Engineered Enzymes and Bioinspired Catalysts for Energy Conversion

Le, Jennifer M.; Bren, Kara L.

doi:10.1021/acsenergylett.9b01308

Title: Engineered Enzymes and Bioinspired Catalysts for Energy Conversion

Journal Article · Mon Aug 05 00:00:00 EDT 2019 · ACS Energy Letters

DOI:https://doi.org/10.1021/acsenergylett.9b01308· OSTI ID:1558717

Le, Jennifer M. ^[1];

^[1]

Department of Chemistry, University of Rochester, Rochester, New York 14627, United States

Metalloenzymes play critical roles in the environment by catalyzing redox reactions in biogeochemical cycles. The elucidation of structure–function relationships in these biocatalysts has provided a foundation for the development of bioinspired catalysts for fuel production and small-molecule activation. In this Perspective, we highlight developments in engineered biomolecular and bioinspired catalysts for the reduction of H⁺, O₂, and CO₂ and for the oxidation of H₂ and H₂O. The roles of proton transfers and second-sphere interactions in particular are highlighted.

View Journal Article

Cite

Export

Save

Research Organization:: Univ. of Rochester, NY (United States)

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

Grant/Contract Number:: FG02-09ER16121; SC0002106

OSTI ID:: 1558717

Alternate ID(s):: OSTI ID: 1561994

Journal Information:: ACS Energy Letters, Journal Name: ACS Energy Letters Vol. 4 Journal Issue: 9; ISSN 2380-8195

Publisher:: American Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 46 works

Citation information provided by
Web of Science

References (96)

