Methane formation across living organisms driven by ROS: new perspectives for understanding of biochemical methane formation and cycling on Earth

Methane (CH₄) is the most abundant hydrocarbon in the atmosphere, largely originating from biogenic sources that recently have been linked to an increasing number of organisms living in both oxic and anoxic environments. Traditionally, biogenic CH₄ has been regarded as the final product of the anoxic decomposition of organic matter by methanogenic Archaea. However, plants, fungi, algae, lichens and cyanobacteria have recently been shown to produce CH₄ in the presence of oxygen. While methanogens produce CH₄ enzymatically during anaerobic energy metabolism, the requirements and pathways for CH₄ production by “non-methanogenic” cells are poorly understood. Here, we present a CH₄ formation mechanism that most likely occurs in all living organisms (Ernst et al. 2022). Firstly, we show results from two bacterial species (Bacillus subtilis and Escherichia coli) demonstrating that CH₄ formation 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, derived from organic compounds containing sulfur- or nitrogen-bonded methyl groups, are key intermediates that ultimately lead to CH₄.

In a second step, we made numerous experiments and collected data from many other model organisms (over 30 species) from the three domains of life (Bacteria, Archaea and Eukarya), including several human cell lines and a non-methanogenic archaeal species. All of the selected species clearly showed CH₄ formation under sterile growth conditions. As the mechanism described for CH₄ formation depends on several factors such as the availability of methylated precursor compounds, free iron, cellular stress factors and antioxidants, production rates can vary by several orders of magnitude. For terrestrial plants and cyanobateria, measured CH₄ emission rates have been reported to vary by almost four orders of magnitude. In both cases, rates were measured for many species and under varying environmental conditions and stressors, although the formation mechanism(s) were unknown. Our proposed ROS-driven pathway not only provides a mechanistic explanation for the observed CH₄ emissions under oxic conditions but also for the large variability of emission rates observed for terrestrial plants, marine and freshwater algae, fungi, lichens and cyanobacteria, which have caused many controversial discussions since their publication. Furthermore, now it is very clear that any global upscaling will be highly challenging given the complex variables that control emissions from specific organisms.

In summary, the observed and experimental validated process of CH₄ formation across all living organisms is a major step to better understand biological CH₄ (in addition to the well-described archaeal methanogenesis) formation and cycling on Earth.

Reference:

Ernst, L., Steinfeld, B., Barayeu, U., Klintzsch, T., Kurth, M., Grimm, D., Dick, T.P., Rebelein, J.G., Bischofs, I.B., Keppler, F. (2022). ROS-driven methane formation across living organisms. Nature, in press.