Abstract
The Arctic cryosphere is collapsing, posing overlapping environmental risks. In particular, thawing permafrost threatens to release biological, chemical and radioactive materials that have been sequestered for tens to hundreds of thousands of years. As these constituents re-enter the environment, they have the potential to disrupt ecosystem function, reduce the populations of unique Arctic wildlife and endanger human health. Here, we review the current state of the science to identify potential hazards currently frozen in Arctic permafrost. We also consider the cascading natural and anthropogenic processes that may compound the impacts of these risks, as it is unclear whether the highly adapted Arctic ecosystems have the resilience to withstand new stresses. We conclude by recommending research priorities to address these underappreciated risks.
Main
The Arctic (above 60° N)1,2 is remote, frozen and largely undisturbed terrain that is uniquely suited for long-term biological and chemical storage. Over millennia, natural processes, accidents and intentional storage have contributed to the accumulation of the diverse compounds that are currently sequestered in northern high-latitude permafrost, ice and snow. With the Arctic warming at two to three times the mean global rate, up to 65% of the Arctic’s near-surface permafrost may be lost by 2100, releasing known and unknown hazards into the global environment3,4,5.
The majority of Arctic permafrost has been present since the Pleistocene (800 kyr to 1 Myr ago) or the Last Glacial Maximum (~10 kyr ago; ka)6. Permafrost depth is a first-order approximation of age, where deeper layers were deposited further in the past. However, permafrost thaw changes this structure, opening new niches, closing old ones, resuscitating dormant microbial communities and enabling transport into the surrounding environment7,8. Gradual thaw releases the most recently sequestered components first, followed by increasingly older constituents as thaw penetrates deeper9,10. This top-down thaw is driven by temperature and precipitation changes and is relatively slow, typically increasing active layer depth at rates of centimetres per decade9. By contrast, abrupt thaw rapidly exposes old permafrost horizons, releasing compounds and microorganisms sequestered in deeper layers11,12. As Arctic landscape change increases with climate warming, tracking the emergence of entrained chemicals and microorganisms is a growing challenge.
Previous reviews summarized Arctic system research, focusing on important topics such as the permafrost carbon feedback and abrupt landscape change13,14. Similarly, the impacts of permafrost degradation on human infrastructure and ecosystem services are discussed in the literature15,16. However, the emergent threats from entrained viruses17,18, bacteria19,20, anthropogenic chemicals21,22, nuclear waste23,24 or other biogeochemical hazards reintroduced into the contemporary environment by thaw (Fig. 1) have received less attention. Here, we review the literature to catalogue emergent microbial, viral and chemical hazards within the new Arctic (Fig. 2), and recommend research priorities to quantify and address these risks25,26,27.
Conceptual diagram of material interaction and movement from the permafrost into adjacent environmental compartments. An idealized representation of first-order flow with minimal spatial variability. Landscape heterogeneity introduces complexity and flow velocity variability, which are not represented in this idealized model.
Biogeochemical hazards from thawing permafrost
Recent degradation of the cryosphere is reintroducing ancient microorganisms that are highly adapted to Arctic conditions. Methuselah microorganisms—organisms with extremotolerant traits that have the ability to maintain viability for a million years or more—are bringing palaeoecosystem dynamics into the contemporary Arctic, with unknown consequences10,28,29. As thaw continues, increased activity from long-dormant microorganisms may already be contributing to changing Arctic ecosystem processes7,30,31,32 (Fig. 3). With atmospheric warming driving permafrost thaw from the top down (referred to as active-layer thickening or gradual thaw), microbial communities entrained within the permafrost simultaneously force change from the bottom up33,34,35 (Fig. 1). This multilevel reorganization presents an unprecedented alteration to the permafrost ecosystem, contributing to Arctic change36.
