De novo protein design of photochemical reaction centers

Ennist, Nathan M.; Zhao, Zhenyu; Stayrook, Steven E.; Discher, Bohdana M.; Dutton, P. Leslie; Moser, Christopher C.

doi:10.1038/s41467-022-32710-5

Title: De novo protein design of photochemical reaction centers

Journal Article · 22 August 2022 · Nature Communications

DOI: https://doi.org/10.1038/s41467-022-32710-5 · OSTI ID:1882990

; Zhao, Zhenyu;

; Discher, Bohdana M.; Dutton, P. Leslie; Moser, Christopher C.

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.

View Journal Article

Cite

Export

Save

Research Organization:: Washington University, St. Louis, MO (United States)

Sponsoring Organization:: USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: SC0001035

OSTI ID:: 1882990

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 13; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (69)

Enhanced Photoinduced Electron Transfer Through a Tyrosine Relay in a De Novo Designed Protein Scaffold Bearing a Photoredox Unit and a Fe ^II S ₄ Site Tebo, Alison; Quaranta, Annamaria; Pecoraro, Vincent L. ChemPhotoChem, Vol. 5, Issue 7 https://doi.org/10.1002/cptc.202100014	journal	April 2021
Spectroscopic and metal-binding properties of DF3: an artificial protein able to accommodate different metal ions Torres Martin de Rosales, Rafael; Faiella, Marina; Farquhar, Erik JBIC Journal of Biological Inorganic Chemistry, Vol. 15, Issue 5 https://doi.org/10.1007/s00775-010-0639-9	journal	March 2010
Biochemistry without oxygen Englander, S. Walter; Calhoun, Dorothy B.; Englander, Joan J. Analytical Biochemistry, Vol. 161, Issue 2 https://doi.org/10.1016/0003-2697(87)90454-4	journal	March 1987
Simultaneous determination of hemes a, b, and c from pyridine hemochrome spectra Berry, Edward A.; Trumpower, Bernard L. Analytical Biochemistry, Vol. 161, Issue 1 https://doi.org/10.1016/0003-2697(87)90643-9	journal	February 1987
Radical-pair energetics and decay mechanisms in reaction centers containing anthraquinones, naphthoquinones or benzoquinones in place of ubiquinone Woodbury, Neal W.; Parson, William W.; Gunner, Marilyn R. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 851, Issue 1 https://doi.org/10.1016/0005-2728(86)90243-4	journal	August 1986
[8] Singular value decomposition: Application to analysis of experimental data Henry, E. R.; Hofrichter, J. Methods in Enzymology https://doi.org/10.1016/0076-6879(92)10010-B	book	January 1992
Electrochemical and spectroelectrochemical studies on cobalt myoglobin Li, Chen-zhong; Nishiyama, Katsuhiko; Taniguchi, Isao Electrochimica Acta, Vol. 45, Issue 18 https://doi.org/10.1016/S0013-4686(00)00363-7	journal	June 2000
Redox potentiometry: Determination of midpoint potentials of oxidation-reduction components of biological electron-transfer systems Leslie Dutton, P. Methods in Enzymology https://doi.org/10.1016/S0076-6879(78)54026-3	book	January 1978
Photo-catalytic oxidation of a di-nuclear manganese centre in an engineered bacterioferritin ‘reaction centre’ Conlan, Brendon; Cox, Nicholas; Su, Ji-Hu Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1787, Issue 9 https://doi.org/10.1016/j.bbabio.2009.04.011	journal	September 2009
Guidelines for tunneling in enzymes Moser, Christopher C.; Anderson, J. L. Ross; Dutton, P. Leslie Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1797, Issue 9 https://doi.org/10.1016/j.bbabio.2010.04.441	journal	September 2010
