O2 versus N2O respiration in a continuous microbial enrichment

Monica Conthe,Robbert Kleerebezem,Camiel Parchen,Gerben Stouten,Mark C M Van Loosdrecht

doi:10.1007/s00253-018-9247-3

Monica Conthe, Robbert Kleerebezem + Show 3 more

Open Access

https://doi.org/10.1007/s00253-018-9247-3

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Abstract

Despite its ecological importance, essential aspects of microbial N2O reduction—such as the effect of O2 availability on the N2O sink capacity of a community—remain unclear. We studied N2O vs. aerobic respiration in a chemostat culture to explore (i) the extent to which simultaneous respiration of N2O and O2 can occur, (ii) the mechanism governing the competition for N2O and O2, and (iii) how the N2O-reducing capacity of a community is affected by dynamic oxic/anoxic shifts such as those that may occur during nitrogen removal in wastewater treatment systems. Despite its prolonged growth and enrichment with N2O as the sole electron acceptor, the culture readily switched to aerobic respiration upon exposure to O2. When supplied simultaneously, N2O reduction to N2 was only detected when the O2 concentration was limiting the respiration rate. The biomass yields per electron accepted during growth on N2O are in agreement with our current knowledge of electron transport chain biochemistry in model denitrifiers like Paracoccus denitrificans. The culture’s affinity constant (KS) for O2 was found to be two orders of magnitude lower than the value for N2O, explaining the preferential use of O2 over N2O under most environmentally relevant conditions.

Highlights

Coping with rising levels of the potent greenhouse gas nitrous oxide (N2O) in the atmosphere calls for the development of mitigation strategies to reduce N2O accumulation and emission in soil management and wastewater treatment (WWT)
A culture enriched from activated sludge using acetate as a carbon source and electron donor and exogenous N2O as the sole electron acceptor was studied for a total period of 155 days (> 100 volume changes) in a chemostat under electron acceptor (N2O) limiting conditions (Figure S1)
Aerobic respiration was distinctly favored over N2O respiration in the enrichment despite the fact that the culture had been operated for an extensive number of generations with N2O as only electron acceptor

Summary

Introduction

Coping with rising levels of the potent greenhouse gas nitrous oxide (N2O) in the atmosphere calls for the development of mitigation strategies to reduce N2O accumulation and emission in soil management and wastewater treatment (WWT). The presence and activity of N2O-reducing organisms in fertilized soils and WWT plants, such as bacteria and archaea harboring nosZ-type genes, may be key in such mitigating strategies (Thomson et al 2012). Nitrous oxide reductase (N2OR), the enzyme encoded by the nosZ gene, is a terminal reductase present in some microbial respiratory electron transport chains (ETC) that catalyzes the only microbial reaction known to consume N2O, converting it to innocuous N2 (which constitutes 79% of the Earth’s atmosphere). Even though N2O is a stronger electron acceptor than O2 in terms of thermodynamics, a number of authors have shown that N2O respiration is energetically less efficient than aerobic respiration, resulting in lower biomass growth yields per substrate (Koike and Hattori 1975; Stouthamer et al 1982; Beun et al 2000).

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