Microbial species from diverse phyla are re-entering an ecosystem that is already stressed by change and contamination37,38. Hazardous compounds transported through atmospheric deposition39,40, infrastructure leaks5, accidental release41,42 and the thawing cryosphere24,39,41,43,44,45,46,47 can cause human health problems and environmental damage when released. Amplified in the pristine conditions found across the Arctic, the convergence of climate change, re-emergence of Methuselah microorganisms and mobilization of anthropogenic chemicals may be converting the polar north into a radically different system. Our ability to forecast these emergent risks is limited by challenges in quantifying where, when, how fast and how deep permafrost will thaw.
Ancient microbial and viral diversity
Within the Arctic, permafrost is a reservoir of minimally characterized microbial life48. A single gram can contain hundreds to thousands of microbial taxa, but the composition and functionality of permafrost species is poorly sampled49. The diversity of microbial and viral species in even small areas of permafrost is considerable. For example, a recent study recovered 1,907 uncharacterized virus populations in 197 samples (10–11 cm cores) across a permafrost thaw gradient in Sweden’s Stordalen Mire18. Over 58% of these unknown microorganisms were still active, indicating a diverse virosphere18. Similarly, a team working in Svalbard found that, within the roots of two species of periglacial ectomycorrhizal plants (Bistorta vivipara and Salix polaris), 25% of the active microbial families were yet unclassified50.
Furthermore, carbon released by permafrost thaw can intensify microorganism proliferation that was previously constrained by temperatures and nutrient limitations, with unknown results31,34,49,51. This knowledge gap introduces substantial uncertainty in risk assessment and forecasting, meaning that the persistence of Methuselah microorganisms within modern ecosystems may emerge as an unfortunate surprise. Any re-emergence of Methuselah microorganisms into the modern Arctic has the potential to change the soil composition, vegetative growth and community composition—further accelerating the environmental transition from climate change7,52,53.
Recovered Methuselah viruses and microorganisms
The ability to survive in extreme environments for extended periods has kept many microorganisms in permafrost viable, regardless of when they were deposited. For example, studies in 500-kyr- to 1-Myr-old permafrost communities have described small populations of non-endospore-forming bacteria that survived through ongoing DNA repair and lessening cellular metabolic activity54. In cold methane seeps, ancient bacteria phylotypes related to Loktanella, Gillisia, Halomonas and Marinobacter spp. were successfully recovered from temperatures below −5 °C (refs. 55,56), while microorganisms from Clostridium and Psychrobacter were isolated in brine lenses from 100–120 ka (Table 1 and Fig. 3)57. In shallower permafrost, just over 30 ka, intact virus species, including mimiviruses, pandoraviruses, Pithovirus sibericum and Mollivirus sibericum, have been identified58,59. More recently, the Glaciecola, a genus of bacteria that is known for its swift consumption of phytoplankton organic material, are adapting to increasing temperatures in cold-water northern fjords by increasing carbon uptake and turnover49.
Research into the genomic diversity of permafrost microorganisms is an emergent field, with metagenomics making microbial catalogues and reconstructions of organisms possible8,49,58,60,61. In a recent example, the genomes of the Sclerotinia sclerotiorum (DNA virus) and the ancient Northwest Territories cripavirus (aNCV) were resynthesized from a reindeer faecal deposit entombed within 700-year-old ice62 (Fig. 2). The revival of nematodes from 30-kyr-old Siberian permafrost and the recovery of a bdelloid rotifer from 24-kyr-old permafrost demonstrate that complex, multicellular organisms have also developed effective survival strategies63.
Adaptations
Methuselah microorganisms and viruses have developed a myriad of adaptations to survive in permafrost for millennia despite static conditions in subzero temperatures with minimal water or nutrients64,65,66. Microbial adaptation strategies include the production of carotenoids67, increases in membrane fluidity64, the ability to scavenge detrital biomass30, high abundance of stress sensing and response genes66, hopanoid unsaturation after cold exposure64,67, dormancy66,68 and even surviving on trace gas constituents69.
