Electroenzymatic Nitrogen Fixation Using an Organic Redox Polymer-Immobilized MoFe Protein System

Lee, Yoo Seok; Ruff, Adrian; Cai, Rong; Lim, Koun; Schuhmann, Wolfgang; Minteer, Shelley D

doi:10.1002/anie.202007198

Title: Electroenzymatic Nitrogen Fixation Using an Organic Redox Polymer-Immobilized MoFe Protein System

Journal Article · 03 June 2020 · Angewandte Chemie (International Edition)

DOI: https://doi.org/10.1002/anie.202007198 · OSTI ID:1633080

Lee, Yoo Seok ^[1]; Ruff, Adrian ^[2]; Cai, Rong ^[3]; Lim, Koun ^[3]; Schuhmann, Wolfgang ^[2]; Minteer, Shelley D ^[3]

Univ. of Utah, Salt Lake City, UT (United States); University of Utah
Ruhr Univ., Bochum (Germany)
Univ. of Utah, Salt Lake City, UT (United States)

Nitrogenase is the single biological catalyst that is understood to convert dinitrogen (N₂) to ammonia (NH₃). Nitrogenase-catalyzed NH₃ formation in vivo is energetically intensive due to a series of events, including a Fe protein cycle coupled with ATP hydrolysis. Furthermore, the complexity of nitrogenase’s cofactors plagues related bioelectrodes by unstable and poor electric wiring between the cofactors and the electrode, thereby lowering the overall bioelectrocatalytic performance. We report an organic redox polymer-based electroenzymatic nitrogen fixation system using a metal-free redox polymer namely neutral red-modified poly(glycidyl methacrylate-co-methylmethacrylate- co-poly(ethyleneglycol)methacrylate) with a low redox potential of -0.58 V vs. SCE. The stable and efficient electric wiring of nitrogenase within the redox polymer matrix enables mediated bioelectrocatalysis of N₃ -, NO₂ - and N₂ to NH₃ catalyzed by the MoFe protein via the polymer-bound redox moieties distributed in the polymer matrix in the absence of the Fe protein. Bulk bioelectrosynthetic experiments produced 209 ± 30 nmol NH₃ nmol MoFe^-1 h^-1 from N₂ reduction. ¹⁵N₂ labeling experiments and NMR analysis were performed to confirm biosynthetic N₂ reduction to NH₃.

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Research Organization:: Fulcrum Bioscience, Salt Lake City, UT (United States)

Sponsoring Organization:: USDOE Office of Energy Efficiency and Renewable Energy (EERE), Advanced Manufacturing Office (EE-5A); German Research Foundation; European Research Council (ERC)

Grant/Contract Number:: SC0017845

OSTI ID:: 1633080

Alternate ID(s):: OSTI ID: 1641851; OSTI ID: 1641854; OSTI ID: 22947374

Journal Information:: Angewandte Chemie (International Edition), Journal Name: Angewandte Chemie (International Edition) Journal Issue: 38 Vol. 59; ISSN 1433-7851

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

References (34)

