Alternative electron pathways of photosynthesis 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 consumption. The great efficiency of algal photosynthesis relies on a mechanism concentrating CO2 (CCM) at the catalytic site of the carboxylating enzyme RuBisCO, thus enhancing CO2 fixation. While many cellular components involved in the transport and sequestration of inorganic carbon (Ci) have been uncovered, the way microalgae supply energy to concentrate CO2 against a thermodynamic gradient remains elusive. Here, by monitoring dissolved CO2 consumption, unidirectional O2 exchange and the chlorophyll fluorescence parameter NPQ in the green alga Chlamydomonas, we show that the complementary effects of cyclic electron flow and O2 photoreduction, respectively mediated by PGRL1 and flavodiiron proteins, generate the proton motive force (pmf) required by Ci transport across thylakoid membranes. We demonstrate that the trans-thylakoid pmf is used by bestrophin-like Ci transporters and further establish that a chloroplast-to-mitochondria electron flow contributes to energize non-thylakoid Ci 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 Ci transporters, thus paving the way to the transfer of a functional algal CCM in plants towards improving crop productivity.

Light-independent regulation of algal photoprotection by CO2availability

“…As expected, bicarbonate enhanced rETR ( Fig. S2B ) and, in line with ( 44 ), almost completely suppressed qE despite the fact both LHCSR3 and LHCSR1 had accumulated in the cells ( Fig. S2 ).…”

“…As expected, bicarbonate enhanced rETR ( Supplementary Fig. 3b ) and, in line with 34 , almost completely suppressed qE despite the fact under the experimental conditions both LHCSR3 and LHCSR1 typically accumulate in the cells (as in Supplementary Fig. 3 ).…”

“…Therefore, the higher accumulation of LHCSR1 protein could account for the higher qE levels under conditions of elevated CO 2 . We also took into consideration the impact of the protonation state of LHCSR proteins on the activation of qE 9, 33 ; it was recently shown that bicarbonate leads to LHCSRs deprotonation in HL-acclimated cells because part of the trans-thylakoid proton motive force is used by bestrophin-like C i transporters 34, 35 . We took HL-acclimated cells that typically accumulate both LHCSR3 and LHCSR1 proteins (as for instance in Supplementary Fig.…”

Interplay between LHCSR proteins and state transitions governs the NPQ response in intact cells of Chlamydomonas during light fluctuations

“…Therefore, these kinetics are directly related to chlorophyll fluorescence quenching, rather than other non-quenching processes that affect chlorophyll fluorescence. This phenomenon of decreasing NPQ during the light has been previously attributed to the consumption of the proton gradient by the activity of the CO 2 concentration mechanism (CCM) (Burlacot et al ., 2021). For fluctuating light periods longer than 4 minutes, upon a transition from HL to dark, the NPQ turned off rapidly but was then followed by a gradual rise in NPQ during further darkness, a trend that was also observed in NPQτ ( Fig.…”

Global proteomic response of unicellular cyanobacterium Synechocystis sp. PCC 6803 to fluctuating light upon CO 2 step‐down

“…Recently, Nikkanen et al (2020) demonstrated functional redundancy between Flv1/Flv3 and NDH‐1 in PSI protection in Synechocystis . The close relationship between FDPs and CCM is also supported by the fact that cyclic electron flow and FDP‐mediated water–water cycle energize the CCM through the generation of a trans‐thylakoidal pmf in the green alga Chlamydomonas reinhardtii (Burlacot et al, 2021). However, the exact mechanism behind the decrease of FDPs under fluctuating light is not clear.…”