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bioRxiv · 10.1101/2024.03.18.585510

Strong heterologous electron sink outcompetes alternative electron transport pathways in photosynthesis

Hubacek, M.·Wey, L. T.·Kourist, R.·Malihan-Yap, L.·Nikkanen, L.·Allahverdiyeva, Y.
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Abstract

Improvement of photosynthesis requires a thorough understanding of electron partitioning under both natural and strong electron sink conditions. We applied a wide array of state-of-the-art biophysical and biochemical techniques to thoroughly investigate the fate of photosynthetic electrons in the engineered cyanobacterium Synechocystis sp. PCC 6803, a blueprint for photosynthetic biotechnology, expressing the heterologous gene for ene-reductase, YqjM. This recombinant enzyme catalyses the reduction of an exogenously added substrate into the desired product by utilising photosynthetically produced NAD(P)H, enabling whole-cell biotransformation. Through coupling the biotransformation reaction with biophysical measurements, we demonstrated that the strong artificial electron sink, outcompetes the natural electron valves, the flavodiiron protein-driven Mehler-like reaction, and cyclic electron transport. These results show that ferredoxin-NAD(P)H-oxidoreductase (FNR) is the preferred route for delivering photosynthetic electrons from reduced ferredoxin and the cellular NADPH/NADP+ ratio as a key factor in orchestrating photosynthetic electron flux. These insights are crucial for understanding molecular mechanisms of photosynthetic electron transport and harnessing photosynthesis for sustainable bioproduction by engineering the cellular source/sink balance. Furthermore, we conclude that identifying the bioenergetic bottleneck of a heterologous electron sink is a crucial prerequisite for targeted engineering of photosynthetic biotransformation platforms. Significance statementWe coupled the photosynthetic and biocatalytic (whole-cell biotransformation) performance of model cyanobacteria. We employed a heterologous NAD(P)H utilising enzyme, as a strong artificial electron sink, allowing us to gain a comprehensive understanding of photosynthetic electron partitioning. We demonstrated that the strong electron sink outcompetes natural electron sinks and cyclic electron transport.

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Hubacek, M., Wey, L. T., Kourist, R., Malihan-Yap, L., Nikkanen, L., Allahverdiyeva, Y.. 2024-03-20. Strong heterologous electron sink outcompetes alternative electron transport pathways in photosynthesis. https://doi.org/10.1101/2024.03.18.585510

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