Kinetics of NH3-oxidation, NO-turnover, N2O-production and electron flow during oxygen depletion in model bacterial and archaeal ammonia oxidisers

Linda Hink, Pawel Lycus, Cécile Gubry-Rangin, Åsa Frostegård, Graeme W. Nicol, James I. Prosser, Lars R. Bakken

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Abstract

Ammonia oxidising bacteria (AOB) are thought to emit more nitrous oxide (N2O) than ammonia oxidising archaea (AOA), due to their higher N2O yield under oxic conditions and denitrification in response to oxygen (O2) limitation. We determined the kinetics of growth and turnover of nitric oxide (NO) and N2O at low cell densities of Nitrosomonas europaea (AOB) and Nitrosopumilus maritimus (AOA) during gradual depletion of TAN (NH3 + NH4+) and O2. Half-saturation constants for O2 and TAN were similar to those determined by others, except for the half-saturation constant for ammonium in N. maritimus (0.2 mM), which is orders of magnitudes higher than previously reported. For both strains, cell-specific rates of NO turnover and N2O production reached maxima near O2 half-saturation constant concentration (2-10 µM O2) and decreased to zero in response to complete O2-depletion. Modelling of the electron flow in N. europaea demonstrated low electron flow to denitrification (≤1.2% of the total electron flow), even at sub-micromolar O2 concentrations. The results corroborate current understanding of the role of NO in the metabolism of AOA and suggest that denitrification is inconsequential for the energy metabolism of AOB, but possibly important as a route for dissipation of electrons at high ammonium concentration. This article is protected by copyright. All rights reserved.
Original languageEnglish
Pages (from-to)4882-4896
Number of pages15
JournalEnvironmental Microbiology
Volume19
Issue number12
Early online date21 Sep 2017
DOIs
Publication statusPublished - Dec 2017

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nitric oxide
nitrous oxide
Ammonia
oxidants
turnover
Nitric Oxide
ammonia
electrons
Electrons
oxidation
Oxygen
oxygen
kinetics
Denitrification
electron
Archaea
Triacetoneamine-N-Oxyl
Nitrosomonas europaea
denitrification
saturation

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Kinetics of NH3-oxidation, NO-turnover, N2O-production and electron flow during oxygen depletion in model bacterial and archaeal ammonia oxidisers. / Hink, Linda; Lycus, Pawel; Gubry-Rangin, Cécile; Frostegård, Åsa; Nicol, Graeme W.; Prosser, James I.; Bakken, Lars R.

In: Environmental Microbiology, Vol. 19, No. 12, 12.2017, p. 4882-4896.

Research output: Contribution to journalArticle

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title = "Kinetics of NH3-oxidation, NO-turnover, N2O-production and electron flow during oxygen depletion in model bacterial and archaeal ammonia oxidisers",
abstract = "Ammonia oxidising bacteria (AOB) are thought to emit more nitrous oxide (N2O) than ammonia oxidising archaea (AOA), due to their higher N2O yield under oxic conditions and denitrification in response to oxygen (O2) limitation. We determined the kinetics of growth and turnover of nitric oxide (NO) and N2O at low cell densities of Nitrosomonas europaea (AOB) and Nitrosopumilus maritimus (AOA) during gradual depletion of TAN (NH3 + NH4+) and O2. Half-saturation constants for O2 and TAN were similar to those determined by others, except for the half-saturation constant for ammonium in N. maritimus (0.2 mM), which is orders of magnitudes higher than previously reported. For both strains, cell-specific rates of NO turnover and N2O production reached maxima near O2 half-saturation constant concentration (2-10 µM O2) and decreased to zero in response to complete O2-depletion. Modelling of the electron flow in N. europaea demonstrated low electron flow to denitrification (≤1.2{\%} of the total electron flow), even at sub-micromolar O2 concentrations. The results corroborate current understanding of the role of NO in the metabolism of AOA and suggest that denitrification is inconsequential for the energy metabolism of AOB, but possibly important as a route for dissipation of electrons at high ammonium concentration. This article is protected by copyright. All rights reserved.",
author = "Linda Hink and Pawel Lycus and C{\'e}cile Gubry-Rangin and {\AA}sa Frosteg{\aa}rd and Nicol, {Graeme W.} and Prosser, {James I.} and Bakken, {Lars R.}",
note = "The authors are members of the Nitrous Oxide Research Alliance (NORA), a Marie Skłodowska-Curie ITN and research project under the EU's seventh framework program (FP7), 316472. GN is funded by the AXA Research Fund and CGR by a Royal Society fellowship. We thank Lars Molstad and Peter D{\"o}rsch for their generous and invaluable technical assistance. We thank Martin G Klotz for a very constructive review of our paper, and especially for pointing out the possible electron dissipation via periplasmic cytochromes, thus providing a possible explanation for the high N2O at high ammonium concentrations.",
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T1 - Kinetics of NH3-oxidation, NO-turnover, N2O-production and electron flow during oxygen depletion in model bacterial and archaeal ammonia oxidisers

