Methane-dependent selenate reduction by a bacterial consortium

Methanotrophic microorganisms play a critical role in controlling the flux of methane from natural sediments into the atmosphere. Methanotrophs have been shown to couple the oxidation of methane to the reduction of diverse electron acceptors (e.g., oxygen, sulfate, nitrate, and metal oxides), either...

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Bibliographic Details
Published in:The ISME Journal 2021-12, Vol.15 (12), p.3683-3692
Main Authors: Shi, Ling-Dong, Lv, Pan-Long, McIlroy, Simon J, Wang, Zhen, Dong, Xiao-Li, Kouris, Angela, Lai, Chun-Yu, Tyson, Gene W, Strous, Marc, Zhao, He-Ping
Format: Article
Language:English
Subjects:
Bacteria - genetics
Biogeochemical cycles
Bioreactors
Consortia
Electron transfer
Electrons
Fermentation
Metagenomics
Metal oxides
Methane
Methanotrophic bacteria
Microbial Consortia
Microorganisms
Nitrates
Oxidation
Oxidation-Reduction
Oxygen
Populations
Proteins
Pseudoxanthomonas
Reductases
Sediments
Selenic Acid
Trophic relationships
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Summary:Methanotrophic microorganisms play a critical role in controlling the flux of methane from natural sediments into the atmosphere. Methanotrophs have been shown to couple the oxidation of methane to the reduction of diverse electron acceptors (e.g., oxygen, sulfate, nitrate, and metal oxides), either independently or in consortia with other microbial partners. Although several studies have reported the phenomenon of methane oxidation linked to selenate reduction, neither the microorganisms involved nor the underlying trophic interaction has been clearly identified. Here, we provide the first detailed evidence for interspecies electron transfer between bacterial populations in a bioreactor community where the reduction of selenate is linked to methane oxidation. Metagenomic and metaproteomic analyses of the community revealed a novel species of Methylocystis as the most abundant methanotroph, which actively expressed proteins for oxygen-dependent methane oxidation and fermentation pathways, but lacked the genetic potential for selenate reduction. Pseudoxanthomonas, Piscinibacter, and Rhodocyclaceae populations appeared to be responsible for the observed selenate reduction using proteins initially annotated as periplasmic nitrate reductases, with fermentation by-products released by the methanotrophs as electron donors. The ability for the annotated nitrate reductases to reduce selenate was confirmed by gene knockout studies in an isolate of Pseudoxanthomonas. Overall, this study provides novel insights into the metabolic flexibility of the aerobic methanotrophs that likely allows them to thrive across natural oxygen gradients, and highlights the potential role for similar microbial consortia in linking methane and other biogeochemical cycles in environments where oxygen is limited.
ISSN:1751-7362
1751-7370
DOI:10.1038/s41396-021-01044-3