Nitrate-dependent anaerobic methane oxidation coupled to Fe(III) reduction as a source of ammonium and nitrous oxide

Xin Tan; Yang Lu; Wen-Bo Nie; Paul Evans; Xiao-Wei Wang; Cheng-Cheng Dang; Xuan Wang; Bing-Feng Liu; De-Feng Xing; Nan-Qi Ren; Guo-Jun Xie

doi:10.1016/j.watres.2024.121571

Nitrate-dependent anaerobic methane oxidation coupled to Fe(III) reduction as a source of ammonium and nitrous oxide

Water Res. 2024 Apr 3:256:121571. doi: 10.1016/j.watres.2024.121571. Online ahead of print.

Authors

Xin Tan¹, Yang Lu², Wen-Bo Nie³, Paul Evans⁴, Xiao-Wei Wang⁵, Cheng-Cheng Dang⁵, Xuan Wang⁵, Bing-Feng Liu⁵, De-Feng Xing⁵, Nan-Qi Ren⁵, Guo-Jun Xie⁶

Affiliations

¹ State Key Laboratory of Urban Water Resource and Environment, School of Environment, Harbin Institute of Technology, Harbin 150090, China; The Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, University of Queensland, St Lucia, Queensland 4072, Australia.
² The Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, University of Queensland, St Lucia, Queensland 4072, Australia.
³ Key Laboratory of the Three Gorges Region's Eco-Environment, Ministry of Education, College of Environment and Ecology, Chongqing University, Chongqing 400044, China.
⁴ The Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, University of Queensland, St Lucia, Queensland 4072, Australia. Electronic address: p.evans3@uq.edu.au.
⁵ State Key Laboratory of Urban Water Resource and Environment, School of Environment, Harbin Institute of Technology, Harbin 150090, China.
⁶ State Key Laboratory of Urban Water Resource and Environment, School of Environment, Harbin Institute of Technology, Harbin 150090, China. Electronic address: xgj@hit.edu.cn.

PMID: 38583332
DOI: 10.1016/j.watres.2024.121571

Abstract

'Candidatus Methanoperedens nitroreducens' is an archaeal methanotroph with global importance that links carbon and nitrogen cycles and great potential for sustainable operation of wastewater treatment. It has been reported to mediate the anaerobic oxidation of methane through a reverse methanogenesis pathway while reducing nitrate to nitrite. Here, we demonstrate that 'Ca. M. nitroreducens' reduces ferric iron forming ammonium (23.1 %) and nitrous oxide (N₂O, 46.5 %) from nitrate. These results are supported with the upregulation of genes coding for proteins responsible for dissimilatory nitrate reduction to ammonium (nrfA), N₂O formation (norV, cyt P460), and multiple multiheme c-type cytochromes for ferric iron reduction. Concomitantly, an increase in the N₂O-reducing SJA-28 lineage and a decrease in the nitrite-reducing 'Candidatus Methylomirabilis oxyfera' are consistent with the changes in 'Ca. M. nitroreducens' end products. These findings demonstrate the highly flexible physiology of 'Ca. M. nitroreducens' in anaerobic ecosystems with diverse electron acceptor conditions, and further reveals its roles in linking methane oxidation to global biogeochemical cycles. 'Ca. M. nitroreducens' could significantly affect the bioavailability of nitrogen sources as well as the emission of greenhouse gas in natural ecosystems and wastewater treatment plants.

Keywords: Anaerobic methane oxidation; Dissimilatory nitrate reduction to ammonium; Greenhouse gas; Nitrogen removal; Nitrous oxide.