Different oxygen affinities of methanotrophs and Comammox Nitrospira inform an electrically induced symbiosis for nitrogen loss

Hao Wu; Wen-Bo Nie; Xin Tan; Guo-Jun Xie; Han Qu; Xin Zhang; Zhihao Xian; Jingyi Dai; Chun Yang; Yi Chen

doi:10.1016/j.watres.2024.121606

Different oxygen affinities of methanotrophs and Comammox Nitrospira inform an electrically induced symbiosis for nitrogen loss

Water Res. 2024 Apr 11:256:121606. doi: 10.1016/j.watres.2024.121606. Online ahead of print.

Authors

Hao Wu¹, Wen-Bo Nie², Xin Tan³, Guo-Jun Xie⁴, Han Qu¹, Xin Zhang¹, Zhihao Xian¹, Jingyi Dai¹, Chun Yang¹, Yi Chen⁵

Affiliations

¹ College of Environment and Ecology, Key Laboratory of the Three Gorges Reservoir Region's Eco-Environment, Ministry of Education, Chongqing University, Chongqing 400045, China.
² College of Environment and Ecology, Key Laboratory of the Three Gorges Reservoir Region's Eco-Environment, Ministry of Education, Chongqing University, Chongqing 400045, China. Electronic address: nwb1994@cqu.edu.cn.
³ The Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, University of Queensland, St Lucia, Queensland 4072, Australia; State Key Laboratory of Urban Water Resource and Environment, School of Environment, Harbin Institute of Technology, Harbin 150090, China.
⁴ State Key Laboratory of Urban Water Resource and Environment, School of Environment, Harbin Institute of Technology, Harbin 150090, China.
⁵ College of Environment and Ecology, Key Laboratory of the Three Gorges Reservoir Region's Eco-Environment, Ministry of Education, Chongqing University, Chongqing 400045, China. Electronic address: chenyi8574@cqu.edu.cn.

PMID: 38631236
DOI: 10.1016/j.watres.2024.121606

Abstract

Aerobic methanotrophs establish a symbiotic association with denitrifiers to facilitate the process of aerobic methane oxidation coupled with denitrification (AME-D). However, the symbiosis has been frequently observed in hypoxic conditions continuing to pose an enigma. The present study has firstly characterized an electrically induced symbiosis primarily governed by Methylosarcina and Hyphomicrobium for the AME-D process in a hypoxic niche caused by Comammox Nitrospira. The kinetic analysis revealed that Comammox Nitrospira exhibited a higher apparent oxygen affinity compared to Methylosarcina. While the coexistence of comammox and AME-D resulted in an increase in methane oxidation and nitrogen loss rates, from 0.82 ± 0.10 to 1.72 ± 0.09 mmol CH₄ d^-1 and from 0.59 ± 0.04 to 1.30 ± 0.15 mmol N₂ d^-1, respectively. Furthermore, the constructed microbial fuel cells demonstrated a pronounced dependence of the biocurrents on AME-D due to oxygen competition, suggesting the involvement of direct interspecies electron transfer in the AME-D process under hypoxic conditions. Metagenomic and metatranscriptomic analysis revealed that Methylosarcina efficiently oxidized methane to formaldehyde, subsequently generating abundant NAD(P)H for nitrate reduction by Hyphomicrobium through the dissimilatory RuMP pathway, leading to CO₂ production. This study challenges the conventional understanding of survival mechanism employed by AME-D symbionts, thereby contributing to the characterization responsible for limiting methane emissions and promoting nitrogen removal in hypoxic regions.

Keywords: Comammox; Direct interspecies electron transfer; Dissimilatory RuMP pathway; Methane oxidation; Nitrogen loss; Oxygen affinity.