Mechanisms to repair DNA are also important adaptations for microorganisms. In ancient permafrost, active DNA repair rather than dormancy can be an important adaptation for microorganisms. DNA damage accumulates over time in dormant cells, eventually becoming fatal, making active DNA repair important for long-term survival66. Endospore-forming cells may also persist as vegetative cells in ancient permafrost (for example, Clostridium from 33-kyr-old permafrost)70 and the upper time limits for the persistence of dormant cells are still being investigated.
In contrast to microorganisms, known viruses recovered from permafrost employ substantially different adaptations. As they are metabolically inert, persistence in subzero temperatures depends on infecting cold-adapted hosts56. This requirement limits the long-term viability of viral pathogens in permafrost, in which microbial communities are relatively sparse. Little is known about permafrost adaptations of viruses, but studies from other subzero and highly saline environments suggest a propensity towards lysogenic (the viral genome is integrated into the host chromosome) rather than lytic (active infection) cycling54,71,72. Thaw may cause virus activity to change to lytic, or active, infection, producing viral particles or modifying host physiology. Subsequently, the virus can encode genes to enhance host cold adaption or promote infection, assembly and release18,59,73. Considerable diversity in virus species and limited linkages between metagenomes and hosts present ongoing challenges in identifying virus adaptation strategies.
Although forecasts and interpretations of the impacts of emergent microorganisms and viruses are forthcoming, prediction uncertainty is large, as the composition and density of permafrost species are largely unknown. Some microorganisms are already transforming the landscape through carbon transformation and emission74, while others are adapting to warmer environments by moving to new environments49. However, it is becoming clear that the emergent microbial composition of a warmer Arctic may alter ecosystem dynamics and introduce new risks to the system.
Anthropogenic contamination
Heavy metals21,75, black carbon76 and other by-products of fossil fuel combustion have been introduced continuously into permafrost environments by long-range atmospheric transport since the beginning of the industrial age77,78,79,80 (Fig. 2 and Table 1). In the last 80 years, anthropogenic contamination has grown to include organochloride species—polychlorinated biphenyls (PCBs)81,82,83, dichloro-diphenyl-trichloroethane (DDT), hexachlorohexane (HCH)39,84—and nuclear waste41,85. Once released back into the environment, these chemicals can negatively impact ecosystem stability4,86, human and animal health87,88,89. For example, persistent organic pollutants (POPs) are known to cause cancer90, congenital disabilities91,92 and long-term health issues93 after human exposure, posing risks to Arctic populations. Moreover, heavy metals lead (Pb), mercury (Hg) and cadmium (Cd) are all known to cause organ damage, developmental issues, cancer and even death94,95,96. It is clear that the chemical footprint of global anthropogenic activities over the last century is unequivocally re-emerging in the Arctic, as studies across the globe have identified the increasing re-release of sequestered anthropogenic compounds in ice, snow, meltwater and sediment97,98. However, the real and future costs of Arctic chemical pollution remain unquantified.
Heavy metals
The Arctic contains natural metal deposits that have been mined for decades. Within mining areas, a variety of heavy metal refuse, including arsenic (As), Cd, nickel (Ni) and Hg, is dispersed through the environment, with concentrations highest in soils below 10 cm (refs. 27,75,79,99). In one example, open-pit mining above the permafrost in the Yamal Peninsula has resulted in dangerous levels of Cd (1–4 mg kg−1), Ni (1,000–1,500 mg kg−1) and Hg (40–120 mg kg−1) in the local soils79. With tens of millions of hectares dedicated to mining across the Arctic, heavy metal contamination from mine waste poses a notable exposure risk to communities and wildlife in regions spanning Scandinavia, Russia, Alaska, Canada and Greenland100.
Direct atmospheric deposition also increases heavy metals in permafrost. Studies of Arctic peat date the first atmospheric deposition of elemental Pb to over 3 ka101. Subsequent atmospheric Pb deposition persisted at relatively constant levels until around 1900 when it began to grow steadily, peaking in 1970 (refs. 101,102). Since then, the Pb concentrations in Arctic soils have decreased. It is speculated that this decline is due in part to the global phase-out of leaded gasoline, but it may also be a result of increased surface erosion and hydrological transport101. Any diffusion of stored Pb throughout the immediate environment may lead to redeposition and biotic uptake downstream, which can then be stored or transferred through the lipid-heavy plant and animal biomass, characteristic of Arctic biota, for decades97,102.
