IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-32710-5.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-32710-5
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-32710-5?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Rana Hussein & Mohamed Ibrahim & Asmit Bhowmick & Philipp S. Simon & Ruchira Chatterjee & Louise Lassalle & Margaret Doyle & Isabel Bogacz & In-Sik Kim & Mun Hon Cheah & Sheraz Gul & Casper Lichtenber, 2021. "Structural dynamics in the water and proton channels of photosystem II during the S2 to S3 transition," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    2. Fangzhu Han & Yiqi Hu & Mengchen Wu & Zhaoxiang He & Hongtao Tian & Long Zhou, 2023. "Structures of Tetrahymena thermophila respiratory megacomplexes on the tubular mitochondrial cristae," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    3. Ralf Steinhilper & Gabriele Höff & Johann Heider & Bonnie J. Murphy, 2022. "Structure of the membrane-bound formate hydrogenlyase complex from Escherichia coli," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    4. Yeonhwa Yu & Yongfan Shi & Young Wan Kwon & Yoobin Choi & Yusik Kim & Jeong-Geol Na & June Huh & Jeewon Lee, 2024. "A rationally designed miniature of soluble methane monooxygenase enables rapid and high-yield methanol production in Escherichia coli," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    5. Anuj Kumar & Florian Kremp & Jennifer Roth & Sven A. Freibert & Volker Müller & Jan M. Schuller, 2023. "Molecular architecture and electron transfer pathway of the Stn family transhydrogenase," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    6. Jiashen Zhou & Lin Zhang & Liping Zeng & Lu Yu & Yuanyuan Duan & Siqi Shen & Jingyan Hu & Pan Zhang & Wenyan Song & Xiaoxue Ruan & Jing Jiang & Yinan Zhang & Lu Zhou & Jia Jia & Xudong Hang & Changlin, 2021. "Helicobacter pylori FabX contains a [4Fe-4S] cluster essential for unsaturated fatty acid synthesis," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    7. Lorenzo Cimmino & Américo G. Duarte & Dongchun Ni & Babatunde E. Ekundayo & Inês A. C. Pereira & Henning Stahlberg & Christof Holliger & Julien Maillard, 2023. "Structure of a membrane-bound menaquinol:organohalide oxidoreductase," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    8. Xiaofeng Cui & Hui Bai & Jun Zhang & Rong Liu & Haiyan Yu & Yangxiang Wang & Tingting Kong & Mei-Yan Gao & Zhou Lu & Yujie Xiong, 2024. "A cluster-nanozyme-coenzyme system mimicking natural photosynthesis for CO2 reduction under intermittent light irradiation," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    9. Jun-ichi Kishikawa & Moe Ishikawa & Takahiro Masuya & Masatoshi Murai & Yuki Kitazumi & Nicole L. Butler & Takayuki Kato & Blanca Barquera & Hideto Miyoshi, 2022. "Cryo-EM structures of Na+-pumping NADH-ubiquinone oxidoreductase from Vibrio cholerae," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    10. Omar Sandoval-Ibáñez & David Rolo & Rabea Ghandour & Alexander P. Hertle & Tegan Armarego-Marriott & Arun Sampathkumar & Reimo Zoschke & Ralph Bock, 2022. "De-etiolation-induced protein 1 (DEIP1) mediates assembly of the cytochrome b6f complex in Arabidopsis," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    11. Suk Min Kim & Sung Heuck Kang & Jinhee Lee & Yoonyoung Heo & Eleni G. Poloniataki & Jingu Kang & Hye-Jin Yoon & So Yeon Kong & Yaejin Yun & Hyunwoo Kim & Jungki Ryu & Hyung Ho Lee & Yong Hwan Kim, 2024. "Identifying a key spot for electron mediator-interaction to tailor CO dehydrogenase’s affinity," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    12. Pushan Bag & Tatyana Shutova & Dmitry Shevela & Jenna Lihavainen & Sanchali Nanda & Alexander G. Ivanov & Johannes Messinger & Stefan Jansson, 2023. "Flavodiiron-mediated O2 photoreduction at photosystem I acceptor-side provides photoprotection to conifer thylakoids in early spring," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    13. Daniel Riepl & Ana P. Gamiz-Hernandez & Terezia Kovalova & Sylwia M. Król & Sophie L. Mader & Dan Sjöstrand & Martin Högbom & Peter Brzezinski & Ville R. I. Kaila, 2024. "Long-range charge transfer mechanism of the III2IV2 mycobacterial supercomplex," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    14. Emanuela Gatto & Raffaella Lettieri & Luigi Vesce & Mariano Venanzi, 2022. "Peptide Materials in Dye Sensitized Solar Cells," Energies, MDPI, vol. 15(15), pages 1-13, August.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-32710-5. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.