Original Design of an Oxygen-Tolerant [NiFe] Hydrogenase: Major Effect of a Valine-to-Cysteine Mutation near the Active Site Liebgott, Pierre-Pol; de Lacey, Antonio L.; Burlat, Bénédicte Journal of the American Chemical Society, Vol. 133, Issue 4 https://doi.org/10.1021/ja108787s	journal	February 2011
Photosystem II repair in plant chloroplasts — Regulation, assisting proteins and shared components with photosystem II biogenesis Järvi, Sari; Suorsa, Marjaana; Aro, Eva-Mari Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1847, Issue 9 https://doi.org/10.1016/j.bbabio.2015.01.006	journal	September 2015
A biosynthetic model of cytochrome c oxidase as an electrocatalyst for oxygen reduction Mukherjee, Sohini; Mukherjee, Arnab; Bhagi-Damodaran, Ambika Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms9467	journal	October 2015
Why copper is preferred over iron for oxygen activation and reduction in haem-copper oxidases Bhagi-Damodaran, Ambika; Michael, Matthew A.; Zhu, Qianhong Nature Chemistry, Vol. 9, Issue 3 https://doi.org/10.1038/nchem.2643	journal	November 2016
Electrochemical Hydrogen Evolution by Cobalt (II) Porphyrins: Effects of Ligand Modification on Catalytic Activity, Efficiency and Overpotential Beyene, Belete B.; Mane, Sandeep B.; Hung, Chen-Hsiung Journal of The Electrochemical Society, Vol. 165, Issue 9 https://doi.org/10.1149/2.0481809jes	journal	January 2018
[FeFe]- and [NiFe]-hydrogenase diversity, mechanism, and maturation Peters, John W.; Schut, Gerrit J.; Boyd, Eric S. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1853, Issue 6 https://doi.org/10.1016/j.bbamcr.2014.11.021	journal	June 2015
[NiFe] and [FeFe] Hydrogenases Studied by Advanced Magnetic Resonance Techniques Lubitz, Wolfgang; Reijerse, Eduard; van Gastel, Maurice Chemical Reviews, Vol. 107, Issue 10 https://doi.org/10.1021/cr050186q	journal	October 2007
Nitrogenase: A Draft Mechanism Hoffman, Brian M.; Lukoyanov, Dmitriy; Dean, Dennis R. Accounts of Chemical Research, Vol. 46, Issue 2 https://doi.org/10.1021/ar300267m	journal	December 2012
Role of pendant proton relays and proton-coupled electron transfer on the hydrogen evolution reaction by nickel hangman porphyrins Bediako, D. Kwabena; Solis, Brian H.; Dogutan, Dilek K. Proceedings of the National Academy of Sciences, Vol. 111, Issue 42 https://doi.org/10.1073/pnas.1414908111	journal	October 2014
Copper Hydroperoxo Species Activated by Hydrogen-Bonding Interaction with Its Distal Oxygen Yamaguchi, Syuhei; Nagatomo, Shigenori; Kitagawa, Teizo Inorganic Chemistry, Vol. 42, Issue 22 https://doi.org/10.1021/ic035080x	journal	November 2003
Designing electrochemically reversible H2 oxidation and production catalysts Dutta, Arnab; Appel, Aaron M.; Shaw, Wendy J. Nature Reviews Chemistry, Vol. 2, Issue 9 https://doi.org/10.1038/s41570-018-0032-8	journal	August 2018
A comprehensive review of Pt electrocatalysts for the oxygen reduction reaction: Nanostructure, activity, mechanism and carbon support in PEM fuel cells Sui, Sheng; Wang, Xiaoying; Zhou, Xintong Journal of Materials Chemistry A, Vol. 5, Issue 5 https://doi.org/10.1039/C6TA08580F	journal	January 2017
Oxygen activation by cytochrome P450 monooxygenase Hamdane, Djemel; Zhang, Haoming; Hollenberg, Paul Photosynthesis Research, Vol. 98, Issue 1-3 https://doi.org/10.1007/s11120-008-9322-1	journal	July 2008