Photo-oxidation of tyrosine in a bio-engineered bacterioferritin ‘reaction centre’—A protein model for artificial photosynthesis Hingorani, Kastoori; Pace, Ron; Whitney, Spencer Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 10 https://doi.org/10.1016/j.bbabio.2014.07.019	journal	October 2014
Reengineering cyt b562 for hydrogen production: A facile route to artificial hydrogenases Sommer, Dayn Joseph; Vaughn, Michael David; Clark, Brett Colby Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1857, Issue 5 https://doi.org/10.1016/j.bbabio.2015.09.001	journal	May 2016
Analysis and Design of Turns in α-Helical Hairpins Lahr, Steven J.; Engel, Donald E.; Stayrook, Steven E. Journal of Molecular Biology, Vol. 346, Issue 5 https://doi.org/10.1016/j.jmb.2004.12.016	journal	March 2005
The ascent of man(made oxidoreductases) Grayson, Katie J.; Anderson, JL Ross Current Opinion in Structural Biology, Vol. 51 https://doi.org/10.1016/j.sbi.2018.04.008	journal	August 2018
Evolution of Photochemical Reaction Centres: More Twists? Cardona, Tanai; Rutherford, A. William Trends in Plant Science, Vol. 24, Issue 11 https://doi.org/10.1016/j.tplants.2019.06.016	journal	November 2019
De Novo Design of Four-Helix Bundle Metalloproteins: One Scaffold, Diverse Reactivities Lombardi, Angela; Pirro, Fabio; Maglio, Ornella Accounts of Chemical Research https://doi.org/10.1021/acs.accounts.8b00674	journal	April 2019
Binding and Energetics of Electron Transfer between an Artificial Four-Helix Mn-Protein and Reaction Centers from Rhodobacter sphaeroides Espiritu, Eduardo; Olson, Tien L.; Williams, JoAnn C. Biochemistry, Vol. 56, Issue 49 https://doi.org/10.1021/acs.biochem.7b00978	journal	November 2017
Semisynthetic and Biomolecular Hydrogen Evolution Catalysts Kandemir, Banu; Chakraborty, Saikat; Guo, Yixing Inorganic Chemistry, Vol. 55, Issue 2 https://doi.org/10.1021/acs.inorgchem.5b02054	journal	November 2015
Formation of porphyrin .pi. cation radical in zinc-substituted horseradish peroxidase Kaneko, Yoshiaki; Tamura, Mamoru; Yamazaki, Isao Biochemistry, Vol. 19, Issue 25 https://doi.org/10.1021/bi00566a020	journal	December 1980
Design of a Redox-Linked Active Metal Site: Manganese Bound to Bacterial Reaction Centers at a Site Resembling That of Photosystem II ^† ^, ^‡ Thielges, M.; Uyeda, G.; Cámara-Artigas, A. Biochemistry, Vol. 44, Issue 20 https://doi.org/10.1021/bi050377n	journal	May 2005
Wiring an [FeFe]-Hydrogenase with Photosystem I for Light-Induced Hydrogen Production Lubner, Carolyn E.; Knörzer, Philipp; Silva, Paulo J. N. Biochemistry, Vol. 49, Issue 48 https://doi.org/10.1021/bi1016167	journal	December 2010
Biochemistry and Theory of Proton-Coupled Electron Transfer Migliore, Agostino; Polizzi, Nicholas F.; Therien, Michael J. Chemical Reviews, Vol. 114, Issue 7 https://doi.org/10.1021/cr4006654	journal	January 2014
Modulating Charge Separation and Charge Recombination Dynamics in Porphyrin−Fullerene Linked Dyads and Triads: Marcus-Normal versus Inverted Region Imahori, Hiroshi; Tamaki, Koichi; Guldi, Dirk M. Journal of the American Chemical Society, Vol. 123, Issue 11 https://doi.org/10.1021/ja003346i	journal	March 2001
Blue Ferrocenium Azurin: An Organometalloprotein with Tunable Redox Properties Hwang, Hee Jung; Carey, James R.; Brower, Evan T. Journal of the American Chemical Society, Vol. 127, Issue 44 https://doi.org/10.1021/ja054983h	journal	October 2005
De Novo Design of a Single-Chain Diphenylporphyrin Metalloprotein Bender, Gretchen M.; Lehmann, Andreas; Zou, Hongling Journal of the American Chemical Society, Vol. 129, Issue 35 https://doi.org/10.1021/ja071199j	journal	September 2007
