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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.

Warming-induced microbial decomposition of organic matter in permafrost soils constitutes a climate-change feedback of uncertain magnitude. While physicochemical constraints on soil functioning are relatively well understood, the constraints attributable to microbial community composition remain unclear. Here we show that biogeochemical processes in permafrost can be impaired by missing functions in the microbial community-functional limitations-probably due to environmental filtering of the microbial community over millennia-long freezing. We inoculated Yedoma permafrost with a functionally diverse exogenous microbial community to test this mechanism by introducing potentially missing microbial functions. This initiated nitrification activity and increased CO2 production by 38% over 161 days. The changes in soil functioning were strongly associated with an altered microbial community composition, rather than with changes in soil chemistry or microbial biomass. The present permafrost microbial community composition thus constrains carbon and nitrogen biogeochemical processes, but microbial colonization, likely to occur upon permafrost thaw in situ, can alleviate such functional limitations. Accounting for functional limitations and their alleviation could strongly increase our estimate of the vulnerability of permafrost soil organic matter to decomposition and the resulting global climate feedback. Carbon dioxide emissions from permafrost thaw are substantially enhanced by relieving microbial functional limitations, according to incubation experiments on Yedoma permafrost.

As global temperatures continue to rise, a key uncertainty of climate projections is the microbial decomposition of vast organic carbon stocks in thawing permafrost soils. Decomposition rates can accelerate up to fourfold in the presence of plant roots, and this mechanism—termed the rhizosphere priming effect—may be especially relevant to thawing permafrost soils as rising temperatures also stimulate plant productivity in the Arctic. However, priming is currently not explicitly included in any model projections of future carbon losses from the permafrost area. Here, we combine high-resolution spatial and depth-resolved datasets of key plant and permafrost properties with empirical relationships of priming effects from living plants on microbial respiration. We show that rhizosphere priming amplifies overall soil respiration in permafrost-affected ecosystems by ~12%, which translates to a priming-induced absolute loss of ~40 Pg soil carbon from the northern permafrost area by 2100. Our findings highlight the need to include fine-scale ecological interactions in order to accurately predict large-scale greenhouse gas emissions, and suggest even tighter restrictions on the estimated 200 Pg anthropogenic carbon emission budget to keep global warming below 1.5 °C.

Thicker snowpacks and their insulation effects cause winter-warming and invoke thaw of permafrost ecosystems. Temperature-dependent decomposition of previously frozen carbon (C) is currently considered one of the strongest feedbacks between the Arctic and the climate system, but the direction and magnitude of the net C balance remains uncertain. This is because winter effects are rarely integrated with C fluxes during the snow-free season and because predicting the net C balance from both surface processes and thawing deep layers remains challenging. In this study, we quantified changes in the long-term net C balance (net ecosystem production) in a subarctic peat plateau subjected to 10 years of experimental winter-warming. By combining(210)Pb and(14)Cdating of peat cores with peat growth models, we investigated thawing effects on year-round primary production and C losses through respiration and leaching from both shallow and deep peat layers. Winter-warming and permafrost thaw had no effect on the net C balance, but strongly affected gross C fluxes. Carbon losses through decomposition from the upper peat were reduced as thawing of permafrost induced surface subsidence and subsequent waterlogging. However, primary production was also reduced likely due to a strong decline in bryophytes cover while losses from the old C pool almost tripled, caused by the deepened active layer. Our findings highlight the need to estimate long-term responses of whole-year production and decomposition processes to thawing, both in shallow and deep soil layers, as they may contrast and lead to unexpected net effects on permafrost C storage.

Environmental changes feedback to climate through their impact on soil functions such as carbon (C) and nutrient sequestration. Abiotic conditions and the interactions between above- and belowground biota drive soil responses to environmental change but these (a)biotic interactions are challenging to study. Nonetheless, better understanding of these interactions would improve predictions of future soil functioning and the soil-climate feedback and, in this context, permafrost soils are of particular interest due to their vast soil C-stores. We need new tools to isolate abiotic (microclimate, chemistry) and biotic (roots, fauna, microorganisms) components and to identify their respective roles in soil processes. We developed a new experimental setup, in which we mimic thermokarst (permafrost thaw-induced soil subsidence) by fitting thawed permafrost and vegetated active layer sods side by side into mesocosms deployed in a subarctic tundra over two growing seasons. In each mesocosm, the two sods were separated from each other by barriers with different mesh sizes to allow varying degrees of physical connection and, consequently, (a)biotic exchange between active layer and permafrost. We demonstrate that our mesh-approach succeeded in controlling 1) lateral exchange of solutes between the two soil types, 2) colonization of permafrost by microbes but not by soil fauna, and 3) ingrowth of roots into permafrost. In particular, experimental thermokarst induced a similar to 60% decline in permafrost nitrogen (N) content, a shift in soil bacteria and a rapid buildup of root biomass (+33.2 g roots m(-2) soil). This indicates that cascading plant-soil-microbe linkages are at the heart of biogeochemical cycling in thermokarst events. We propose that this novel setup can be used to explore the effects of (a)biotic ecosystem components on focal biogeochemical processes in permafrost soils and beyond.

