The Chlamydomonas reinhardtii chloroplast envelope protein LCIA transports bicarbonate in planta

• Published in: Journal of experimental botany Vol. 74; no. 12; pp. 3651 - 3666
• Main Authors: Förster, Britta, Rourke, Loraine M, Weerasooriya, Hiruni N, Pabuayon, Isaiah C M, Rolland, Vivien, Au, Eng Kee, Bala, Soumi, Bajsa-Hirschel, Joanna, Kaines, Sarah, Kasili, Remmy W, LaPlace, Lillian M, Machingura, Marylou C, Massey, Baxter, Rosati, Viviana C, Stuart-Williams, Hilary, Badger, Murray R, Price, G Dean, Moroney, James V
• Format: Journal Article
• Language: English
• Published: England 27-06-2023
• Subjects: Bicarbonates - metabolism; Carbon Dioxide - metabolism; Carbonic Anhydrases - genetics; Carbonic Anhydrases - metabolism; Chlamydomonas reinhardtii - genetics; Chlamydomonas reinhardtii - metabolism; Chloroplasts - metabolism; Photosynthesis; Plants - metabolism; Bicarbonate transport; photosynthesis; carbonic anhydrase; βca5; DCAKO; CCM; LCIA
• ISSN: 0022-0957; 1460-2431
• DOI: 10.1093/jxb/erad116

LCIA (low CO2-inducible protein A) is a chloroplast envelope protein associated with the CO2-concentrating mechanism of the green alga Chlamydomonas reinhardtii. LCIA is postulated to be a HCO3- channel, but previous studies were unable to show that LCIA was actively transporting bicarbonate in planta. Therefore, LCIA activity was investigated more directly in two heterologous systems: an Escherichia coli mutant (DCAKO) lacking both native carbonic anhydrases and an Arabidopsis mutant (βca5) missing the plastid carbonic anhydrase βCA5. Neither DCAKO nor βca5 can grow in ambient CO2 conditions, as they lack carbonic anhydrase-catalyzed production of the necessary HCO3- concentration for lipid and nucleic acid biosynthesis. Expression of LCIA restored growth in both systems in ambient CO2 conditions, which strongly suggests that LCIA is facilitating HCO3- uptake in each system. To our knowledge, this is the first direct evidence that LCIA moves HCO3- across membranes in bacteria and plants. Furthermore, the βca5 plant bioassay used in this study is the first system for testing HCO3- transport activity in planta, an experimental breakthrough that will be valuable for future studies aimed at improving the photosynthetic efficiency of crop plants using components from algal CO2-concentrating mechanisms.