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De novo protein design of photochemical reaction centers

Author

Listed:
  • Nathan M. Ennist

    (University of Pennsylvania
    University of Washington
    University of Washington)

  • Zhenyu Zhao

    (University of Pennsylvania)

  • Steven E. Stayrook

    (University of Pennsylvania
    Yale University School of Medicine
    Yale University West Campus)

  • Bohdana M. Discher

    (University of Pennsylvania)

  • P. Leslie Dutton

    (University of Pennsylvania)

  • Christopher C. Moser

    (University of Pennsylvania)

Abstract

Natural photosynthetic protein complexes capture sunlight to power the energetic catalysis that supports life on Earth. Yet these natural protein structures carry an evolutionary legacy of complexity and fragility that encumbers protein reengineering efforts and obfuscates the underlying design rules for light-driven charge separation. De novo development of a simplified photosynthetic reaction center protein can clarify practical engineering principles needed to build new enzymes for efficient solar-to-fuel energy conversion. Here, we report the rational design, X-ray crystal structure, and electron transfer activity of a multi-cofactor protein that incorporates essential elements of photosynthetic reaction centers. This highly stable, modular artificial protein framework can be reconstituted in vitro with interchangeable redox centers for nanometer-scale photochemical charge separation. Transient absorption spectroscopy demonstrates Photosystem II-like tyrosine and metal cluster oxidation, and we measure charge separation lifetimes exceeding 100 ms, ideal for light-activated catalysis. This de novo-designed reaction center builds upon engineering guidelines established for charge separation in earlier synthetic photochemical triads and modified natural proteins, and it shows how synthetic biology may lead to a new generation of genetically encoded, light-powered catalysts for solar fuel production.

Suggested Citation

  • Nathan M. Ennist & Zhenyu Zhao & Steven E. Stayrook & Bohdana M. Discher & P. Leslie Dutton & Christopher C. Moser, 2022. "De novo protein design of photochemical reaction centers," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-32710-5
    DOI: 10.1038/s41467-022-32710-5
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    References listed on IDEAS

    as
    1. Christopher C. Page & Christopher C. Moser & Xiaoxi Chen & P. Leslie Dutton, 1999. "Natural engineering principles of electron tunnelling in biological oxidation–reduction," Nature, Nature, vol. 402(6757), pages 47-52, November.
    2. L. Kálmán & R. LoBrutto & J. P. Allen & J. C. Williams, 1999. "Modified reaction centres oxidize tyrosine in reactions that mirror photosystem II," Nature, Nature, vol. 402(6762), pages 696-699, December.
    3. Lorna A. Malone & Pu Qian & Guy E. Mayneord & Andrew Hitchcock & David A. Farmer & Rebecca F. Thompson & David J. K. Swainsbury & Neil A. Ranson & C. Neil Hunter & Matthew P. Johnson, 2019. "Cryo-EM structure of the spinach cytochrome b6 f complex at 3.6 Å resolution," Nature, Nature, vol. 575(7783), pages 535-539, November.
    4. Jan Kern & Ruchira Chatterjee & Iris D. Young & Franklin D. Fuller & Louise Lassalle & Mohamed Ibrahim & Sheraz Gul & Thomas Fransson & Aaron S. Brewster & Roberto Alonso-Mori & Rana Hussein & Miao Zh, 2018. "Structures of the intermediates of Kok’s photosynthetic water oxidation clock," Nature, Nature, vol. 563(7731), pages 421-425, November.
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