Structural changes in the Mn4Ca cluster and the mechanism of photosynthetic water splitting Pushkar, Y.; Yano, J.; Sauer, K. Proceedings of the National Academy of Sciences, Vol. 105, Issue 6 https://doi.org/10.1073/pnas.0707092105	journal	February 2008
Protein secondary-shell interactions enhance the photoinduced hydrogen production of cobalt protoporphyrin IX Sommer, Dayn Joseph; Vaughn, Michael David; Ghirlanda, Giovanna Chem. Commun., Vol. 50, Issue 100 https://doi.org/10.1039/C4CC06700B	journal	January 2014
Hydrogen Evolution Catalyzed by Cobaloximes Dempsey, Jillian L.; Brunschwig, Bruce S.; Winkler, Jay R. Accounts of Chemical Research, Vol. 42, Issue 12 https://doi.org/10.1021/ar900253e	journal	December 2009
Investigating the Kinetic Mechanisms of the Oxygen Reduction Reaction in a Nonaqueous Solvent Galiote, Nelson A.; de Azevedo, Dayse C.; Oliveira, Osvaldo N. The Journal of Physical Chemistry C, Vol. 118, Issue 38 https://doi.org/10.1021/jp5053584	journal	September 2014
Dioxygen activation and bond cleavage by mixed-valence cytochrome c oxidase Proshlyakov, D. A.; Pressler, M. A.; Babcock, G. T. Proceedings of the National Academy of Sciences, Vol. 95, Issue 14 https://doi.org/10.1073/pnas.95.14.8020	journal	July 1998
Redox Reactivity of a Mononuclear Manganese-Oxo Complex Binding Calcium Ion and Other Redox-Inactive Metal Ions Sankaralingam, Muniyandi; Lee, Yong-Min; Pineda-Galvan, Yuliana Journal of the American Chemical Society, Vol. 141, Issue 3 https://doi.org/10.1021/jacs.8b11492	journal	December 2018
Pendant Hydrogen-Bond Donors in Cobalt Catalysts Independently Enhance CO ₂ Reduction Chapovetsky, Alon; Welborn, Matthew; Luna, John M. ACS Central Science, Vol. 4, Issue 3 https://doi.org/10.1021/acscentsci.7b00607	journal	February 2018
Electronic Structure Analysis of the Oxygen-Activation Mechanism by Fe ^II - and α-Ketoglutarate (αKG)-Dependent Dioxygenases Ye, Shengfa; Riplinger, Christoph; Hansen, Andreas Chemistry - A European Journal, Vol. 18, Issue 21 https://doi.org/10.1002/chem.201102829	journal	April 2012
A pendant proton shuttle on [Fe ₄ N(CO) ₁₂ ] ⁻ alters product selectivity in formate vs. H ₂ production via the hydride [H–Fe ₄ N(CO) ₁₂ ] ⁻ Loewen, Natalia D.; Thompson, Emily J.; Kagan, Michael Chemical Science, Vol. 7, Issue 4 https://doi.org/10.1039/C5SC03169A	journal	January 2016
Artificial Metalloproteins Containing Co ₄ O ₄ Cubane Active Sites Olshansky, Lisa; Huerta-Lavorie, Raúl; Nguyen, Andy I. Journal of the American Chemical Society, Vol. 140, Issue 8 https://doi.org/10.1021/jacs.7b13052	journal	February 2018
Structure and Valency of a Cobalt−Phosphate Water Oxidation Catalyst Determined by in Situ X-ray Spectroscopy Kanan, Matthew W.; Yano, Junko; Surendranath, Yogesh Journal of the American Chemical Society, Vol. 132, Issue 39 https://doi.org/10.1021/ja1023767	journal	October 2010
Tetranuclear Manganese Models of the OEC Displaying Hydrogen Bonding Interactions: Application to Electrocatalytic Water Oxidation to Hydrogen Peroxide Han, Zhiji; Horak, Kyle T.; Lee, Heui Beom Journal of the American Chemical Society, Vol. 139, Issue 27 https://doi.org/10.1021/jacs.7b03044	journal	June 2017
Frequency and potential dependence of reversible electrocatalytic hydrogen interconversion by [FeFe]-hydrogenases Pandey, Kavita; Islam, Shams T. A.; Happe, Thomas Proceedings of the National Academy of Sciences, Vol. 114, Issue 15 https://doi.org/10.1073/pnas.1619961114	journal	March 2017
