A CO 2 -limitation-induced cytosolic repressor enables shutdown of the algal CO 2 -concentrating mechanism
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Aquatic photosynthetic organisms face limited CO 2 availability because CO 2 diffuses slowly in water and most dissolved inorganic carbon (Ci) exists as HCO 3 − at physiological pH. To overcome this limitation, aquatic photoautotrophs operate CO 2 -concentrating mechanisms (CCMs) that elevate CO 2 around Rubisco and sustain carbon fixation. Because CCM operation consumes energy, it must be suppressed when CO 2 becomes abundant, but how this shutdown occurs remains poorly understood. In Chlamydomonas reinhardtii , the nuclear protein CBP1 was identified as a CCM repressor, but its loss causes only partial derepression under high CO 2 , indicating that an additional mechanism is required for complete shutdown. Here, we identify High-Affinity CCM Repressor 1 (HCR1), a cytosolic protein related to CBP1, as a second repressor. Under high CO 2 , hcr1 mutants retained high affinity for Ci and derepressed CCM and photoacclimation genes. Combined disruption of HCR1 and CBP1 further increased Ci affinity, approaching that of wild-type cells with a fully induced CCM under CO 2 limitation, and promoted the accumulation of Ci transporters. HCR1 loss also prevented redistribution of the chloroplast regulator CAS away from the pyrenoid and was accompanied by retention of a pyrenoid starch sheath. In contrast, LCIB, a chloroplast CO 2 -recapture protein, relocated normally. Unexpectedly, HCR1 accumulated during CO 2 limitation and declined after transfer to high CO 2 . These results show that CCM shutdown is an active transition rather than the passive reversal of induction. We propose that CBP1 restrains CCM1-dependent transcription, while HCR1 is preloaded during CO 2 limitation to terminate the CAS-associated, starch-sheathed, high-affinity state when CO 2 becomes replete.
Significance Statement
Aquatic photosynthetic organisms often expend energy to concentrate CO 2 around Rubisco, the enzyme that fixes CO 2 into organic carbon. Research has emphasized how this system is activated under CO 2 limitation, while its shutdown has usually been viewed as a simple reversal. We show that shutdown is instead an active process that coordinates gene repression, chloroplast signaling, and remodeling of the pyrenoid, the compartment where Rubisco and CO 2 are concentrated. Unexpectedly, part of the shutdown machinery accumulates while CO 2 remains limiting, suggesting that cells prepare the off-switch before conditions improve. This finding suggests a general strategy for reversible environmental adaptation and offers a framework for engineering photosynthesis that captures carbon efficiently without wasting energy as CO 2 availability changes in fluctuating environments.
