Off the beaten pathway: Powering carbon capture with alternative photosynthetic electron transfer pathways

During photosynthesis, light drives the formation of NADPH by powering a linear electron flow (LEF) from water, through photosystems (PS) II and I, to NADP.Additionally, LEF generates a proton motive force (pmf) across the thylakoid membrane, which is utilized to generate ATP.However, LEF is insufficient for providing the ATP requirements for various metabolic processes, including carbon fixation in the Calvin-Benson-Bassham cycle.Proposedly, alternative electron pathways may provide the additional required energy (Allen 2003).During cyclic electron flow (CEF), electrons are recycled around PSI (Nawrocki et al. 2019).In pseudo-CEF (PCEF), electrons are ejected from the photosynthetic electron chain by reducing O2 on the PSI acceptor side (Chaux et al. 2017).Both pathways promote pmf generation and ATP production (Fig. ).Transferring reductants from the chloroplast to the mitochondria, where they are converted to ATP in the respiratory chain and shuttled back to the chloroplast, may also provide additional ATP for carbon fixation (Raghavendra and Padmasree 2003).This process is termed chloroplast to mitochondria electron flow (CMEF; Fig. ).Although the mechanisms of alternative photosynthetic electron flows were described, the importance of each pathway for carbon fixation remains elusive.Following the discovery by Burlacot et al. ( 2022) that CEF, PCEF, and CMEF provide energy for the carbon concentrating mechanism, in this issue, Gilles Peltier and colleagues (Peltier et al. 2024) quantify the contribution, extent, and efficiency of each pathway by measuring their capacity to sustain net photosynthesis and CO2 fixation in the microalga Chlamydomonas (C.reinhardtii).The authors measured the O2 exchange rates in Chlamydomonas mutants which are impaired in both CEF and PCEF and showed that they are capable of maintaining near-maximal net photosynthesis, suggesting that CMEF compensates for the absence of CEF and PCEF.However, if respiration (CMEF) is inhibited additionally, photosynthesis is completely abolished.In wild-type (WT) cells, inhibiting respiration leads to a ~15% decrease in net photosynthesis, suggesting that CEF and PCEF can mostly compensate for the loss of CMEF.Inhibiting respiration in Chlamydomonas mutated in either pgrl1 (CEF) or flvB (PCEF) showed that each pathway may energize 60% of net photosynthesis.Together, these results show that all three pathways are the predominant ATP producers for the cell.