Cyclic and pseudo-cyclic electron pathways play antagonistic roles during nitrogen deficiency in Chlamydomonas reinhardtii

Nitrogen (N) scarcity frequently constrains global biomass productivity. N deficiency halts cell division, downregulates photosynthetic electron transfer (PET), and enhances carbon storage. However, the molecular mechanism downregulating photosynthesis during N deficiency and its relationship with carbon storage are not fully understood. Proton gradient regulator-like 1 (PGRL1) controlling cyclic electron flow (CEF) and flavodiiron proteins (FLV) involved in pseudo-CEF (PCEF) are major players in the acclimation of photosynthesis. To determine the role of PGRL1 or FLV in photosynthesis under N deficiency, we measured PET, oxygen gas exchange, and carbon storage in Chlamydomonas reinhardtii pgrl1 and flvB knockout mutants. Under N deficiency, pgrl1 maintained higher net photosynthesis and O2 photoreduction rates and higher levels of cytochrome b6f and PSI compared with the control and flvB. The photosynthetic activity of flvB and pgrl1 flvB double mutants decreased in response to N deficiency, similar to the control strains. Furthermore, the preservation of photosynthetic activity in pgrl1 was accompanied by an increased accumulation of triacylglycerol in certain genetic backgrounds but not all, highlighting the importance of gene-environment interaction in determining traits such as oil content. Our results suggest that in the absence of PGRL1-controlled CEF, FLV-mediated PCEF maintains net photosynthesis at a high level and that CEF and PCEF play antagonistic roles during N deficiency. This study further illustrate how a strain's nutrient status and genetic makeup can affect the regulation of photosynthetic energy conversion in relation to carbon storage and provide additional strategies for improving lipid productivity in algae. In the absence of cyclic electron flow, flavodiiron proteins maintain net photosynthesis by mediating a pseudo-cyclic electron flow in nitrogen-deficient Chlamydomonas reinhardtii.