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

ABSTRACT In the nitrogen biogeochemical cycle, the reduction of nitrous oxide (N 2 O) to N 2 by N 2 O reductase, which is encoded by nos gene cluster, is the only biological pathway for N 2 O consumption. However, the capability and mechanisms of microbial N 2 O reduction are poorly understood. In this study, we investigated the ability to obtain energy for growth of Paracoccus denitrificans R-1 by coupling the oxidation of various electron donors to N 2 O reduction. This strain has strong N 2 O reduction capability, and the average N 2 O reduction rate was 5.10±0.11×10 -9 μmol·h -1 ·cell -1 under 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 N 2 O served as the sole electron acceptor and the reduction can yield energy to support microbial growth, suggesting that microbial N 2 O reduction is an electron transport process. Cu 2+ , silver nanoparticles, O 2 , and acidic conditions can strongly inhibit the reduction, whereas NO 3 - or NH 4 + can promote it. Genomic analysis showed that the gene cluster encoding N 2 O reductase of P. denitrificans R-1 was composed of nos R, nos Z, nos D, nos F, nos Y, and nos L, and nos Z, which was identified as clade I. The respiratory inhibitors test indicated that the pathway of electron transport for N 2 O reduction was different from that of the traditional electron transport chain for aerobic respiration. These findings suggest that modular N 2 O reduction by P. denitrificans R-1 is linked to the electron transport chain and energy conservation, and that dissimilatory N 2 O reduction is a form of microbial anaerobic respiration. IMPOETANCE In the nitrogen biogeochemical cycle, the reduction of N 2 O to N 2 by N 2 O reductase, which is encoded by nos genes , is the only biological pathway for N 2 O consumption. However, the capacity and mechanisms of microbial N 2 O 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 N 2 O reduction. Our study showed that the nosZ type I bacterium, P. denitrificans R-1, can respire N 2 O as the sole electron donor. Thus, the modular N 2 O reduction process of clade I denitrifiers not only can consume N 2 O produced by themselves but can also consume the external N 2 O generated from non-denitrification biological or abiotic pathways under suitable conditions, which is critical for controlling the release of N 2 O from ecosystems into the atmosphere.