Recent mechanistic developments for cytochrome c nitrite reductase, the key enzyme in the dissimilatory nitrate reduction to ammonium pathway

Hird, Krystina; Campeciño, Julius O.; Lehnert, Nicolai; Hegg, Eric L.

doi:10.1016/j.jinorgbio.2024.112542

Recent mechanistic developments for cytochrome c nitrite reductase, the key enzyme in the dissimilatory nitrate reduction to ammonium pathway

Journal Article · Sun Mar 24 00:00:00 EDT 2024 · Journal of Inorganic Biochemistry

DOI:https://doi.org/10.1016/j.jinorgbio.2024.112542· OSTI ID:2339604

^[1]; ^[2]; ^[3]; ^[2]

Michigan State University, East Lansing, MI (United States); Michigan State University
Michigan State University, East Lansing, MI (United States)
University of Michigan, Ann Arbor, MI (United States)

Cytochrome c nitrite reductase, NrfA, is a soluble, periplasmic pentaheme cytochrome responsible for the reduction of nitrite to ammonium in the Dissimilatory Nitrate Reduction to Ammonium (DNRA) pathway, a vital reaction in the global nitrogen cycle. NrfA catalyzes this six-electron and eight-proton reduction of nitrite at a single active site with the help of its quinol oxidase partners. In this study, we summarize the latest progress in elucidating the reaction mechanism of ammonia production, including new findings about the active site architecture of NrfA, as well as recent results that elucidate electron transfer and storage in the pentaheme scaffold of this enzyme.

View Accepted Manuscript (DOE)

Research Organization:: Michigan State University, East Lansing, MI (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); National Science Foundation Graduate Research Fellowship Program

Grant/Contract Number:: SC0017952; SC0018173

OSTI ID:: 2339604

Alternate ID(s):: OSTI ID: 2337747

Journal Information:: Journal of Inorganic Biochemistry, Journal Name: Journal of Inorganic Biochemistry Vol. 256; ISSN 0162-0134

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (77)

