oxygen as a resource that is equally predictably available. On the contrary, there are environments where oxygen is simply absent – often described as ‘extreme’, such as hot springs or deep in the ocean – and many others in which oxygen levels are depleted by biological activity at rates that cannot be counteracted by diffusion or by the activities of photoautotrophs. This is the case, for example, when organic matter decomposes in aquatic environments, and microbial respiration makes a demand for oxygen that exceeds the immediate supply. It is true, too, in water bodies that suffer eutrophication (see Section 21.1.3) when they are overly enriched with nutrients, particularly nitrates and phosphates, often as pollutants, inducing excessive growth of plants and algae that may again deplete oxygen faster than it can be replaced. Many microorganisms living in all these types of environment respire anaerobically, using alternative resources to oxygen as the final electron acceptor in the respiratory process: nitrates, sulphates, CO2, ferric iron and many others. Of course, where oxygen is absent altogether, all those respiring actively must do so anaerobically.
anaerobic respiration: widespread and varied
Anaerobic respiration is generally far less efficient (produces much less energy) than aerobic respiration. Hence, when oxygen is in ready supply, aerobes thrive and anaerobes are little in evidence. However, the balance within ecological communities can change rapidly. One reason is that many microbes are facultatively anaerobic – capable of both aerobic and anaerobic respiration. We see an example in Figure 3.27a, where pitcher plants (carnivorous plants that trap their prey in pitcher‐shaped modified leaves) contain a digestive liquid that supports a community of microbes. Natural communities of pitchers of the northern pitcher plant, Sarracenia purpurea, from Vermont, USA, were compared with pitchers that had been enriched through the repeated addition of finely ground insects (without a microbial community of their own) similar to the plants’ natural prey. Such excess loading of organic material leads to an increase in microbial activity and hypoxic (low oxygen) conditions within the experimental pitchers, as can happen naturally in pitcher plants, and as it does in much large water bodies such as ponds and lakes. The microbial activity within the communities of the control and experimental pitchers were very different, as judged by the peptides within them, which could be extracted, identified and assigned to the types of microbes producing them (Figure 3.27a). When oxygen was readily available as a resource, most of the peptides were contributed by aerobic bacteria. But when oxygen was in very short supply, most came from facultative anaerobes that could rapidly switch their metabolism from aerobic to anaerobic respiration. It is also notable, therefore, that in neither case was there a major contribution from bacteria that were obligatory anaerobes.
Figure 3.27 Enrichment commonly leads to a switch from oxygen to (anaerobic) alternatives as a resource for respiration. (a) The proportion of microbial peptides in communities occupying the pitchers of Sarracenia purpurea that were either controls or enriched, originating from microbes with different respiratory modes. (b) The percentage of taxa that were dormant (metabolically inactive) in control and nitrogen‐enriched plots in saltmarshes over four years. Bold lines are medians, boxes represent 25–75 percentiles and whiskers show ranges, with outliers also shown.
Source: (a) After Northrop et al. (2017). (b) After Kearns et al. (2016).
Similarly, but on a larger scale, enrichment of salt marshes in Massachusetts, USA, led to soil microbial communities in which a much increased proportion of the taxa was dormant, that is, metabolically inactive (Figure 3.27b), but among those that were active, there was a major shift from aerobic to (in this case) obligatorily anaerobic taxa, many using sulphate or sulphur rather than oxygen as their respiratory resource. Clearly the prevalence of dormancy and the presence of facultative anaerobes mean that communities can switch rapidly from a widespread reliance on oxygen to the use of alternative resources for respiration.
APPLICATION 3.5 Permafrost, methanogenic anaerobic respiration and global warming
As the earth warms (see Section 22.2) regions of permafrost near the poles (where the soil remains frozen, year‐round, for at least two consecutive years, see Section 1.5) are thawing. This is leading to a transition in these regions initially to ‘palsa’ habitats – mounds in the landscape supporting lichens and low shrubs – then to partly thawed bogs dominated by mosses (Sphagnum spp.), and then to fully thawed mires dominated by sedges (e.g. Eriophorum spp). This transition itself has potential implications for global warming, since it involves a shift from CO2‐emitting palsas to mires and fens that take up CO2 but emit methane, a more potent greenhouse gas. High‐methane emitting fen habitats contribute seven times as much greenhouse impact as palsa, per unit area (McCalley et al., 2014). Our understanding of the roles played by the microbial communities of the soils in these habitats remains poor. But this is likely to be crucial if we wish to predict the trajectory of the positive feedback loop through which warming leads to thawing, leading to methane emission, more warming, more thawing, and so on. (In Section 17.3 we discuss permafrost as an example of an ecosystem that, on thawing, can pass a ‘tipping point’, shifting it from one regime to another.)
Microbes that produce methane as a respiratory by‐product are Archaea, not bacteria. Most are hydrogenotrophic, using hydrogen as an electron acceptor. However, there is another smaller, but important group that are acetoclastic, cleaving acetate into methane and CO2, and the methane produced by the two groups can be distinguished by characteristic isotopic signatures. Over a natural gradient of thawing in northern Sweden, methane emissions were greater from fully thawed mires than from partly thawed bogs, but were also more dominated by acetoclastic methanogens (Figure 3.28). Crucially, this shifting balance was associated in turn with variation in the ratio of methane‐to‐CO2 production from anaerobic respiration (much higher from mires than from bogs) with consequences in turn for the models currently being used to predict future climate change, which typically assume the fraction of anaerobically metabolised carbon that becomes methane to be fixed (McCalley et al., 2014). Results like those in Figure 3.28 therefore throw doubt on the validity of this simplifying assumption and press the case for further work on the dynamics of anaerobic resource use in these rapidly changing systems.
Figure 3.28 Methane production increases when permafrost thaws,
