Rainfall Alters Permafrost Soil Redox Conditions, but Meta-Omics Show Divergent Microbial Community Responses by Tundra Type in the Arctic

Karl J Romanowicz,Byron C Crump,George W Kling

doi:10.3390/soilsystems5010017

Karl J Romanowicz, Byron C Crump + Show 1 more

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https://doi.org/10.3390/soilsystems5010017

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Abstract

Soil anoxia is common in the annually thawed surface (‘active’) layer of permafrost soils, particularly when soils are saturated, and supports anaerobic microbial metabolism and methane (CH4) production. Rainfall contributes to soil saturation, but can also introduce oxygen, causing soil oxidation and altering anoxic conditions. We simulated a rainfall event in soil mesocosms from two dominant tundra types, tussock tundra and wet sedge tundra, to test the impacts of rainfall-induced soil oxidation on microbial communities and their metabolic capacity for anaerobic CH4 production and aerobic respiration following soil oxidation. In both types, rainfall increased total soil O2 concentration, but in tussock tundra there was a 2.5-fold greater increase in soil O2 compared to wet sedge tundra due to differences in soil drainage. Metagenomic and metatranscriptomic analyses found divergent microbial responses to rainfall between tundra types. Active microbial taxa in the tussock tundra community, including bacteria and fungi, responded to rainfall with a decline in gene expression for anaerobic metabolism and a concurrent increase in gene expression for cellular growth. In contrast, the wet sedge tundra community showed no significant changes in microbial gene expression from anaerobic metabolism, fermentation, or methanogenesis following rainfall, despite an initial increase in soil O2 concentration. These results suggest that rainfall induces soil oxidation and enhances aerobic microbial respiration in tussock tundra communities but may not accumulate or remain in wet sedge tundra soils long enough to induce a community-wide shift from anaerobic metabolism. Thus, rainfall may serve only to maintain saturated soil conditions that promote CH4 production in low-lying wet sedge tundra soils across the Arctic.

Highlights

Permafrost soils consist of permanently frozen ground overlain by a shallow, seasonally thawed active soil layer
Genes identified as oxygen-regulated infers that their expression can be either positively or negatively affected by O2 availability and the differential expression of these genes is an indication that simulated rainfall changed soil redox conditions through an increase in dissolved O2 concentration
Within significant Kyoto Encyclopedia of Genes and Genomes database (KEGG)-Metabolism categories (ANOVA; Figure 4), we found several KEGG orthologs (KOs) explicitly identified as oxygen-regulated [75] that were significantly differentially expressed to a lower extent at T4 relative to T0 in the tussock tundra community using Differential gene expression (DGE) analysis (DGE; FDR < 0.05 for all; Table 4)

Summary

Introduction

Permafrost soils consist of permanently frozen ground (permafrost) overlain by a shallow, seasonally thawed active soil layer (the ‘active layer’). These soils store nearly half of all global belowground organic carbon (~1300 Pg) [1]. The decomposition and net storage of organic carbon is controlled in large part by redox conditions in the active layer that are regulated by the availability of oxygen [2]. Permafrost affects redox conditions by confining soil water to the active layer, resulting in soil saturation and periodic or persistent soil anoxia [3,4]. Anoxic conditions develop when oxygen is consumed through biochemical processes (e.g., aerobic respiration) or geochemical reactions (e.g., iron oxidation) faster than it is introduced to the soil by diffusion, plant roots, or infiltrating rainwater [5,6].

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