A nuclear CobW/WW-domain factor represses the CO2-concentrating mechanism in the green alga Chlamydomonas reinhardtii

TL;DR

Scientists discovered a protein in green algae that turns off a CO2-concentrating mechanism when CO2 is abundant, helping algae save energy.

Contribution

Identification of CBP1, a nuclear repressor of the CO2-concentrating mechanism in Chlamydomonas reinhardtii.

Findings

CBP1 interacts with CCM1 and represses CCM gene expression under high CO2 conditions.

CBP1 disruption leads to unnecessary CCM activity and growth delays under high CO2.

CBP1 may link zinc-dependent protein chemistry to CCM regulation.

Abstract

Algae flourish by activating a CO2-concentrating mechanism (CCM) when dissolved CO2 is limited but must deactivate it when CO2 levels increase to conserve energy. We have identified the nuclear protein that represses CCM gene expression under high CO2 conditions in the model green alga. Deletion of this regulator leads to the derepression of CCM transporters and enzymes, maintaining CCM activity even under high-CO2 conditions and imposing an unnecessary energetic burden. This finding illuminates how algae balance energy consumption with carbon capture and offers a target for engineering strains that fix CO2 more efficiently for biofuel production or climate-mitigation technologies.

Microalgae induce a CO2-concentrating mechanism (CCM) to maintain photosynthesis when CO2 is limited. Because this system consumes a substantial portion of photosynthetically generated ATP, its suppression when CO2 levels rise is critical for energy balance, yet the underlying mechanism remains unclear. Here, we identify a nuclear repressor of the CCM in the green alga Chlamydomonas reinhardtii. A pull-down screen for interacting partners of the master activator CCM1/CIA5 revealed an uncharacterized protein that tightly associates with CCM1. This protein, CCM1-binding protein 1 (CBP1), combines a CobW/CobW_C GTP-binding metallochaperone module with a WW-domain characteristic of protein–protein interactions. CBP1 colocalizes and interacts with CCM1 in the nucleus regardless of CO2 conditions. Disruption of CBP1 does not affect growth or CCM induction under CO2 limitation but derepresses 27 of 41 CCM1-dependent low-CO2 inducible genes under high-CO2 conditions. These include the periplasmic and intracellular carbonic anhydrases (CAH1 and LCIB) and inorganic carbon transporters/channels (LCIA, LCI1, BST1, and BST3). Consistently, cbp1 mutants accumulate CAH1 and LCIB proteins and exhibit 40% higher inorganic carbon affinity under high-CO2 conditions; this phenotype is rescued by CBP1 complementation or by acetazolamide treatment. Crucially, cbp1 mutants exhibit significant growth delays under high-CO2 conditions, especially when light is limiting, providing direct evidence that CBP1-mediated repression is essential for energy conservation. Thus, CBP1 prevents unnecessary CCM activity when CO2 is abundant, acting upstream of both transporter/channel and carbonic anhydrase modules. Our findings suggest a regulatory mechanism potentially linking zinc-dependent protein chemistry to CCM gene repression, providing insights into energy-efficient CO2 sensing in aquatic photosynthetic organisms.

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