Permafrost Hg deposition and re-emergence also pose a growing risk. Permafrost regions store an estimated 600 Gg Hg (384–750 Gg)103 to 1,656 ± 962 Gg Hg in the top 3 m of soil, of which an estimated 800 ± 500 Gg Hg is frozen in permafrost104. Arctic Hg emission from thawing permafrost is estimated to increase 14–200% by 2300, driven by Arctic warming105. Already, up to 70% of mobilized Hg is absorbed by vegetation when deposited onto the soil surface104,106. Ensuing ecosystem uptake through bioaccumulation in fish (an increase of up to 222% by 2300), vegetation and sediment (82.5% of total uptake) increases with logarithmic thaw rates, exceeding the US Environmental Protection Agency water quality criteria by 2100 (ref. 105).
Migratory seabirds represent another notable biovector of heavy metals in remote Arctic environments and move recently exposed metals regionally107,108,109,110. Pond sediment in areas with frequent bird use shows high concentrations of Hg (25× the background), with colony proximity further increasing sediment contamination in the local area107. At Devon Island, Canada, ecosystems less than 1 km from colony breeding grounds had the highest contamination of As (9.20 μg g−1 maximum), Cd (8.40 μg g−1 maximum) and Zn (343.20 μg g−1)108. Bioaccumulation within specific species drives concentration, with the large glaucous gull species maintaining high levels of Hg (4.9 μg g−1), PCB (3,326 ng g−1) and DDT (2,367 μg g−1) in both tissue and shell samples110. In heterogeneous wetland and pond environments that are reliant on the influx of nutrients from seabird guano, this toxic input may create additional ecosystem stress and degradation over time108,111.
Legacy organic chemicals
Research from across high alpine and polar ecosystems globally has identified chemicals that were banned in the early 2000s that are still stored in permafrost and glacier ice39,112,113. Preferential chemical attachment to snow (snow scavenging) and polar magnification in cold regions concentrates POPs well above background levels98,114,115. In the Arctic, these physical dynamics combine to trap atmospherically transported organic and inorganic pollutants in ice, snow and permafrost116,117.
Cryospheric release of organic compounds is an exposure route of growing concern and is predicted to increase over the next 20 years, proportional to permafrost and ice loss118,119,120. The high concentrations of DDT (10 ng l−1)121, PCB (~4.5 ng l−1)122 and HCH (~20 ng l−1)121 recovered from glacial ice cores are also observed in below-glacier watersheds, confirming wider ecosystem transport98,123,124. After secondary emergence from ice and snow, chemical exposure expands through transport in the food web (Fig. 1), where the abundance of fatty tissue required by animals to survive frigid Arctic temperatures increases their contaminant load and subsequent biomagnification potential117,125.
Uptake of POPs by invertebrates34, seabirds107,110, salmon125,126,127 and mammals81,128,129 reflects the penetration of these chemicals into all trophic levels. Currently, the concentrations of PCBs and organochlorine pesticides are higher in Arctic vegetation than in the surrounding soils, suggesting that the lipophilicity of chemicals has already made trophic transport a primary dispersal mechanism75,130,131. As thaw elevates chemical release, uptake by organisms will mirror environmental output116,128. The consequences of this uptake and increasing contaminant load include decreasing populations as the multigenerational impacts of high contamination levels may limit the population size and offspring health, creating cascading system vulnerabilities43,117.
Despite the known consequences for ecosystem health, the impacts to Arctic inhabitants and ecosystems as POPs and other hazardous organic compounds move through adjacent environmental compartments (Fig. 1) are largely undetermined. Risk assessments of chemicals released by glacier melt show that the potential for human uptake increases with exposure and time39,119,125. However, few studies have traced POP transport and risk, and it is probable that the impact of these chemicals within Arctic systems is underestimated.
