Journal Article

Methane formation driven by reactive oxygen species across all living organisms

Ernst, Leonard, Grimm, Dirk, Dick, Tobias P., Klintzsch, Thomas, Kurth, Markus, Rebelein, Johannes G., Barayeu, Uladzimir, Bischofs, Ilka B., Steinfeld, Benedikt, Keppler, Frank

2022

Overview

Methane (CH 4 ), the most abundant hydrocarbon in the atmosphere, originates largely from biogenic sources 1 linked to an increasing number of organisms occurring in oxic and anoxic environments. Traditionally, biogenic CH 4 has been regarded as the final product of anoxic decomposition of organic matter by methanogenic archaea. However, plants 2 , 3 , fungi 4 , algae 5 and cyanobacteria 6 can produce CH 4 in the presence of oxygen. Although methanogens are known to produce CH 4 enzymatically during anaerobic energy metabolism 7 , the requirements and pathways for CH 4 production by non-methanogenic cells are poorly understood. Here, we demonstrate that CH 4 formation by Bacillus subtilis and Escherichia coli is triggered by free iron and reactive oxygen species (ROS), which are generated by metabolic activity and enhanced by oxidative stress. ROS-induced methyl radicals, which are derived from organic compounds containing sulfur- or nitrogen-bonded methyl groups, are key intermediates that ultimately lead to CH 4 production. We further show CH 4 production by many other model organisms from the Bacteria, Archaea and Eukarya domains, including in several human cell lines. All these organisms respond to inducers of oxidative stress by enhanced CH 4 formation. Our results imply that all living cells probably possess a common mechanism of CH 4 formation that is based on interactions among ROS, iron and methyl donors, opening new perspectives for understanding biochemical CH 4 formation and cycling. Methane formation by a ROS-mediated process is linked to metabolic activity and is identified as a conserved feature across living systems.

• Publisher: Nature Publishing Group UK,Nature Publishing Group
• Subject: 13 / 631/45/47/4113 / 64 / 704/106/47/4113 / Archaea / Archaea - metabolism / Bacteria / Cell Line / Cell lines / Cell Physiological Phenomena / Cyanobacteria / E coli / Euryarchaeota / Experiments / Glucose / Humanities and Social Sciences / Humans / Hydrocarbons / Intermediates / Iron / Iron - metabolism / Labeling / Metabolism / Metabolites / Methane / Methane - chemistry / Methane - metabolism / Methanogenic archaea / Methanogenic bacteria / Methyl radicals / multidisciplinary / Nitrogen / Nitrogen - metabolism / Organic compounds / Organic matter / Organisms / Oxidative stress / Oxygen / Reactive oxygen species / Reactive Oxygen Species - metabolism / Science / Science (multidisciplinary) / Sulfur / Sulfur - metabolism