Methane-dependent selenate reduction by a bacterial consortium

Abstract

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.

pH-Dependent Hydrogenotrophic Denitratation Based on Self-Alkalization

“…During the whole denitrification process involving a series of enzymes, nitrate and nitrite reductases are responsible for producing and consuming nitrite. Consistent with the observation of nitrate reduction, the microbial consortium harbored 11 periplasmic nitrate reductase genes ( napA ) and 16 respiratory nitrate reductase genes ( narG ), both belonging to the dimethyl sulfoxide reductase (DMSOR) family (Figure a) . The gene and transcript abundances of napA were obviously decreased, as well as the absolute transcription level, after acetate was replaced with H 2 as the sole electron donor (Figure b,c).…”

Coupled Aerobic Methane Oxidation and Arsenate Reduction Contributes to Soil-Arsenic Mobilization in Agricultural Fields

“…Overall, reaction stoichiometry, metagenomic analyses, and metabolite measurements all support a synergistic nature of methane-dependent arsenate reduction, carried out by the aerobic methanotrophs and members of Burkholderiaceae, with formate as the interspecies electron carrier. Formate is well known to support methanogenesis-based syntrophy − and was demonstrated to mediate the methane-oxidation-based selenate reduction recently . The present study provides another clear example for formate coupling aeMO to the reduction of oxides, highlighting the possibility that similar trophic relationships may link methane metabolism to a range of terminal electron acceptors in (hyp)­oxic environments.…”

“…Formate is well known to support methanogenesis-based syntrophy 74−76 and was demonstrated to mediate the methane-oxidation-based selenate reduction recently. 77 The present study provides another clear example for formate coupling aeMO to the reduction of oxides, highlighting the possibility that similar trophic relationships may link methane metabolism to a range of terminal electron acceptors in (hyp)oxic environments.…”

Formate as an Alternative Electron Donor for the Anaerobic Methanotrophic Archaeon Candidatus ‘Methanoperedens nitroreducens’

“…For instance, methanotrophs are widely distributed in freshwater sediment and groundwater and have been reported to metabolize methane under oxygen-limited conditions and produce formate. The methane-derived products can be further utilized by synergistic populations. , Environmental surveys also suggested that methanotrophs thrive under hypoxic conditions where ANME are active. , This implies a potential syntrophic relationship between methanotrophs and ANME in environments with limited methane and/or oxygen.…”