Large quantities of organic carbon are stored in frozen soils (permafrost) within Arctic and sub-Arctic regions. A warming climate can induce environmental changes that accelerate the microbial breakdown of organic carbon and the release of the greenhouse gases carbon dioxide and methane. This feedback can accelerate climate change, but the magnitude and timing of greenhouse gas emission from these regions and their impact on climate change remain uncertain. Here we find that current evidence suggests a gradual and prolonged release of greenhouse gas emissions in a warming climate and present a research strategy with which to target poorly understood aspects of permafrost carbon dynamics.

The carbon (C) storage capacity of northern latitude ecosystems may diminish as warming air temperatures increase permafrost thaw and stimulate decomposition of previously frozen soil organic C. However, warming may also enhance plant growth so that photosynthetic carbon dioxide (CO 2 ) uptake may, in part, offset respiratory losses. To determine the effects of air and soil warming on CO 2 exchange in tundra, we established an ecosystem warming experiment -the Carbon in Permafrost Experimental Heating Research (CiPEHR) project -in the northern foothills of the Alaska Range in Interior Alaska. We used snow fences coupled with spring snow removal to increase deep soil temperatures and thaw depth (winter warming) and open-top chambers to increase growing season air temperatures (summer warming). Winter warming increased soil temperature (integrated 5-40 cm depth) by 1.5 1C, which resulted in a 10% increase in growing season thaw depth. Surprisingly, the additional 2 kg of thawed soil C m À2 in the winter warming plots did not result in significant changes in cumulative growing season respiration, which may have been inhibited by soil saturation at the base of the active layer. In contrast to the limited effects on growing-season C dynamics, winter warming caused drastic changes in winter respiration and altered the annual C balance of this ecosystem by doubling the net loss of CO 2 to the atmosphere. While most changes to the abiotic environment at CiPEHR were driven by winter warming, summer warming effects on plant and soil processes resulted in 20% increases in both gross primary productivity and growing season ecosystem respiration and significantly altered the age and sources of CO 2 respired from this ecosystem. These results demonstrate the vulnerability of organic C stored in near surface permafrost to increasing temperatures and the strong potential for warming tundra to serve as a positive feedback to global climate change.

Summary1. The response of northern tundra plant communities to warming temperatures is of critical concern because permafrost ecosystems play a key role in global carbon (C) storage, and climateinduced ecological shifts in the plant community will affect the transfer of carbon-dioxide between biological and atmospheric pools. 2. This study, which focuses on the response of tundra plant growth and phenology to experimental warming, was conducted at the Carbon in Permafrost Experimental Heating Research project, located in the northern foothills of the Alaska Range. We used snow fences coupled with spring snow removal to increase deep-soil temperatures and thaw depth (winter warming), and open-top chambers to increase summer air temperatures (summer warming). 3. Winter warming increased wintertime soil temperature (5-40 cm) by 2.3°C, resulting in a 10% increase in growing season thaw depth. Summer warming significantly increased growing season air temperature; peak temperature differences occurred near midday when summer warming plots were approximately 1.0°C warmer than ambient plots. 4. Changes in the soil environment as a result of winter warming treatment resulted in a 20% increase in above-ground biomass and net primary productivity (ANPP), while there was no detected summer warming effect on ecosystem-level ANPP or biomass. Both summer and winter warming extended the growing season through earlier bud break and delayed senescence, despite equivalent snow-free days across treatments. As with ANPP, winter warming increased canopy N mass by 20%, while there was no summer warming effect on canopy N. 5. The warming-mediated increase in N availability, coupled with phenological shifts, may have driven higher rates of ANPP in the winter warming plots, and the lack of ecosystem-level N and ANPP response to summer warming suggest continued N limitation in the summer warming plots. 6. Synthesis: These results highlight the role of soil and permafrost dynamics in regulating plant response to climate change and provide evidence that warming may promote greater C accumulation in tundra plant biomass. While warming temperatures are expected to enhance microbial decomposition of the large pool of organic matter stored in tundra soils and permafrost, these respiratory losses may be offset, at least in part, by warming-mediated increases in plant growth.

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Microbial decomposition of soil carbon in high-latitude tundra underlain with permafrost is one of the most important, but poorly understood, potential positive feedbacks of greenhouse gas emissions from terrestrial ecosystems into the atmosphere in a warmer world 1,2,3,4. Using integrated metagenomic technologies, we showed that the microbial functional community structure in the active layer of tundra soil was significantly altered after only 1.5 years of warming, a rapid response demonstrating the high sensitivity of this ecosystem to warming. The abundances of microbial functional genes involved in both aerobic and anaerobic carbon decomposition were also markedly increased by this short-term warming. Consistent with this, ecosystem respiration (R eco) increased up to 38%. In addition, warming enhanced genes involved in nutrient cycling, which very likely contributed to an observed increase (30%) in gross primary productivity (GPP). However, the GPP increase did not offset the extra R eco , resulting in significantly more net carbon loss in warmed plots compared with control plots. Altogether, our results demonstrate the vulnerability of active-layer soil carbon in this permafrost-based tundra ecosystem to climate warming and the importance of microbial communities in mediating such vulnerability.