Nature-Driven Photochemistry for Catalytic Solar Hydrogen Production: A Photosystem I–Transition Metal Catalyst Hybrid Utschig, Lisa M.; Silver, Sunshine C.; Mulfort, Karen L. Journal of the American Chemical Society, Vol. 133, Issue 41 https://doi.org/10.1021/ja206012r	journal	October 2011
Engineering the Assembly of Heme Cofactors in Man-Made Proteins Solomon, Lee A.; Kodali, Goutham; Moser, Christopher C. Journal of the American Chemical Society, Vol. 136, Issue 8 https://doi.org/10.1021/ja411845f	journal	February 2014
Using α-Helical Coiled-Coils to Design Nanostructured Metalloporphyrin Arrays McAllister, Karen A.; Zou, Hongling; Cochran, Frank V. Journal of the American Chemical Society, Vol. 130, Issue 36 https://doi.org/10.1021/ja800697g	journal	September 2008
Design, Synthesis, and Properties of a Novel Cytochrome b Model Rau, Harald K.; Haehnel, Wolfgang Journal of the American Chemical Society, Vol. 120, Issue 3 https://doi.org/10.1021/ja973018r	journal	January 1998
Wiring of Photosystem II to Hydrogenase for Photoelectrochemical Water Splitting Mersch, Dirk; Lee, Chong-Yong; Zhang, Jenny Zhenqi Journal of the American Chemical Society, Vol. 137, Issue 26 https://doi.org/10.1021/jacs.5b03737	journal	June 2015
Nature of biological electron transfer Moser, Christopher C.; Keske, Jonathan M.; Warncke, Kurt Nature, Vol. 355, Issue 6363 https://doi.org/10.1038/355796a0	journal	February 1992
Design and synthesis of multi-haem proteins Robertson, Dan E.; Farid, Ramy S.; Moser, Christopher C. Nature, Vol. 368, Issue 6470, p. 425-432 https://doi.org/10.1038/368425a0	journal	March 1994
Modified reaction centres oxidize tyrosine in reactions that mirror photosystem II Kálmán, L.; LoBrutto, R.; Allen, J. P. Nature, Vol. 402, Issue 6762 https://doi.org/10.1038/45300	journal	December 1999
Natural engineering principles of electron tunnelling in biological oxidation–reduction Page, Christopher C.; Moser, Christopher C.; Chen, Xiaoxi Nature, Vol. 402, Issue 6757 https://doi.org/10.1038/46972	journal	November 1999
A bioinspired redox relay that mimics radical interactions of the Tyr–His pairs of photosystem II Megiatto Jr, Jackson D.; Méndez-Hernández, Dalvin D.; Tejeda-Ferrari, Marely E. Nature Chemistry, Vol. 6, Issue 5 https://doi.org/10.1038/nchem.1862	journal	February 2014
De novo design of a hyperstable non-natural protein–ligand complex with sub-Å accuracy Polizzi, Nicholas F.; Wu, Yibing; Lemmin, Thomas Nature Chemistry, Vol. 9, Issue 12 https://doi.org/10.1038/nchem.2846	journal	August 2017
Elementary tetrahelical protein design for diverse oxidoreductase functions Farid, Tammer A.; Kodali, Goutham; Solomon, Lee A. Nature Chemical Biology, Vol. 9, Issue 12 https://doi.org/10.1038/nchembio.1362	journal	October 2013
An artificial di-iron oxo-protein with phenol oxidase activity Faiella, Marina; Andreozzi, Concetta; de Rosales, Rafael Torres Martin Nature Chemical Biology, Vol. 5, Issue 12 https://doi.org/10.1038/nchembio.257	journal	November 2009
Structures of the intermediates of Kok’s photosynthetic water oxidation clock Kern, Jan; Chatterjee, Ruchira; Young, Iris D. Nature, Vol. 563, Issue 7731 https://doi.org/10.1038/s41586-018-0681-2	journal	November 2018
Cryo-EM structure of the spinach cytochrome b6 f complex at 3.6 Å resolution Malone, Lorna A.; Qian, Pu; Mayneord, Guy E. Nature, Vol. 575, Issue 7783 https://doi.org/10.1038/s41586-019-1746-6	journal	November 2019
