Seasonal patterns of microbial extracellular enzyme activities in an arctic tundra soil: Identifying direct and indirect effects of long-term summer warming

Abstract

Arctic systems, which store ∼50% of global soil carbon, are undergoing rapid climatic warming that may drive significant carbon release to the atmosphere. To better understand how warming impacts arctic decomposition, we characterized the effects of a twenty-two year long tundra greenhouse warming experiment on decomposer-produced extracellular enzymes, nutrients, and microbial biomass across a year. This experiment, which is the longest running tundra ecosystem warming study in existence, was previously shown to have altered the plant and soil communities. The greenhouse treatment has also changed the seasonal soil temperature regime by indirectly increasing winter soil temperature, an effect that was likely facilitated through an increase in snow-trapping shrub biomass. Irrespective of the warming treatment, we observed that peak nutrient pools, microbial biomass, and hydrolytic enzyme activities all occurred from the late winter through thaw. This pattern was decoupled from peak oxidative enzyme activities, which occurred during the summer. The greenhouse treatment amplified the natural seasonal cycle of extracellular enzyme activities, suggesting that tundra decomposer communities maintain a temporal niche space which is critical to understanding how arctic biogeochemical cycling will respond to warming. A spatial separation was also observed; extracellular enzyme activities in the deeper soil horizons were more sensitive to warming than at the surface. Direct greenhouse warming did not strongly stimulate decomposition: only oxidative enzyme activities in the surface horizon increased during the summer. Unexpectedly, the strongest treatment effect observed was a stimulation of hydrolytic enzyme activities at depth in the mineral horizon from the late winter through thaw (which also affected extracellular enzyme stoichiometry, increasing C:N and C:P acquisition activities), before the greenhouse treatment was directly active. This effect declined during senescence and was reversed in early winter, suggesting that negative biotic-abiotic feedbacks may curtail increased decomposer activity in warming arctic systems.