Microbial assemblages in Arctic coastal thermokarst lakes and lagoons.

Several studies have investigated changes in microbial community composition in thawing permafrost landscapes, but microbial assemblages in the transient ecosystems of the Arctic coastline remain poorly understood. Thermokarst lakes, abrupt permafrost thaw features, are widespread along the pan-Arctic coast and transform into thermokarst lagoons upon coastal erosion and sea-level rise. This study looks at the effect of marine water inundation (imposing a sulfate-rich, saline environment on top of former thermokarst lake sediments) on microbial community composition and the processes potentially driving microbial community assembly. In the uppermost lagoon sediment influenced from marine water inflow, the microbial structures were significantly different from those deeper in the lagoon sediment and from those of the lakes. In addition, they became more similar along depth compared with lake communities. At the same time, the diversity of core microbial consortia community decreased compared with the lake sediments. This work provides initial observational evidence that Arctic thermokarst lake to lagoon transitions do not only substantially alter microbial communities but also that this transition has a larger effect than permafrost thaw and lake formation history.

An Update on Eukaryotic Viruses Revived from Ancient Permafrost.

One quarter of the Northern hemisphere is underlain by permanently frozen ground, referred to as permafrost. Due to climate warming, irreversibly thawing permafrost is releasing organic matter frozen for up to a million years, most of which decomposes into carbon dioxide and methane, further enhancing the greenhouse effect. Part of this organic matter also consists of revived cellular microbes (prokaryotes, unicellular eukaryotes) as well as viruses that have remained dormant since prehistorical times. While the literature abounds on descriptions of the rich and diverse prokaryotic microbiomes found in permafrost, no additional report about "live" viruses have been published since the two original studies describing pithovirus (in 2014) and mollivirus (in 2015). This wrongly suggests that such occurrences are rare and that "zombie viruses" are not a public health threat. To restore an appreciation closer to reality, we report the preliminary characterizations of 13 new viruses isolated from seven different ancient Siberian permafrost samples, one from the Lena river and one from Kamchatka cryosol. As expected from the host specificity imposed by our protocol, these viruses belong to five different clades infecting Acanthamoeba spp. but not previously revived from permafrost: Pandoravirus, Cedratvirus, Megavirus, and Pacmanvirus, in addition to a new Pithovirus strain.

Microbial methane cycling in sediments of Arctic thermokarst lagoons.

Thermokarst lagoons represent the transition state from a freshwater lacustrine to a marine environment, and receive little attention regarding their role for greenhouse gas production and release in Arctic permafrost landscapes. We studied the fate of methane (CH4 ) in sediments of a thermokarst lagoon in comparison to two thermokarst lakes on the Bykovsky Peninsula in northeastern Siberia through the analysis of sediment CH4 concentrations and isotopic signature, methane-cycling microbial taxa, sediment geochemistry, lipid biomarkers, and network analysis. We assessed how differences in geochemistry between thermokarst lakes and thermokarst lagoons, caused by the infiltration of sulfate-rich marine water, altered the microbial methane-cycling community. Anaerobic sulfate-reducing ANME-2a/2b methanotrophs dominated the sulfate-rich sediments of the lagoon despite its known seasonal alternation between brackish and freshwater inflow and low sulfate concentrations compared to the usual marine ANME habitat. Non-competitive methylotrophic methanogens dominated the methanogenic community of the lakes and the lagoon, independent of differences in porewater chemistry and depth. This potentially contributed to the high CH4 concentrations observed in all sulfate-poor sediments. CH4 concentrations in the freshwater-influenced sediments averaged 1.34 ± 0.98 µmol g-1 , with highly depleted δ13 C-CH4 values ranging from -89‰ to -70‰. In contrast, the sulfate-affected upper 300 cm of the lagoon exhibited low average CH4 concentrations of 0.011 ± 0.005 µmol g-1 with comparatively enriched δ13 C-CH4 values of -54‰ to -37‰ pointing to substantial methane oxidation. Our study shows that lagoon formation specifically supports methane oxidizers and methane oxidation through changes in pore water chemistry, especially sulfate, while methanogens are similar to lake conditions.

A globally relevant stock of soil nitrogen in the Yedoma permafrost domain.

