Functional redundancy between flavodiiron proteins and NDH‐1 in Synechocystis sp. PCC 6803

Abstract

Summary In oxygenic photosynthetic organisms, excluding angiosperms, flavodiiron proteins (FDPs) catalyze light‐dependent reduction of O2 to H2O. This alleviates electron pressure on the photosynthetic apparatus and protects it from photodamage. In Synechocystis sp. PCC 6803, four FDP isoforms function as hetero‐oligomers of Flv1 and Flv3 and/or Flv2 and Flv4. An alternative electron transport pathway mediated by the NAD(P)H dehydrogenase‐like complex (NDH‐1) also contributes to redox hemostasis and the photoprotection of photosynthesis. Four NDH‐1 types have been characterized in cyanobacteria: NDH‐11 and NDH‐12, which function in respiration; and NDH‐13 and NDH‐14, which function in CO2 uptake. All four types are involved in cyclic electron transport. Along with single FDP mutants (∆flv1 and Δflv3) and the double NDH‐1 mutants (∆d1d2, which is deficient in NDH‐11,2 and ∆d3d4, which is deficient in NDH‐13,4), we studied triple mutants lacking one of Flv1 or Flv3, and NDH‐11,2 or NDH‐13,4. We show that the presence of either Flv1/3 or NDH‐11,2, but not NDH‐13,4, is indispensable for survival during changes in growth conditions from high CO2/moderate light to low CO2/high light. Our results show functional redundancy between FDPs and NDH‐11,2 under the studied conditions. We suggest that ferredoxin probably functions as a primary electron donor to both Flv1/3 and NDH‐11,2, allowing their functions to be dynamically coordinated for efficient oxidation of photosystem I and for photoprotection under variable CO2 and light availability.

Electron flow through NDH-1 complexes is the major driver of cyclic electron flow-dependent proton pumping in cyanobacteria

“…Therefore, these complexes must contribute only a minor amount to the total CEF, at least under these growth conditions. Together with the data presented here, data on the presence of the Flv1/3 system consuming electrons in their Mehler-like reaction, resulting in no additional proton pumping but acting as an electron sink to compensate for the loss of the NDH-11/2 systems [66], additionally implies that the NDH-13/4 complexes are incapable not only of dealing with the excess reductant but also of compensating for the loss of the NDH-11/2 complexes in terms of either electron transport or proton pumping in these conditions. The proton pumping results are consistent with studies of Bernat and colleagues, showing that the respiratory forms of the NDH-1 complexes (NDH-11/2) dominate the corresponding cyclic electron fluxes and that the CO2-uptake forms (NDH-13/4) contribute less strongly [22].…”

Engineering of NADPH Supply Boosts Photosynthesis-Driven Biotransformations

“… 34 It must be noted, however, that the ΔFlv mutants may be more light sensitive under specific conditions. 31 , 58 Nonetheless, engineering heterologous strong electron sinks (e.g., YqjM) should overcome the imbalance between energy input and electron outlet eliminating oxidative stress and feedback reactions.…”

Regulatory electron transport pathways of photosynthesis in cyanobacteria and microalgae: Recent advances and biotechnological prospects

“…A shared electron donor between FDPs and NDH-1 may, therefore, enable coordination of the two electron transfer pathways. Accordingly, we reported recently on partial redundancy between Flv1/3 and NDH-1 1/2 in protecting PSI by maintaining efficient oxidation of PSI in high light and air-level CO 2 concentration (Nikkanen et al, 2020).…”

“…While RTOs only have a minor effect on the redox poise of the PETC in steady-state light conditions (Helman et al, 2005), they appear to tune the redox poise of cyanobacterial thylakoids when illumination ceases. Dark respiratory rates in Synechocystis are reportedly higher after illumination than before (Nikkanen et al, 2020;Santana-Sanchez et al, 2019). It is possible that relaxing photosynthetic control and/or increased concentration of O 2 stimulates RTOs.…”