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

Abstract

Ammonia (NH 3)-oxidizing bacteria (AOB) emit substantial amounts of nitric oxide (NO) and nitrous oxide (N 2O), both of which contribute to the harmful environmental side effects of large-scale agriculture. The currently accepted model for AOB metabolism involves NH 3 oxidation to nitrite (NO 2 ) via a single obligate intermediate, hydroxylamine (NH 2OH). Within this model, the multiheme enzyme hydroxylamine oxidoreductase (HAO) catalyzes the four-electron oxidation of NH 2OH to NO 2 . In this paper, we provide evidence that HAO oxidizes NH 2OH by only three electrons to NO under both anaerobic and aerobic conditions. NO 2 observed in HAO activity assays is a nonenzymatic product resulting from the oxidation of NO by O 2 under aerobic conditions. Finally, our present study implies that aerobic NH 3 oxidation by AOB occurs via two obligate intermediates, NH 2OH and NO, necessitating a mediator of the third enzymatic step.

Authors:
 [1]; ORCiD logo [1]
  1. Cornell Univ., Ithaca, NY (United States). Dept. of Chemistry and Chemical Biology
Publication Date:
Research Org.:
Cornell Univ., Ithaca, NY (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1371603
Alternate Identifier(s):
OSTI ID: 1465961
Grant/Contract Number:  
SC0013997
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 114; Journal Issue: 31; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; 59 BASIC BIOLOGICAL SCIENCES; nitrification; nitric oxide; enzymology; bioinorganic chemistry

Citation Formats

Caranto, Jonathan D., and Lancaster, Kyle M. Nitric oxide is an obligate bacterial nitrification intermediate produced by hydroxylamine oxidoreductase. United States: N. p., 2017. Web. doi:10.1073/pnas.1704504114.
Caranto, Jonathan D., & Lancaster, Kyle M. Nitric oxide is an obligate bacterial nitrification intermediate produced by hydroxylamine oxidoreductase. United States. doi:10.1073/pnas.1704504114.
Caranto, Jonathan D., and Lancaster, Kyle M. Mon . "Nitric oxide is an obligate bacterial nitrification intermediate produced by hydroxylamine oxidoreductase". United States. doi:10.1073/pnas.1704504114.
@article{osti_1371603,
title = {Nitric oxide is an obligate bacterial nitrification intermediate produced by hydroxylamine oxidoreductase},
author = {Caranto, Jonathan D. and Lancaster, Kyle M.},
abstractNote = {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.},
doi = {10.1073/pnas.1704504114},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 31,
volume = 114,
place = {United States},
year = {2017},
month = {7}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: 10.1073/pnas.1704504114

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Cited by: 35 works
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Works referenced in this record:

Principles of structure, bonding, and reactivity for metal nitrosyl complexes
journal, September 1974


Nitrite Reductase of Nitrosomonas europaea Is Not Essential for Production of Gaseous Nitrogen Oxides and Confers Tolerance to Nitrite
journal, May 2002


Oxidation of Inorganic Nitrogen Compounds
journal, June 1970


The metabolism of hydroxylamine to nitrite by Nitrosomonas
journal, April 1964


Interaction of Nitric Oxide with Catalase: Structural and Kinetic Analysis
journal, May 2011

  • Purwar, Namrta; McGarry, Jennifer M.; Kostera, Joshua
  • Biochemistry, Vol. 50, Issue 21
  • DOI: 10.1021/bi200130r

Bidirectional Catalysis by Copper-Containing Nitrite Reductase
journal, August 2004

  • Wijma, Hein J.; Canters, Gerard W.; de Vries, Simon
  • Biochemistry, Vol. 43, Issue 32
  • DOI: 10.1021/bi0496687

Hydroxylamine oxidoreductase of Nitrosomonas
journal, November 1979


Nitrosomonas europaea cytochrome P460 is a direct link between nitrification and nitrous oxide emission
journal, November 2016

  • Caranto, Jonathan D.; Vilbert, Avery C.; Lancaster, Kyle M.
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 51
  • DOI: 10.1073/pnas.1611051113

Hydroxylamine metabolism of Nitrosomonas europaea. I. Purification of hydroxylamine oxidase
journal, January 1968


