Genome-Scale, Constraint-Based Modeling of Nitrogen Oxide Fluxes during Coculture of Nitrosomonas europaea and Nitrobacter winogradskyi

Brett L Mellbye; Andrew T Giguere; Ganti S Murthy; Peter J Bottomley; Luis A Sayavedra-Soto; Frank W R Chaplen

doi:10.1128/mSystems.00170-17

Genome-Scale, Constraint-Based Modeling of Nitrogen Oxide Fluxes during Coculture of Nitrosomonas europaea and Nitrobacter winogradskyi

mSystems. 2018 Mar 13;3(3):e00170-17. doi: 10.1128/mSystems.00170-17. eCollection 2018 May-Jun.

Authors

Brett L Mellbye¹, Andrew T Giguere², Ganti S Murthy³, Peter J Bottomley^{2

4}, Luis A Sayavedra-Soto¹, Frank W R Chaplen³

Affiliations

¹ Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon, USA.
² Department of Crop and Soil Science, Oregon State University, Corvallis, Oregon, USA.
³ Biological and Ecological Engineering, Oregon State University, Corvallis, Oregon, USA.
⁴ Department of Microbiology, Oregon State University, Corvallis, Oregon, USA.

Abstract

Nitrification, the aerobic oxidation of ammonia to nitrate via nitrite, emits nitrogen (N) oxide gases (NO, NO₂, and N₂O), which are potentially hazardous compounds that contribute to global warming. To better understand the dynamics of nitrification-derived N oxide production, we conducted culturing experiments and used an integrative genome-scale, constraint-based approach to model N oxide gas sources and sinks during complete nitrification in an aerobic coculture of two model nitrifying bacteria, the ammonia-oxidizing bacterium Nitrosomonas europaea and the nitrite-oxidizing bacterium Nitrobacter winogradskyi. The model includes biotic genome-scale metabolic models (iFC578 and iFC579) for each nitrifier and abiotic N oxide reactions. Modeling suggested both biotic and abiotic reactions are important sources and sinks of N oxides, particularly under microaerobic conditions predicted to occur in coculture. In particular, integrative modeling suggested that previous models might have underestimated gross NO production during nitrification due to not taking into account its rapid oxidation in both aqueous and gas phases. The integrative model may be found at https://github.com/chaplenf/microBiome-v2.1. IMPORTANCE Modern agriculture is sustained by application of inorganic nitrogen (N) fertilizer in the form of ammonium (NH₄⁺). Up to 60% of NH₄⁺-based fertilizer can be lost through leaching of nitrifier-derived nitrate (NO₃^-), and through the emission of N oxide gases (i.e., nitric oxide [NO], N dioxide [NO₂], and nitrous oxide [N₂O] gases), the latter being a potent greenhouse gas. Our approach to modeling of nitrification suggests that both biotic and abiotic mechanisms function as important sources and sinks of N oxides during microaerobic conditions and that previous models might have underestimated gross NO production during nitrification.

Keywords: Nitrobacter winogradskyi; Nitrosomonas europaea; genome-scale; hydroxylamine; metabolic modeling; nitric oxide; nitrification; nitrous oxide.