Nitric oxide is an obligate bacterial nitrification intermediate produced by hydroxylamine oxidoreductase

Caranto, Jonathan D.; Lancaster, Kyle M.

doi:10.1073/pnas.1704504114

Title: Nitric oxide is an obligate bacterial nitrification intermediate produced by hydroxylamine oxidoreductase

Journal Article · Mon Jul 17 00:00:00 EDT 2017 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1704504114· OSTI ID:1371603

Caranto, Jonathan D. ^[1];

^[1]

Department of Chemistry and Chemical Biology, Cornell University, Ithaca, NY 14853

Ammonia (NH₃)-oxidizing bacteria (AOB) emit substantial amounts of nitric oxide (NO) and nitrous oxide (N₂O), both of which contribute to the harmful environmental side effects of large-scale agriculture. The currently accepted model for AOB metabolism involves NH₃ oxidation to nitrite (NO₂^–) via a single obligate intermediate, hydroxylamine (NH₂OH). Within this model, the multiheme enzyme hydroxylamine oxidoreductase (HAO) catalyzes the four-electron oxidation of NH₂OH to NO₂^–. In this paper, we provide evidence that HAO oxidizes NH₂OH by only three electrons to NO under both anaerobic and aerobic conditions. NO₂^– observed in HAO activity assays is a nonenzymatic product resulting from the oxidation of NO by O₂ under aerobic conditions. Finally, our present study implies that aerobic NH₃ oxidation by AOB occurs via two obligate intermediates, NH₂OH and NO, necessitating a mediator of the third enzymatic step.

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Research Organization:: Cornell Univ., Ithaca, NY (United States)

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

Grant/Contract Number:: SC0013997

OSTI ID:: 1371603

Alternate ID(s):: OSTI ID: 1465961

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Vol. 114 Journal Issue: 31; ISSN 0027-8424

Publisher:: Proceedings of the National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 257 works

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References (35)

