Due to climate change, increased microbial activity in high-latitude soils may lead to higher greenhouse gas (GHG) emissions. However, microbial GHG production and consumption mechanisms in tundra soils are not thoroughly understood. To investigate how the diversity and functional potential of bacterial and archaeal communities vary across vegetation types and soil layers, we analyzed 116 soil metatranscriptomes from 73 sites in the Finnish sub-Arctic. Meadow soils were characterized by higher pH and lower soil organic matter (SOM) and carbon/nitrogen ratio. In contrast, dwarf shrub-dominated ecosystems had higher SOM and lower pH. Although Actinobacteria, Acidobacteria, Alphaproteobacteria, and Planctomycetes were dominant in all communities, there were significant differences at the genus level between vegetation types; plant polymer degrading groups were more active in shrub-dominated soils than in meadows. Given that climate-change scenarios predict the expansion of shrubs at high latitudes, our results indicate that tundra soil microbial communities harbor potential decomposers of increased plant litter, which may affect the rate of carbon turnover in tundra soils. Additionally, transcripts of methanotrophs were detected in the mineral layer of all soils, which may moderate methane fluxes. This study provides new insights into possible shifts in tundra microbial diversity and activity due to climate change.