Effects of Sulfate Limitation on Photosynthesis and Cell Composition of Unicellular Marine Microalgae of Different Phylogenies

Sulfur (S) is an essential macroelement for photosynthetic organisms and is acquired as sulfate and assimilated as sulfide into cysteine through a highly demanding reductive process. S is a key component of proteins, lipids, and various other cellular metabolites and plays a direct role in photosynthesis, both in the electron transport and in carbon fixation reactions. Despite such central functions, most of our knowledge on S metabolism is focused on plant species, while in microalgae it is still fragmented, particularly concerning their huge phylogenetic diversity. Here, we investigated responses to continuous low sulfate availability in three marine microalgae, two Chlorophytes, Tetraselmis suecica and Dunaliella salina, and the diatom Phaeodactylum tricornutum, by characterizing their growth, photosynthesis, elemental, and macromolecular composition. As a general trend, all the microalgae acclimated to the low sulfate medium prioritized the allocation of available resources to photosynthesis. By modulating their pigment content per cell and the stoichiometry of their photosynthetic apparatus, S-limited cells kept in vivo photosynthetic activity close to that of control cultures. Conversely, growth and cell composition were modulated in a species-specific manner. Results are discussed also in an evolutionary perspective, taking into consideration that, throughout Earth's history, sulfate concentration significantly increased from ancient to modern oceans, and such variation was paralleled by changes in the ecological abundances between algal groups, with the red algae lineage of present-day oceans supplanting the green algae, more abundant in the past.