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

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.

Summer thaw duration is a strong predictor of the soil microbiome and its response to permafrost thaw in arctic tundra

“…The relative abundance of archaeal taxa was <3% at any given site or depth (Figure 3, Figure S2) but still differed statistically between tundra types (ANOVA; p < 0.001). Archaeal taxa consisted primarily of methanogenic Euryarchaeota such as Methanobacteriales and Methanosarcinales, consistent with similar observations across the tundra region (Deng et al, 2015;Hultman et al, 2015;Lipson et al, 2013;Romanowicz et al, 2021;Tripathi et al, 2018).…”

“…The higher abundance of Pseudomonadota in the active layer could be related to their preference for higher concentrations of nutrients (Kim et al, 2016 ), especially given that the relative abundance of Alphaproteobacteria and Gammaproteobacteria taxa were shown to increase after fertilization compared with control plots at Toolik (Campbell et al, 2010 ; Koyama et al, 2014 ). Also, the greater abundance of bacterial taxa such as Geobacterales (Desulfobacterota) in the active‐layer microbiome of WS tundra (Table 1 ) is likely because they thrive under saturated conditions common in the active layer of WS tundra (Emerson et al, 2015 ), as has been previously reported from the Toolik Lake region (Romanowicz et al, 2021 ). This suggests that the depth‐dependent variations in the soil microbiome could be related to the different resource needs of each bacterial taxon.…”

“…In the active layer, the composition of the soil microbiome is influenced by geographic distance between sites (Malard et al, 2019 ) and variations in landscape topography that control dominant plant species and soil physicochemical properties (Judd et al, 2006 ; Judd & Kling, 2002 ; Taş et al, 2018 ; Zak & Kling, 2006 ). For example, geographic distance and plant species can change the regional composition of the active‐layer microbiome given its direct connection with aboveground environmental conditions (Chu et al, 2011 ; Malard & Pearce, 2018 ; Romanowicz et al, 2021 ; Taş et al, 2018 ; Tripathi et al, 2018 ; Wallenstein et al, 2007 ). Additional environmental factors such as active‐layer depth or soil type (Malard et al, 2019 ) as well as climatic variables such as temperature and precipitation (Castro et al, 2010 ; Nielsen & Ball, 2015 ) can also influence the composition of the active‐layer microbiome.…”

Methane production byMethanothrix thermoacetophilavia direct interspecies electron transfer withGeobacter metallireducens

“…Species from this genus are frequently the most abundant methanogens in methanogenic terrestrial environments such as natural wetlands and flooded rice paddy soils and in many anaerobic digester systems (2)(3)(4)(5)(6)(7)(8). Methanothrix species are also important members of the methanogenic community in Arctic and Antarctic sediments (9)(10)(11), and scientists are particularly concerned with increases in methane production linked to melting permafrost in these polar terrestrial sediments as this will lead to a positive feedback loop that will further exacerbate climate change (12)(13)(14).…”

Global soil metagenomics reveals ubiquitous yet previously-hidden predominance ofDeltaproteobacteriain nitrogen-fixing microbiome

“…Moreover, the datasets from rhizosphere soils were not used in this study because they are extensively and dynamically affected by the plant roots (Zhalnina et al, 2018) and not representative of the soil microbial communities. In total, we collected 1445 datasets as listed in Table S1 (Angle et al, 2017; Bahram et al, 2018; Berkelmann et al, 2020; Black and Just, 2018; Cania et al, 2019; Cha et al, 2021; Chen et al, 2019; Chu et al, 2018; Crits-Christoph et al, 2018; Hartman et al, 2017; Huber et al, 2018; Jiang et al, 2018; Johnston et al, 2016; Li et al, 2018, 2020; Links et al, 2021; Liu et al, 2018; Ma et al, 2018; Neal et al, 2021; Nelkner et al, 2019; Orellana et al, 2018; Ouyang and Norton, 2020; Paungfoo-Lonhienne et al, 2017; Romanowicz et al, 2021; Sukhum et al, 2021; Suttner et al, 2020; Hang Wang et al, 2021; Wang et al, 2020; Woodcroft et al, 2018; Wu et al, 2021; Xiao et al, 2016; Xue et al, 2019; Yu et al, 2019; Yurgel et al, 2019; Zhang et al, 2019; Zheng et al, 2021). The latitude and longitude of each sampling site were obtained from public databases [INSDC BioSamples database (Courtot et al, 2022) and MG-RAST] and verified with the descriptions in each publication.…”