Enhanced Oxygen-Tolerance of the Full Heterotrimeric Membrane-Bound [NiFe]-Hydrogenase of Ralstonia eutropha Radu, Valentin; Frielingsdorf, Stefan; Evans, Stephen D. Journal of the American Chemical Society, Vol. 136, Issue 24 https://doi.org/10.1021/ja503138p	journal	June 2014
Thermodynamic assessment of the oxygen reduction activity in aqueous solutions Tripkovic, Vladimir Physical Chemistry Chemical Physics, Vol. 19, Issue 43 https://doi.org/10.1039/C7CP05448C	journal	January 2017
Probing Protonation/Deprotonation of Tyrosine Residues in Cytochrome ba3 Oxidase from Thermus thermophilus by Time-resolved Step-scan Fourier Transform Infrared Spectroscopy Koutsoupakis, Constantinos; Kolaj-Robin, Olga; Soulimane, Tewfik Journal of Biological Chemistry, Vol. 286, Issue 35 https://doi.org/10.1074/jbc.M111.252213	journal	September 2011
The complex architecture of oxygenic photosynthesis Nelson, Nathan; Ben-Shem, Adam Nature Reviews Molecular Cell Biology, Vol. 5, Issue 12 https://doi.org/10.1038/nrm1525	journal	December 2004
Evaluating the role of acidic, basic, and polar amino acids and dipeptides on a molecular electrocatalyst for H ₂ oxidation Boralugodage, Nilusha Priyadarshani; Arachchige, Rajith Jayasingha; Dutta, Arnab Catalysis Science & Technology, Vol. 7, Issue 5 https://doi.org/10.1039/C6CY02579J	journal	January 2017
Structure of the catalytic, inorganic core of oxygen-evolving photosystem II at 1.9Å resolution Kawakami, Keisuke; Umena, Yasufumi; Kamiya, Nobuo Journal of Photochemistry and Photobiology B: Biology, Vol. 104, Issue 1-2 https://doi.org/10.1016/j.jphotobiol.2011.03.017	journal	July 2011
Structure of the 2 2 Ni-dependent CO dehydrogenase component of the Methanosarcina barkeri acetyl-CoA decarbonylase/synthase complex Gong, W.; Hao, B.; Wei, Z. Proceedings of the National Academy of Sciences, Vol. 105, Issue 28 https://doi.org/10.1073/pnas.0800415105	journal	July 2008
Carbonyl sulfide and carbon dioxide as new substrates, and carbon disulfide as a new inhibitor, of nitrogenase Seefeldt, Lance C.; Rasche, Madeline E.; Ensign, Scott A. Biochemistry, Vol. 34, Issue 16 https://doi.org/10.1021/bi00016a009	journal	April 1995
The superfamily of heme–copper oxygen reductases: Types and evolutionary considerations Sousa, Filipa L.; Alves, Renato J.; Ribeiro, Miguel A. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 4 https://doi.org/10.1016/j.bbabio.2011.09.020	journal	April 2012
Catalytic Reduction of Dioxygen to Water with a Monomeric Manganese Complex at Room Temperature Shook, Ryan L.; Peterson, Sonja M.; Greaves, John Journal of the American Chemical Society, Vol. 133, Issue 15 https://doi.org/10.1021/ja106564a	journal	April 2011
Mechanistic Insights into Catalytic H ₂ Oxidation by Ni Complexes Containing a Diphosphine Ligand with a Positioned Amine Base Yang, Jenny Y.; Bullock, R. Morris; Shaw, Wendy J. Journal of the American Chemical Society, Vol. 131, Issue 16 https://doi.org/10.1021/ja900483x	journal	April 2009
Amino acid modified Ni catalyst exhibits reversible H ₂ oxidation/production over a broad pH range at elevated temperatures Dutta, Arnab; DuBois, Daniel L.; Roberts, John A. S. Proceedings of the National Academy of Sciences, Vol. 111, Issue 46 https://doi.org/10.1073/pnas.1416381111	journal	November 2014