At high latitudes, winter warming facilitates vegetation expansion into barren frost-affected soils. The interplay of changes in winter climate and plant presence may alter soil functioning via effects on decomposers. Responses of decomposer soil fauna and microorganisms to such changes likely differ from each other, since their life histories, dispersal mechanisms and microhabitats vary greatly.

We investigated the relative impacts of short-term winter warming and increases in plant cover on bacteria and collembola community composition in cryoturbated, non-sorted circle tundra. By covering non-sorted circles with insulating gardening fibre cloth (fleeces) or using stone walls accumulating snow, we imposed two climate-change scenarios: snow accumulation increased autumn-to-late winter soil temperatures (−1 cm) by 1.4 °C, while fleeces warmed soils during that period by 1 °C and increased spring temperatures by 1.1 °C. Summer bacteria and collembola communities were sampled from within-circle locations differing in vegetation abundance and soil properties.

Two years of winter warming had no effects on either decomposer community. Instead, their community compositions were strongly determined by sampling location: communities in barren circle centres were distinct from those in vegetated outer rims, while communities in sparsely vegetated patches of circle centres were intermediate. Diversity patterns indicate that collembola communities are tightly linked to plant presence while bacteria communities correlated with soil properties.

Our results thus suggest that direct effects of short-term winter warming are likely to be minimal, but that vegetation encroachment on barren cryoturbated ground will affect decomposer community composition substantially. At decadal timescales, collembola community changes may follow relatively fast after warming-driven plant establishment into barren areas, whereas bacteria communities may take longer to respond. If shifts in decomposer community composition are indicative for changes in their activity, vegetation overgrowth will likely have much stronger effects on soil functioning in frost-affected tundra than short-term winter warming.

Permafrost-affected soils store a large quantity of soil organic matter (SOM) – ca. half of worldwide soil carbon – and currently undergo rapid and severe warming due to climate change. Increased SOM decomposition by microorganisms and soil fauna due to climate change, poses the risk of a positive climate feedback through the release of greenhouse gases. Direct effects of climate change on SOM decomposition, through such mechanisms as deepening of the seasonally-thawing active layer and increasing soil temperatures, have gathered considerable scientific attention in the last two decades. Yet, indirect effects mediated by changes in plant, microbial, and fauna communities, remain poorly understood. Microbial communities, which may be affected by climate change-induced changes in vegetation composition or rooting patterns, and may in turn affect SOM decomposition, are the primary focus of the work described in this thesis.

We used (I) a field-scale permafrost thaw experiment in a palsa peatland, (II) a laboratory incubation of Yedoma permafrost with inoculation by exotic microorganisms, (III) a microcosm experiment with five plant species grown either in Sphagnum peat or in newly-thawed permafrost peat, and (IV) a field-scale cold season warming experiment in cryoturbated tundra to address the indirect effects of climate change on microbial drivers of SOM decomposition. Community composition data for bacteria and fungi were obtained by amplicon sequencing and phospholipid fatty acid extraction, and for collembola by Tullgren extraction, alongside measurements of soil chemistry, CO₂ emissions and root density.

We showed that in situ thawing of a palsa peatland caused colonization of permafrost soil by overlying soil microbes. Further, we observed that functional limitations of permafrost microbial communities can hamper microbial metabolism in vitro. Relieving these functional limitations in vitro increased cumulative CO₂ emissions by 32% over 161 days and introduced nitrification. In addition, we found that different plant species did not harbour different rhizosphere bacterial communities in Sphagnum peat topsoil, but did when grown in newly-thawed permafrost peat. Plant species may thus differ in how they affect functional limitations in thawing permafrost soil. Therefore, climate change-induced changes in vegetation composition might alter functioning in the newly-thawed, subsoil permafrost layer of northern peatlands, but less likely so in the topsoil. Finally, we observed that vegetation encroachment in barren cryoturbated soil, due to reduced cryogenic activity with higher temperatures, change both bacterial and collembola community composition, which may in turn affect soil functioning.