Nuclear materials
Radioactive materials have been sequestered in the Arctic since the beginning of nuclear testing in the 1950s132,133,134, with additional inputs from accidents, weapons tests and intentional dumping of nuclear waste that have since increased point-source concentrations23,24,135.
Between 1955 and 1990, the Soviet Union conducted 130 nuclear weapons tests in the atmosphere and near-surface ocean of the Novaya Zemlya Archipelago135,136. The tests used 224 separate explosive devices, releasing ~265 megatons of nuclear energy135. In the nearby Kara and Barents seas, over 100 decommissioned nuclear submarines were also scuttled136,137,138. Dispersed contamination from these radionuclides persists in multiple substrates across the region. For example, sediments in the bottom of the Chernaya Inlet of the Kara Sea contain 2,500–11,000 Bq kg−1 of plutonium, 3–4 orders of magnitude larger than the background level (0–3 Bq kg−1)139. The neighbouring Severny Island ice sheet also yielded high levels of radioactive caesium (137Cs; 450–650 Bq kg−1) in boreholes and snow pits140. These concentrations were further reflected in the vegetation (610 Bq kg−1) and soils (450 Bq kg−1) below the glacier140. The recent implementation of a strategic clean-up plan has led to the disposal of submarines and spent nuclear fuel, although sunken ships excluded from the plan account for ~8,860 TBq of radiation138. These remaining vessels may add to ongoing problems as radionucleotides in sediment mobilize into the greater environment141,142.
Camp Century (~240 km from Thule, Greenland) was a nuclear-powered Arctic research centre carved into the ice cap >9 m below the ice surface in 1959 by the US Army Corps of Engineers24. The research and laboratory facilities were powered by a portable nuclear reactor (Alco PM-2A) and produced considerable nuclear and diesel waste143. When the site was decommissioned in 1967, all wastes were left below the accumulating ice, which is now rapidly receding (~268 tons of ice loss per year)23,24,42. These combined wastes have an estimated bulk radioactivity of ~1.2 × 109 Bq, representing ~9.2 × 103 tons of physical waste, 2.0 × 105 l of diesel fuel and PCBs, and 2.4 × 107 l of sewage41,144. While there still remains a small window of opportunity for removal, ongoing meltwater infiltration could disperse materials widely145 (Fig. 1).
Near Camp Century, the 1968 Thule bomber crash scattered >4.6 × 1012 Bq of uranium and plutonium on the surface of the Greenland ice sheet41. Though it is not entirely clear how far the bomb debris dispersed, bioturbation, sediment leaching and hydrological transport are expected to increase the radioactivity’s range144,145.
Taken together, nuclear contamination in the Arctic may be considerable and mobile. Research from the 1990s into the transport and uptake of 137Cs suggested that harmful levels of radioactivity may be present until the year 2500 (ref. 85), but critical analysis has not incorporated recent changes from climate warming.
Interactions between emerging hazards in thawing permafrost
Microorganisms and chemicals released from thawing permafrost may interact, with the potential for partial risk mitigation through biodegradation146,147. Methuselah microorganisms may experience additional protection under contaminated conditions due to their extremophilic adaptations, as severe, limiting conditions are not new for these species. For example, in Arctic soils contaminated by oil, researchers discovered the new species Flavobacterium petrolei sp., which is both cold-adapted and able to biodegrade oil148. F. petrolei is notable for its ability to uptake almost 60% of the oil in its immediate environment, suggesting that it could have a potential remedial use in Arctic oil spills147. Moreover, recovered Acidobacteria and Sphingomonadales species degrade dioxins and furans, making them dominant in contaminated conditions149. Other new species isolated from soil, permafrost, streams and wetlands may stem from existing genera, including Hymenobacter. Hymenobacter psychrophilus sp. nov. is one of the more recently discovered members of the genus, the psychrophilic properties and lipid membrane of which increase its survival in both harsh and polluted Arctic soil54,150. It is unclear how the interaction between permafrost microorganisms and anthropogenic chemicals will progress, and the consequences of these new interactions across the Arctic remain unknown.