Principles of structure, bonding, and reactivity for metal nitrosyl complexes Enemark, J. H.; Feltham, R. D. Coordination Chemistry Reviews, Vol. 13, Issue 4 https://doi.org/10.1016/S0010-8545(00)80259-3	journal	September 1974
Nitrite Reductase of Nitrosomonas europaea Is Not Essential for Production of Gaseous Nitrogen Oxides and Confers Tolerance to Nitrite Beaumont, H. J. E.; Hommes, N. G.; Sayavedra-Soto, L. A. Journal of Bacteriology, Vol. 184, Issue 9 https://doi.org/10.1128/JB.184.9.2557-2560.2002	journal	May 2002
Oxidation of Inorganic Nitrogen Compounds Aleem, M. I. H. Annual Review of Plant Physiology, Vol. 21, Issue 1 https://doi.org/10.1146/annurev.pp.21.060170.000435	journal	June 1970
A review of chemical reactions of nitrification intermediates and their role in nitrogen cycling and nitrogen trace gas formation in soil: Chemical reactions of nitrification intermediates in soil Heil, J.; Vereecken, H.; Brüggemann, N. European Journal of Soil Science, Vol. 67, Issue 1 https://doi.org/10.1111/ejss.12306	journal	November 2015
The metabolism of hydroxylamine to nitrite by Nitrosomonas Anderson, Jh Biochemical Journal, Vol. 91, Issue 1 https://doi.org/10.1042/bj0910008	journal	April 1964
Characterization of Hydroxylamine-Cytochrome c Reductase from the Chemoautotrophs Nitrosomonas europaea and Nitrosocystis oceanus Hooper, Alan B.; Nason, Alvin Journal of Biological Chemistry, Vol. 240, Issue 10 https://doi.org/10.1016/S0021-9258(18)97148-6	journal	October 1965
Interaction of Nitric Oxide with Catalase: Structural and Kinetic Analysis Purwar, Namrta; McGarry, Jennifer M.; Kostera, Joshua Biochemistry, Vol. 50, Issue 21 https://doi.org/10.1021/bi200130r	journal	May 2011
Bidirectional Catalysis by Copper-Containing Nitrite Reductase ^† Wijma, Hein J.; Canters, Gerard W.; de Vries, Simon Biochemistry, Vol. 43, Issue 32 https://doi.org/10.1021/bi0496687	journal	August 2004
Spectroscopic Characteristics and Some Chemical Properties of N-Methylphenazinium Methyl Sulfate (Phenazine Methosulfate) and Pyocyanine at the Semiquinoid Oxidation Level Zaugg, Waldo S. Journal of Biological Chemistry, Vol. 239, Issue 11 https://doi.org/10.1016/S0021-9258(18)91229-9	journal	November 1964
Hydroxylamine oxidoreductase of Nitrosomonas Hooper, Alan B.; Terry, K. R. Biochimica et Biophysica Acta (BBA) - Enzymology, Vol. 571, Issue 1 https://doi.org/10.1016/0005-2744(79)90220-1	journal	November 1979
Nitrosomonas europaea cytochrome P460 is a direct link between nitrification and nitrous oxide emission Caranto, Jonathan D.; Vilbert, Avery C.; Lancaster, Kyle M. Proceedings of the National Academy of Sciences, Vol. 113, Issue 51 https://doi.org/10.1073/pnas.1611051113	journal	November 2016
Hydroxylamine metabolism of Nitrosomonas europaea. I. Purification of hydroxylamine oxidase Rees, Michael K. Biochemistry, Vol. 7, Issue 1 https://doi.org/10.1021/bi00841a045	journal	January 1968
Nitrous Oxide (N2O): The Dominant Ozone-Depleting Substance Emitted in the 21st Century Ravishankara, A. R.; Daniel, J. S.; Portmann, R. W. Science, Vol. 326, Issue 5949 https://doi.org/10.1126/science.1176985	journal	August 2009
Processes regulating nitric oxide emissions from soils Pilegaard, Kim Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 368, Issue 1621 https://doi.org/10.1098/rstb.2013.0126	journal	July 2013
Nitroxyl and its anion in aqueous solutions: Spin states, protic equilibria, and reactivities toward oxygen and nitric oxide Shafirovich, V.; Lymar, S. V. Proceedings of the National Academy of Sciences, Vol. 99, Issue 11 https://doi.org/10.1073/pnas.112202099	journal	May 2002
Identification of the sources of nitrous oxide produced by oxidative and reductive processes in Nitrosomonas europaea Ritchie, G. A. F.; Nicholas, D. J. D. Biochemical Journal, Vol. 126, Issue 5 https://doi.org/10.1042/bj1261181	journal	March 1972
The reaction of NO· with O2·− and HO2·−: A pulse radiolysis study Goldstein, Sara; Czapski, Gidon Free Radical Biology and Medicine, Vol. 19, Issue 4 https://doi.org/10.1016/0891-5849(95)00034-U	journal	October 1995
Energy Metabolism in Chemolithotropic Bacteria Lees, H. Annual Review of Microbiology, Vol. 14, Issue 1 https://doi.org/10.1146/annurev.mi.14.100160.000503	journal	October 1960
Properties of 5-methylphenazinium methyl sulfate. Reaction of the oxidized form with NADH and of the reduced form with oxygen. Halaka, F. G.; Babcock, G. T.; Dye, J. L. Journal of Biological Chemistry, Vol. 257, Issue 3 https://doi.org/10.1016/S0021-9258(19)68215-3	journal	February 1982
