TY - JOUR

T1 - Kinetics of NH3 -oxidation, NO-turnover, N2 O-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 - Funding information: The authors are members of the Nitrous Oxide Research Alliance (NORA), a Marie Sk?odowska-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 Do€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.

PY - 2017/12

Y1 - 2017/12

N2 - Ammonia oxidising bacteria (AOB) are thought to emit more nitrous oxide (N2 O) than ammonia oxidising archaea (AOA), due to their higher N2 O 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 N2 O 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 N2 O 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.

AB - Ammonia oxidising bacteria (AOB) are thought to emit more nitrous oxide (N2 O) than ammonia oxidising archaea (AOA), due to their higher N2 O 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 N2 O 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 N2 O 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.

KW - Ammonia/metabolism

KW - Ammonium Compounds/metabolism

KW - Archaea/metabolism

KW - Denitrification/physiology

KW - Electrons

KW - Kinetics

KW - Nitric Oxide/biosynthesis

KW - Nitrosomonas europaea/metabolism

KW - Nitrous Oxide/metabolism

KW - Oxidation-Reduction

KW - Oxygen/metabolism

UR - http://www.scopus.com/inward/record.url?scp=85030097868&partnerID=8YFLogxK

U2 - 10.1111/1462-2920.13914

DO - 10.1111/1462-2920.13914

M3 - Article

C2 - 28892283

VL - 19

SP - 4882

EP - 4896

JO - Environmental microbiology

JF - Environmental microbiology

SN - 1462-2912

IS - 12

ER -