Positron-emitting radiotracers spatially resolve unexpected biogeochemical relationships linked with methane oxidation in Arctic soils

Authors: Schmidt, Michael - Mike; MAMET, STEVEN - University Of Saskatchewan; SENGER, CURTIS - University Of Saskatchewan; SCHEBEL, ALIXANDRA - University Of Saskatchewan; OTA, MITSUAKI - University Of Saskatchewan; TIAN, W. TONY - University Of Saskatchewan; AZIZ, UMAIR - University Of Saskatchewan; STEIN, LISA - University Of Alberta; REGIER, TOM - Canadian Light Source Inc; STANLEY, KEVIN - University Of Saskatchewan; PEAK, DEREK - University Of Saskatchewan; SICILIANO, STEVEN - University Of Saskatchewan

Submitted to: Global Change Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/26/2022
Publication Date: 4/4/2022
Citation: Schmidt, M.P., Mamet, S.D., Senger, C., Schebel, A., Ota, M., Tian, W., Aziz, U., Stein, L.Y., Regier, T., Stanley, K., Peak, D., Siciliano, S.D. 2022. Positron-emitting radiotracers spatially resolve unexpected biogeochemical relationships linked with methane oxidation in Arctic soils. Global Change Biology. 28(13):4211-4224. https://doi.org/10.1111/gcb.16188.
DOI: https://doi.org/10.1111/gcb.16188

Interpretive Summary: Methane is a greenhouse gas that represents a small volume of the atmosphere relative to carbon dioxide, yet has a disproportionately large influence on global warming. A process known to remove methane from the atmosphere and, therefore, mitigate its warming influence, is microbial methane oxidation in soils. By this process, atmospheric methane is removed from the atmosphere and converted into soil microbial biomass. While it is known that soil microbial methane oxidation plays an important role in global carbon cycling, it is a difficult process to study as it is influenced by many soil characteristics that spatially vary within soil samples, making it challenging to know where and how active microhabitats develop. In this work we used a novel radioisotope imaging strategy to visualize the uptake of radiolabelled methane in an Arctic soil with and without freeze-thaw induced nutrient addition. Next, we extracted active soils to better understand the biological and chemical properties of those areas. Active methane uptake spatially associated with a greater proportion of mineralized nitrogen species in soils with cryoturbic nutrient addition. We found that a specific microbial species (Ralstonia pickettii) was spatially related to methane oxidation in these soils and had an enrichment of mineral nitrogen assimilation related genes. This work highlights the importance of nitrogen when considering the cycling of carbon greenhouse gases in natural Arctic soils. The experimental method developed here may be used to study and predict greenhouse gas dynamics in agricultural systems as well. Furthermore, this work establishes a framework for future soil studies with several different isotopes relevant to other topics, including solute transport, plant stress and microbial metabolic processes.

Technical Abstract: Arctic soils are marked by cryoturbic features, which impact soil-atmosphere methane (CH4) dynamics vital to global climate regulation. Cryoturbic diapirism alters C/N chemistry within frost boils by introducing soluble organic carbon and nutrients, potentially influencing microbial CH4 oxidation. CH4 oxidation in soils, however, requires a spatio-temporal convergence of ecological factors to occur. Spatial delineation of microbial activity with respect to these key microbial and biogeochemical factors at relevant scales is experimentally challenging in inherently complex and heterogeneous natural soil matrices. This work aims to overcome this barrier by spatially linking microbial CH4 oxidation with C/N chemistry and metagenomic characteristics. This is achieved by using positron-emitting radiotracers to visualize millimeter-scale active CH4 uptake areas in Arctic soils with and without diapirism. X-ray absorption spectroscopic speciation of active and inactive areas shows CH4 uptake spatially associates with greater proportions of inorganic N in diapiric frost boils. Metagenomic analyses reveal Ralstonia pickettii associates with CH4 uptake across soils along with pertinent CH4 and inorganic N metabolism associated genes. This study highlights the critical relationship between CH4 and N cycles in Arctic soils, with potential implications for better understanding future climate. Furthermore, our experimental framework presents a novel, widely applicable strategy for unraveling ecological relationships underlying greenhouse gas dynamics under global change.