Abstract

SummaryMethanotrophic bacteria play a key role in limiting methane emissions from lakes. It is generally assumed that methanotrophic bacteria are mostly active at the oxic‐anoxic transition zone in stratified lakes, where they use oxygen to oxidize methane. Here, we describe a methanotroph of the genera Methylobacter that is performing high‐rate (up to 72 μM day−1) methane oxidation in the anoxic hypolimnion of the temperate Lacamas Lake (Washington, USA), stimulated by both nitrate and sulfate addition. Oxic and anoxic incubations both showed active methane oxidation by a Methylobacter species, with anoxic rates being threefold higher. In anoxic incubations, Methylobacter cell numbers increased almost two orders of magnitude within 3 days, suggesting that this specific Methylobacter species is a facultative anaerobe with a rapid response capability. Genomic analysis revealed adaptations to oxygen‐limitation as well as pathways for mixed‐acid fermentation and H2 production. The denitrification pathway was incomplete, lacking the genes narG/napA and nosZ, allowing only for methane oxidation coupled to nitrite‐reduction. Our data suggest that Methylobacter can be an important driver of the conversion of methane in oxygen‐limited lake systems and potentially use alternative electron acceptors or fermentation to remain active under oxygen‐depleted conditions.

Highlights

  • The concentration of atmospheric methane, a potent greenhouse gas, has increased strongly since the preindustrial era. Knittel and Boetius (2009) estimated that 10–20% of all reactive organic matter buried in sediments is converted to methane

  • Freshwater anaerobic oxidation of methane (AOM) with sulfate has been suggested to take place in freshwater sediments (Schubert et al, 2011). Both nitrate and nitrite were used as electron acceptors for AOM in methanotrophic cultures originating from freshwater sediments or water (Raghoebarsing et al, 2006; Ettwig et al, 2010; Deutzmann and Schink, 2011; Kits et al, 2015b; Oswald et al, 2017)

  • Freshwater methane oxidation under anoxic conditions has been observed to be performed by ANME (Eller et al, 2005; Zigah et al, 2015), by methane-oxidizing bacteria working in close cooperation with photosynthetic oxygen producers (Oswald et al, 2015), or by bacteria of the Ca

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Summary

Introduction

The concentration of atmospheric methane, a potent greenhouse gas, has increased strongly since the preindustrial era. Knittel and Boetius (2009) estimated that 10–20% of all reactive organic matter buried in sediments is converted to methane. Iron and manganese oxides have been suggested to function as potential electron acceptors for methane oxidation in brackish sediments (Egger et al, 2014; Ettwig et al, 2016). Freshwater anaerobic oxidation of methane (AOM) with sulfate has been suggested to take place in freshwater sediments (Schubert et al, 2011) Both nitrate and nitrite were used as electron acceptors for AOM in methanotrophic cultures originating from freshwater sediments or water (Raghoebarsing et al, 2006; Ettwig et al, 2010; Deutzmann and Schink, 2011; Kits et al, 2015b; Oswald et al, 2017). The humic acid analogues quinone and anthraquinone-2,7-disulphonate have been implicated in anaerobic methane oxidation, a direct coupling between methane oxidation and reduction of organic material has not yet been demonstrated (Reed et al, 2017)

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