Nitrogenase Bioelectrochemistry for Synthesis Applications Milton, Ross D.; Minteer, Shelley D. Accounts of Chemical Research, Vol. 52, Issue 12 https://doi.org/10.1021/acs.accounts.9b00494	journal	November 2019
Nitrogenase bioelectrocatalysis: heterogeneous ammonia and hydrogen production by MoFe protein Milton, Ross D.; Abdellaoui, Sofiene; Khadka, Nimesh Energy & Environmental Science, Vol. 9, Issue 8 https://doi.org/10.1039/C6EE01432A	journal	January 2016
Electron Transfer from Semiconductor Nanocrystals to Redox Enzymes Utterback, James K.; Ruzicka, Jesse L.; Keller, Helena R. Annual Review of Physical Chemistry, Vol. 71, Issue 1 https://doi.org/10.1146/annurev-physchem-050317-014232	journal	April 2020
Redox polymers in bioelectrochemistry: Common playgrounds and novel concepts Ruff, Adrian Current Opinion in Electrochemistry, Vol. 5, Issue 1 https://doi.org/10.1016/j.coelec.2017.06.007	journal	October 2017
Bioelectrochemical Haber-Bosch Process: An Ammonia-Producing H 2 /N 2 Fuel Cell Milton, Ross D.; Cai, Rong; Abdellaoui, Sofiene Angewandte Chemie, Vol. 129, Issue 10 https://doi.org/10.1002/ange.201612500	journal	February 2017
Mechanism of Molybdenum Nitrogenase Burgess, Barbara K.; Lowe, David J. Chemical Reviews, Vol. 96, Issue 7 https://doi.org/10.1021/cr950055x	journal	January 1996
Nitrogenase reactivity: azide reduction Rubinson, Judith F.; Burgess, Barbara K.; Corbin, James L. Biochemistry, Vol. 24, Issue 2 https://doi.org/10.1021/bi00323a006	journal	January 1985
Pyrene hydrogel for promoting direct bioelectrochemistry: ATP-independent electroenzymatic reduction of N ₂ Hickey, David P.; Lim, Koun; Cai, Rong Chemical Science, Vol. 9, Issue 23 https://doi.org/10.1039/C8SC01638K	journal	January 2018
Nitrogenase Structure and Function: A Biochemical-Genetic Perspective Peters, J. W.; Fisher, K.; Dean, D. R. Annual Review of Microbiology, Vol. 49, Issue 1 https://doi.org/10.1146/annurev.mi.49.100195.002003	journal	October 1995
Efficient NADH Regeneration by a Redox Polymer-Immobilized Enzymatic System Yuan, Mengwei; Kummer, Matthew J.; Milton, Ross D. ACS Catalysis, Vol. 9, Issue 6 https://doi.org/10.1021/acscatal.9b00513	journal	May 2019
Construction of Uniform Monolayer- and Orientation-Tunable Enzyme Electrode by a Synthetic Glucose Dehydrogenase without Electron-Transfer Subunit via Optimized Site-Specific Gold-Binding Peptide Capable of Direct Electron Transfer Lee, Yoo Seok; Baek, Seungwoo; Lee, Hyeryeong ACS Applied Materials & Interfaces, Vol. 10, Issue 34 https://doi.org/10.1021/acsami.8b08876	journal	August 2018
Mechanism of Mo-Dependent Nitrogenase Seefeldt, Lance C.; Hoffman, Brian M.; Dean, Dennis R. Annual Review of Biochemistry, Vol. 78, Issue 1 https://doi.org/10.1146/annurev.biochem.78.070907.103812	journal	June 2009
QM/MM Molecular Modeling and Marcus Theory in the Molecular Design of Electrodes for Enzymatic Fuel Cells Vazquez-Duhalt , Rafael; Aguila, Sergio A.; Arrocha, Andrés A. ChemElectroChem, Vol. 1, Issue 3 https://doi.org/10.1002/celc.201300096	journal	October 2013
Redoxproteinschichten auf leitenden Trägern – Systeme für bioelektronische Anwendungen Willner, Itamar; Katz, Eugenii Angewandte Chemie, Vol. 112, Issue 7 https://doi.org/10.1002/(SICI)1521-3757(20000403)112:7<1230::AID-ANGE1230>3.0.CO;2-3	journal	April 2000
Electron-transfer kinetics in organized thiol monolayers with attached pentaammine(pyridine)ruthenium redox centers Finklea, Harry O.; Hanshew, Dwight D. Journal of the American Chemical Society, Vol. 114, Issue 9 https://doi.org/10.1021/ja00035a001	journal	April 1992
Integration of Layered Redox Proteins and Conductive Supports for Bioelectronic Applications Willner, Itamar; Katz, Eugenii Angewandte Chemie International Edition, Vol. 39, Issue 7 https://doi.org/10.1002/(SICI)1521-3773(20000403)39:7<1180::AID-ANIE1180>3.0.CO;2-E	journal	April 2000
Creating a Low‐Potential Redox Polymer for Efficient Electroenzymatic CO ₂ Reduction Yuan, Mengwei; Sahin, Selmihan; Cai, Rong Angewandte Chemie, Vol. 130, Issue 22 https://doi.org/10.1002/ange.201803397	journal	April 2018
Bioelectrochemical Haber-Bosch Process: An Ammonia-Producing H ₂ /N ₂ Fuel Cell Milton, Ross D.; Cai, Rong; Abdellaoui, Sofiene Angewandte Chemie International Edition, Vol. 56, Issue 10 https://doi.org/10.1002/anie.201612500	journal	February 2017