Clarifying the regulation of NO/N2O production in Nitrosomonas europaea during anoxic–oxic transition via flux balance analysis of a metabolic network model Perez-Garcia, Octavio; Villas-Boas, Silas G.; Swift, Simon Water Research, Vol. 60 https://doi.org/10.1016/j.watres.2014.04.049	journal	September 2014
Hydroxylamine oxidoreductase of Nitrosomonas. Oxidation of diethyldithiocarbamate concomitant with stimulation of nitrite synthesis Hooper, Alan B.; Terry, Kathleen R.; Maxwell, Peter C. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 462, Issue 1 https://doi.org/10.1016/0005-2728(77)90196-7	journal	October 1977
Hydroxylamine as an Intermediate in Nitrification Lees, Howard Nature, Vol. 169, Issue 4291 https://doi.org/10.1038/169156a0	journal	January 1952
Oxidation of hydroxylamine by cytochrome P-460 of the obligate methylotroph Methylococcus capsulatus Bath. Zahn, J. A.; Duncan, C.; DiSpirito, A. A. Journal of Bacteriology, Vol. 176, Issue 19 https://doi.org/10.1128/jb.176.19.5879-5887.1994	journal	October 1994
The Crystal Structure of Cytochrome P460 of Nitrosomonas europaea Reveals a Novel Cytochrome Fold and Heme−Protein Cross-link ^† ^, ^‡ Pearson, Arwen R.; Elmore, Bradley O.; Yang, Cheng Biochemistry, Vol. 46, Issue 28 https://doi.org/10.1021/bi700086r	journal	July 2007
Preliminary characterization of a variant co-binding heme protein from Nitrosomonas Erickson, R. H.; Hooper, A. B. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 275, Issue 2 https://doi.org/10.1016/0005-2728(72)90044-8	journal	August 1972
Mössbauer, EPR, and optical studies of the P-460 center of hydroxylamine oxidoreductase from Nitrosomonas. A ferrous heme with an unusually large quadrupole splitting. Andersson, K. K.; Kent, T. A.; Lipscomb, J. D. Journal of Biological Chemistry, Vol. 259, Issue 11 https://doi.org/10.1016/S0021-9258(17)39803-4	journal	June 1984
Kinetic and product distribution analysis of NO· reductase activity in Nitrosomonas europaea hydroxylamine oxidoreductase Kostera, Joshua; Youngblut, Matthew D.; Slosarczyk, Jeffrey M. JBIC Journal of Biological Inorganic Chemistry, Vol. 13, Issue 7 https://doi.org/10.1007/s00775-008-0393-4	journal	June 2008
Oxidation of hydroxylamine to nitrite catalyzed by hydroxylamine oxidoreductase purified fromNitrosomonas europaea Yamanaka, Tateo; Sakano, Yasuo Current Microbiology, Vol. 4, Issue 4 https://doi.org/10.1007/BF02605864	journal	July 1980
Nitrous oxide production by nitrification and denitrification in soil aggregates as affected by O2 concentration Khalil, K.; Mary, B.; Renault, P. Soil Biology and Biochemistry, Vol. 36, Issue 4 https://doi.org/10.1016/j.soilbio.2004.01.004	journal	April 2004
Autoxidation kinetics of aqueous nitric oxide Ford, Peter C.; Wink, David A.; Stanbury, David M. FEBS Letters, Vol. 326, Issue 1-3 https://doi.org/10.1016/0014-5793(93)81748-O	journal	July 1993
Nitrogen Cycles: Past, Present, and Future Galloway, J. N.; Dentener, F. J.; Capone, D. G. Biogeochemistry, Vol. 70, Issue 2 https://doi.org/10.1007/s10533-004-0370-0	journal	September 2004
Structural Basis of Biological NO Generation by Octaheme Oxidoreductases Maalcke, Wouter J.; Dietl, Andreas; Marritt, Sophie J. Journal of Biological Chemistry, Vol. 289, Issue 3 https://doi.org/10.1074/jbc.M113.525147	journal	December 2013
Complete Genome Sequence of the Ammonia-Oxidizing Bacterium and Obligate Chemolithoautotroph Nitrosomonas europaea Chain, P.; Lamerdin, J.; Larimer, F. Journal of Bacteriology, Vol. 185, Issue 9 https://doi.org/10.1128/JB.185.9.2759-2773.2003	journal	May 2003
Revision of N ₂ O-Producing Pathways in the Ammonia-Oxidizing Bacterium Nitrosomonas europaea ATCC 19718 Kozlowski, Jessica A.; Price, Jennifer; Stein, Lisa Y. Applied and Environmental Microbiology, Vol. 80, Issue 16 https://doi.org/10.1128/AEM.01061-14	journal	June 2014
Spectrophotometric Method for Determining Hydroxylamine Reductase Activity in Higher Plants Frear, D. S.; Burrell, R. C. Analytical Chemistry, Vol. 27, Issue 10 https://doi.org/10.1021/ac60106a054	journal	October 1955

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Title: Nitric oxide is an obligate bacterial nitrification intermediate produced by hydroxylamine oxidoreductase

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