Microbial community response to permafrost thaw in the Canadian High Arctic

Permafrost is one of Earth’s most crucial carbon reservoirs, as the perennially frozen state of permafrost protects stored carbon from microbial metabolisms. Increasing surface temperatures are causing the permafrost to thaw, making permafrost carbon more bioavailable to microbial processes, which can transform this newly available carbon to greenhouses gasses such as methane and carbon dioxide. Permafrost thaw additionally shifts the environmental conditions of the newly thawed soil, which changes the selective pressures that shape the microbial community composition. The active layer, which is exposed to seasonal freezing and thawing cycles, lies above the permafrost and contains a microbial community that differs in composition compared to the permafrost microbial community. Thawing of the permafrost induces the mixing of the permafrost and active layer communities, as well as the mixing of the nutrients between these two layers. How the changes in selective pressures, the mixing of nutrients, and the mixing of microbial communities affect the microbial community composition in the newly thawed soil is not well understood. This study examined the microbial community response to permafrost thaw using soil samples collected from two field sites in the Canadian High Arctic, near Cambridge Bay, Nunavut: Long Point and Augustus Hills. Treatments were designed to evaluate the importance of two factors that influence microbial community assembly processes during thaw: microbial dispersal and shifting selective pressures that accompany permafrost thaw. Microcosms of permafrost and active layer soil samples were established in sterile serum bottles and incubated at 8 °C for up to 5 months. The influence of nutrient mixing on post-thaw microbial community composition was examined by the addition of nutrients extracted from one soil layer to a microcosm containing soil of the opposite layer, while the influence of microbial dispersal on microbial community composition following thaw was investigated by inoculating each soil type with soil from the opposite layer. The collective influence of nutrient mixing and microbial dispersal on microbial community composition following permafrost thaw was examined by adding both the extracted nutrients and the soil inoculum from one soil type to the opposite soil type. As a control, the effects of the changing selective pressures associated with thaw on the permafrost microbial community composition and the active layer microbial community composition were examined without the influence of nutrient mixing or microbial dispersal. Samples were taken monthly and changes in the microbial community composition were assessed by 16S rRNA gene amplicon sequencing. The microbial community compositions differed significantly between the two fields sites (permafrost: Pr(>F) = 0.011; active layer: Pr(>F) = 0.003). The results of the Augustus Hills microcosms showed consistent shifts in microbial community composition following thaw, which indicates that the selective pressures induced by thaw are important drivers of shifts in microbial community composition following permafrost thaw. The results of the Long Point microcosms showed consistent shifts in microbial community composition only in the active layer-dominant microcosms. The Long Point permafrost-dominant microcosms showed no consistent shifts following permafrost thaw; however, these were the only microcosms that showed that microbial dispersal had a stronger influence on post-thaw microbial community composition than the selective pressures associated with thaw. The results suggest that the change in selective pressures that accompany permafrost thaw are the most important ecological factors that influence post-thaw microbial community composition, and that initial microbial community composition is an important factor in determining microbial community composition following permafrost thaw. The heterogeneity observed in community composition and in response to thaw between sites indicates that extrapolating results from a limited range of sites is highly problematic, and therefore many areas need to be studied to understand the response to permafrost thaw across the Canadian High Arctic.