AU - Hink, Linda

AU - Lycus, Pawel

AU - Gubry-Rangin, Cécile

AU - Frostegård, Åsa

AU - Nicol, Graeme W.

AU - Prosser, James I.

AU - Bakken, Lars R.

N1 - The authors are members of the Nitrous Oxide Research Alliance (NORA), a Marie Skłodowska-Curie ITN and research project under the EU's seventh framework program (FP7), 316472. GN is funded by the AXA Research Fund and CGR by a Royal Society fellowship. We thank Lars Molstad and Peter Dörsch for their generous and invaluable technical assistance. We thank Martin G Klotz for a very constructive review of our paper, and especially for pointing out the possible electron dissipation via periplasmic cytochromes, thus providing a possible explanation for the high N2O at high ammonium concentrations.

PY - 2017/12

Y1 - 2017/12

N2 - Ammonia oxidising bacteria (AOB) are thought to emit more nitrous oxide (N2O) than ammonia oxidising archaea (AOA), due to their higher N2O yield under oxic conditions and denitrification in response to oxygen (O2) limitation. We determined the kinetics of growth and turnover of nitric oxide (NO) and N2O at low cell densities of Nitrosomonas europaea (AOB) and Nitrosopumilus maritimus (AOA) during gradual depletion of TAN (NH3 + NH4+) and O2. Half-saturation constants for O2 and TAN were similar to those determined by others, except for the half-saturation constant for ammonium in N. maritimus (0.2 mM), which is orders of magnitudes higher than previously reported. For both strains, cell-specific rates of NO turnover and N2O production reached maxima near O2 half-saturation constant concentration (2-10 µM O2) and decreased to zero in response to complete O2-depletion. Modelling of the electron flow in N. europaea demonstrated low electron flow to denitrification (≤1.2% of the total electron flow), even at sub-micromolar O2 concentrations. The results corroborate current understanding of the role of NO in the metabolism of AOA and suggest that denitrification is inconsequential for the energy metabolism of AOB, but possibly important as a route for dissipation of electrons at high ammonium concentration. This article is protected by copyright. All rights reserved.

AB - Ammonia oxidising bacteria (AOB) are thought to emit more nitrous oxide (N2O) than ammonia oxidising archaea (AOA), due to their higher N2O yield under oxic conditions and denitrification in response to oxygen (O2) limitation. We determined the kinetics of growth and turnover of nitric oxide (NO) and N2O at low cell densities of Nitrosomonas europaea (AOB) and Nitrosopumilus maritimus (AOA) during gradual depletion of TAN (NH3 + NH4+) and O2. Half-saturation constants for O2 and TAN were similar to those determined by others, except for the half-saturation constant for ammonium in N. maritimus (0.2 mM), which is orders of magnitudes higher than previously reported. For both strains, cell-specific rates of NO turnover and N2O production reached maxima near O2 half-saturation constant concentration (2-10 µM O2) and decreased to zero in response to complete O2-depletion. Modelling of the electron flow in N. europaea demonstrated low electron flow to denitrification (≤1.2% of the total electron flow), even at sub-micromolar O2 concentrations. The results corroborate current understanding of the role of NO in the metabolism of AOA and suggest that denitrification is inconsequential for the energy metabolism of AOB, but possibly important as a route for dissipation of electrons at high ammonium concentration. This article is protected by copyright. All rights reserved.

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SN - 1462-2912

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ER -