Aqueous light driven hydrogen production by a Ru–ferredoxin–Co biohybrid Soltau, S. R.; Niklas, J.; Dahlberg, P. D. Chemical Communications, Vol. 51, Issue 53 https://doi.org/10.1039/C5CC03006D	journal	January 2015
Design and engineering of water-soluble light-harvesting protein maquettes Kodali, Goutham; Mancini, Joshua A.; Solomon, Lee A. Chemical Science, Vol. 8, Issue 1 https://doi.org/10.1039/C6SC02417C	journal	January 2017
Tunneling in PSII Moser, Christopher C.; Page, Christopher C.; Leslie Dutton, P. Photochemical & Photobiological Sciences, Vol. 4, Issue 12 https://doi.org/10.1039/b507352a	journal	January 2005
637. The stability of transition-metal complexes Irving, H.; Williams, R. J. P. Journal of the Chemical Society (Resumed), Vol. 0, Issue 0, p. 3192-3210 https://doi.org/10.1039/jr9530003192	journal	January 1953
Engineering oxidoreductases: maquette proteins designed from scratch Lichtenstein, Bruce R.; Farid, Tammer A.; Kodali, Goutham Biochemical Society Transactions, Vol. 40, Issue 3 https://doi.org/10.1042/BST20120067	journal	May 2012
Reversible voltammograms and a Pourbaix diagram for a protein tyrosine radical Berry, B. W.; Martinez-Rivera, M. C.; Tommos, C. Proceedings of the National Academy of Sciences, Vol. 109, Issue 25 https://doi.org/10.1073/pnas.1112057109	journal	June 2012
Allosteric cooperation in a de novo-designed two-domain protein Pirro, Fabio; Schmidt, Nathan; Lincoff, James Proceedings of the National Academy of Sciences, Vol. 117, Issue 52 https://doi.org/10.1073/pnas.2017062117	journal	December 2020
D1-Asn-298 in photosystem II is involved in a hydrogen-bond network near the redox-active tyrosine Y _Z for proton exit during water oxidation Nagao, Ryo; Ueoka-Nakanishi, Hanayo; Noguchi, Takumi Journal of Biological Chemistry, Vol. 292, Issue 49 https://doi.org/10.1074/jbc.M117.815183	journal	October 2017
Requirement for Asn298 on D1 Protein for Oxygen Evolution: Analyses by Exhaustive Amino Acid Substitution in the Green Alga Chlamydomonas reinhardtii Kuroda, Hiroshi; Kodama, Natsumi; Sun, Xiao-Yu Plant and Cell Physiology, Vol. 55, Issue 7 https://doi.org/10.1093/pcp/pcu073	journal	May 2014
From natural to artificial photosynthesis Barber, James; Tran, Phong D. Journal of The Royal Society Interface, Vol. 10, Issue 81 https://doi.org/10.1098/rsif.2012.0984	journal	April 2013
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
Model bias in macromolecular crystal structures Hodel, A.; Kim, S. H.; Brünger, A. T. Acta Crystallographica Section A Foundations of Crystallography, Vol. 48, Issue 6 https://doi.org/10.1107/S0108767392006044	journal	November 1992
Maximum-likelihood density modification Terwilliger, Thomas C. Acta Crystallographica Section D Biological Crystallography, Vol. 56, Issue 8 https://doi.org/10.1107/S0907444900005072	journal	August 2000
REFMAC 5 dictionary: organization of prior chemical knowledge and guidelines for its use Vagin, Alexei A.; Steiner, Roberto A.; Lebedev, Andrey A. Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12 https://doi.org/10.1107/S0907444904023510	journal	November 2004
Scaling and assessment of data quality Evans, Philip Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 1, p. 72-82 https://doi.org/10.1107/S0907444905036693	journal	December 2005
Iterative-build OMIT maps: map improvement by iterative model building and refinement without model bias Terwilliger, Thomas C.; Grosse-Kunstleve, Ralf W.; Afonine, Pavel V. Acta Crystallographica Section D Biological Crystallography, Vol. 64, Issue 5 https://doi.org/10.1107/S0907444908004319	journal	April 2008