Nitrogen regulates multiple aspects of the permafrost climate feedback, including plant growth, organic matter decomposition, and the production of the potent greenhouse gas nitrous oxide. Despite its importance, current estimates of permafrost nitrogen are highly uncertain. Here, we compiled a dataset of >2000 samples to quantify nitrogen stocks in the Yedoma domain, a region with organic-rich permafrost that contains ~25% of all permafrost carbon. We estimate that the Yedoma domain contains 41.2 gigatons of nitrogen down to ~20 metre for the deepest unit, which increases the previous estimate for the entire permafrost zone by ~46%. Approximately 90% of this nitrogen (37 gigatons) is stored in permafrost and therefore currently immobile and frozen. Here, we show that of this amount, ¾ is stored >3 metre depth, but if partially mobilised by thaw, this large nitrogen pool could have continental-scale consequences for soil and aquatic biogeochemistry and global-scale consequences for the permafrost feedback.

Degrading permafrost river catchments and their impact on Arctic Ocean nearshore processes.

Arctic warming is causing ancient perennially frozen ground (permafrost) to thaw, resulting in ground collapse, and reshaping of landscapes. This threatens Arctic peoples' infrastructure, cultural sites, and land-based natural resources. Terrestrial permafrost thaw and ongoing intensification of hydrological cycles also enhance the amount and alter the type of organic carbon (OC) delivered from land to Arctic nearshore environments. These changes may affect coastal processes, food web dynamics and marine resources on which many traditional ways of life rely. Here, we examine how future projected increases in runoff and permafrost thaw from two permafrost-dominated Siberian watersheds-the Kolyma and Lena, may alter carbon turnover rates and OC distributions through river networks. We demonstrate that the unique composition of terrestrial permafrost-derived OC can cause significant increases to aquatic carbon degradation rates (20 to 60% faster rates with 1% permafrost OC). We compile results on aquatic OC degradation and examine how strengthening Arctic hydrological cycles may increase the connectivity between terrestrial landscapes and receiving nearshore ecosystems, with potential ramifications for coastal carbon budgets and ecosystem structure. To address the future challenges Arctic coastal communities will face, we argue that it will become essential to consider how nearshore ecosystems will respond to changing coastal inputs and identify how these may affect the resiliency and availability of essential food resources.

Metagenomic survey of the microbiome of ancient Siberian permafrost and modern Kamchatkan cryosols.

In the context of global warming, the melting of Arctic permafrost raises the threat of a reemergence of microorganisms some of which were shown to remain viable in ancient frozen soils for up to half a million years. In order to evaluate this risk, it is of interest to acquire a better knowledge of the composition of the microbial communities found in this understudied environment. Here, we present a metagenomic analysis of 12 soil samples from Russian Arctic and subarctic pristine areas: Chukotka, Yakutia and Kamchatka, including nine permafrost samples collected at various depths. These large datasets (9.2 × 1011 total bp) were assembled (525 313 contigs > 5 kb), their encoded protein contents predicted, and then used to perform taxonomical assignments of bacterial, archaeal and eukaryotic organisms, as well as DNA viruses. The various samples exhibited variable DNA contents and highly diverse taxonomic profiles showing no obvious relationship with their locations, depths or deposit ages. Bacteria represented the largely dominant DNA fraction (95%) in all samples, followed by archaea (3.2%), surprisingly little eukaryotes (0.5%), and viruses (0.4%). Although no common taxonomic pattern was identified, the samples shared unexpected high frequencies of ß-lactamase genes, almost 0.9 copy/bacterial genome. In addition to known environmental threats, the particularly intense warming of the Arctic might thus enhance the spread of bacterial antibiotic resistances, today's major challenge in public health. ß-Lactamases were also observed at high frequency in other types of soils, suggesting their general role in the regulation of bacterial populations.

Seasonal nitrogen fluxes of the Lena River Delta.

The Arctic is nutrient limited, particularly by nitrogen, and is impacted by anthropogenic global warming which occurs approximately twice as fast compared to the global average. Arctic warming intensifies thawing of permafrost-affected soils releasing their large organic nitrogen reservoir. This organic nitrogen reaches hydrological systems, is remineralized to reactive inorganic nitrogen, and is transported to the Arctic Ocean via large rivers. We estimate the load of nitrogen supplied from terrestrial sources into the Arctic Ocean by sampling in the Lena River and its Delta. We took water samples along one of the major deltaic channels in winter and summer in 2019 and sampling station in the central delta over a one-year cycle. Additionally, we investigate the potential release of reactive nitrogen, including nitrous oxide from soils in the Delta. We found that the Lena transported nitrogen as dissolved organic nitrogen to the coastal Arctic Ocean and that eroded soils are sources of reactive inorganic nitrogen such as ammonium and nitrate. The Lena and the Deltaic region apparently are considerable sources of nitrogen to nearshore coastal zone. The potential higher availability of inorganic nitrogen might be a source to enhance nitrous oxide emissions from terrestrial and aquatic sources to the atmosphere.

