Alternative photosynthesis pathways drive the algal CO2-concentrating mechanism

Global photosynthesis consumes ten times more CO2 than net anthropogenic emissions, and microalgae account for nearly half of this consumption(1). 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 fixation(2). 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 O-2 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.

Automated summary

Global photosynthesis consumes ten times more CO2 than net anthropogenic emissions, and microalgae account for nearly half of this consumption. In the green alga Chlamydomonas reinhardtii, cyclic electron flow and O-2 photoreduction generate a low luminal pH essential for CO2 concentration, while electron flow from chloroplast to mitochondria energizes inorganic carbon transport.