Risks and impacts arising through transport
Researchers have only begun to understand the impacts of biogeochemical hazards remobilized from thawing permafrost. What is clear is that established transport pathways could rapidly disperse hazardous compounds through atmospheric, hydrologic and terrestrial systems after emergence151,152,153. When materials move through adjacent environments, they are subject to biotic and abiotic transformation, creating secondary and tertiary impacts throughout the Arctic system52,153,154 (Fig. 1). Permafrost carbon may further serve as a nutrient source and vector, increasing the range of pollutants and microorganisms as thaw increases7,53. As the cryosphere collapses under climate change, higher temperatures alter dispersion pathways, heighten transport, accelerate chemical degradation and increase bioaccumulation of hazardous materials34,155,156. As such, international efforts to reduce the release of anthropogenic chemicals into the environment must account for secondary remobilization from degrading systems116,157,158.
Quantifying the risks to rapidly changing Arctic ecosystems from entrained permafrost biochemical compounds is an ongoing challenge9. The dominant Arctic transport mechanisms of atmospheric remobilization159,160, hydrological transport83,161,162, direct transport (through human or animal migration)110,163 and trophic-level flow all need to be assessed for dispersion potential86,88,111. The transport rates and efficiency differ tremendously between these mechanisms, releasing sequestered compounds into recently thawed ecosystems160,164,165.
Hydrologic and atmospheric transport
Permafrost thaw opens new hydrologic transport pathways, increasing connectivity and providing more efficient delivery for chemicals and microorganisms49 (Fig. 1). Freshwater lakes and ponds currently cover ~16% of the Arctic landscape166, but thaw and glacier melt further activates groundwater pathways, linking lakes, rivers and the coastal ocean167,168. Carbon9, mercury105, microorganisms169, legacy pollutants39,77 and any soluble materials can then flow between ecosystem compartments, increasing potential interaction. Microbial genes also move in meltwater between ecosystems. For example, a recent study of pelagic Chloroflexi (a diverse phylum of aerobic microorganisms) within the Arctic Ocean identified a lateral transfer of genes that were previously found only in terrestrial genomes169. These terrestrial genes markedly increase aquatic Chloroflexi’s efficiency in metabolizing terrestrial carbon, a new adaptation for the Arctic Ocean species169.
As the Arctic warms and permafrost thaws, atmospheric dynamics will continue to fluctuate, transferring volatile chemicals and particulated microorganisms into near-surface air155,170,171,172. It is unclear whether this flux will increase the number of ice nucleating particles from the soil, changing the density, range and precipitation from Arctic clouds172,173 (Fig. 1). Changes in albedo and circulation patterns will continue to drive fluctuations in Arctic atmospheric conditions, but lesser-understood drivers such as ice nucleating particles may have a growing role.
Human transport
The probability of direct anthropogenic transport increases with increased tourism, commerce and resource extraction in the warming Arctic. Reductions in sea ice enable cruise ships and commercial operations to bring more visitors to the north174. Over 1,000 settlements—including those focused on resource extraction, military and scientific endeavours—have been erected on permafrost in the last 70 years175. This growing non-resident population creates more opportunities for both intentional and accidental transport of Methuselah microorganisms and viruses throughout the Arctic and to lower latitudes176.
The scientific extraction and regeneration of ancient DNA, pathogens and microorganisms from permafrost further increases opportunities for accidental contact or release49,62,65. Although the immediate risk of release is low, a growing human population moving minerals, fossil fuels and biota out of the Arctic could increase the risks for both the local population and more heavily populated regions to the south.
Risks to human populations
As of 2017, approximately 3 million people in the high northern latitudes lived on permafrost, where degradation imperils local infrastructure and increases the risk of exposure to emergent constituents175. As the new Arctic evolves, increasing pollution, shipping, natural resource exploitation, tourism and population growth leave resident communities vulnerable to even small ecosystem disruptions125,177,178.