Bis-histidine-coordinated hemes in four-helix bundles: how the geometry of the bundle controls the axial imidazole plane orientations in transmembrane cytochromes of mitochondrial Complexes II and III and related proteins Berry, Edward A.; Walker, F. Ann JBIC Journal of Biological Inorganic Chemistry, Vol. 13, Issue 4 https://doi.org/10.1007/s00775-008-0372-9	journal	April 2008
Substrate binding and activation in the active site of cytochrome c nitrite reductase: a density functional study Bykov, Dmytro; Neese, Frank JBIC Journal of Biological Inorganic Chemistry, Vol. 16, Issue 3 https://doi.org/10.1007/s00775-010-0739-6	journal	December 2010
Laue crystal structure of Shewanella oneidensis cytochrome c nitrite reductase from a high-yield expression system Youngblut, Matthew; Judd, Evan T.; Srajer, Vukica JBIC Journal of Biological Inorganic Chemistry, Vol. 17, Issue 4 https://doi.org/10.1007/s00775-012-0885-0	journal	March 2012
Reductive activation of the heme iron–nitrosyl intermediate in the reaction mechanism of cytochrome c nitrite reductase: a theoretical study Bykov, Dmytro; Neese, Frank JBIC Journal of Biological Inorganic Chemistry, Vol. 17, Issue 5 https://doi.org/10.1007/s00775-012-0893-0	journal	March 2012
Contrasting catalytic profiles of multiheme nitrite reductases containing CxxCK heme-binding motifs Doyle, Rose-Marie A. S.; Marritt, Sophie J.; Gwyer, James D. JBIC Journal of Biological Inorganic Chemistry, Vol. 18, Issue 6 https://doi.org/10.1007/s00775-013-1011-7	journal	June 2013
Heme-bound nitroxyl, hydroxylamine, and ammonia ligands as intermediates in the reaction cycle of cytochrome c nitrite reductase: a theoretical study Bykov, Dmytro; Plog, Matthias; Neese, Frank JBIC Journal of Biological Inorganic Chemistry, Vol. 19, Issue 1 https://doi.org/10.1007/s00775-013-1065-6	journal	November 2013
Nature's nitrite-to-ammonia expressway, with no stop at dinitrogen Kroneck, Peter M. H. JBIC Journal of Biological Inorganic Chemistry, Vol. 27, Issue 1 https://doi.org/10.1007/s00775-021-01921-4	journal	December 2021
Enzymes and associated electron transport systems that catalyse the respiratory reduction of nitrogen oxides and oxyanions Berks, Ben C.; Ferguson, Stuart J.; Moir, James W. B. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1232, Issue 3 https://doi.org/10.1016/0005-2728(95)00092-5	journal	December 1995
Regulation of the hexaheme nitrite/nitric oxide reductase of Desulfovibrio desulfuricans, Wolinella succinogenes and Escherichia coli : A mass spectrometric study Costa, C.; Macedo, A.; Moura, I. FEBS Letters, Vol. 276, Issue 1-2 https://doi.org/10.1016/0014-5793(90)80508-G	journal	December 1990
Structure and Function of Formate-Dependent Cytochrome c Nitrite Reductase, NrfA Einsle, Oliver Methods in Enzymology https://doi.org/10.1016/B978-0-12-386489-5.00016-6	book	January 2011
Escherichia coli Cytochrome c Nitrite Reductase NrfA Clarke, Thomas A.; Mills, Paul C.; Poock, Susie R. Globins and Other Nitric Oxide-Reactive Proteins, Part B https://doi.org/10.1016/S0076-6879(07)37004-3	book	April 2008
Bacterial cytochrome c nitrite reductase: new structural and functional aspects1Presented in part at the 5th ISABC, Corfu, Greece, 1999.1 Stach, Petra; Einsle, Oliver; Schumacher, Wolfram Journal of Inorganic Biochemistry, Vol. 79, Issue 1-4 https://doi.org/10.1016/S0162-0134(99)00248-2	journal	April 2000
Characterization of a heme c nitrite reductase from a non-ammonifying microorganism, Desulfovibrio vulgaris Hildenborough Pereira, Inês A. C.; LeGall, Jean; Xavier, António V. Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology, Vol. 1481, Issue 1 https://doi.org/10.1016/S0167-4838(00)00111-4	journal	August 2000