Electrocatalytic reduction of carbon dioxide by using macrocycles of nickel and cobalt Fisher, Barbara J.; Eisenberg, Richard Journal of the American Chemical Society, Vol. 102, Issue 24, p. 7361-7363 https://doi.org/10.1021/ja00544a035	journal	September 1980
Proton-Coupled Electron Transfer in Solution, Proteins, and Electrochemistry ^† Hammes-Schiffer, Sharon; Soudackov, Alexander V. The Journal of Physical Chemistry B, Vol. 112, Issue 45 https://doi.org/10.1021/jp805876e	journal	November 2008
Understanding the Role of the Essential Asp251 in Cytochrome P450cam Using Site-Directed Mutagenesis, Crystallography, and Kinetic Solvent Isotope Effect ^† Vidakovic, Momcilo; Sligar, Stephen G.; Li, Huiying Biochemistry, Vol. 37, Issue 26 https://doi.org/10.1021/bi980189f	journal	June 1998
Vanadium Nitrogenase Reduces CO Lee, C. C.; Hu, Y.; Ribbe, M. W. Science, Vol. 329, Issue 5992 https://doi.org/10.1126/science.1191455	journal	August 2010
Understanding and Tuning the Catalytic Bias of Hydrogenase Abou Hamdan, Abbas; Dementin, Sébastien; Liebgott, Pierre-Pol Journal of the American Chemical Society, Vol. 134, Issue 20 https://doi.org/10.1021/ja301802r	journal	May 2012
Hydrogenases Lubitz, Wolfgang; Ogata, Hideaki; Rüdiger, Olaf Chemical Reviews, Vol. 114, Issue 8 https://doi.org/10.1021/cr4005814	journal	March 2014
Molecular Catalysts for Water Oxidation Blakemore, James D.; Crabtree, Robert H.; Brudvig, Gary W. Chemical Reviews, Vol. 115, Issue 23 https://doi.org/10.1021/acs.chemrev.5b00122	journal	July 2015
A Photocatalyst–Enzyme Coupled Artificial Photosynthesis System for Solar Energy in Production of Formic Acid from CO ₂ Yadav, Rajesh K.; Baeg, Jin-Ook; Oh, Gyu Hwan Journal of the American Chemical Society, Vol. 134, Issue 28 https://doi.org/10.1021/ja3009902	journal	July 2012
Homogeneous Catalysis of Electrochemical Hydrogen Evolution by Iron(0) Porphyrins Bhugun, Iqbal; Lexa, Doris; Savéant, Jean-Michel Journal of the American Chemical Society, Vol. 118, Issue 16 https://doi.org/10.1021/ja954326x	journal	January 1996
Nickel phlorin intermediate formed by proton-coupled electron transfer in hydrogen evolution mechanism Solis, Brian H.; Maher, Andrew G.; Dogutan, Dilek K. Proceedings of the National Academy of Sciences, Vol. 113, Issue 3 https://doi.org/10.1073/pnas.1521834112	journal	December 2015
Damage Management in Water-Oxidizing Catalysts: From Photosystem II to Nanosized Metal Oxides Najafpour, Mohammad Mahdi; Fekete, Monika; Sedigh, Davood Jafarian ACS Catalysis, Vol. 5, Issue 3 https://doi.org/10.1021/cs5015157	journal	February 2015
Rational Design of Mononuclear Iron Porphyrins for Facile and Selective 4e ^– /4H ⁺ O ₂ Reduction: Activation of O–O Bond by 2nd Sphere Hydrogen Bonding Bhunia, Sarmistha; Rana, Atanu; Roy, Pronay Journal of the American Chemical Society, Vol. 140, Issue 30 https://doi.org/10.1021/jacs.8b02983	journal	July 2018
Photocatalytic hydrogen evolution by a diiron hydrogenase model based on a peptide fragment of cytochrome c556 with an attached diiron carbonyl cluster and an attached ruthenium photosensitizer Sano, Yohei; Onoda, Akira; Hayashi, Takashi Journal of Inorganic Biochemistry, Vol. 108 https://doi.org/10.1016/j.jinorgbio.2011.07.010	journal	March 2012
Oxygen Reduction by Homogeneous Molecular Catalysts and Electrocatalysts Pegis, Michael L.; Wise, Catherine F.; Martin, Daniel J. Chemical Reviews, Vol. 118, Issue 5 https://doi.org/10.1021/acs.chemrev.7b00542	journal	December 2017
