Alternative photosynthesis pathways drive the algal CO2-concentrating mechanism

Abstract

Global photosynthesis consumes ten times more CO₂ than net anthropogenic emissions, and microalgae account for nearly half of this consumption¹. The high efficiency of algal photosynthesis relies on a mechanism concentrating CO₂ (CCM) at the catalytic site of the carboxylating enzyme RuBisCO, which enhances CO₂ fixation². Although many cellular components involved in the transport and sequestration of inorganic carbon have been identified^3,4, how microalgae supply energy to concentrate CO₂ against a thermodynamic gradient remains unknown^4-6. Here we show that in the green alga Chlamydomonas reinhardtii, the combined action of cyclic electron flow and O₂ photoreduction-which depend on PGRL1 and flavodiiron proteins, respectively-generate a low luminal pH that is essential for CCM function. We suggest that luminal protons are used downstream of thylakoid bestrophin-like transporters, probably for the conversion of bicarbonate to CO₂. We further establish that an electron flow from chloroplast to mitochondria contributes to energizing non-thylakoid inorganic carbon transporters, probably by supplying ATP. We propose an integrated view of the network supplying energy to the CCM, and describe how algal cells distribute energy from photosynthesis to power different CCM processes. These results suggest a route for the transfer of a functional algal CCM to plants to improve crop productivity.