Redox-triggered events in cytochrome c nitrite reductase Gwyer, James D.; Angove, Hayley C.; Richardson, David J. Bioelectrochemistry, Vol. 63, Issue 1-2 https://doi.org/10.1016/j.bioelechem.2003.10.013	journal	June 2004
A needle in a haystack: The active site of the membrane-bound complex cytochrome c nitrite reductase Almeida, M. Gabriela; Silveira, Célia M.; Guigliarelli, Bruno FEBS Letters, Vol. 581, Issue 2 https://doi.org/10.1016/j.febslet.2006.12.023	journal	December 2006
An octaheme c‐type cytochrome from Shewanella oneidensis can reduce nitrite and hydroxylamine Atkinson, Sally J.; Mowat, Christopher G.; Reid, Graeme A. FEBS Letters, Vol. 581, Issue 20 https://doi.org/10.1016/j.febslet.2007.07.005	journal	July 2007
Detection and widespread distribution of the nrfA gene encoding nitrite reduction to ammonia, a short circuit in the biological nitrogen cycle that competes with denitrification Mohan, Sudesh B.; Schmid, Markus; Jetten, Mike FEMS Microbiology Ecology, Vol. 49, Issue 3 https://doi.org/10.1016/j.femsec.2004.04.012	journal	September 2004
Microbial nitrate respiration – Genes, enzymes and environmental distribution Kraft, Beate; Strous, Marc; Tegetmeyer, Halina E. Journal of Biotechnology, Vol. 155, Issue 1 https://doi.org/10.1016/j.jbiotec.2010.12.025	journal	August 2011
The trans effect of nitroxyl (HNO) in ferrous heme systems: Implications for soluble guanylate cyclase activation by HNO Goodrich, Lauren E.; Lehnert, Nicolai Journal of Inorganic Biochemistry, Vol. 118 https://doi.org/10.1016/j.jinorgbio.2012.07.024	journal	January 2013
High-Resolution Structural Analysis of a Novel Octaheme Cytochrome c Nitrite Reductase from the Haloalkaliphilic Bacterium Thioalkalivibrio nitratireducens Polyakov, Konstantin M.; Boyko, Konstantin M.; Tikhonova, Tamara V. Journal of Molecular Biology, Vol. 389, Issue 5 https://doi.org/10.1016/j.jmb.2009.04.037	journal	June 2009
Structure-Based Insights into the Role of the Cys–Tyr Crosslink and Inhibitor Recognition by Mammalian Cysteine Dioxygenase Driggers, Camden M.; Kean, Kelsey M.; Hirschberger, Lawrence L. Journal of Molecular Biology, Vol. 428, Issue 20 https://doi.org/10.1016/j.jmb.2016.07.012	journal	October 2016
Dissimilatory nitrate reduction to ammonium conserves nitrogen in anthropogenically affected subtropical mangrove sediments in Southeast China Cao, Wenzhi; Yang, Jingxin; Li, Ying Marine Pollution Bulletin, Vol. 110, Issue 1 https://doi.org/10.1016/j.marpolbul.2016.06.068	journal	September 2016
DNRA: A short-circuit in biological N-cycling to conserve nitrogen in terrestrial ecosystems Pandey, C. B.; Kumar, Upendra; Kaviraj, Megha Science of The Total Environment, Vol. 738 https://doi.org/10.1016/j.scitotenv.2020.139710	journal	October 2020
Elucidating Electron Storage and Distribution within the Pentaheme Scaffold of Cytochrome c Nitrite Reductase (NrfA) Sosa Alfaro, Victor; Campeciño, Julius; Tracy, Matthew Biochemistry, Vol. 60, Issue 23 https://doi.org/10.1021/acs.biochem.0c00977	journal	June 2021
A Kinetic Investigation of the Early Steps in Cytochrome c Nitrite Reductase (ccNiR)-Catalyzed Reduction of Nitrite Shahid, Shahid; Ali, Mahbbat; Legaspi-Humiston, Desiree Biochemistry, Vol. 60, Issue 26 https://doi.org/10.1021/acs.biochem.1c00172	journal	June 2021
Correlations between the Electronic Properties of Shewanella oneidensis Cytochrome c Nitrite Reductase (ccNiR) and Its Structure: Effects of Heme Oxidation State and Active Site Ligation Stein, Natalia; Love, Daniel; Judd, Evan T. Biochemistry, Vol. 54, Issue 24 https://doi.org/10.1021/acs.biochem.5b00330	journal	June 2015
