Nitrogenase Bioelectrocatalysis: ATP-Independent Ammonia Production Using a Redox Polymer/MoFe Protein System

Lee, Yoo Seok; Yuan, Mengwei; Cai, Rong; Lim, Koun; Minteer, Shelley D.

doi:10.1021/acscatal.0c01397

Nitrogenase Bioelectrocatalysis: ATP-Independent Ammonia Production Using a Redox Polymer/MoFe Protein System

Journal Article · Fri Jun 05 00:00:00 EDT 2020 · ACS Catalysis

DOI:https://doi.org/10.1021/acscatal.0c01397· OSTI ID:1633077

Lee, Yoo Seok ^[1]; Yuan, Mengwei ^[2]; ^[3]; Lim, Koun ^[2]; ^[2]

Univ. of Utah, Salt Lake City, UT (United States); University of Utah
Univ. of Utah, Salt Lake City, UT (United States)
Univ. of Utah, Salt Lake City, UT (United States); Univ. of California, Berkeley, CA (United States)

Nitrogenase is the only biological catalyst that is understood to be able to convert nitrogen gas to ammonia. In microorganisms, the MoFe catalytic protein of nitrogenase is reduced by a transient Fe protein binding and separate hydrolysis of ATP. Yet, the requirement of 16 ATP molecules by the Fe protein for the 8 electron transfer is an energy-intense caveat to the enzymatic synthesis of NH₃ and is challenging from an electrochemical perspective. Thus, we report the redox polymer-based ATP-free mediated electron-transfer system of MoFe nitrogenase using cobaltocene-functionalized poly(allylamine) (Cc-PAA), which is able to reduce the MoFe nitrogenase directly with a low redox potential of -0.58 V vs SHE. An efficient immobilization of MoFe nitrogenase via Cc-PAA allowed for the bioelectrocatalytic reduction of N₃^–, NO₂^–, and N₂ to NH₃. Bulk bioelectrosynthetic experiments produced 7 ± 2 and 30 ± 5 nmol of NH₃ from NO₂^– and N₃^– reduction for 30 min, respectively. In addition, biosynthetic N₂ reduction to NH₃ was confirmed by ¹⁵N₂ labeling experiments with NMR analysis. This mediated electron-transfer approach of the immobilized nitrogenase using the Cc-PAA redox polymer provides a valuable technological basis for scale-up and industrial uses in the future of bioelectrosynthesis.

View Accepted Manuscript (DOE)

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)

Grant/Contract Number:: SC0017845

OSTI ID:: 1633077

Journal Information:: ACS Catalysis, Journal Name: ACS Catalysis Journal Issue: 12 Vol. 10; ISSN 2155-5435

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

References (38)

