Arctic permafrost soils store one third of the world’s soil carbon, and amplified warming in the Arctic is causing permafrost thaw. Permafrost thaw allows microorganisms to access previously unavailable soil organic matter and release CO2 and CH4 through decomposition. Thaw-induced changes in microbial community structure and functional capacity determine the rate and proportion of CO2 and CH4 released during decomposition. However, predicting these community changes and the subsequent carbon release is challenging since changes in community assembly are the result of nonlinear feedbacks between microbial traits and environmental controls. Furthermore, without a mechanistic understanding of the eco-evolutionary forces involved in community assembly, predicting the complex feedbacks from multi-year effects of thaw on communities is challenging. To better understand how environmental forces and traits structure the assembly of microbial communities over time, we used shotgun metagenomic sequencing to investigate the changes in active layer soil microbial communities over six years (2011 - 2017) in three habitats (palsa, bog, and fen) that represent a gradient of thawing permafrost in Stordalen Mire near Abisko, Sweden. We then used ecological assembly modeling to identify environmental and microbial traits involved in carbon, nitrogen, and sulfur cycling that govern microbial assembly.
We found that community change attributable to dispersal and drift decreased over time while selective forces increased over time, and observed a transition from phylogenetically clustered to phylogenetically over-dispersed communities across habitats in the permafrost thaw gradient. These results suggest a switch from environmental selection to competition across the habitat thaw gradient and this effect also became more pronounced from 2011 to 2017. We then investigated the relative effects of environmental factors on microbial community assembly and found that habitat and depth were primary environmental drivers of assembly within the communities, however within habitat more direct measurements of environmental factors such as thaw depth and soil temperature showed weak or insignificant associations with stochastic or deterministic turnover in our communities. Finally, we identified carbon, nitrogen, and sulfur cycling pathways that were most associated with selective forces and thus most likely to be affected in thawing permafrost. The results from this study give us a better idea of the ecological forces driving post-thaw community assembly, and will help us better understand the mechanisms underlying microbial community change in thawing permafrost ecosystems.