13.4: Methane

Like carbon dioxide, microorganisms can both make and consume methane. Microorganisms that produce methane as a major product of their catabolism are known as methanogens, whereas those that consume it as an electron donor are known as methanotrophs. In addition to these groups, there are also microorganisms that produce methane as a byproduct of their metabolism. Some key information for each of these groups is briefly summarized below and more details are available in the discussion of the carbon cycle in Chapter 5 (sections 5.1.4 and 5.1.6).

Methanogens are all members of domain Archaea and are considered to be obligate anaerobes, meaning they are only able to survive under anoxic conditions. Moreover, their activity also tends to be limited where nitrate and sulfate are available and in some cases where ferric (oxyhydr)oxides are available (Marquart et al., 2019) (Sections 8.5, 9.3, and 10.2.5). Anoxic conditions with low nitrate and sulfate availability often occur in wetland soils, lake and river sediments, and animal intestines. Zones hosting active methanogens are also found in the subsurface, especially in organic-rich layers such as coalbeds and black shales, where electron acceptors needed for alternative microbial metabolisms are often in low supply.

Recent studies have shined a bright light on methane production by microbial groups not considered to be methanogens. These microorganisms can form methane as a byproduct when they cleave methyl groups from organic matter as they scavenge for nutrients (Repeta et al., 2016; Yao Mengyin et al., 2016) or through the reaction of some nitrogenases and nitrogenase-like enzymes (North Justin A. et al., 2020; Zheng et al., 2018). Recent research also shows that cyanobacteria can produce methane at significant rates under both oxic and anoxic conditions (Bižić M. et al., 2020). Although methanogenic Archaea deserve much attention as methane producers, these alternative pathways can also be significant. Thottathil et al. (2022) demonstrated that oxic methane production accounted for up to 76% of the methane in the five small lakes they studied.

Methanotrophs can couple oxidation of methane to reduction of oxygen, nitrate, ferric iron, and sulfate, in some cases with assistance from partner microorganisms (Section 5.1.6). Thus, they can be active in both oxic and anoxic environments. A recent review of published studies indicated that methane oxidation is primarily carried out by anaerobes in the oceans, where it mostly occurs within sediments (Gao et al., 2022). In contrast, the study found that aerobic methanotrophs typically consume more methane than anaerobic methanotrophs in wetlands, rice paddies, lakes, and rivers (Gao et al., 2022). Collectively, aerobic and anaerobic methanotrophs play a major role in helping limit atmospheric methane levels. For example, annual methane formation in ocean sediment is estimated to be \(85 \text{-} 300 \text{Tg/yr}\). Most (>90%) is consumed by methanotrophs before it can reach the atmosphere (Knittel and Boetius, 2009). In general, the amount of methane emitted from an ecosystem ultimately reflects the balance between methane production and methane oxidation (Bridgham et al., 2013).

As first example of these reactions in an environmental context, we consider microbial methane production in wetlands. Wetlands are the single largest natural source of methane and estimated to account for about a third of global emissions (Bridgham et al., 2013). Water saturation within wetlands can create anoxic conditions that are conducive to methanogen growth. Specifically, when soil pores are filled with water, oxygen transport within them becomes limited. If the rate of electron acceptor use exceeds that rate at which oxygen can be supplied, anoxic conditions can develop that may be suitable for methanogens, depending on the availability of nitrate, sulfate, and ferric iron. Food sources for methanogens in wetlands typically include degradation of organic matter as well as organic substrates delivered by plants through root exudates (Bridgham et al., 2013).

Soils that are largely oxic in wetlands may also host methanogens within anoxic microenvironments. For example, Angle et al. (2017) examined methanogenesis in soils beneath three wetland land coverage types: areas covered with plants, periodically exposed mudflats, and continuously submerged soils. They observed similar oxygen depth profiles at all three sites. Depths shallower than 10 cm were always oxic and those deeper than 25 cm were always anoxic. Net methane production occurred at all three land-use types during their sampling seasons, and the largest methane generation occurred in oxygenated layers. An analysis of the microbial community demonstrated that the microorganisms forming the methane were methanogenic Archaea, not those that produce it as a byproduct. There was also no evidence that the methanogens had oxygen tolerance genes, leading the researchers to suggest that methanogen activity occurred in anoxic microenvironments within oxic zones of the wetland soils.

Methane can leave a wetland by diffusion, bubble release (i.e., ebullition), and plant-mediated transport (Bridgham et al., 2013). The extent to which methane is exposed to methanotrophy likely differs between these pathways. Ebullition and transport through plants may allow methane to bypass zones of aerobic methanotrophy (Bridgham et al., 2013). In contrast, relatively slow transport by diffusion may provide greater opportunity for methanotrophs to consume the methane before it escapes to the atmosphere. Thus, differences in methane transport may contribute to differences in the balance between methanotrophy and methanogenesis between systems or over time with an individual system.

As a second example, we briefly consider the recent study by D’Ambrosio and Harrison (2021), who studied methane sources and sinks in lake sediments. Data collected from 60 different lakes and reservoirs showed that methane was more likely to escape oxidation by methanotrophs if methane was being rapidly produced. In other words, methanotrophy was less efficient as a microbial filter for methane removal where methane production was high. Furthermore, they observed a strong positive correlation between methane production rate and the availability of nutrients. Eutrophic lakes, those rich in nutrients and biological productivity, tend to have high methane emissions. Taken together, these observations imply, therefore, that lower methane oxidation efficiencies contribute to greater methane emissions in such systems.

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