Greenhouse gas production and lipid biomarker distribution in Yedoma and Alas thermokarst lake sediments in Eastern Siberia.

Permafrost thaw leads to thermokarst lake formation and talik growth tens of meters deep, enabling microbial decomposition of formerly frozen organic matter (OM). We analyzed two 17-m-long thermokarst lake sediment cores taken in Central Yakutia, Russia. One core was from an Alas lake in a Holocene thermokarst basin that underwent multiple lake generations, and the second core from a young Yedoma upland lake (formed ~70 years ago) whose sediments have thawed for the first time since deposition. This comparison provides a glance into OM fate in thawing Yedoma deposits. We analyzed total organic carbon (TOC) and dissolved organic carbon (DOC) content, n-alkane concentrations, and bacterial and archaeal membrane markers. Furthermore, we conducted 1-year-long incubations (4°C, dark) and measured anaerobic carbon dioxide (CO2 ) and methane (CH4 ) production. The sediments from both cores contained little TOC (0.7 ± 0.4 wt%), but DOC values were relatively high, with the highest values in the frozen Yedoma lake sediments (1620 mg L-1 ). Cumulative greenhouse gas (GHG) production after 1 year was highest in the Yedoma lake sediments (226 ± 212 µg CO2 -C g-1  dw, 28 ± 36 µg CH4 -C g-1  dw) and 3 and 1.5 times lower in the Alas lake sediments, respectively (75 ± 76 µg CO2 -C g-1  dw, 19 ± 29 µg CH4 -C g-1  dw). The highest CO2 production in the frozen Yedoma lake sediments likely results from decomposition of readily bioavailable OM, while highest CH4 production in the non-frozen top sediments of this core suggests that methanogenic communities established upon thaw. The lower GHG production in the non-frozen Alas lake sediments resulted from advanced OM decomposition during Holocene talik development. Furthermore, we found that drivers of CO2 and CH4 production differ following thaw. Our results suggest that GHG production from TOC-poor mineral deposits, which are widespread throughout the Arctic, can be substantial. Therefore, our novel data are relevant for vast ice-rich permafrost deposits vulnerable to thermokarst formation.

Taxonomic and functional analyses of intact microbial communities thriving in extreme, astrobiology-relevant, anoxic sites.

BACKGROUND: Extreme terrestrial, analogue environments are widely used models to study the limits of life and to infer habitability of extraterrestrial settings. In contrast to Earth's ecosystems, potential extraterrestrial biotopes are usually characterized by a lack of oxygen. METHODS: In the MASE project (Mars Analogues for Space Exploration), we selected representative anoxic analogue environments (permafrost, salt-mine, acidic lake and river, sulfur springs) for the comprehensive analysis of their microbial communities. We assessed the microbiome profile of intact cells by propidium monoazide-based amplicon and shotgun metagenome sequencing, supplemented with an extensive cultivation effort. RESULTS: The information retrieved from microbiome analyses on the intact microbial community thriving in the MASE sites, together with the isolation of 31 model microorganisms and successful binning of 15 high-quality genomes allowed us to observe principle pathways, which pinpoint specific microbial functions in the MASE sites compared to moderate environments. The microorganisms were characterized by an impressive machinery to withstand physical and chemical pressures. All levels of our analyses revealed the strong and omnipresent dependency of the microbial communities on complex organic matter. Moreover, we identified an extremotolerant cosmopolitan group of 34 poly-extremophiles thriving in all sites. CONCLUSIONS: Our results reveal the presence of a core microbiome and microbial taxonomic similarities between saline and acidic anoxic environments. Our work further emphasizes the importance of the environmental, terrestrial parameters for the functionality of a microbial community, but also reveals a high proportion of living microorganisms in extreme environments with a high adaptation potential within habitability borders. Video abstract.

Spatial heterogeneity and environmental predictors of permafrost region soil organic carbon stocks.