Heme Enzyme Structure and Function Poulos, Thomas L. Chemical Reviews, Vol. 114, Issue 7 https://doi.org/10.1021/cr400415k	journal	January 2014
Hydrogen Generation by Hangman Metalloporphyrins Lee, Chang Hoon; Dogutan, Dilek K.; Nocera, Daniel G. Journal of the American Chemical Society, Vol. 133, Issue 23 https://doi.org/10.1021/ja202136y	journal	June 2011
Cobalt-catalyzed evolution of molecular hydrogen Connolly, Philip; Espenson, James H. Inorganic Chemistry, Vol. 25, Issue 16 https://doi.org/10.1021/ic00236a006	journal	July 1986
Oxygen-Tolerant H ₂ Production by [FeFe]-H ₂ ase Active Site Mimics Aided by Second Sphere Proton Shuttle Ahmed, Md Estak; Dey, Subal; Darensbourg, Marcetta Y. Journal of the American Chemical Society, Vol. 140, Issue 39 https://doi.org/10.1021/jacs.8b05983	journal	September 2018
From Myoglobin to Heme-Copper Oxidase: Design and Engineering of a Cu _B Center into Sperm Whale Myoglobin Sigman, Jeffrey A.; Kwok, Brian C.; Lu, Yi Journal of the American Chemical Society, Vol. 122, Issue 34 https://doi.org/10.1021/ja0015343	journal	August 2000
Hydrogen evolution from water catalyzed by cobalt-mimochrome VI*a, a synthetic mini-protein Firpo, Vincenzo; Le, Jennifer M.; Pavone, Vincenzo Chemical Science, Vol. 9, Issue 45 https://doi.org/10.1039/C8SC01948G	journal	January 2018
Hydrogen Evolution from Water under Aerobic Conditions Catalyzed by a Cobalt ATCUN Metallopeptide Kandemir, Banu; Kubie, Lenore; Guo, Yixing Inorganic Chemistry, Vol. 55, Issue 4 https://doi.org/10.1021/acs.inorgchem.5b02157	journal	January 2016
Design and engineering of artificial oxygen-activating metalloenzymes Nastri, Flavia; Chino, Marco; Maglio, Ornella Chemical Society Reviews, Vol. 45, Issue 18 https://doi.org/10.1039/C5CS00923E	journal	January 2016
Importance of the Protein Framework for Catalytic Activity of [FeFe]-Hydrogenases Knörzer, Philipp; Silakov, Alexey; Foster, Carina E. Journal of Biological Chemistry, Vol. 287, Issue 2 https://doi.org/10.1074/jbc.M111.305797	journal	November 2011
Peroxide Activation Regulated by Hydrogen Bonds within Artificial Cu Proteins Mann, Samuel I.; Heinisch, Tillmann; Ward, Thomas R. Journal of the American Chemical Society, Vol. 139, Issue 48 https://doi.org/10.1021/jacs.7b10452	journal	November 2017
Phenol-Induced O–O Bond Cleavage in a Low-Spin Heme–Peroxo–Copper Complex: Implications for O ₂ Reduction in Heme–Copper Oxidases Schaefer, Andrew W.; Kieber-Emmons, Matthew T.; Adam, Suzanne M. Journal of the American Chemical Society, Vol. 139, Issue 23 https://doi.org/10.1021/jacs.7b03292	journal	June 2017
A bioinspired soluble manganese cluster as a water oxidation electrocatalyst with low overpotential Maayan, Galia; Gluz, Naama; Christou, George Nature Catalysis, Vol. 1, Issue 1 https://doi.org/10.1038/s41929-017-0004-2	journal	November 2017
Oxygen-18 kinetic isotope effects in the dopamine .beta.-monooxygenase reaction: Evidence for a new chemical mechanism in non-heme, metallomonooxygenase Tian, Gaochao; Berry, Joseph A.; Klinman, Judith P. Biochemistry, Vol. 33, Issue 1 https://doi.org/10.1021/bi00167a030	journal	January 1994
Ammonia Binds to the Dangler Manganese of the Photosystem II Oxygen-Evolving Complex Oyala, Paul H.; Stich, Troy A.; Debus, Richard J. Journal of the American Chemical Society, Vol. 137, Issue 27 https://doi.org/10.1021/jacs.5b04768	journal	July 2015
