Methane formation driven by reactive oxygen species across all living organisms

Abstract

Methane (CH4) is the most abundant organic compound in the atmosphere, largely originating from anthropogenic and natural biogenic sources1. Traditionally, biogenic CH4 has been regarded as the nal product of the anoxic decomposition of organic matter by methanogenic Archaea. However, plants2-4, fungi5, algae6,7 and cyanobacteria8 have recently been shown to produce CH4 in the presence of oxygen. While methanogens produce CH4 enzymatically during anaerobic energy metabolism9, the requirements and pathways for CH4 production by "non-methanogenic" cells are poorly understood. Here we demonstrate that CH4 formation by Bacillus subtilis is triggered by free iron species, enhanced by oxidative stress and restricted to metabolically active life-cycle stages. We also show that other model organisms from Bacteria and Eukarya including a human cell line release CH4 and respond to inducers of oxidative stress by enhanced CH4 formation. Our results imply that all living cells possess a common mechanism of CH4 formation without the need for speci c enzymes. We propose that CH4 formation is a conserved feature of living systems which is coupled to metabolic activity and the concomitant generation of reactive oxygen species. Our ndings open new perspectives for our understanding of environmental CH4 cycling, oxidative stress responses and the search for extraterrestrial life. BackgroundMethane is a highly potent greenhouse gas that affects Earth's climate. Around 70 % of all emissions to the atmosphere derive from biogenic sources 10 . Biological CH 4 formation has long been considered to occur only under strictly anoxic conditions in organisms belonging to the domain Archaea. To generate the cellular fuel ATP, methanogenic archaea convert simple compounds, such as CO 2 , H 2 or acetate, into CH 4 . This process of methanogenesis depends on reactions that are catalysed by unique sets of enzymes and co-enzymes 9 . In addition, small amounts of CH 4 can be formed via 'mini-methanogenesis' in several sulphate-reducing bacteria which contain the enzyme carbon monoxide dehydrogenase 11,12 . However, during the past 15 years, evidence has been accumulating that other organisms produce CH 4 under aerobic conditions. These include both multicellular organisms, such as plants 2-4 and saprotrophic fungi 5 , and unicellular organisms, including marine and freshwater algae 6,13 and cyanobacteria 8 . These organisms generate energy via photosynthesis and/or respiration, and it is unclear why and how they release CH 4 . Multiple marine and freshwater bacteria harbouring the C-P lyase pathway have been reported to generate CH 4 from methylphosphonate [14][15][16][17][18] . Several bacteria and archaea have also been shown to possess alternative nitrogenases 19,20 or nitrogenase-like reductases 21 , which can produce CH 4 and other hydrocarbons. In addition -as we will demonstrate here -living systems can form CH 4 without the need for speci c enzymes, and such pathways could drive CH 4 formation in all cells.In plants, CH 4 formation is enha...

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