Microorganisms drive many aspects of organic carbon cycling in thawing permafrost soils, but the compositional trajectory of the post-thaw microbiome and its metabolic activity remain uncertain, which limits our ability to predict permafrost–climate feedbacks in a warming world. Using quantitative metabarcoding and metagenomic sequencing, we determined relative and absolute changes in microbiome composition and functional gene abundance during thaw incubations of wet sedge tundra collected from northern Alaska, USA. Organic soils from the tundra active-layer (0–50 cm), transition-zone (50–70 cm), and permafrost (70+ cm) depths were incubated under reducing conditions at 4 °C for 30 days to mimic an extended thaw duration. Following extended thaw, we found that iron (Fe)-cycling Gammaproteobacteria, specifically the heterotrophic Fe(III)-reducing Rhodoferax sp. and chemoautotrophic Fe(II)-oxidizing Gallionella sp., increased by 3–5 orders of magnitude in absolute abundance within the transition-zone and permafrost microbiomes, accounting for 65% of community abundance. We also found that the abundance of genes for Fe(III) reduction (e.g., MtrE) and Fe(II) oxidation (e.g., Cyc1) increased concurrently with genes for benzoate degradation and pyruvate metabolism, in which pyruvate is used to generate acetate that can be oxidized, along with benzoate, to CO2 when coupled with Fe(III) reduction. Gene abundance for CH4 metabolism decreased following extended thaw, suggesting dissimilatory Fe(III) reduction suppresses acetoclastic methanogenesis under reducing conditions. Our genomic evidence indicates that microbial carbon degradation is dominated by iron redox metabolism via an increase in gene abundance associated with Fe(III) reduction and Fe(II) oxidation during initial permafrost thaw, likely increasing microbial respiration while suppressing methanogenesis in wet sedge tundra.
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Abstract -
Dissolved organic carbon (DOC) was leached from permafrost soils near the Toolik Field Station in the Alaskan Arctic, either kept in the dark or exposed to light treatments, and then incubated with native permafrost microbial communities. The radiocarbon (14C) and stable carbon (13C) isotopic compositions of the initial DOC present in the dark or light-exposed permafrost soil leachates and the carbon dioxide (CO2) produced by microbial respiration of dark or light-exposed permafrost DOC were quantified.more » « less
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Dissolved organic carbon (DOC) was leached from permafrost soils collected from the frozen permafrost layer at four sites underlying tussock tundra or wet sedge tundra vegetation and from both undisturbed soil and a thermokarst failure on the North Slope of Alaska during the summers of 2018 and 2022.more » « less
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Leachates of dissolved organic carbon (DOC) from permafrost soils were prepared from soils collected from the North Slope of Alaska in 2018 and 2022. Soil leachates were then either kept in the dark or exposed to light from LEDs at 305 nm (UV) and 405 nm (visible), and then inoculated with native microbial communities and incubated. At the start of the biological incubations, single replicates of the DOC after dark or light treatment and inoculation were assigned accession numbers and analyzed for 14C and 13C at the National Ocean Sciences Accelerator Mass Spectrometry (NOSAMS) facility. At the end of the biological incubations, duplicates of the dissolved inorganic carbon (DIC) in those waters were assigned accession numbers and analyzed for 14C and 13C at the NOSAMS facility.more » « less
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Dissolved organic carbon (DOC) was leached from permafrost soils near the Toolik Field Station in the Alaskan Arctic. Daily rates of sunlight absorption by chromophoric dissolved organic matter (CDOM) from the permafrost soil leachates over the water column depth of an arctic headwater stream were quantified.more » « less
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Effects of long-term climate trends on the methane and CO2 exchange processes of Toolik Lake, AlaskaMethane and carbon dioxide effluxes from aquatic systems in the Arctic will affect and likely amplify global change. As permafrost thaws in a warming world, more dissolved organic carbon (DOC) and greenhouse gases are produced and move from soils to surface waters where the DOC can be oxidized to CO 2 and also released to the atmosphere. Our main study objective is to measure the release of carbon to the atmosphere via effluxes of methane (CH 4 ) and carbon dioxide (CO 2 ) from Toolik Lake, a deep, dimictic, low-arctic lake in northern Alaska. By combining direct eddy covariance flux measurements with continuous gas pressure measurements in the lake surface waters, we quantified the k 600 piston velocity that controls gas flux across the air–water interface. Our measured k values for CH 4 and CO 2 were substantially above predictions from several models at low to moderate wind speeds, and only converged on model predictions at the highest wind speeds. We attribute this higher flux at low wind speeds to effects on water-side turbulence resulting from how the surrounding tundra vegetation and topography increase atmospheric turbulence considerably in this lake, above the level observed over large ocean surfaces. We combine this process-level understanding of gas exchange with the trends of a climate-relevant long-term (30 + years) meteorological data set at Toolik Lake to examine short-term variations (2015 ice-free season) and interannual variability (2010–2015 ice-free seasons) of CH 4 and CO 2 fluxes. We argue that the biological processing of DOC substrate that becomes available for decomposition as the tundra soil warms is important for understanding future trends in aquatic gas fluxes, whereas the variability and long-term trends of the physical and meteorological variables primarily affect the timing of when higher or lower than average fluxes are observed. We see no evidence suggesting that a tipping point will be reached soon to change the status of the aquatic system from gas source to sink. We estimate that changes in CH 4 and CO 2 fluxes will be constrained with a range of +30% and −10% of their current values over the next 30 years.more » « less
