Abstract

Anaerobic oxidation of methane (AOM) is one of the major processes limiting the release of the greenhouse gas methane from natural environments. In Lake Kinneret sediments, iron-coupled AOM (Fe-AOM) was suggested to play a substantial role (10–15 % relative to methanogenesis) in the methanic zone (> 20 cm sediment depth), based on geochemical profiles and experiments on fresh sediments. Apparently, the oxidation of methane is mediated by a combination of mcr gene bearing archaea and aerobic bacterial methanotrophs. Here we aimed to investigate the survival of this complex microbial interplay under controlled conditions. We followed the AOM process during long-term (~18 months) anaerobic slurry experiments of these methanic sediments with two stages of incubations and additions of 13C-labeled methane, multiple electron acceptors and inhibitors. After these incubation stages carbon isotope measurements in the dissolved inorganic pool still showed considerable AOM (3–8 % relative to methanogenesis). Specific lipid carbon isotope measurements and metagenomic analyses indicate that after the prolonged incubation aerobic methanotrophic bacteria were no longer involved in the oxidation process, whereas mcr gene bearing archaea were most likely responsible for oxidizing the methane. Humic substances and iron oxides are likely electron acceptors to support this oxidation, whereas sulfate, manganese, nitrate, and nitrite did not support the AOM in these methanic sediments. Our results suggest in the natural lake sediments methanotrophic bacteria are responsible for part of the methane oxidation by the reduction of combined micro levels of oxygen and iron oxides in a cryptic cycle, while the rest of the methane is converted by reverse methanogenesis. After long-term incubation, the latter prevails without bacterial methanotropic activity and with a different iron reduction pathway.

Highlights

  • Methane (CH4) is an effective greenhouse gas (Wuebbles and Hayhoe, 2002) with anthropogenic and natural origins

  • This is by quantifying the modifications between experiments conducted on fresh sediments from the methanic zone

  • The geochemical experiments tested the potential of several electron acceptors to perform and stimulate this considerable Anaerobic oxidation of methane (AOM) process

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Summary

Introduction

Methane (CH4) is an effective greenhouse gas (Wuebbles and Hayhoe, 2002) with anthropogenic and natural origins. Aerobic as well as anaerobic oxidation of methane (AOM) control the release of this greenhouse gas to the atmosphere from its natural sources (Conrad, 2009; Reeburgh, 2007; Knittel and Boetius, 2009). While sulfate-dependent AOM, which is catalyzed by ANaerobic MEthanotrophs ANMEs 1-3, is widespread in marine environments (Hoehler et al, 1994; Boetius et al, 2000; Orphan et al, 2001; Treude et al, 2005, 2014), methane oxidation could theoretically be coupled to other electron acceptors. Humic substances, which shuttle electrons in anaerobic environments, may act as the terminal electron acceptors for AOM by ANME-2 (Scheller et al, 2016; Valenzuela et al., 2017; 2019; Bai et al, 2019)

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