Methane Cycling Communities Under Global Climate Change

Arctic surface temperatures have increased on average to a greater extent than those of the rest of the earth (IPCC 2001), causing a particular susceptibility of Arctic permafrost to degradation. Global warming could degrade 25% of the total permafrost area by 2100 (Anisimov et al. 1999). Also, Nelson et al. (2001) predicted a high potential for large areas of Siberian permafrost to be degraded, which would primarily lead to a thickening of the seasonally thawed layer (active layer). In the period 1956-1990, the active layer in Russian permafrost already increased by on average 20 cm (IPCC 2007). By the end of the twenty-first century, an increase of mean annual ground temperature by up to 6°C and of active-layer depth by up to 2 m is expected for East Siberia (Stendel et al. 2007). Although the estimated size of the carbon pool in Arctic permafrost-affected tundra varies between 190 Gt and, in more recent studies, approximately 900 Gt, it accounts for at least 13-15% of the global carbon pool in soils (Post et al. 1982; Zimov et al. 2006). Thawing of 10% of the total Siberian permafrost carbon reservoir was suggested to initially release about 1 Pg carbon, followed by respiration of about 40 Pg carbon to the atmosphere over a period of four decades (Dutta et al. 2006). Model calculations suggest that methane currently emitted from Arctic permafrost environments may enhance the greenhouse effect with a portion of approx. 20% (Wuebbles and Hayhoe 2002). Palaeoclimate reconstruction combined with biogeochemical biomarker analysis, for example, revealed an increase in production and release of methane from the terrestrial biosphere during the Palaeocene-Eocene thermal maximum, a period of intense global warming 55 million years ago (Pancost et al. 2007). It has also been shown that an increase of the permafrost temperature in Holocene permafrost deposits of northern Siberia would lead to a substantial rise in microbiologically produced methane (Wagner et al. 2007). Serious concerns are thus associated with the potential impact that thawing permafrost may have on the global climate system through release of greenhouse gases (Friborg et al. 2003; Christensen et al. 2004; Wagner et al. 2007). Methane flux models do indeed predict increasing methane emissions in latitudes above 60°N by 19-25% (Cao et al. 1998; Walter et al. 2001; Zhuang et al. 2004). These estimates are challenged, though, by other studies suggesting that increasing methane fluxes from Russian permafrost regions will change atmospheric methane concentrations by only 0.04 ppm (2.3%), leading to 0.012°C temperature rise globally (Anisimov 2007).

Models of modern methane emissions from Arctic wetlands determine methane production and methane oxidation rates primarily as functions of substrate availability, substrate concentration, and temperature, as well as indirectly of water table and thaw depth (Walter et al. 2001; Zhuang et al. 2004; Anisimov 2007). Changes of these parameters will consequently lead to short-term alterations of methane production and methane oxidation rates. Whether, however, the currently observed global climate change will effectively alter modern methane fluxes from Arctic permafrost-affected wetlands will particularly depend on its long-term impact on the methane-cycling communities and their ability to adapt to the new environmental conditions. This ability is very likely dependant on the level of specialisation and diversity of the indigenous microbial communities. It has been observed that an increase of temperature and precipitation altered the community structure and relative abundance of methane oxidizers in rice, forest and grassland soils (Horz et al. 2005; Mohanty et al. 2007). Also, the overall relative abundance and diversity of methanogenic archaea in a high Arctic peat from Spitsbergen increased with increasing temperature, in conjunction with a strong stimulation of methane production rates (H0j et al. 2008).

In contrast, the population structure of methanogenic archaea in permafrost-affected peat in Siberia remained constant over a wide temperature range (Metje and Frenzel 2007). Also, a psychrophilic and little diverse methanotrophic community as detected near the permafrost table of Siberian polygonal tundra soils (Liebner and Wagner 2007; Liebner et al. 2008) will likely require more time for resilience than the diverse mesophilic-psychrotolerant methanogenic community detected in permafrost soils of the same region (Ganzert et al. 2007).

There is, however, a lack of experimental research investigating the long-term effect of simulated climate change on the methane-cycling communities in permafrost soils, which would be essential to prove or disprove the previously mentioned assumptions. Also, an account of the entire plant-microbe-animal syste, and the interactions between metabolic networks which are important for methanogenesis, is missing in modern methane flux models (Panikov 1999). Due to this poor knowledge, it is worthwhile considering microbial communities in the context of global climate change in general. Simulating the effects of warming on the competition between psychrophilic and mesophilic sub-populations of Pseudomonas, for example, displayed a high degree of stability of this artificial community (Panikov 1999). Psychrophiles dominated the bacterial community under cold conditions, and an increase in temperature by 5°C did not affect their domination. Further warming of another 5°C resulted in a rapid 50% substitution of psychrophiles by mesophiles over 2 years, finally reaching a stable coexistence between the two sub-populations. In the same model, the main effect of rising temperatures on the carbon balance of the ecosystem was a considerable activation of organic matter decomposition due to higher production of hydrolytic enzymes. Experimental setups revealed a rather low direct impact of rising temperatures on the decomposition of soil organic matter, but rather attributed increased decomposition rates most strongly to be due to changes in local substrate characteristics and vegetation type (Zhang et al. 2005; Bokhorst et al. 2007). Still, a shift in the microbial community structure induced by warming was again observed, at least in the first study.

To summarize, there is an urgent need for modelling the response of methane-cycling communities in permafrost regions to global climate change on the one hand, and to validate these models by empirical data on the other hand. This is not only due to the importance of these communities for the atmospheric methane budget and thus for the global climate. It is also inevitable, given the close connection between physiology and function of these communities in permafrost soils that allows for a general understanding of how important the stability of microbial communities is for the greenhouse gases budget of Arctic permafrost-affected wetlands.

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