The Soil Microbiome and Its Response to Permafrost Thaw in Arctic Tundra

Abstract

A majority (~60%) of the global belowground organic carbon (OC) pool is trapped in a perennially frozen state in permafrost soils underlying the Arctic tundra. Climate warming has initiated thaw in large regions of permafrost. Such thaw will likely trigger increased microbial activity leading to faster degradation of previously frozen OC and its release as carbon dioxide (CO2) and methane (CH4) to the atmosphere. Yet it remains uncertain how the soil microbiome (community of microorganisms) will respond to permafrost thaw or modulate the relative proportions of CO2 and CH4 produced by the decomposition of OC in thawing permafrost soils. This dissertation advances our understanding of the dynamics and functions of the tundra soil microbiome in response to permafrost thaw using field-based and laboratory experiments. Permafrost soils remain water-saturated during thaw, leading to oxygen (O2) limitations that promote anaerobic and fermentative microbial processes responsible for OC degradation. Rainfall contributes to soil saturation but can also introduce an influx of O2, potentially altering anaerobic metabolism and reducing CH4 production. A rainfall event was simulated in tundra soil mesocosms and the genomic response of the soil microbiome was assessed through a multi-omics sequencing approach. Soil drainage rates had the greatest effect on soil oxygenation following the rainfall event. Specifically, rainfall-induced soil oxidation increased aerobic microbial metabolism and CO2 respiration in a slow-draining tundra soil. However, the residence time of oxygenated rainwater in a rapidly-draining tundra soil was insufficient to alter anaerobic and fermentative microbial processes that continued to promote CH4 production. Thus, the microbial response to rainfall in thawing permafrost soils depends on drainage rates that differ by tundra type. The microbial response to permafrost thaw also depends on how thaw duration (thaw days in summer) affects the composition of the soil microbiome. Field observations revealed that the composition of the soil microbiome was strongly correlated with annual thaw duration by depth. Compositional differences were greatest across transition depths from thawed to permafrost soil. Multi-decadal thaw surveys showed that differences in thaw duration by depth were significantly positively correlated with dominant taxa in the surface active-layer depths and negatively correlated with dominant taxa in the permafrost. Microbial composition within the transition-zone (recently thawed permafrost) depths was statistically similar to that in the permafrost, indicating that recent decades of intermittent thaw have not yet induced a shift from permafrost to active-layer microbes. These results suggest that thaw duration rather than thaw frequency has a greater impact on the composition of the microbiome within tundra soils. Monitoring thaw duration and microbial composition at depth may help predict the microbial response to future permafrost thaw. To test the microbial response to thaw duration, a laboratory incubation experiment was conducted to simulate thaw along a tundra soil profile. An extended thaw duration of 30 days induced a microbiome-wide shift in composition and genomic potential dominated by an increase in iron (Fe) cycling bacteria. This shift was greatest within the transition-zone and permafrost microbiomes where the relative abundance of Fe-cycling bacteria accounted for ~80% of the community after 30 days. Microbial gene expression for Fe(III) reduction, Fe(II) oxidation, as well as OC degradation also increased concurrently with thaw duration. The growth of Fe-cycling bacteria and subsequent degradation of OC through Fe(III) reduction could promote greater CO2 production over CH4 production with extended thaw duration in permafrost soils.