title: The production of nitric oxide by marine ammonia-oxidizing archaea and inhibition of archaeal ammonia oxidation by a nitric oxide scavenger.
abstract: Nitrification is a critical process for the balance of reduced and oxidized nitrogen pools in nature, linking mineralization to the nitrogen loss processes of denitrification and anammox. Recent studies indicate a significant contribution of ammonia-oxidizing archaea (AOA) to nitrification. However, quantification of the relative contributions of AOA and ammonia-oxidizing bacteria (AOB) to in situ ammonia oxidation remains challenging. We show here the production of nitric oxide (NO) by Nitrosopumilus maritimus SCM1. Activity of SCM1 was always associated with the release of NO with quasi-steady state concentrations between 0.05 and 0.08 μM. NO production and metabolic activity were inhibited by the nitrogen free radical scavenger 2-phenyl-4,4,5,5,-tetramethylimidazoline-1-oxyl-3-oxide (PTIO). Comparison of marine and terrestrial AOB strains with SCM1 and the recently isolated marine AOA strain HCA1 demonstrated a differential sensitivity of AOB and AOA to PTIO and allylthiourea (ATU). Similar to the investigated AOA strains, bulk water column nitrification at coastal and open ocean sites with sub-micromolar ammonia/ammonium concentrations was inhibited by PTIO and insensitive to ATU. These experiments support predictions from kinetic, molecular and biogeochemical studies, indicating that marine nitrification at low ammonia/ammonium concentrations is largely driven by archaea and suggest an important role of NO in the archaeal metabolism.
authors.affiliation: Department of Civil and Environmental Engineering, University of Washington, Seattle, WA, 98195, USA.
authors.forename: Willm
authors.initials: W
authors.lastname: Martens-Habbena
authors.affiliation: Department of Civil and Environmental Engineering, University of Washington, Seattle, WA, 98195, USA.
authors.forename: Wei
authors.initials: W
authors.lastname: Qin
authors.affiliation: School of Oceanography, University of Washington, Seattle, WA, 98195, USA.
authors.forename: Rachel E A
authors.initials: RE
authors.lastname: Horak
authors.affiliation: Department of Marine and Ecological Sciences, Florida Gulf Coast University, Fort Myers, FL, 33965, USA.
authors.forename: Hidetoshi
authors.initials: H
authors.lastname: Urakawa
authors.affiliation: Department of Earth and Space Sciences, University of Washington, Seattle, WA, 98195, USA.
authors.forename: Andrew J
authors.initials: AJ
authors.lastname: Schauer
authors.affiliation: Department of Biological Sciences, University of Southern California, Los Angeles, CA, 90089, USA.
authors.forename: James W
authors.initials: JW
authors.lastname: Moffett
authors.affiliation: School of Oceanography, University of Washington, Seattle, WA, 98195, USA.
authors.forename: E Virginia
authors.initials: EV
authors.lastname: Armbrust
authors.affiliation: School of Oceanography, University of Washington, Seattle, WA, 98195, USA.
authors.forename: Anitra E
authors.initials: AE
authors.lastname: Ingalls
authors.affiliation: School of Oceanography, University of Washington, Seattle, WA, 98195, USA.
authors.forename: Allan H
authors.initials: AH
authors.lastname: Devol
authors.affiliation: Department of Civil and Environmental Engineering, University of Washington, Seattle, WA, 98195, USA.
authors.forename: David A
authors.initials: DA
authors.lastname: Stahl
mesh_terms: D000641:Ammonia / Q000378:metabolism*; D064751:Ammonium Compounds / Q000378:metabolism; D059001:Aquatic Organisms / Q000378:metabolism; D001105:Archaea / Q000378:metabolism*; D020562:Betaproteobacteria / Q000378:metabolism; D003497:Cyclic N-Oxides / Q000494:pharmacology*; D058440:Denitrification; D007093:Imidazoles / Q000494:pharmacology*; D009569:Nitric Oxide / Q000096:biosynthesis / Q000378:metabolism*; D058465:Nitrification; D009584:Nitrogen / Q000378:metabolism; D010084:Oxidation-Reduction; D013890:Thiourea / Q000031:analogs & derivatives* / Q000494:pharmacology
chemical_list: D064751:Ammonium Compounds; D003497:Cyclic N-Oxides; D007093:Imidazoles; C079391:2-phenyl-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide; D009569:Nitric Oxide; C009842:allylthiourea; D000641:Ammonia; D013890:Thiourea; D009584:Nitrogen