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
Pyrene‐Based Noncovalent Immobilization of Nitrogenase on Carbon Surfaces Patel, Janki; Cai, Rong; Milton, Ross ChemBioChem, Vol. 21, Issue 12 https://doi.org/10.1002/cbic.201900697	journal	January 2020
Combining Noble Metals and Enzymes for Relay Cascade Electrocatalysis of Nitrate Reduction to Ammonia at Neutral pH Duca, Matteo; Weeks, Justin R.; Fedor, Justin G. ChemElectroChem, Vol. 2, Issue 8 https://doi.org/10.1002/celc.201500166	journal	May 2015
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
Methodologies for “Wiring” Redox Proteins/Enzymes to Electrode Surfaces Yates, Nicholas D. J.; Fascione, Martin A.; Parkin, Alison Chemistry - A European Journal, Vol. 24, Issue 47 https://doi.org/10.1002/chem.201800750	journal	June 2018
New electropolymerizable amphiphilic viologens for the immobilization and electrical wiring of a nitrate reductase Cosnier, Serge; Galland, Bruno; Innocent, Christophe Journal of Electroanalytical Chemistry, Vol. 433, Issue 1-2 https://doi.org/10.1016/S0022-0728(97)00207-6	journal	August 1997
Principles of direct (mediator free) bioelectrocatalysis Karyakin, Arkady A. Bioelectrochemistry, Vol. 88 https://doi.org/10.1016/j.bioelechem.2012.05.001	journal	December 2012
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 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
Improvement of enzyme electrocatalysis using substrate containing electroactive polymers. Towards limiting efficiencies of bioelectrocatalysis Karyakin, Arkady A.; Vinogradova, Darya V.; Morozov, Sergey V. Electrochimica Acta, Vol. 55, Issue 26 https://doi.org/10.1016/j.electacta.2009.09.081	journal	November 2010
Fabrication of Vertically aligned Copper Nanotubes as a Novel Electrode for Enzymatic Biofuel Cells Kashyap, Diwakar; Yadav, Raghvendra Singh; Gohil, Smita Electrochimica Acta, Vol. 167 https://doi.org/10.1016/j.electacta.2015.03.164	journal	June 2015
Three-dimensional carbon nanotube–polypyrrole–[NiFe] hydrogenase electrodes for the efficient electrocatalytic oxidation of H2 Baur, Jessica; Le Goff, Alan; Dementin, Sébastien International Journal of Hydrogen Energy, Vol. 36, Issue 19 https://doi.org/10.1016/j.ijhydene.2011.06.122	journal	September 2011
Concentration-dependent effects of metronidazole, inhibiting nitrogenase, on hydrogen photoproduction and proton-translocating ATPase activity of Rhodobacter sphaeroides Sargsyan, Harutyun; Gabrielyan, Lilit; Trchounian, Armen International Journal of Hydrogen Energy, Vol. 39, Issue 1 https://doi.org/10.1016/j.ijhydene.2013.10.049	journal	January 2014
Improvement of biosensor performances for nitrate determination using a new hydrophilic poly(pyrrole-viologen) film Da Silva, S.; Shan, D.; Cosnier, S. Sensors and Actuators B: Chemical, Vol. 103, Issue 1-2 https://doi.org/10.1016/j.snb.2004.04.068	journal	September 2004
Nitrate biosensors and biological methods for nitrate determination Sohail, Manzar; Adeloju, Samuel B. Talanta, Vol. 153 https://doi.org/10.1016/j.talanta.2016.03.002	journal	June 2016
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
Evidence That the P _i Release Event Is the Rate-Limiting Step in the Nitrogenase Catalytic Cycle Yang, Zhi-Yong; Ledbetter, Rhesa; Shaw, Sudipta Biochemistry, Vol. 55, Issue 26 https://doi.org/10.1021/acs.biochem.6b00421	journal	June 2016
Inhibition of nitrogenase-catalyzed ammonia formation by hydrogen Guth, Joseph H.; Burris, Robert H. Biochemistry, Vol. 22, Issue 22 https://doi.org/10.1021/bi00291a010	journal	October 1983
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
An Atomic-Level Mechanism for Molybdenum Nitrogenase. Part 2. Proton Reduction, Inhibition of Dinitrogen Reduction by Dihydrogen, and the HD Formation Reaction ^† Durrant, Marcus C. Biochemistry, Vol. 41, Issue 47 https://doi.org/10.1021/bi025624r	journal	November 2002
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
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
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
The Hydrogen Chemistry of the FeMo-co Active Site of Nitrogenase Dance, Ian Journal of the American Chemical Society, Vol. 127, Issue 31 https://doi.org/10.1021/ja0504946	journal	August 2005
Nitrite and Hydroxylamine as Nitrogenase Substrates: Mechanistic Implications for the Pathway of N ₂ Reduction Shaw, Sudipta; Lukoyanov, Dmitriy; Danyal, Karamatullah Journal of the American Chemical Society, Vol. 136, Issue 36 https://doi.org/10.1021/ja507123d	journal	August 2014
Role of Quinones in Electron Transfer of PQQ–Glucose Dehydrogenase Anodes—Mediation or Orientation Effect Babanova, Sofia; Matanovic, Ivana; Chavez, Madelaine Seow Journal of the American Chemical Society, Vol. 137, Issue 24 https://doi.org/10.1021/jacs.5b03053	journal	June 2015
Highly Efficient Flavin–Adenine Dinucleotide Glucose Dehydrogenase Fused to a Minimal Cytochrome C Domain Algov, Itay; Grushka, Jennifer; Zarivach, Raz Journal of the American Chemical Society, Vol. 139, Issue 48 https://doi.org/10.1021/jacs.7b07011	journal	September 2017
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
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
Nitrogenase: a general hydrogenator of small molecules Dance, Ian Chemical Communications, Vol. 49, Issue 93 https://doi.org/10.1039/c3cc46864j	journal	January 2013
Electron transfer precedes ATP hydrolysis during nitrogenase catalysis Duval, S.; Danyal, K.; Shaw, S. Proceedings of the National Academy of Sciences, Vol. 110, Issue 41 https://doi.org/10.1073/pnas.1311218110	journal	September 2013
STRUCTURE: Nitrogenase Reveals Its Inner Secrets Smith, B. E. Science, Vol. 297, Issue 5587 https://doi.org/10.1126/science.1076659	journal	September 2002
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
A simple and precise method for measuring ammonium in marine and freshwater ecosystems Holmes, Robert M.; Aminot, Alain; Kérouel, Roger Canadian Journal of Fisheries and Aquatic Sciences, Vol. 56, Issue 10 https://doi.org/10.1139/f99-128	journal	October 1999
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
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
Dinitrogen reduction on a polypyrrole coated Pt electrode under high-pressure conditions: electrochemical impedance spectroscopy studies Balun Kayan, Didem; KÖLelİ, Fatih TURKISH JOURNAL OF CHEMISTRY, Vol. 39 https://doi.org/10.3906/kim-1501-80	journal	January 2015

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