Alternative electron pathways of photosynthesis drive the algal CO 2 concentrating mechanism

Abstract Global photosynthesis consumes ten times more CO 2 than net anthropogenic emissions, and microalgae account for nearly half of this consumption 1 . The great efficiency of algal photosynthesis relies on a mechanism concentrating CO 2 (CCM) at the catalytic site of the carboxylating enzyme RuBisCO, thus enhancing CO 2 fixation 2 . While many cellular components involved in the transport and sequestration of inorganic carbon (C i ) have been uncovered 3,4 , the way microalgae supply energy to concentrate CO 2 against a thermodynamic gradient remains elusive 4-6 . Here, by monitoring dissolved CO 2 consumption, unidirectional O 2 exchange and the chlorophyll fluorescence parameter NPQ in the green alga Chlamydomonas , we show that the complementary effects of cyclic electron flow and O 2 photoreduction, respectively mediated by PGRL1 and flavodiiron proteins, generate the proton motive force ( pmf ) required by C i transport across thylakoid membranes. We demonstrate that the trans-thylakoid pmf is used by bestrophin-like C i transporters and further establish that a chloroplast-to-mitochondria electron flow contributes to energize non-thylakoid C i transporters, most likely by supplying ATP. We propose an integrated view of the CCM energy supply network, describing how algal cells distribute photosynthesis energy to power different C i transporters, thus paving the way to the transfer of a functional algal CCM in plants towards improving crop productivity. One sentence summary Photosynthetic alternative electron flows and mitochondrial respiration drive the algal CO 2 concentrating mechanism