Plant-specific rhizosphere influences on soil redox and soil biogeochemistry affect methane release from thawing permafrost soils

Thawing of permafrost soils results in drastic changes in soil biogeochemistry and plant community composition. Specifically, the thawing process in subarctic regions can transform previously stable permafrost soils, home to slow growing, shallow-rooted shrubs into water-saturated, oxygen-depleted soils with fast-growing, deep-rooted graminoids. This change in soil biogeochemistry, along with the distinct characteristics and requirements of these contrasting plant types, leads to the hypothesis that the way these plants interact with the soil may impact biogeochemical cycles. Consequently, this could result in changes in the amounts and ratios of released greenhouse gases, influencing climate-relevant processes. On the one hand, tall graminoids may increase CO2 fixation. On the other hand, root exudation might prime the formation of CH4 and the root internal CH4 transport protecting it from oxidation outweighing increased CO2 fixation in thawed permafrost soils as compared to intact permafrost soil. To explore this idea, we conducted a study in Stordalen, Abisko, Sweden, at a permafrost site with three different thawing stages. Sampling locations in intact, intermediately, and fully thawed permafrost soil were selected, each with varying densities of shrubs and graminoids. Representative plants were sampled to analyze the quantity and composition of root exudates. Data on soil redox potential at different depths were combined with porewater geochemical parameters like the amount and speciation of dissolved iron, dissolved organic carbon, inorganic nitrogen species, dissolved porewater gases, and soil microbial functional genes. Net emissions of CO2, CH4, and N2O were tracked using static gas flux chambers. Most reducing redox conditions were observed in fully thawed soils compared to intact and intermediately thawed permafrost soils. Additionally, redox potentials decreased at greater depth in the soil and with higher graminoid density. At the same time graminoid roots exuded larger amounts of organic carbon than shrub roots with a high fraction of easily available organic molecules. We relate the decreasing redox potentials with increasing graminoid density to the rapid depletion of available electron acceptors such as iron(III) caused by an increased supply of easily available organic molecules through root exudation. This, in turn, might prime CH4 production, indicated by increased porewater CH4 at depth. Given the net CH4 flux increase at an increased porewater CH4 at depth, we suggest that this is partly from CH4-priming and partly from aerenchyma transport of CH4 from the soil to the atmosphere (Strm et al. 2005). Since thawing permafrost areas are rapidly expanding and contribute to climate change, the plant-specific alterations of these contrasting rhizosphere biogeochemical systems are important to consider altering greenhouse gas fluxes and warming potentials. Strm, L. et al. Species-specific Effects of Vascular Plants on Carbon Turnover and Methane Emissions from Wetlands. Biogeochemistry 75, 6582 (2005).