Cited by 15Photosynthetic Processes and MechanismsMetalloenzymes and iron-sulfur proteinsPlant biochemistry and biosynthesis

Strong heterologous electron sink outcompetes alternative electron transport pathways in photosynthesis

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Hubáček, Michal, Wey, Laura T., Kourist, Robert, Malihan‐Yap, Lenny, Nikkanen, Lauri, Allahverdiyeva, Yagut·2024·The Plant Journal

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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 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.

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Crossref · 10.1111/tpj.16935

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  • Engineered pathways demanding substantial reducing power may compete with native metabolic processes for cofactors, potentially constraining overall pathway performance.

    “This dynamic means that engineered pathways demanding substantial reducing power may compete with native metabolic processes for these cofactors, thereby potentially constraining overall pathway performance [172].”
  • In cyanobacteria, intracellular levels of ATP and NADPH are closely tied to photosynthetic electron transport, and variations in light intensity, carbon sources, or environmental conditions can alter the cell's redox state.

    “In cyanobacteria, the intracellular levels of ATP and NADPH are closely tied to PET. Consequently, variations in light intensity, carbon sources, or environmental conditions can alter the cell’s redox state.”

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Authors
Hubáček, M., Wey, L. T., Kourist, R., Malihan‐Yap, L., Nikkanen, L., & Allahverdiyeva, Y.
Affiliations
  • University of Turku (FI)
  • Graz University of Technology (AT)
Corresponding author
Allahverdiyeva, Yagut
Venue
The Plant Journal
Publisher
Wiley
Published
2024-07-15
Volume
119
Issue
5
Pages
2500-2513
ISSN
  • 0960-7412 (ISSN-L)
  • 1365-313X
OpenAlex
W4400648575
Cited by
15
References
79
Citations by year
2026: 7 · 2025: 7 · 2024: 1
FWCI
2.03
Type
journal article
Language
en
Open access
Locations
  • The Plant Journal (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
  • PubMed (publishedVersion)
  • UTUPub (University of Turku) (submittedVersion)
  • UTUPub (University of Turku) (submittedVersion, cc-by)
Funders
  • European Commission (899576)
  • Academy of Finland (315119, 322754)
  • Novo Nordisk Fonden (NNF20OC0064371)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Photosynthetic Processes and Mechanisms
  • Physical Sciences › Energy › Renewable Energy, Sustainability and the Environment › Metalloenzymes and iron-sulfur proteins
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Plant biochemistry and biosynthesis
Keywords
photosynthetic electron transport, Synechocystis sp. PCC 6803, whole-cell biocatalysis, Mehler reaction, cyclic electron flow, electron partitioning, NADPH/NADP+ ratio, flavodiiron proteins
MeSH terms
Bacterial Proteins, Electron Transport, Electrons, Ferredoxin-NADP Reductase, Ferredoxins, NADP, Photosynthesis, Synechocystis

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