SLC4 family transporters in a marine diatom directly pump bicarbonate from seawater

Photosynthesis in marine diatoms is a vital fraction of global primary production empowered by CO2-concentrating mechanisms. Acquisition of HCO3- from seawater is a critical primary step of the CO2-concentrating mechanism, allowing marine photoautotrophic eukaryotes to overcome CO2 limitation in alkaline high-salinity water. However, little is known about molecular mechanisms governing this process. Here, we show the importance of a plasma membrane-type HCO3- transporter for CO2 acquisition in a marine diatom. Ten putative solute carrier (SLC) family HCO3- transporter genes were found in the genome of the marine pennate diatom Phaeodactylum tricornutum. Homo logs also exist in marine centric species, Thalassiosira pseudonana, suggesting a general occurrence of SLC transporters in marine diatoms. Seven genes were found to encode putative mammalian-type SLC4 family transporters in P. tricornutum, and three of seven genes were specifically transcribed under low CO2 conditions. One of these gene products, PtSLC4-2, was localized at the plasmalemma and significantly stimulated both dissolved inorganic carbon (DIC) uptake and photosynthesis in P. tricornutum. DIC uptake by PtSLC4-2 was efficiently inhibited by an anion-exchanger inhibitor, 4,4'-diisothiocyanostilbene-2,2'-disulfonic acid, in a concentration-dependent manner and highly dependent on Na+ ions at concentrations over 100 mM. These results show that DIC influx into marine diatoms is directly driven at the plasmalemma by a specific HCO3- transporter with a significant halophilic nature.