Large stocks of soil organic carbon (SOC) have accumulated in the Northern Hemisphere permafrost region, but their current amounts and future fate remain uncertain. By analyzing dataset combining >2700 soil profiles with environmental variables in a geospatial framework, we generated spatially explicit estimates of permafrost-region SOC stocks, quantified spatial heterogeneity, and identified key environmental predictors. We estimated that Pg C are stored in the top 3 m of permafrost region soils. The greatest uncertainties occurred in circumpolar toe-slope positions and in flat areas of the Tibetan region. We found that soil wetness index and elevation are the dominant topographic controllers and surface air temperature (circumpolar region) and precipitation (Tibetan region) are significant climatic controllers of SOC stocks. Our results provide first high-resolution geospatial assessment of permafrost region SOC stocks and their relationships with environmental factors, which are crucial for modeling the response of permafrost affected soils to changing climate.

Fast response of cold ice-rich permafrost in northeast Siberia to a warming climate.

The ice- and organic-rich permafrost of the northeast Siberian Arctic lowlands (NESAL) has been projected to remain stable beyond 2100, even under pessimistic climate warming scenarios. However, the numerical models used for these projections lack processes which induce widespread landscape change termed thermokarst, precluding realistic simulation of permafrost thaw in such ice-rich terrain. Here, we consider thermokarst-inducing processes in a numerical model and show that substantial permafrost degradation, involving widespread landscape collapse, is projected for the NESAL under strong warming (RCP8.5), while thawing is moderated by stabilizing feedbacks under moderate warming (RCP4.5). We estimate that by 2100 thaw-affected carbon could be up to three-fold (twelve-fold) under RCP4.5 (RCP8.5), of what is projected if thermokarst-inducing processes are ignored. Our study provides progress towards robust assessments of the global permafrost carbon-climate feedback by Earth system models, and underlines the importance of mitigating climate change to limit its impacts on permafrost ecosystems.

Organic Carbon and Nitrogen Stocks Along a Thermokarst Lake Sequence in Arctic Alaska.

Thermokarst lake landscapes are permafrost regions, which are prone to rapid (on seasonal to decadal time scales) changes, affecting carbon and nitrogen cycles. However, there is a high degree of uncertainty related to the balance between carbon and nitrogen cycling and storage. We collected 12 permafrost soil cores from six drained thermokarst lake basins (DTLBs) along a chronosequence north of Teshekpuk Lake in northern Alaska and analyzed them for carbon and nitrogen contents. For comparison, we included three lacustrine cores from an adjacent thermokarst lake and one soil core from a non thermokarst affected remnant upland. This allowed to calculate the carbon and nitrogen stocks of the three primary landscape units (DTLB, lake, and upland), to reconstruct the landscape history, and to analyze the effect of thermokarst lake formation and drainage on carbon and nitrogen stocks. We show that carbon and nitrogen contents and the carbon-nitrogen ratio are considerably lower in sediments of extant lakes than in the DTLB or upland cores indicating degradation of carbon during thermokarst lake formation. However, we found similar amounts of total carbon and nitrogen stocks due to the higher density of lacustrine sediments caused by the lack of ground ice compared to DTLB sediments. In addition, the radiocarbon-based landscape chronology for the past 7,000 years reveals five successive lake stages of partially, spatially overlapping DTLBs in the study region, reflecting the dynamic nature of ice-rich permafrost deposits. With this study, we highlight the importance to include these dynamic landscapes in future permafrost carbon feedback models.

Widespread global peatland establishment and persistence over the last 130,000 y.

Glacial-interglacial variations in CO2 and methane in polar ice cores have been attributed, in part, to changes in global wetland extent, but the wetland distribution before the Last Glacial Maximum (LGM, 21 ka to 18 ka) remains virtually unknown. We present a study of global peatland extent and carbon (C) stocks through the last glacial cycle (130 ka to present) using a newly compiled database of 1,063 detailed stratigraphic records of peat deposits buried by mineral sediments, as well as a global peatland model. Quantitative agreement between modeling and observations shows extensive peat accumulation before the LGM in northern latitudes (>40°N), particularly during warmer periods including the last interglacial (130 ka to 116 ka, MIS 5e) and the interstadial (57 ka to 29 ka, MIS 3). During cooling periods of glacial advance and permafrost formation, the burial of northern peatlands by glaciers and mineral sediments decreased active peatland extent, thickness, and modeled C stocks by 70 to 90% from warmer times. Tropical peatland extent and C stocks show little temporal variation throughout the study period. While the increased burial of northern peats was correlated with cooling periods, the burial of tropical peat was predominately driven by changes in sea level and regional hydrology. Peat burial by mineral sediments represents a mechanism for long-term terrestrial C storage in the Earth system. These results show that northern peatlands accumulate significant C stocks during warmer times, indicating their potential for C sequestration during the warming Anthropocene.