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
Overview of the CCP 4 suite and current developments Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910045749	journal	March 2011
Towards automated crystallographic structure refinement with phenix.refine Afonine, Pavel V.; Grosse-Kunstleve, Ralf W.; Echols, Nathaniel Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 4 https://doi.org/10.1107/S0907444912001308	journal	March 2012
Automated MAD and MIR structure solution Terwilliger, Thomas C.; Berendzen, Joel Acta Crystallographica Section D Biological Crystallography, Vol. 55, Issue 4 https://doi.org/10.1107/S0907444999000839	journal	April 1999
The PDB_REDO server for macromolecular structure model optimization Joosten, Robbie P.; Long, Fei; Murshudov, Garib N. IUCrJ, Vol. 1, Issue 4 https://doi.org/10.1107/S2052252514009324	journal	May 2014
Polder maps: improving OMIT maps by excluding bulk solvent Liebschner, Dorothee; Afonine, Pavel V.; Moriarty, Nigel W. Acta Crystallographica Section D Structural Biology, Vol. 73, Issue 2, p. 148-157 https://doi.org/10.1107/S2059798316018210	journal	February 2017
Macromolecular structure determination using X-rays, neutrons and electrons: recent developments in Phenix Liebschner, Dorothee; Afonine, Pavel V.; Baker, Matthew L. Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 10 https://doi.org/10.1107/S2059798319011471	journal	October 2019
Comparing Photosynthetic and Photovoltaic Efficiencies and Recognizing the Potential for Improvement Blankenship, R. E.; Tiede, D. M.; Barber, J. Science, Vol. 332, Issue 6031, p. 805-809 https://doi.org/10.1126/science.1200165	journal	May 2011
Photosystem II: The Reaction Center of Oxygenic Photosynthesis Vinyard, David J.; Ananyev, Gennady M.; Charles Dismukes, G. Annual Review of Biochemistry, Vol. 82, Issue 1 https://doi.org/10.1146/annurev-biochem-070511-100425	journal	June 2013
Progress Toward a Molecular Mechanism of Water Oxidation in Photosystem II Vinyard, David J.; Brudvig, Gary W. Annual Review of Physical Chemistry, Vol. 68, Issue 1 https://doi.org/10.1146/annurev-physchem-052516-044820	journal	May 2017
Light-driven Hydrogen Production by a Hybrid Complex of a [NiFe]-Hydrogenase and the Cyanobacterial Photosystem I Ihara, Masaki; Nishihara, Hirofumi; Yoon, Ki-Seok Photochemistry and Photobiology, Vol. 82, Issue 3 https://doi.org/10.1562/2006-01-16-RA-778	journal	January 2006

Similar Records

De novo design of proteins housing excitonically coupled chlorophyll special pairs

Journal Article · 2024 · Nature Chemical Biology · OSTI ID:2468711

Ennist, Nathan M.; Wang, Shunzhi; Kennedy, Madison A.; +28 more

Rational design of photosynthetic reaction center protein maquettes

Journal Article · 2022 · Frontiers in Molecular Biosciences · OSTI ID:1888591

Ennist, Nathan M.; Stayrook, Steven E.; Dutton, P. Leslie; +1 more

Multistep photoinduced electron transfer in a de Novo helix bundle: Multimer self-assembly of peptide chains including a chromophore special pair

Journal Article · 2000 · Journal of the American Chemical Society · OSTI ID:20017331

Jones, G II; Vullev, V; Braswell, E H; +1 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
photobiology
protein design
x-ray crystallography

Title: De novo protein design of photochemical reaction centers

Citation Formats

References (69)

Similar Records

Related Subjects