Antibiotic resistance
Deep permafrost (>3 m) is one of the few environments on Earth that has not been exposed to modern antibiotics, yet antibiotic-resistant bacteria are prevalent in these soil horizons179,180,181. In Siberia, over 100 diverse microorganisms, including Firmicutes, Arthrobacter and Bacteroidetes, were determined to be resistant to aminoglycoside, tetracycline and chloramphenicol antibiotics181 (Table 1). These antibiotic-resistant bacteria were identified in permafrost dated 15–290 ka, with species even more abundant in active layers in older, deeper permafrost181,182. Subsequently, concerns have been raised about the potential for the exchange of genetic material between antibiotic-resistant permafrost microorganisms and contemporary bacteria to create new antibiotic-resistant strains183. To date, bacteria resistant to chloramphenicol, streptomycin, kanamycin, gentamicin, tetracycline, spectinomycin and neomycin have been recovered from permafrost soils18,184.
Pathogen emergence
Changing Arctic ecology combined with permafrost thaw raises the prospect of disease emergence. Stable conditions in permafrost have preserved fragmented genomic material from smallpox and influenza viruses, pre-dating the first known human smallpox case by over 1 kyr (ref. 61). While these viruses may not be preserved in infectious forms, recovery and reconstruction of viral genomes is ongoing185,186. The release of intact viral pathogens from permafrost are limited by host community density and longevity, preventing long-term persistence for many virus species. However, any potential research reconstructing ancient viruses must be weighed against the risks of release or mutation185,187. As the pathogenic risks from all Methuselah microorganisms and viruses are not fully characterized, laboratory security is critical.
Although the direct infection of humans from permafrost pathogens is currently improbable, questions abounded after a 2016 outbreak of anthrax in Russia188,189. The hardy endospores of anthrax (Bacillus anthracis) endure entombment within permafrost for decades to centuries, raising concerns about re-emergence. While the 2016 outbreak was most likely a result of reindeer overpopulation and undervaccination, increasing vector transfer potential is a growing concern20,189,190. Similarly, a new pox virus termed Alaskapox has recently been identified in the Alaskan Arctic, with its origins, rate of spread and risk of illness still poorly quantified191.
Legacy pollution
Chemical and heavy metal wastes left a legacy of health problems for northern populations, and these risks are exacerbated by the impacts of permafrost degradation27,79,119,125,169. The accumulation of hazardous chemicals in the top layers of ice and permafrost can rapidly reach harmful levels if mobilized101. The bioaccumulation of POPs in salmon and large marine mammals poses a critical problem for subsistence communities across the Arctic125. Organochlorine concentrations in Arctic fish already show non-geographically constrained bioaccumulation trends, transporting DDT, HCH and PCB throughout the local environment192,193. One study indicated that the probability of biomagnification was nearly 100% for slowly metabolized compounds (such as PCB and DDT) in freshwater systems, substantially elevating the risk to human consumers101. Lipophilic chemicals are difficult to trace in humans, so the full consequences of POP re-emergence in the Arctic may not be understood for a generation194,195,196. This is also true for other waste stored in the Arctic. For example, the health risks from the uptake of nuclear materials are substantial and range from radiation sickness and burns to lung scarring and cancer197,198.
The worst effects of known toxins on human populations in the Arctic may be yet to come. The increasing load of chemical mixtures158 from permafrost can bioaccumulate across generations, weakening the immune system and increasing vulnerability to new pathogens37,38,88,111,119,125.
Future research priorities
For most of human history, the Arctic has been dominated by the year-round persistence of snow, ice and permafrost. Inaccessible for the majority of the Earth’s population, it was considered to be ideal by far-away decision-makers for the ‘permanent’ disposal of chemicals, biological hazards and even military assets of lower-latitude regions. Thus, the risks from emergent microorganisms and chemicals sequestered in permafrost are poorly understood and largely unquantified. Under climate change, a new Arctic devoid of a perpetual cryosphere has the potential to distribute previously sequestered compounds at large scales (Fig. 1). These shocks present an additional challenge to fragile Arctic stability, and establishing methodologies for locating and assessing emerging risks is critical. Synthesizing the current state of knowledge on the emergent biogeochemical risks from thawing permafrost has revealed three critical research priorities—improving permafrost models, quantifying the abundances and spatial distributions of permafrost pollutants and microbial communities, and developing rapid risk assessment tools tailored for the Arctic.
