The green algae CO2 concentrating mechanism and photorespiration jointly operate during acclimation to low CO2

Due to low availability of CO2 in aquatic environment, microalgae have evolved a CO2 concentrating mechanism (CCM). It has long been thought that operation of CCM would suppress photorespiration by increasing the CO2 concentration at the Rubisco active site, but experimental evidence is scarce. To better explore the function of photorespiration in algae, we first characterized a Chlamydomonas reinhardtii mutant defected in low-CO2 inducible 20 (LCI20) and show that LCI20 is a chloroplast-envelope glutamate/malate transporter playing a role in photorespiration. By monitoring growth and glycolate excretion in mutants deficient in either CCM or photorespiration, we conclude that: (i.) CCM induction does not depend on photorespiration, (ii.) glycolate excretion together with glycolate dehydrogenase down-regulation prevents the toxic accumulation of non-metabolized photorespiratory metabolites, and (iii.) photorespiration is active at low CO2 when the CCM is operational. This work provides a foundation for a better understanding of the carbon cycle in the ocean where significant glycolate concentrations have been found.