Microbial community responses to decadal drainage on a Siberian floodplain

Abstract

Drainage induced by permafrost thaw considerably transforms terrestrial landscapes and ecosystem characteristics in the Arctic. There have been continuous studies on the effects of drainage on greenhouse gas (GHG) flux and soil geochemistry, but the mechanistic links of microbial processes to GHG dynamics have not been well elucidated. We examined changes in microbial communities using shotgun metagenomics on an Arctic floodplain subject to decadal drainage, and linked microbial metabolism to GHG flux (CO2 and CH4) and soil geochemistry. The study site is located near Chersky, Russia, and consists of two sites one that has been drained since 2004 and the other that has not received any treatment. Decadal drainage lowered water tables by ca. 20 cm at the peak of the growing season, and it has changed dominant plant species from Eriophorum angustifolium to Carex spp and shrubs. During the growing season in 2014, CO2 and CH4 fluxes were measured, and 5 soil cores up to the permafrost table were taken from each control and drained site. There were no discernible differences in microbial richness; however, microbial taxa and functions shifted due to changes in soil environment from anoxic to oxic conditions in response to drainage. In the drained site, the relative abundance of Alphaproteobacteria and Acidobacteria as well as fungal:bacterial ratios increased. Genes involved in methanogenesis, methane oxidation, and fermentation decreased in the drained site. In particular, Methanoregula and Methanoflorens, which play key roles in methanogenesis under saturated conditions, markedly decreased following drainage. In addition, higher Type I:Type II methanotrophs ratios in wet conditions were reversed due to drainage. These modifications were well aligned with reduced CH4 emissions in the drained site. Genes related to organic matter degradation became more abundant following drainage, and this can be associated with slightly increased heterotrophic respiration, i.e., CO2 emissions by microorganisms. Collectively, these results demonstrate that permafrost thaw-induced drainage result in noticeable shifts in microbial communities, and these modifications well explained changes in CO2 and CH4 emissions, enabling us to gain a mechanistic understanding of microbial processes regulating GHG dynamics.