The western North American Arctic is currently experiencing the fastest rate of warming on earth. Here, the rate of temperature increase has reached 0.1 °C per year over the last 35 years (Anisimov et al., 2007), highlighting the relevance of Polar Regions as sensitive indicators of global climate trends. Of particular concern are the globally significant C-stores that have accumulated in tundra soils in response to cold and short growing seasons and the presence of permafrost, which restricts drainage. Current Arctic warming is associated with increased microbial activity leading to higher plant N availability (Chapin, 1983; Nadelhoffer et al., 1992; Aerts, 2006) and faster C turnover in soils (Hobbie & Chapin, 1998; Shaver et al., 2006; Rinnan et al., 2007b; Biasi et al., 2008). These findings have led to a growing concern that warming threatens the stability of Arctic C-stores, which upon release are likely to result in significant, additional, positive climate forcing (Cox et al., 2000; Schuur et al., 2009).
Soil bacteria and fungi are central to the C balance of tundra ecosystems because of their dual role as decomposers of soil organic matter and as determinants of plant community diversity (Van der Heijden et al., 1998, 2008), which in turn controls the quality and quantity of C inputs to soils (De Deyn et al., 2008). Currently, Arctic soil microorganisms experience temperatures substantially below their apparent physiological optima. While significant bacterial growth has been observed in frozen soils (McMahon et al., 2009) and in soils as cold as −6 °C (Rinnan et al., 2011), the optimal temperature for bacterial growth in a sub-Arctic heath soil was 25 °C (Rinnan et al., 2011), and measured Q10 values for respiration in Arctic tundra soils are similar (Mano et al., 2003) or equivalent (Anderson, 2010) to the median global Q10 of 2.4 (Raich & Schlesinger, 1992). These findings suggest that warmer Arctic soils should lead to substantially greater microbial activity and growth and to greater CO2 losses to the atmosphere. Evidence to suggest that this happens, is however, somewhat lacking. For example, experimental warming by open-top greenhouses for 7 or 17 years led to 28% and 73% reductions in bacterial growth in a sub-Arctic heath, which was interpreted to reflect decreased availabilities of labile substrates with warming (Rinnan et al., 2011). Likewise, the very few studies that have measured the response of soil fungi to warming have found small or no changes in the concentrations of their lipid or sterol biomarkers (Rinnan et al., 2007a, 2008, 2009).
Warming-induced changes in the composition of soil microbial communities have the potential to cause sustained changes in microbial activity (Schimel & Gulledge, 1998; Bardgett et al., 2008), yet despite their importance to the stability of Arctic C-stores we lack a sound understanding of the response of soil microbial communities to warming. Progress is hampered by: (1) the many interacting biotic and abiotic factors that structure microbial communities, which may in themselves be altered by warming; (2) the response time of belowground communities to experimental warming is often slow (Rinnan et al., 2007a; Biasi et al., 2008; Lamb et al., 2011); and (3) the vast diversity in physiology and function of soil microorganisms means that their response to warming is unlikely to be monotonic. This last point is well illustrated in a series of studies that sought to examine the response of N-cycling soil bacteria to warming treatment on Ellesmere Island, Canada. Warming treatment had strong impacts on the structure of nitrogen-fixing bacterial communities as characterized by analysis of nifH genes (Deslippe et al., 2005), but similar analysis of nosZ communities found site factors to be more important than warming in structuring denitrifier communities (Walker et al., 2008) and no significant effect of warming was found on ammonia oxidizing bacterial amoA communities (Lamb et al., 2011). The diversity of responses of soil microorganisms to warming treatment suggests that it may be necessary to employ methods that allow for high taxonomic resolution of microorganisms to gain a comprehensive understanding of the response of the community as a whole.
In this study, we tested the hypothesis that long-term warming alters the composition and structure of soil bacterial and fungal communities in Low-Arctic tundra. We utilized warming treatments maintained as part of the Arctic Long-Term Ecological Research (LTER) experiment at Toolik Lake Alaska, which had been in place for 18 years, allowing us insight to longer-term responses. Despite good evidence for winter-time bacterial activity and growth in frozen Arctic tundra soils (McMahon et al., 2009, 2011), studies that have included a temporal component to their sampling report fairly stable bacterial community assemblages across seasons (Männistö et al., 2007; Wallenstein et al., 2007; McMahon et al., 2011). Thus, we predicted that microbial community change resulting from warming would be greater than that because of normal seasonal succession during the thawed-soil seasons (spring–autumn). Given that no field experiment could completely partition all interacting factors that influence soil microbial community structure, one advantage of the LTER experiment is that it allows for the combined effects of warming on biota to be evaluated, including the nonlinear responses that may have been difficult to predict. In moist acidic tundra (MAT), the LTER warming treatments lead to the increasing dominance of the deciduous ectomycorrhizal (ECM) shrub Betula nana (Chapin et al., 1995). This change is associated with increased ECM fungal biomass (Clemmensen et al., 2006) and strong changes in the composition of ECM fungal communities (Deslippe et al., 2011). The strong responses of plants and their symbionts to warming are likely to influence the physical and chemical environments experienced by soil microorganisms. These factors, which are indirect effects of warming, have in combination the potential to be important proximal drivers of soil microbial communities. Our study design allowed us to test the combined effects of warming treatment on microbial community composition and structure over time. We used a molecular approach to achieve the high taxonomic resolution necessary to detect changes in microbial community composition and structure with warming treatment.