Learning Objectives

• Describe methanogenesis, the organisms that perform this type of metabolism and the environments in which it occurs
• Explain the concept of syntrophy and why it is a critical component of the anaerobic degradation of organics
• Describe how aerobic methanotrophy differs from the anaerobic oxidation of methane
• Describe the risks and benefits of biogenic methane

Methane gas is also known as natural gas. The majority of this gas, both in subsurface reserves, and in various ecosystems, is biogenic. Methanogenesis is catalyzed by a small number of related organisms in the domain Archaea, all of which have genus names with the suffix “Methano” (Figure 10.12).

Methanogens and Methanogenesis

Most methanogens are strict anaerobes. They occur in anoxic environments that are high in organics. They are microbial community members in fresh and salt-water marshes, lake and ocean sediments, hot springs, deep sea vents, animal GI tracts, and environments related to man’s activities: rice paddies, landfills  and the anaerobic digesters in waste water treatment facilities.

Two common pathways of methanogenesis are the hydrogenotrophic and the acetotrophic pathways:

Hydrogenotrophic methanogens are the more predominant type of methanogen. They are litho(auto)trophs, using hydrogen gas as their energy source and fixing CO₂. Like other lithotrophs, oxidation of the H₂ electron donor gives rise to a proton motive force across the plasma membrane. However, this type of methanogenesis is more complex than normal anaerobic respiration. CO₂ also serves as a terminal electron acceptor, but its reduction involves a series of transfers of increasingly reduced carbon molecules between methanogen-specific cofactors. The end result is CH₄ and both proton motive, and sodium motive, force. Methanogens may also derive carbon and energy from simple organic molecules such as acetic acid (acetate), formic acid (formate) and methanol; the first of these, the acetotrophic pathway, is the more common but not as well characterized as the hydrogenotrophic pathway. All of the substrates for methanogenesis, CO₂, H₂, and the organic molecules, are fermentation products of neighbouring organisms. These may be primary fermenters, oxidizing organic molecules NOT produced by fermentation, or secondary fermenters, which oxidize the organic end products of primary fermenters. The methanogenic degradation of organics is depicted in Figure 10.13. 

The methanogens are key players in the anaerobic carbon cycle,  and combined with aerobic and anaerobic methanotrophs, which consume CH_4, allow for the complete recycling of organic matter to CO₂. Methanotrophy is critical, given that methane is a potent greenhouse gas with a 100 year global warming potential approximately 25 times that of CO₂. In lakes and oceans, these processes are relatively well balanced, however anthropogenic methane production, i.e. production related to man’s activities, this is not the case: methanogenesis predominates.

As is true of most anaerobic metabolic processes, the energy yield from methanogenesis is not as high as from aerobic processes. For the hydrogenotrophic pathway, where the electron donor is H₂ and the electron acceptor is CO₂, the is positive, so the reaction yields energy. For aerobic methanotrophs, which would be exposed to methane gas bubbles percolating up through a water column, the is also positive (Figure 10.14).

Syntrophy and Methanogenesis

Unlike heterotrophs performing aerobic or anaerobic respiration, primary fermenters gain ATP only through substrate level phosphorylation. Some of that ATP is used to generate PMF. In addition, the fermentation products are incompletely oxidized organic molecules and therefore still contain some energy. However, fermentation of glucose, using any of  the myriad fermentation pathways that exist, is still exergonic:

Secondary fermenters, on the other hand, may be regarded as thermodynamic extremophiles. They use the organics released by the primary fermenters as their carbon and energy sources, despite the standard Gibbs free energy change of their fermentation reactions being positive: 

In order to grow, secondary fermenters such as Syntrophomonas and Syntrophus, rely on a type of metabolic cooperation called syntrophy: literally, “cross feeding”. Recall from Energy, Redox Reactions and Enzymes that the is the standard free energy change of a reaction when the concentration of reactants and products is the same. For the secondary fermenters, the ability to derive energy from a substrate such as butyrate or benzoate is dependent upon their H₂ end-product and methanogenic partners that rapidly consume that H₂. The reduction in concentration of the H₂ end product shifts the ΔG of the secondary fermentation to a negative sign, making it exergonic. In contrast, the hydrogenotrophic pathway of methanogenesis on its own, is exergonic:

The basis for most types of syntrophy is interspecies H₂ transfer: H₂ production by the syntroph, and H₂ consumption by its partner. The most common type is that involving the methanogens. However, recently the anaerobic oxidation of methane (AOM) has been described, and this is another example of a catabolic process that on its own, should not yield energy. While not well characterized, in some cases, it appears to be mediated by a syntrophic aggregation of methanotrophic archaea and sulphate-reducing bacteria. In others, the syntrophic pairings are able to oxidize methane with nitrate instead of sulphate. Anaerobic methanotrophy is an important process in reducing the emission of methane from the ocean into the atmosphere. It is estimated that almost 90% of all the methane that arises from marine sediments is oxidized anaerobically.

Biogenic Methane: Benefits and Risks

Methane absorbs infrared light and is a potent greenhouse gas, but it is also a renewable energy source. Biogenic methane can be collected and used as a sustainable alternative to fossil fuels. In fact, although older waste water treatment plants burn the CH₄ from their anaerobic digesters (releasing CO₂, a less powerful green-house gas), some of the newer plants trap the methane, using it to power their energy requirements.

In aquatic and marine environments, methanogenesis is largely balanced by methanotrophy. However atmospheric levels have been increasing, as have CO₂ levels, since the advent of the industrial age, and while CO₂ levels are roughly 200x those of CH₄, methane is considerably more potent, and its atmospheric concentration has increased at almost 4x the rate of CO₂. Natural wetlands are by far the major source, followed by numerous anthropogenic sources: rice agriculture, ruminants, the energy sector and waste disposal (biomass burning + landfills)^[1]. In the rumen of cattle and other ruminants, anaerobic organisms, including methanogens, cooperate to digest cellulose into forms usable by the animal. Without these microorganisms, ruminants would not be able to break down the plant material that represents their entire diet. With an increasing global population has come an increase in cattle and dairy farming, and this is often accompanied by the felling of trees to create pasture. Given that an average cow emits an estimated 250 litres of methane per day (in addition to CO₂), and that methane represents a loss of potential energy, methane mitigation in cattle is an active area of research. Cows with fistulas (Figure 10.15) are a common site at veterinary schools; these fistulas allow scientists to access the rumen fluid and hopefully, will one day lead to discoveries that will be of benefit to cattle, cattle farmers, and the planet.

Methane Hydrates

Methane hydrates are reservoirs of methane in the form of CH₄ molecules trapped within a lattice of hydrogen-bonded, frozen water molecules (Figure 10.16). They form under very specific high pressure/low temperature conditions that are associated with marine sediments around continental margins and below arctic permafrost. As long as surrounding temperatures do not rise, these hydrates are stable, and represent massive reservoirs of natural gas, conservatively estimated at ~1.8×10³ Gt carbon^[2]. These reservoirs are therefore of tremendous interest as a potential supply of energy. However, in the face of a warming planet, they also have implications for future climate change. Although there is considerable uncertainty about how much of the hydrates are susceptible to destabilization or “melting”, there is no question that if a tipping point were reached and there was a sudden and massive release of methane, this would also represent a tipping point for the ability of the methanotrophs to consume that methane. Recent evidence suggests that such events have happened over the past millenia, long before the advent of industrialization^[3].