A shifting paradigm – Archaea aren’t the only organisms that produce methane

Most methane is produced by anaerobic Archaea. The formation and fate of methane has been the study of intensive research over several decades, because of its great importance in aquatic, terrestrial and atmospheric processes. Methane has a global warming potential ~28 times that of CO2 over 100 years. Until recently, methanogenesis was thought to be unique to members of certain genera of the Euryarchaeota (one of major phyla of the Archaea) which possess specific co-enzymes for the transfer of electrons from hydrogen (or other electron donors) and act as carriers for the C1 unit from the CO2 substrate to the CH4 end-product.  These methanogens occur widely in terrestrial soils, wetlands, the guts of animals (especially ruminants and termites), decomposing waste, and aquatic sediments.

Source: Global Carbon Project; CC-BY-4.0 via Wikimedia Commons

Methanogenesis in marine sediments. Methanogenesis is the final step in the anaerobic degradation of organic material that falls to the sea floor. In this process, CO2 serves both as an oxidant for energy generation and as a source of carbon for incorporation into cellular material. Methane produced in anoxic marine sediments has several fates. Under appropriate geological conditions of pressure and temperature, this methane can be trapped in crystalline form (clathrate), which forms vast deposits under the continental shelf. Much of the methane is used by anaerobic consortia of archaeal and bacterial cells that couple its oxidation to reduction of sulfate.  Methane that seeps upwards into the oxic layers of the seabed has a major role in deep ocean processes, as it is used by a wide range of methylotrophic bacteria, including symbionts of invertebrates. Almost none of this methane reaches the atmosphere.

Bubbles of methane emerging from a methane seep. Credit: NOAA Okeanos Explorer Program, Gulf of Mexico 2012.

Aerobic production of methane from methylphosphonates. The paradox that well-oxygenated surface seawater is supersaturated with methane has baffled oceanographers for many years. An important consequence is that 3-4% of atmospheric methane comes from oceanic sources. Some of this methane is produced in anoxic niches inside marine snow particles or by the intestinal microbiota of marine animals, but we now know that another route is the release of methane from methylphosphonate (MPn)­–containing compounds that are present is seawater (Karl et al., 2008) . These have a stable phosphonate (C-P) bond, but this can be cleaved by a lyase enzyme. Microbial genes encoding C-P lyase have since been found in marine metagenomes and demonstrated in a range of aerobic bacterioplankton, including the dominant SAR11 clade (Carini et al., 2014) in phosphate-limited ocean regions (Sosa et al., 2019). The methane is a by-product of the C-P lyase reaction, whose main function for the bacteria appears to be to provide phosphate for synthesis of nucleotides and lipids. This process also occurs in large freshwater lakes; Grossart et al. (2011) demonstrated high levels of methane in the upper, well-oxygenated layers of large freshwater lakes—far from the anoxic sediments and shore-based sources— and Yao et al. (2016) confirmed that this is due to C-P lyase under phosphate limitation. An alternative reaction, recently shown in the cyanobacterium Prochlorococcus is the oxidation of MPn, providing carbon from the methyl group which is used in biosynthesis (Sosa et al., 2019.)

Cyanobacteria can produce methane directly. The latest evidence to overturn the paradigm that anaerobic Archaea are the only organisms to make methane comes from a study by Bižić et al. (2020) of the Leibniz Institute in Germany. In the freshwater Lake Stechlin, increased levels of methane have often been associated with blooms of cyanobacteria. To confirm this, Mina Bižić and colleagues cultured 13 different filamentous and unicellular cyanobacteria from marine, freshwater and terrestrial environments in ambient water containing bicarbonate labelled with the stable isotope 13C (NaH13CO3). Mass spectrometry showed that 13CH4 was formed in the cultures. This might be explained by the provision of hydrogen arising from the metabolism of the cyanobacteria to associated methanogenic archaea (in anoxic niches) This was ruled out as a mechanism because the oxygen levels in the cultures were above saturation level and transcriptomic and Q-PCR analysis found no evidence for the activity of genes linked to archaeal methanogenesis. Thus, cyanobacteria appear to form methane directly, probably linked to general cell metabolism. It also doesn’t seem to be due to the cleavage of MPn, because there is no limitation of phosphate in this lake and no evidence for expression of C-P lyase genes could be detected in the experimental cultures. Indeed, several of the cyanobacteria used do not possess the C-P lyase genes. Further experiments showed that methane is formed under both light and dark conditions, but the process appears to be closely linked to photosynthesis. The authors suggest that there may be a direct connection to the photosynthetic electron transport chain, but the mechanism is currently unknown. There may be complex interactions, perhaps involving use of freshly fixed carbon compounds in the light and use of storage compounds in the dark. Cyanobacteria possess many of the genes involved in methanogenesis but, crucially, they lack methyl coenzyme reductase (mcr). How significant is this process? Bižić et al. note that the rate of methane production in these cyanobacteria is very low (~103–104 times lower than methanogenic archaea under optimal conditions), so it is difficult to assess how significant cyanobacterial production is to the global methane budget. However, they point out the ubiquitous presence of this group of organisms in aquatic and terrestrial habitats and their propensity to form large blooms due to eutrophication and rising temperatures means that it is important to obtain better understanding of the process.

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