Respiration and growth of Paracoccus denitrificans R-1 with nitrous oxide as an electron acceptor

In the nitrogen biogeochemical cycle, the reduction of nitrous oxide (N₂O) to N₂ by N₂O reductase, which is encoded by nosZ gene, is the only biological pathway for N₂O consumption. In this study, we successfully isolated a strain of denitrifying Paracoccus denitrificans R-1 from sewage treatment plant sludge. This strain has strong N₂O reduction capability, and the average N₂O reduction rate was 5.10 ± 0.11 × 10^-9 µmol·h^-1·cell^-1 under anaerobic condition 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 related to the energy generation process. Genomic analysis showed that the gene cluster encoding N₂O reductase of P. denitrificans R-1 was composed of nosR, nosZ, nosD, nosF, nosY, nosL, and nosZ, which was identified as that in other strains in clade I. 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. Cu²⁺, silver nanoparticles, O₂, and acidic conditions can strongly inhibit the reduction, whereas NO₃^- or NH₄⁺ can promote it. These findings suggest that modular N₂O reduction of P. denitrificans R-1 is linked to the electron transport and energy conservation, and dissimilatory N₂O reduction is a form of microbial anaerobic respiration.

Nitrous oxide (N₂O) is a potent greenhouse gas and contributor to ozone layer destruction, and atmospheric N₂O has increased steadily over the past century due to human activities. The release of N₂O from fixed N is almost entirely controlled by microbial N₂O reductase activities. Here, we investigated the ability to obtain energy for the growth of Paracoccus denitrificans R-1 by coupling the oxidation of various electron donors to N₂O reduction. The modular N₂O reduction process of denitrifying microorganism not only can consume N₂O produced by itself but also can consume the external N₂O generated from biological or abiotic pathways under suitable condition, which should be critical for controlling the release of N₂O from ecosystems into the atmosphere.