An O ₂ Tolerant Polymer/Glucose Oxidase Based Bioanode as Basis for a Self-powered Glucose Sensor Lopez, Francesca; Zerria, Sarra; Ruff, Adrian Electroanalysis, Vol. 30, Issue 7 https://doi.org/10.1002/elan.201700785	journal	January 2018
Electron Transfer within Nitrogenase: Evidence for a Deficit-Spending Mechanism Danyal, Karamatullah; Dean, Dennis R.; Hoffman, Brian M. Biochemistry, Vol. 50, Issue 43 https://doi.org/10.1021/bi201003a	journal	November 2011
Creating a Low‐Potential Redox Polymer for Efficient Electroenzymatic CO ₂ Reduction Yuan, Mengwei; Sahin, Selmihan; Cai, Rong Angewandte Chemie International Edition, Vol. 57, Issue 22 https://doi.org/10.1002/anie.201803397	journal	May 2018
Rational wiring of photosystem II to hierarchical indium tin oxide electrodes using redox polymers Sokol, Katarzyna P.; Mersch, Dirk; Hartmann, Volker Energy & Environmental Science, Vol. 9, Issue 12 https://doi.org/10.1039/C6EE01363E	journal	January 2016
Nitrogenase: a general hydrogenator of small molecules Dance, Ian Chemical Communications, Vol. 49, Issue 93 https://doi.org/10.1039/c3cc46864j	journal	January 2013
The In Vivo Potential-Regulated Protective Protein of Nitrogenase in Azotobacter vinelandii Supports Aerobic Bioelectrochemical Dinitrogen Reduction In Vitro Milton, Ross D.; Cai, Rong; Sahin, Selmihan Journal of the American Chemical Society, Vol. 139, Issue 26 https://doi.org/10.1021/jacs.7b04893	journal	June 2017
Extending the Carbon Chain: Hydrocarbon Formation Catalyzed by Vanadium/Molybdenum Nitrogenases Hu, Y.; Lee, C. C.; Ribbe, M. W. Science, Vol. 333, Issue 6043 https://doi.org/10.1126/science.1206883	journal	August 2011
Amino-acid-encoded biocatalytic self-assembly enables the formation of transient conducting nanostructures Kumar, Mohit; Ing, Nicole L.; Narang, Vishal Nature Chemistry, Vol. 10, Issue 7 https://doi.org/10.1038/s41557-018-0047-2	journal	April 2018
Electroenzymatic CO ₂ Fixation Using Redox Polymer/Enzyme-Modified Gas Diffusion Electrodes Szczesny, Julian; Ruff, Adrian; Oliveira, Ana R. ACS Energy Letters, Vol. 5, Issue 1 https://doi.org/10.1021/acsenergylett.9b02436	journal	November 2019
Investigating the Impact of Multi-Heme Pyrroloquinoline Quinone-Aldehyde Dehydrogenase Orientation on Direct Bioelectrocatalysis via Site Specific Enzyme Immobilization Xu, Shuai; Minteer, Shelley D. ACS Catalysis, Vol. 3, Issue 8 https://doi.org/10.1021/cs400316b	journal	July 2013
Viologens and Their Application as Functional Materials Striepe, Laura; Baumgartner, Thomas Chemistry - A European Journal, Vol. 23, Issue 67 https://doi.org/10.1002/chem.201703348	journal	September 2017
Wiring of Photosystem I and Hydrogenase on an Electrode for Photoelectrochemical H 2 Production by using Redox Polymers for Relatively Positive Onset Potential Tapia, Cristina; Milton, Ross D.; Pankratova, Galina ChemElectroChem, Vol. 4, Issue 1 https://doi.org/10.1002/celc.201600506	journal	September 2016
Molybdenum-Dependent Formate Dehydrogenase for Formate Bioelectrocatalysis in a Formate/O 2 Enzymatic Fuel Cell Sahin, Selmihan; Cai, Rong; Milton, Ross D. Journal of The Electrochemical Society, Vol. 165, Issue 3 https://doi.org/10.1149/2.0431803jes	journal	January 2018
Electron-conducting redox hydrogels: design, characteristics and synthesis Heller, A. Current Opinion in Chemical Biology, Vol. 10, Issue 6 https://doi.org/10.1016/j.cbpa.2006.09.018	journal	December 2006
Redox polymers in electrochemical systems: From methods of mediation to energy storage Yuan, Mengwei; Minteer, Shelley D. Current Opinion in Electrochemistry, Vol. 15 https://doi.org/10.1016/j.coelec.2019.03.003	journal	June 2019
Establishing a Thermodynamic Landscape for the Active Site of Mo-Dependent Nitrogenase Hickey, David P.; Cai, Rong; Yang, Zhi-Yong Journal of the American Chemical Society, Vol. 141, Issue 43 https://doi.org/10.1021/jacs.9b06546	journal	October 2019

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32 ENERGY CONSERVATION, CONSUMPTION, AND UTILIZATION
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Title: Electroenzymatic Nitrogen Fixation Using an Organic Redox Polymer-Immobilized MoFe Protein System

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