Respiration and growth ofParacoccus denitrificansR-1 with nitrous oxide as an electron acceptor

Abstract

ABSTRACTIn the nitrogen biogeochemical cycle, the reduction of nitrous oxide (N2O) to N2by N2O reductase, which is encoded bynosgene cluster, is the only biological pathway for N2O consumption. However, the capability and mechanisms of microbial N2O reduction are poorly understood. In this study, we investigated the ability to obtain energy for growth ofParacoccus denitrificansR-1 by coupling the oxidation of various electron donors to N2O reduction. This strain has strong N2O reduction capability, and the average N2O reduction rate was 5.10±0.11×10-9μmol·h-1·cell-1under anaerobic condition at 30℃ using acetate as the electron donor in a defined medium. This reduction was accompanied by the stoichiometric consumption of acetate over time when N2O served as the sole electron acceptor and the reduction can yield energy to support microbial growth, suggesting that microbial N2O reduction is an electron transport process. Cu2+, silver nanoparticles, O2, and acidic conditions can strongly inhibit the reduction, whereas NO3-or NH4+can promote it. Genomic analysis showed that the gene cluster encoding N2O reductase ofP. denitrificansR-1 was composed ofnosR,nosZ,nosD,nosF,nosY, andnosL, andnosZ, which was identified as clade I. The respiratory inhibitors test indicated that the pathway of electron transport for N2O reduction was different from that of the traditional electron transport chain for aerobic respiration. These findings suggest that modular N2O reduction byP. denitrificansR-1 is linked to the electron transport chain and energy conservation, and that dissimilatory N2O reduction is a form of microbial anaerobic respiration.IMPOETANCEIn the nitrogen biogeochemical cycle, the reduction of N2O to N2by N2O reductase, which is encoded bynos genes, is the only biological pathway for N2O consumption. However, the capacity and mechanisms of microbial N2O reduction are poorly understood. We investigated the ability to obtain energy for growth of Paracoccus denitrificans R-1 by coupling the oxidation of various electron donors to N2O reduction. Our study showed that the nosZ type I bacterium, P. denitrificans R-1, can respire N2O as the sole electron donor. Thus, the modular N2O reduction process of clade I denitrifiers not only can consume N2O produced by themselves but can also consume the external N2O generated from non-denitrification biological or abiotic pathways under suitable conditions, which is critical for controlling the release of N2O from ecosystems into the atmosphere.