Sedimentary and geochemical characteristics of two small permafrost-dominated Arctic river deltas in northern Alaska.

Arctic river deltas are highly dynamic environments in the northern circumpolar permafrost region that are affected by fluvial, coastal, and permafrost-thaw processes. They are characterized by thick sediment deposits containing large but poorly constrained amounts of frozen organic carbon and nitrogen. This study presents new data on soil organic carbon and nitrogen storage as well as accumulation rates from the Ikpikpuk and Fish Creek river deltas, two small, permafrost-dominated Arctic river deltas on the Arctic Coastal Plain of northern Alaska. A soil organic carbon storage of 42.4 ± 1.6 and 37.9 ± 3.5 kg C m- 2 and soil nitrogen storage of 2.1 ± 0.1 and 2.0 ± 0.2 kg N m- 2 was found for the first 2 m of soil for the Ikpikpuk and Fish Creek river delta, respectively. While the upper meter of soil contains 3.57 Tg C, substantial amounts of carbon (3.09 Tg C or 46%) are also stored within the second meter of soil (100-200 cm) in the two deltas. An increasing and inhomogeneous distribution of C with depth is indicative of the dominance of deltaic depositional rather than soil forming processes for soil organic carbon storage. Largely, mid- to late Holocene radiocarbon dates in our cores suggest different carbon accumulation rates for the two deltas for the last 2000 years. Rates up to 28 g C m- 2 year- 1 for the Ikpikpuk river delta are about twice as high as for the Fish Creek river delta. With this study, we highlight the importance of including these highly dynamic permafrost environments in future permafrost carbon estimations.

Transformation of terrestrial organic matter along thermokarst-affected permafrost coasts in the Arctic.

The changing climate in the Arctic has a profound impact on permafrost coasts, which are subject to intensified thermokarst formation and erosion. Consequently, terrestrial organic matter (OM) is mobilized and transported into the nearshore zone. Yet, little is known about the fate of mobilized OM before and after entering the ocean. In this study we investigated a retrogressive thaw slump (RTS) on Qikiqtaruk - Herschel Island (Yukon coast, Canada). The RTS was classified into an undisturbed, a disturbed (thermokarst-affected) and a nearshore zone and sampled systematically along transects. Samples were analyzed for total and dissolved organic carbon and nitrogen (TOC, DOC, TN, DN), stable carbon isotopes (δ13C-TOC, δ13C-DOC), and dissolved inorganic nitrogen (DIN), which were compared between the zones. C/N-ratios, δ13C signatures, and ammonium (NH4-N) concentrations were used as indicators for OM degradation along with biomarkers (n-alkanes, n-fatty acids, n-alcohols). Our results show that OM significantly decreases after disturbance with a TOC and DOC loss of 77 and 55% and a TN and DN loss of 53 and 48%, respectively. C/N-ratios decrease significantly, whereas NH4-N concentrations slightly increase in freshly thawed material. In the nearshore zone, OM contents are comparable to the disturbed zone. We suggest that the strong decrease in OM is caused by initial dilution with melted massive ice and immediate offshore transport via the thaw stream. In the mudpool and thaw stream, OM is subject to degradation, whereas in the slump floor the nitrogen decrease is caused by recolonizing vegetation. Within the nearshore zone of the ocean, heavier portions of OM are directly buried in marine sediments close to shore. We conclude that RTS have profound impacts on coastal environments in the Arctic. They mobilize nutrients from permafrost, substantially decrease OM contents and provide fresh water and nutrients at a point source.

The deep permafrost carbon pool of the Yedoma region in Siberia and Alaska.

[1] Estimates for circumpolar permafrost organic carbon (OC) storage suggest that this pool contains twice the amount of current atmospheric carbon. The Yedoma region sequestered substantial quantities of OC and is unique because its deep OC, which was incorporated into permafrost during ice age conditions. Rapid inclusion of labile organic matter into permafrost halted decomposition and resulted in a deep long-term sink. We show that the deep frozen OC in the Yedoma region consists of two distinct major subreservoirs: Yedoma deposits (late Pleistocene ice- and organic-rich silty sediments) and deposits formed in thaw-lake basins (generalized as thermokarst deposits). We quantified the OC pool based on field data and extrapolation using geospatial data sets to 83 + 61/-57 Gt for Yedoma deposits and to 128 + 99/-96 Gt for thermokarst deposits. The total Yedoma region 211 + 160/-153 Gt is a substantial amount of thaw-vulnerable OC that must be accounted for in global models.