Nitrous Oxide (N2O): The Dominant Ozone-Depleting Substance Emitted in the 21st Century
journal, August 2009


Processes regulating nitric oxide emissions from soils
journal, July 2013

  • Pilegaard, Kim
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 368, Issue 1621
  • DOI: 10.1098/rstb.2013.0126

Nitroxyl and its anion in aqueous solutions: Spin states, protic equilibria, and reactivities toward oxygen and nitric oxide
journal, May 2002

  • Shafirovich, V.; Lymar, S. V.
  • Proceedings of the National Academy of Sciences, Vol. 99, Issue 11
  • DOI: 10.1073/pnas.112202099

Identification of the sources of nitrous oxide produced by oxidative and reductive processes in Nitrosomonas europaea
journal, March 1972

  • Ritchie, G. A. F.; Nicholas, D. J. D.
  • Biochemical Journal, Vol. 126, Issue 5
  • DOI: 10.1042/bj1261181

The reaction of NO· with O2·− and HO2·−: A pulse radiolysis study
journal, October 1995


Energy Metabolism in Chemolithotropic Bacteria
journal, October 1960


Hydroxylamine oxidoreductase of Nitrosomonas. Oxidation of diethyldithiocarbamate concomitant with stimulation of nitrite synthesis
journal, October 1977

  • Hooper, Alan B.; Terry, Kathleen R.; Maxwell, Peter C.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 462, Issue 1
  • DOI: 10.1016/0005-2728(77)90196-7

Hydroxylamine as an Intermediate in Nitrification
journal, January 1952


Oxidation of hydroxylamine by cytochrome P-460 of the obligate methylotroph Methylococcus capsulatus Bath.
journal, October 1994


The Crystal Structure of Cytochrome P460 of Nitrosomonas europaea Reveals a Novel Cytochrome Fold and Heme−Protein Cross-link ,
journal, July 2007

  • Pearson, Arwen R.; Elmore, Bradley O.; Yang, Cheng
  • Biochemistry, Vol. 46, Issue 28
  • DOI: 10.1021/bi700086r

Preliminary characterization of a variant co-binding heme protein from Nitrosomonas
journal, August 1972


Kinetic and product distribution analysis of NO· reductase activity in Nitrosomonas europaea hydroxylamine oxidoreductase
journal, June 2008

  • Kostera, Joshua; Youngblut, Matthew D.; Slosarczyk, Jeffrey M.
  • JBIC Journal of Biological Inorganic Chemistry, Vol. 13, Issue 7
  • DOI: 10.1007/s00775-008-0393-4

Oxidation of hydroxylamine to nitrite catalyzed by hydroxylamine oxidoreductase purified fromNitrosomonas europaea
journal, July 1980

  • Yamanaka, Tateo; Sakano, Yasuo
  • Current Microbiology, Vol. 4, Issue 4
  • DOI: 10.1007/BF02605864

Nitrous oxide production by nitrification and denitrification in soil aggregates as affected by O2 concentration
journal, April 2004


Autoxidation kinetics of aqueous nitric oxide
journal, July 1993


Nitrogen Cycles: Past, Present, and Future
journal, September 2004


Structural Basis of Biological NO Generation by Octaheme Oxidoreductases
journal, December 2013

  • Maalcke, Wouter J.; Dietl, Andreas; Marritt, Sophie J.
  • Journal of Biological Chemistry, Vol. 289, Issue 3
  • DOI: 10.1074/jbc.M113.525147

Complete Genome Sequence of the Ammonia-Oxidizing Bacterium and Obligate Chemolithoautotroph Nitrosomonas europaea
journal, May 2003


Revision of N 2 O-Producing Pathways in the Ammonia-Oxidizing Bacterium Nitrosomonas europaea ATCC 19718
journal, June 2014

  • Kozlowski, Jessica A.; Price, Jennifer; Stein, Lisa Y.
  • Applied and Environmental Microbiology, Vol. 80, Issue 16
  • DOI: 10.1128/AEM.01061-14

Spectrophotometric Method for Determining Hydroxylamine Reductase Activity in Higher Plants
journal, October 1955

  • Frear, D. S.; Burrell, R. C.
  • Analytical Chemistry, Vol. 27, Issue 10
  • DOI: 10.1021/ac60106a054