Biophysical principles of the <i>Chlamydomonas reinhardtii</i> CO₂-concentrating mechanism

Photosynthesis allows human life on Earth: it harvests light energy to fix atmospheric CO₂ which produces food and fuels. Its efficiency is limited by the catalytic properties of the CO₂-fixing enzyme Rubisco – which works at only 10% of its maximum rate under air-level CO₂. The alga Chlamydomonas reinhardtii operates a CO₂-concentrating mechanism (CCM) that locally elevates the CO₂ level around Rubisco in a phase-separated organelle called the pyrenoid, thus enhancing photosynthetic performance. To better understand how this CCM works, we developed a multi-compartment reaction-diffusion model. We find that diffusion barriers preventing CO₂ efflux from the pyrenoid are key to a functional and energetically efficient CCM. Our model reveals two distinct CCM strategies: (1) passive uptake of CO₂ which is then trapped in the chloroplast as HCO₃^-; (2) active pumping in of HCO₃^-. Interestingly, our model predicts that feasible CCM strategies vary with environmental CO₂ levels, which sheds light on a long confounding growth phenotype. Finally, our model provides insights into the localization of key CCM components, and can guide engineering a CCM into higher plants.