Dispersal of bacteria and stimulation of permafrost decomposition by Collembola

Abstract

Abstract. Contrary to most soils, permafrost soils have the atypical feature of being almost entirely deprived of soil fauna. Abiotic constraints on the fate of permafrost carbon after thawing are increasingly understood, but biotic constraints remain scarcely investigated. Incubation studies, essential to estimate effects of permafrost thaw on carbon cycling, typically measure the consequences of permafrost thaw in isolation from the topsoil and thus do not account for the effects of altered biotic interactions because of e.g. colonization by soil fauna. Microarthropods facilitate the dispersal of microorganisms in soil, both on their cuticle (ectozoochory) and through their digestive tract (endozoochory), which may be particularly important in permafrost soils, considering that microbial community composition can strongly constrain permafrost biogeochemical processes. Here we tested how a model species of microarthropod (the Collembola Folsomia candida) affected aerobic CO2 production of permafrost soil over a 25 d incubation. By using Collembola stock cultures grown on permafrost soil or on an arctic topsoil, we aimed to assess the potential for endo- and ectozoochory of soil bacteria, while cultures grown on gypsum and sprayed with soil suspensions would allow the observation of only ectozoochory. The presence of Collembola introduced bacterial amplicon sequence variants (ASVs) absent in the no-Collembola control, regardless of their microbiome manipulation, when considering presence–absence metrics (unweighted UniFrac metrics), which resulted in increased species richness. However, these introduced ASVs did not induce changes in bacterial community composition as a whole (accounting for relative abundances, weighted UniFrac), which might only become detectable in the longer term. CO2 production was increased by 25.85 % in the presence of Collembola, about half of which could be attributed to Collembola respiration based on respiration rates measured in the absence of soil. We argue that the rest of the CO2 being respired can be considered a priming effect of the presence of Collembola, i.e. a stimulation of permafrost CO2 production in the presence of active microarthropod decomposers. Overall, our findings underline the importance of biotic interactions in permafrost biogeochemical processes and the need to explore the additive or interactive effects of other soil food web groups of which permafrost soils are deprived.