Evaluation of Homogeneous Electrocatalysts by Cyclic Voltammetry Rountree, Eric S.; McCarthy, Brian D.; Eisenhart, Thomas T. Inorganic Chemistry, Vol. 53, Issue 19 https://doi.org/10.1021/ic500658x	journal	September 2014
Hydride Binding to the Active Site of [FeFe]-Hydrogenase Chernev, Petko; Lambertz, Camilla; Brünje, Annika Inorganic Chemistry, Vol. 53, Issue 22 https://doi.org/10.1021/ic502047q	journal	October 2014
Theoretical Analysis of Cobalt Hangman Porphyrins: Ligand Dearomatization and Mechanistic Implications for Hydrogen Evolution Solis, Brian H.; Maher, Andrew G.; Honda, Tatsuhiko ACS Catalysis, Vol. 4, Issue 12 https://doi.org/10.1021/cs501454y	journal	November 2014
Versatile Photocatalytic Systems for H ₂ Generation in Water Based on an Efficient DuBois-Type Nickel Catalyst Gross, Manuela A.; Reynal, Anna; Durrant, James R. Journal of the American Chemical Society, Vol. 136, Issue 1 https://doi.org/10.1021/ja410592d	journal	December 2013
An Iron Electrocatalyst for Selective Reduction of CO ₂ to Formate in Water: Including Thermochemical Insights Taheri, Atefeh; Thompson, Emily J.; Fettinger, James C. ACS Catalysis, Vol. 5, Issue 12 https://doi.org/10.1021/acscatal.5b01708	journal	November 2015
Structure, Function, and Mechanism of the Nickel Metalloenzymes, CO Dehydrogenase, and Acetyl-CoA Synthase Can, Mehmet; Armstrong, Fraser A.; Ragsdale, Stephen W. Chemical Reviews, Vol. 114, Issue 8 https://doi.org/10.1021/cr400461p	journal	February 2014
Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses Suga, Michihiro; Akita, Fusamichi; Hirata, Kunio Nature, Vol. 517, Issue 7532 https://doi.org/10.1038/nature13991	journal	November 2014
Hydrogen Evolution from Neutral Water under Aerobic Conditions Catalyzed by Cobalt Microperoxidase-11 Kleingardner, Jesse G.; Kandemir, Banu; Bren, Kara L. Journal of the American Chemical Society, Vol. 136, Issue 1 https://doi.org/10.1021/ja406818h	journal	December 2013
High-valent oxomanganese clusters: structural and mechanistic work relevant to the oxygen-evolving center in photosystem II Manchanda, Rajesh; Brudvig, Gary W.; Crabtree, Robert H. Coordination Chemistry Reviews, Vol. 144 https://doi.org/10.1016/0010-8545(95)01147-H	journal	October 1995
Proton-Coupled Electron Flow in Protein Redox Machines Dempsey, Jillian L.; Winkler, Jay R.; Gray, Harry B. Chemical Reviews, Vol. 110, Issue 12 https://doi.org/10.1021/cr100182b	journal	December 2010
The proton donor for OO bond scission by cytochrome c oxidase Gorbikova, E. A.; Belevich, I.; Wikstrom, M. Proceedings of the National Academy of Sciences, Vol. 105, Issue 31 https://doi.org/10.1073/pnas.0802512105	journal	July 2008
A Local Proton Source Enhances CO ₂ Electroreduction to CO by a Molecular Fe Catalyst Costentin, Cyrille; Drouet, Samuel; Robert, Marc Science, Vol. 338, Issue 6103 https://doi.org/10.1126/science.1224581	journal	October 2012
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
Amino Terminal Cu(II)- and Ni(II)-Binding (ATCUN) Motif of Proteins and Peptides: Metal Binding, DNA Cleavage, and Other Properties Harford, Catherine; Sarkar, Bibudhendra Accounts of Chemical Research, Vol. 30, Issue 3 https://doi.org/10.1021/ar9501535	journal	March 1997
Improved Electro- and Photocatalytic Water Reduction by Confined Cobalt Catalysts in Streptavidin Call, Arnau; Casadevall, Carla; Romero-Rivera, Adrian ACS Catalysis, Vol. 9, Issue 7 https://doi.org/10.1021/acscatal.8b04981	journal	May 2019