The Biologically Relevant Coordination Chemistry of Iron and Nitric Oxide: Electronic Structure and Reactivity Lehnert, Nicolai; Kim, Eunsuk; Dong, Hai T. Chemical Reviews, Vol. 121, Issue 24 https://doi.org/10.1021/acs.chemrev.1c00253	journal	December 2021
Six-Electron Reduction of Nitrite to Ammonia by Cytochrome c Nitrite Reductase: Insights from Density Functional Theory Studies Bykov, Dmytro; Neese, Frank Inorganic Chemistry, Vol. 54, Issue 19 https://doi.org/10.1021/acs.inorgchem.5b01506	journal	August 2015
Distinguishing Nitro vs Nitrito Coordination in Cytochrome c′ Using Vibrational Spectroscopy and Density Functional Theory Nilsson, Zach N.; Mandella, Brian L.; Sen, Kakali Inorganic Chemistry, Vol. 56, Issue 21 https://doi.org/10.1021/acs.inorgchem.7b01945	journal	October 2017
Structure and Spectroscopy of the Periplasmic Cytochrome c Nitrite Reductase from Escherichia coli ^† Bamford, Vicki A.; Angove, Hayley C.; Seward, Harriet E. Biochemistry, Vol. 41, Issue 9 https://doi.org/10.1021/bi015765d	journal	March 2002
Direct Electrochemistry of Shewanella oneidensis Cytochrome c Nitrite Reductase: Evidence of Interactions across the Dimeric Interface Judd, Evan T.; Youngblut, Matthew; Pacheco, A. Andrew Biochemistry, Vol. 51, Issue 51 https://doi.org/10.1021/bi3011708	journal	December 2012
Shewanella oneidensis Cytochrome c Nitrite Reductase (ccNiR) Does Not Disproportionate Hydroxylamine to Ammonia and Nitrite, Despite a Strongly Favorable Driving Force Youngblut, Matthew; Pauly, Daniel J.; Stein, Natalia Biochemistry, Vol. 53, Issue 13 https://doi.org/10.1021/bi401705d	journal	March 2014
Hydrogen Bonding Networks Tune Proton-Coupled Redox Steps during the Enzymatic Six-Electron Conversion of Nitrite to Ammonia Judd, Evan T.; Stein, Natalia; Pacheco, A. Andrew Biochemistry, Vol. 53, Issue 35 https://doi.org/10.1021/bi500854p	journal	August 2014
Binding and Reduction of Sulfite by Cytochrome c Nitrite Reductase ^† ^, ^‡ Lukat, Peer; Rudolf, Marc; Stach, Petra Biochemistry, Vol. 47, Issue 7 https://doi.org/10.1021/bi7021415	journal	February 2008
Role of a Conserved Glutamine Residue in Tuning the Catalytic Activity of Escherichia coli Cytochrome c Nitrite Reductase ^† Clarke, Thomas A.; Kemp, Gemma L.; Wonderen, Jessica H. Van Biochemistry, Vol. 47, Issue 12 https://doi.org/10.1021/bi702175w	journal	March 2008
Manganese Cluster in Photosynthesis: Where Plants Oxidize Water to Dioxygen Yachandra, Vittal K.; Sauer, Kenneth; Klein, Melvin P. Chemical Reviews, Vol. 96, Issue 7 https://doi.org/10.1021/cr950052k	journal	January 1996
Aqueous nitrosyliron(II) chemistry. 1. Reduction of nitrite and nitric oxide by iron(II) and (trioxodinitrato)iron(II) in acetate buffer. Intermediacy of nitrosyl hydride Bonner, Francis T.; Pearsall, Kenneth A. Inorganic Chemistry, Vol. 21, Issue 5 https://doi.org/10.1021/ic00135a053	journal	May 1982
Mechanism of the Six-Electron Reduction of Nitrite to Ammonia by Cytochrome c Nitrite Reductase Einsle, Oliver; Messerschmidt, Albrecht; Huber, Robert Journal of the American Chemical Society, Vol. 124, Issue 39 https://doi.org/10.1021/ja0206487	journal	October 2002
Resolution of Key Roles for the Distal Pocket Histidine in Cytochrome c Nitrite Reductases Lockwood, Colin W. J.; Burlat, Bénédicte; Cheesman, Myles R. Journal of the American Chemical Society, Vol. 137, Issue 8 https://doi.org/10.1021/ja512941j	journal	February 2015
Spectroelectrochemical Characterization of a Pentaheme Cytochrome in Solution and as Electrocatalytically Active Films on Nanocrystalline Metal-Oxide Electrodes Marritt, Sophie J.; Kemp, Gemma L.; Xiaoe, Li Journal of the American Chemical Society, Vol. 130, Issue 27 https://doi.org/10.1021/ja802641a	journal	June 2008