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To understand patterns in CO2 partial pressure (PCO2) over time in wetlands’ surface water and porewater, we examined the relationship between PCO2 and land–atmosphere flux of CO2 at the ecosystem scale at 22 Northern Hemisphere wetland sites synthesized through an open call. Sites spanned 6 major wetland types (tidal, alpine, fen, bog, marsh, and prairie pothole/karst), 7 Köppen climates, and 16 different years. Ecosystem respiration (Reco) and gross primary production (GPP), components of vertical CO2 flux, were compared to PCO2, a component of lateral CO2 flux, to determine if photosynthetic rates and soil respiration consistently influence wetland surface and porewater CO2 concentrations across wetlands. Similar to drivers of primary productivity at the ecosystem scale, PCO2 was strongly positively correlated with air temperature (Tair) at most sites. Monthly average PCO2 tended to peak towards the middle of the year and was more strongly related to Reco than GPP. Our results suggest Reco may be related to biologically driven PCO2 in wetlands, but the relationship is site-specific and could be an artifact of differently timed seasonal cycles or other factors. Higher levels of discharge do not consistently alter the relationship between Reco and temperature normalized PCO2. This work synthesizes relevant data and identifies key knowledge gaps in drivers of wetland respiration.more » « less
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Nojiri, Hideaki (Ed.)ABSTRACT In the oligotrophic oceans, key autotrophs depend on “helper” bacteria to reduce oxidative stress from hydrogen peroxide (H 2 O 2 ) in the extracellular environment. H 2 O 2 is also a ubiquitous stressor in freshwaters, but the effects of H 2 O 2 on autotrophs and their interactions with bacteria are less well understood in freshwaters. Naturally occurring H 2 O 2 in freshwater systems is proposed to impact the proportion of microcystin-producing (toxic) and non-microcystin-producing (nontoxic) Microcystis in blooms, which influences toxin concentrations and human health impacts. However, how different strains of Microcystis respond to naturally occurring H 2 O 2 concentrations and the microbes responsible for H 2 O 2 decomposition in freshwater cyanobacterial blooms are unknown. To address these knowledge gaps, we used metagenomics and metatranscriptomics to track the presence and expression of genes for H 2 O 2 decomposition by microbes during a cyanobacterial bloom in western Lake Erie in the summer of 2014. katG encodes the key enzyme for decomposing extracellular H 2 O 2 but was absent in most Microcystis cells. katG transcript relative abundance was dominated by heterotrophic bacteria. In axenic Microcystis cultures, an H 2 O 2 scavenger (pyruvate) significantly improved growth rates of one toxic strain while other toxic and nontoxic strains were unaffected. These results indicate that heterotrophic bacteria play a key role in H 2 O 2 decomposition in Microcystis blooms and suggest that their activity may affect the fitness of some Microcystis strains and thus the strain composition of Microcystis blooms but not along a toxic versus nontoxic dichotomy. IMPORTANCE Cyanobacterial harmful algal blooms (CHABs) threaten freshwater ecosystems globally through the production of toxins. Toxin production by cyanobacterial species and strains during CHABs varies widely over time and space, but the ecological drivers of the succession of toxin-producing species remain unclear. Hydrogen peroxide (H 2 O 2 ) is ubiquitous in natural waters, inhibits microbial growth, and may determine the relative proportions of Microcystis strains during blooms. However, the mechanisms and organismal interactions involved in H 2 O 2 decomposition are unexplored in CHABs. This study shows that some strains of bloom-forming freshwater cyanobacteria benefit from detoxification of H 2 O 2 by associated heterotrophic bacteria, which may impact bloom development.more » « less
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Abstract Climate warming has increased permafrost thaw in arctic tundra and extended the duration of annual thaw (number of thaw days in summer) along soil profiles. Predicting the microbial response to permafrost thaw depends largely on knowing how increased thaw duration affects the composition of the soil microbiome. Here, we determined soil microbiome composition from the annually thawed surface active layer down through permafrost from two tundra types at each of three sites on the North Slope of Alaska, USA. Variations in soil microbial taxa were found between sites up to ~90 km apart, between tundra types, and between soil depths. Microbiome differences at a site were greatest across transitions from thawed to permafrost depths. Results from correlation analysis based on multi‐decadal thaw surveys show that differences in thaw duration by depth were significantly, positively correlated with the abundance of dominant taxa in the active layer and negatively correlated with dominant taxa in the permafrost. Microbiome composition within the transition zone 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. We suggest that thaw duration rather than thaw frequency has a greater impact on the composition of microbial taxa within arctic soils.