Proton-Assisted Reduction of CO ₂ by Cobalt Aminopyridine Macrocycles Chapovetsky, Alon; Do, Thomas H.; Haiges, Ralf Journal of the American Chemical Society, Vol. 138, Issue 18 https://doi.org/10.1021/jacs.6b01980	journal	April 2016
Hydrogen Oxidation and Production Using Nickel-Based Molecular Catalysts with Positioned Proton Relays Wilson, Aaron D.; Newell, Rachel H.; McNevin, Michael J. Journal of the American Chemical Society, Vol. 128, Issue 1 https://doi.org/10.1021/ja056442y	journal	January 2006
A Biomimetic Copper Water Oxidation Catalyst with Low Overpotential Zhang, Teng; Wang, Cheng; Liu, Shubin Journal of the American Chemical Society, Vol. 136, Issue 1 https://doi.org/10.1021/ja409267p	journal	December 2013
Nitrogenase reduction of carbon-containing compounds Seefeldt, Lance C.; Yang, Zhi-Yong; Duval, Simon Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 8-9 https://doi.org/10.1016/j.bbabio.2013.04.003	journal	August 2013
Pendant Acid–Base Groups in Molecular Catalysts: H-Bond Promoters or Proton Relays? Mechanisms of the Conversion of CO ₂ to CO by Electrogenerated Iron(0)Porphyrins Bearing Prepositioned Phenol Functionalities Costentin, Cyrille; Passard, Guillaume; Robert, Marc Journal of the American Chemical Society, Vol. 136, Issue 33 https://doi.org/10.1021/ja506193v	journal	August 2014
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
Microperoxidase 11: a model system for porphyrin networks and heme–protein interactions Verbaro, Daniel; Hagarman, Andrew; Kohli, Ajay JBIC Journal of Biological Inorganic Chemistry, Vol. 14, Issue 8 https://doi.org/10.1007/s00775-009-0574-9	journal	July 2009
Heme/Copper Terminal Oxidases Ferguson-Miller, Shelagh; Babcock, Gerald T. Chemical Reviews, Vol. 96, Issue 7 https://doi.org/10.1021/cr950051s	journal	January 1996
The iron–oxygen bond in human oxyhaemoglobin Shaanan, Boaz Nature, Vol. 296, Issue 5858 https://doi.org/10.1038/296683a0	journal	April 1982
An internal electron reservoir enhances catalytic CO ₂ reduction by a semisynthetic enzyme Schneider, Camille R.; Shafaat, Hannah S. Chemical Communications, Vol. 52, Issue 64 https://doi.org/10.1039/C6CC03901D	journal	January 2016
Hydrogen bonds and proton transfer in general-catalytic transition-state stabilization in enzyme catalysis Schowen, K. B.; Limbach, H. -H.; Denisov, G. S. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1458, Issue 1 https://doi.org/10.1016/S0005-2728(00)00059-1	journal	May 2000
Proton-Pumping Mechanism of Cytochrome c Oxidase Yoshikawa, Shinya; Muramoto, Kazumasa; Shinzawa-Itoh, Kyoko Annual Review of Biophysics, Vol. 40, Issue 1 https://doi.org/10.1146/annurev-biophys-042910-155341	journal	June 2011
Frontiers, Opportunities, and Challenges in Biochemical and Chemical Catalysis of CO ₂ Fixation Appel, Aaron M.; Bercaw, John E.; Bocarsly, Andrew B. Chemical Reviews, Vol. 113, Issue 8 https://doi.org/10.1021/cr300463y	journal	June 2013
Electrocatalytic CO2 reduction catalyzed by nitrogenase MoFe and FeFe proteins Hu, Bo; Harris, Derek F.; Dean, Dennis R. Bioelectrochemistry, Vol. 120 https://doi.org/10.1016/j.bioelechem.2017.12.002	journal	April 2018
Cobaloxime-Based Artificial Hydrogenases Bacchi, Marine; Berggren, Gustav; Niklas, Jens Inorganic Chemistry, Vol. 53, Issue 15 https://doi.org/10.1021/ic501014c	journal	July 2014