Evolutionarily distinct strategies for the acquisition of inorganic carbon from seawater in marine diatoms

The acquisition of dissolved inorganic carbon (DIC) in CO₂-limited seawater is a central issue to understand in marine primary production. We previously demonstrated the occurrence of direct HCO₃⁻ uptake by solute carrier (SLC) 4 transporters in a diatom, a major marine primary producer. Homologs of SLC are found in both centric and pennate marine diatoms, suggesting that SLC transporters are generally conserved. Here, the generality of SLC-mediated DIC uptake in diatoms was examined using an SLC inhibitor, diisothiocyano-2,2ʹ-stilbenedisulfonic acid (DIDS), and an inhibitor of external carbonic anhydrase, acetazolamide. DIDS suppressed high-DIC-affinity photosynthesis in the pennate diatom Phaeodactylum tricornutum and the centric diatom Chaetoceros muelleri, but there was no effect on either the pennate Cylindrotheca fusiformis or the centric Thalassiosira pseudonana. Interestingly, the DIC affinity of DIDS-insensitive strains was sensitive to treatment with up to 100 μM acetazolamide, displaying a 2–4-fold increase in K 0.5[DIC]. In contrast, acetazolamide did not affect the DIDS-sensitive group. These results indicate the occurrence of two distinct strategies for DIC uptake—one primarily facilitated by SLC and the other being passive CO₂ entry facilitated by external carbonic anhydrase. The phylogenetic independence of these strategies suggests that environmental demands drove the evolution of distinct DIC uptake mechanisms in diatoms.