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

Author:

Zhou Jiaxian12ORCID,Deng Wenfang1,Wu Jiapeng1,Xiang Hua1,Shen Xiaomei1,Lin Jih-Gaw3,Hong Yiguo1ORCID

Affiliation:

1. Institute of Environmental Research at Greater Bay Area; Key Laboratory for Water Quality and Conservation of the Pearl River Delta, Ministry of Education, Guangzhou University, Guangzhou, China

2. School of Environmental Science and Engineering, Guangzhou University, Guangzhou, China

3. Institute of Environmental Engineering, National Yangming Chiao Tung University, Hsinchu City, Taiwan

Abstract

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 nosZ gene, is the only biological pathway for N 2 O consumption. In this study, we successfully isolated a strain of denitrifying Paracoccus denitrificans R-1 from sewage treatment plant sludge. 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 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 related to the energy generation process. 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, nos L, and nos Z, which was identified as that in other strains in clade I. 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. Cu 2+ , silver nanoparticles, O 2 , and acidic conditions can strongly inhibit the reduction, whereas NO 3 - or NH 4 + can promote it. These findings suggest that modular N 2 O reduction of P. denitrificans R-1 is linked to the electron transport and energy conservation, and dissimilatory N 2 O reduction is a form of microbial anaerobic respiration. IMPORTANCE Nitrous oxide (N 2 O) is a potent greenhouse gas and contributor to ozone layer destruction, and atmospheric N 2 O has increased steadily over the past century due to human activities. The release of N 2 O from fixed N is almost entirely controlled by microbial N 2 O 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 N 2 O reduction. The modular N 2 O reduction process of denitrifying microorganism not only can consume N 2 O produced by itself but also can consume the external N 2 O generated from biological or abiotic pathways under suitable condition, which should be critical for controlling the release of N 2 O from ecosystems into the atmosphere.

Funder

MOST | National Natural Science Foundation of China

Publisher

American Society for Microbiology

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