The HNO Adduct of Myoglobin: Synthesis and Characterization Lin, Rong; Farmer, Patrick J. Journal of the American Chemical Society, Vol. 122, Issue 10 https://doi.org/10.1021/ja994079n	journal	March 2000
Stabilization of a Heme-HNO Model Complex Using a Bulky Bis-Picket Fence Porphyrin and Reactivity Studies with NO Manickas, Elizabeth C.; LaLonde, Ashley B.; Hu, Michael Y. Journal of the American Chemical Society, Vol. 145, Issue 42 https://doi.org/10.1021/jacs.3c05333	journal	October 2023
Hydride Attack on a Coordinated Ferric Nitrosyl: Experimental and DFT Evidence for the Formation of a Heme Model–HNO Derivative Abucayon, Erwin G.; Khade, Rahul L.; Powell, Douglas R. Journal of the American Chemical Society, Vol. 138, Issue 1 https://doi.org/10.1021/jacs.5b12008	journal	December 2015
Trapping of a Putative Intermediate in the Cytochrome c Nitrite Reductase (ccNiR)-Catalyzed Reduction of Nitrite: Implications for the ccNiR Reaction Mechanism Ali, Mahbbat; Stein, Natalia; Mao, Yingxi Journal of the American Chemical Society, Vol. 141, Issue 34 https://doi.org/10.1021/jacs.9b03036	journal	August 2019
Substrate Binding to a Nitrite Reductase Induces a Spin Transition Martins, Gabriel; Rodrigues, Luisa; Cunha, Filipa M. The Journal of Physical Chemistry B, Vol. 114, Issue 16 https://doi.org/10.1021/jp9118502	journal	April 2010
Structure of cytochrome c nitrite reductase Einsle, Oliver; Messerschmidt, Albrecht; Stach, Petra Nature, Vol. 400, Issue 6743 https://doi.org/10.1038/22802	journal	July 1999
New processes and players in the nitrogen cycle: the microbial ecology of anaerobic and archaeal ammonia oxidation Francis, Christopher A.; Beman, J. Michael; Kuypers, Marcel M. M. The ISME Journal, Vol. 1, Issue 1 https://doi.org/10.1038/ismej.2007.8	journal	May 2007
Addressing agricultural nitrogen losses in a changing climate Bowles, Timothy M.; Atallah, Shady S.; Campbell, Eleanor E. Nature Sustainability, Vol. 1, Issue 8 https://doi.org/10.1038/s41893-018-0106-0	journal	August 2018
X-ray structure of the membrane-bound cytochrome c quinol dehydrogenase NrfH reveals novel haem coordination Rodrigues, Maria Luisa; Oliveira, Tânia F.; Pereira, Inês A. C. The EMBO Journal, Vol. 25, Issue 24 https://doi.org/10.1038/sj.emboj.7601439	journal	November 2006
Nitrogen-limited mangrove ecosystems conserve N through dissimilatory nitrate reduction to ammonium Fernandes, Sheryl Oliveira; Bonin, Patricia C.; Michotey, Valérie D. Scientific Reports, Vol. 2, Issue 1 https://doi.org/10.1038/srep00419	journal	May 2012
The relationship between redox enzyme activity and electrochemical potential—cellular and mechanistic implications from protein film electrochemistry Gates, Andrew J.; Kemp, Gemma L.; To, Chun Yip Physical Chemistry Chemical Physics, Vol. 13, Issue 17 https://doi.org/10.1039/c0cp02887h	journal	January 2011
The crystal structure of the pentahaem c-type cytochrome NrfB and characterization of its solution-state interaction with the pentahaem nitrite reductase NrfA Clarke, Thomas A.; Cole, Jeffrey A.; Richardson, David J. Biochemical Journal, Vol. 406, Issue 1 https://doi.org/10.1042/BJ20070321	journal	July 2007
Cytochrome c nitrite reductase: from structural to physicochemical analysis Burlat, B.; Gwyer, J. D.; Poock, S. Biochemical Society Transactions, Vol. 33, Issue 1 https://doi.org/10.1042/BST0330137	journal	February 2005
Molecular interactions between multihaem cytochromes: probing the protein–protein interactions between pentahaem cytochromes of a nitrite reductase complex Lockwood, Colin; Butt, Julea N.; Clarke, Thomas A. Biochemical Society Transactions, Vol. 39, Issue 1 https://doi.org/10.1042/BST0390263	journal	January 2011