This thesis shows that microbial community dynamics and plant-decomposer interactions play an important role in the functioning of warming permafrost-affected soils. More specifically, it demonstrates that the effects of climate change on plants can trickle down on microbial communities, in turn affecting SOM decomposition in thawing permafrost.

The emergence of high-throughput DNA sequencing methods provides unprecedented opportunities to further unravel bacterial biodiversity and its worldwide role from human health to ecosystem functioning. However, despite the abundance of sequencing studies, combining data from multiple individual studies to address macroecological questions of bacterial diversity remains methodically challenging and plagued with biases. Here, using a machine-learning approach that accounts for differences among studies and complex interactions among taxa, we merge 30 independent bacterial data sets comprising 1,998 soil samples from 21 countries. Whereas previous meta-analysis efforts have focused on bacterial diversity measures or abundances of major taxa, we show that disparate amplicon sequence data can be combined at the taxonomy-based level to assess bacterial community structure. We find that rarer taxa are more important for structuring soil communities than abundant taxa, and that these rarer taxa are better predictors of community structure than environmental factors, which are often confounded across studies. We conclude that combining data from independent studies can be used to explore bacterial community dynamics, identify potential 'indicator' taxa with an important role in structuring communities, and propose hypotheses on the factors that shape bacterial biogeography that have been overlooked in the past.

The decomposition of large stocks of soil organic carbon in thawing permafrost might depend on more than climate change-induced temperature increases: indirect effects of thawing via altered bacterial community structure (BCS) or rooting patterns are largely unexplored. We used a 10-year in situ permafrost thaw experiment and aerobic incubations to investigate alterations in BCS and potential respiration at different depths, and the extent to which they are related with each other and with root density. Active layer and permafrost BCS strongly differed, and the BCS in formerly frozen soils (below the natural thawfront) converged under induced deep thaw to strongly resemble the active layer BCS, possibly as a result of colonization by overlying microorganisms. Overall, respiration rates decreased with depth and soils showed lower potential respiration when subjected to deeper thaw, which we attributed to gradual labile carbon pool depletion. Despite deeper rooting under induced deep thaw, root density measurements did not improve soil chemistry-based models of potential respiration. However, BCS explained an additional unique portion of variation in respiration, particularly when accounting for differences in organic matter content. Our results suggest that by measuring bacterial community composition, we can improve both our understanding and the modeling of the permafrost carbon feedback.

At high latitudes, winter warming facilitates vegetation expansion into barren frost-affected soils. The interplay of changes in winter climate and plant presence may alter soil carbon dynamics via effects on decomposers. Responses of decomposer soil fauna and microorganisms to such changes likely differ from each other, since their life histories, dispersal mechanisms and microhabitats vary greatly. We investigated the relative impacts of short-term winter warming and long-term increases in plant cover on bacteria and collembola community composition in cryoturbated, non-sorted circle (NSC) tundra. By covering NSCs with insulating gardening fiber cloth (fleeces) or using stone walls accumulating snow, we imposed two climate-change scenarios: snow accumulation increased autumn-to-late winter soil temperatures by 1.4°C, while fleeces warmed soils during that period by 1°C and increased spring temperatures by 1.1°C. Summer bacteria and collembola communities were sampled from within-circle locations differing in vegetation abundance and soil properties, representing stages in long-term NSC overgrowth. Two years of winter warming had no effects on both decomposer communities. Instead, their community compositions were strongly determined by sampling location: communities in barren circle centers were distinct from those in vegetated outer rims, while communities in sparsely vegetated patches of circle centers were intermediate. Diversity patterns indicate that collembola communities are tightly linked to plant presence while bacteria communities correlated with soil properties. Our results thus suggest that short-term effects of winter warming are likely to be minimal, but longer-term vegetation overgrowth of NSCs affects decomposer community composition substantially. At decadal timescales, collembola community changes may follow rapidly after plant establishment into barren areas, whereas bacteria communities may take longer to respond. If shifts in decomposer community composition are indicative for changes in their decomposition activity, vegetation overgrowth will likely have much stronger effects on carbon losses from frost-affected tundra than short-term winter warming.