different phases of the cell cycle and algal bloom. In addition, the SPXc genes in Symbiodiniaceae respond not only to P stress but also to thermal variations. These results are consistent with a role of dino-SPXc in maintaining P homeostasis in dinoflagellates and suggest the importance of SPX-related genes in enabling dinoflagellates to sustain population growth in nutrient-variable oceans, warranting further research.