Pentahaem cytochrome c nitrite reductase: reaction with hydroxylamine, a potential reaction intermediate and substrate Rudolf, M.; Einsle, O.; Neese, F. Biochemical Society Transactions, Vol. 30, Issue 4 https://doi.org/10.1042/bst0300649	journal	August 2002
A NapC/NirT-type cytochrome c (NrfH) is the mediator between the quinone pool and the cytochrome c nitrite reductase of Wolinella succinogenes: Cytochrome c nitrite reductase of Wolinella succinogenes Simon, Jörg; Gross, Roland; Einsle, Oliver Molecular Microbiology, Vol. 35, Issue 3 https://doi.org/10.1046/j.1365-2958.2000.01742.x	journal	February 2000
Four genes are required for the system II cytochrome c biogenesis pathway in Bordetella pertussis , a unique bacterial model : A bacterial model for system II cytochrome Beckett, Caroline S.; Loughman, Jennifer A.; Karberg, Katherine A. Molecular Microbiology, Vol. 38, Issue 3 https://doi.org/10.1046/j.1365-2958.2000.02174.x	journal	November 2000
The nrfI gene is essential for the attachment of the active site haem group of Wolinella succinogenes cytochrome c nitrite reductase: Maturation of W. succinogenes nitrite reductase Pisa, René; Stein, Torsten; Eichler, Robert Molecular Microbiology, Vol. 43, Issue 3 https://doi.org/10.1046/j.1365-2958.2002.02784.x	journal	February 2002
The isolation and characterization of cytochrome c nitrite reductase subunits (NrfA and NrfH) from Desulfovibrio desulfuricans ATCC 27774 Almeida, Maria Gabriela; Macieira, Sofia; Gonçalves, Luisa L. European Journal of Biochemistry, Vol. 270, Issue 19 https://doi.org/10.1046/j.1432-1033.2003.03772.x	journal	September 2003
Redox Properties of Cytochrome Nitrite Reductase from ATCC 27774 Costa, Cristina; Moura, José J. G.; Moura, Isabel Journal of Biological Chemistry, Vol. 271, Issue 38 https://doi.org/10.1074/jbc.271.38.23191	journal	September 1996
Cytochrome c Nitrite Reductase from Wolinella succinogenes: STRUCTURE AT 1.6 Å RESOLUTION, INHIBITOR BINDING, AND HEME-PACKING MOTIFS Einsle, Oliver; Stach, Petra; Messerschmidt, Albrecht Journal of Biological Chemistry, Vol. 275, Issue 50 https://doi.org/10.1074/jbc.M006188200	journal	September 2000
Protein Film Voltammetry Reveals Distinctive Fingerprints of Nitrite and Hydroxylamine Reduction by a Cytochrome c Nitrite Reductase Angove, Hayley C.; Cole, Jeffrey. A.; Richardson, David J. Journal of Biological Chemistry, Vol. 277, Issue 26 https://doi.org/10.1074/jbc.M200495200	journal	April 2002
Respiratory Detoxification of Nitric Oxide by the Cytochrome c Nitrite Reductase of Escherichia coli Poock, Susannah R.; Leach, Emily R.; Moir, James W. B. Journal of Biological Chemistry, Vol. 277, Issue 26 https://doi.org/10.1074/jbc.M200731200	journal	April 2002
Cytochrome c Nitrite Reductase from Desulfovibrio desulfuricans ATCC 27774: THE RELEVANCE OF THE TWO CALCIUM SITES IN THE STRUCTURE OF THE CATALYTIC SUBUNIT (NrfA) Cunha, Carlos A.; Macieira, Sofia; Dias, João M. Journal of Biological Chemistry, Vol. 278, Issue 19 https://doi.org/10.1074/jbc.M211777200	journal	March 2003
Purification and Spectropotentiometric Characterization of Escherichia coli NrfB, a Decaheme Homodimer That Transfers Electrons to the Decaheme Periplasmic Nitrite Reductase Complex Clarke, Thomas A.; Dennison, Victoria; Seward, Harriet E. Journal of Biological Chemistry, Vol. 279, Issue 40 https://doi.org/10.1074/jbc.M407604200	journal	October 2004
The Nitric Oxide Reductase Activity of Cytochrome c Nitrite Reductase from Escherichia coli van Wonderen, Jessica H.; Burlat, Bénédicte; Richardson, David J. Journal of Biological Chemistry, Vol. 283, Issue 15 https://doi.org/10.1074/jbc.M709090200	journal	February 2008
Cytochrome c nitrite reductase from the bacterium Geobacter lovleyi represents a new NrfA subclass Campeciño, Julius; Lagishetty, Satyanarayana; Wawrzak, Zdzislaw Journal of Biological Chemistry, Vol. 295, Issue 33 https://doi.org/10.1074/jbc.RA120.013981	journal	August 2020
