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

Abstract

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.