50 year trends in nitrogen use efficiency of world cropping systems: the relationship between yield and nitrogen input to cropland Lassaletta, Luis; Billen, Gilles; Grizzetti, Bruna Environmental Research Letters, Vol. 9, Issue 10 https://doi.org/10.1088/1748-9326/9/10/105011	journal	October 2014
An unusual active site architecture in cytochrome c nitrite reductase NrfA-1 from Geobacter metallireducens Denkhaus, Lukas; Siffert, Fanny; Einsle, Oliver FEMS Microbiology Letters, Vol. 370 https://doi.org/10.1093/femsle/fnad068	journal	January 2023
Covalent modifications of the catalytic tyrosine in octahaem cytochromecnitrite reductase and their effect on the enzyme activity Trofimov, Anton A.; Polyakov, Konstantin M.; Tikhonova, Tamara V. Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 2 https://doi.org/10.1107/S0907444911052632	journal	January 2012
The oxidative and nitrosative stress defence network of Wolinella succinogenes: cytochrome c nitrite reductase mediates the stress response to nitrite, nitric oxide, hydroxylamine and hydrogen peroxide: Stress defence networks in W. succinogenes Kern, Melanie; Volz, Jennifer; Simon, Jörg Environmental Microbiology, Vol. 13, Issue 9 https://doi.org/10.1111/j.1462-2920.2011.02520.x	journal	June 2011
Enzymology and bioenergetics of respiratory nitrite ammonification Simon, Jörg FEMS Microbiology Reviews, Vol. 26, Issue 3 https://doi.org/10.1111/j.1574-6976.2002.tb00616.x	journal	August 2002
Current Understanding of the Mechanism of Water Oxidation in Photosystem II and Its Relation to XFEL Data Cox, Nicholas; Pantazis, Dimitrios A.; Lubitz, Wolfgang Annual Review of Biochemistry, Vol. 89, Issue 1 https://doi.org/10.1146/annurev-biochem-011520-104801	journal	June 2020
Nitrogen in Agriculture: Balancing the Cost of an Essential Resource Robertson, G. Philip; Vitousek, Peter M. Annual Review of Environment and Resources, Vol. 34, Issue 1 https://doi.org/10.1146/annurev.environ.032108.105046	journal	November 2009
Measuring the CytochromecNitrite Reductase Activity—Practical Considerations on the Enzyme Assays Silveira, Célia M.; Besson, Stéphane; Moura, Isabel Bioinorganic Chemistry and Applications, Vol. 2010 https://doi.org/10.1155/2010/634597	journal	January 2010
Have we overemphasized the role of denitrification in aquatic ecosystems? A review of nitrate removal pathways Burgin, Amy J.; Hamilton, Stephen K. Frontiers in Ecology and the Environment, Vol. 5, Issue 2 https://doi.org/10.1890/1540-9295(2007)5[89:HWOTRO]2.0.CO;2	journal	March 2007
Restoring Soil Fertility on Degraded Lands to Meet Food, Fuel, and Climate Security Needs via Perennialization Mosier, Samantha; Córdova, S. Carolina; Robertson, G. Philip Frontiers in Sustainable Food Systems, Vol. 5 https://doi.org/10.3389/fsufs.2021.706142	journal	October 2021

Similar Records

Functional roles of CymA and NapC in reduction of nitrate and nitrite by Shewanella putrefaciens W3-18-1

Journal Article · Wed Jun 01 00:00:00 EDT 2016 · Microbiology · OSTI ID:1342331

Elucidating Electron Storage and Distribution within the Pentaheme Scaffold of Cytochrome c Nitrite Reductase (NrfA)

Journal Article · Tue Jun 01 00:00:00 EDT 2021 · Biochemistry · OSTI ID:1865050

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Crystal structure
Cytochrome c nitrite reductase
Dissimilatory nitrate reduction to ammonium (DNRA)
Mechanism
NrfA
Pentaheme

Recent mechanistic developments for cytochrome c nitrite reductase, the key enzyme in the dissimilatory nitrate reduction to ammonium pathway

Citation Formats

References (77)

Similar Records

Related Subjects