First, permafrost thaw mechanisms are poorly understood. Knowledge of abrupt thaw is evolving rapidly9,199,200, yet questions remain about where permafrost is most vulnerable201, how biophysical mechanisms drive thaw202,203 and how fast thaw (or abrupt thaw) will occur12,13. In particular, studies that quantify the rates of permafrost degradation from fire disturbance and thermokarst are urgently needed. Accurate models of the dynamics driving thaw are required to forecast the evolution of post-permafrost ecosystems. Without a clearer understanding of permafrost structure and underlying thaw processes, forecasting risk from emerging permafrost constituents will be nearly impossible.
Transport and permafrost thaw models should be used in tandem to characterize the transition from frozen to thawed permafrost and quantify potential risks from emergent biogeochemical hazards. This is particularly urgent for nuclear waste and heavy metals, which are very likely to have immediate health impacts shortly after release. Transport models spanning scales are essential to quantify the potential dispersal of permafrost components beyond the Arctic39,204.
Second, the heterogeneity of much of the Arctic has contributed to major uncertainties concerning the location, function and composition of permafrost microorganism and virus communities49,70. Owing to this vastness and the lack of access to deep permafrost, the diversity of microbial life has yet to be systematically quantified17,49,160. To forecast hazard emergence and routes of exposure, systematic studies of the biogeochemical constituents sequestered in permafrost are required.
In particular, it is unclear whether Methuselah microorganisms will be able to thrive in or colonize modern conditions and adapt to climate change. To answer these questions and understand their functions and potential threats to contemporary ecosystems, emergent microorganisms must be characterized using metagenomic sequencing and taxonomic analyses.
Similarly, the presence of high-risk anthropogenic materials across the Arctic has yet to be systematically catalogued, minimizing the opportunity for forecasting ecosystem change or potential health impacts as long-sequestered hazards emerge. As the Arctic warms, it is unclear whether chemical degradation rates will change or whether environmental transport will continue unabated. Additional questions about the emission rate and range of point source and non-point source pollutants must be answered.
Third, the Arctic is home to millions of people, many of whom engage in subsistence practices and live in settlements that have been populated continuously for millennia. Arctic peoples are immediately impacted by landscape changes, industrial resource extraction and, now, potential emergent health threats. The health and safety of the resident populace and connected populations at lower latitudes are first-order priorities. There is an urgent need for rapid risk assessment tools tailored to the Arctic. Methodologies to swiftly assess health risks from emergent pollution125 and to forecast interactions between emergent microorganisms and humans are critical. This may require a combination of field, laboratory and modelling tools, integrating knowledge from disciplines as diverse as microbiology, environmental toxicology and Earth systems modelling. It also entails proper valuation of Arctic lifestyles, cultures and natural resources, indexing the rapid changes that Arctic warming will bring to local regions and the entire Earth system. Collaboration between scientists in lower latitudes and the Arctic must integrate intergenerational knowledge and guardianship. The long-ranging and first-hand knowledge of Arctic residents is an underutilized resource that is invaluable to future research. Thus, future research endeavours must incorporate the input and knowledge of all regional groups affected by Arctic changes.
The Arctic has often been considered to be one of the last remaining pristine environments, far from the impacts of global industrialization and commerce. However, geographical asymmetries between anthropogenic greenhouse gas emissions and their projected warming impacts reveal steep inequalities, with warming especially amplified above 60° N. The resulting collapse of the Arctic cryosphere and the subsequent potential for exposure to emergent biogeochemical hazards highlights the fact that no element of the Earth system remains isolated. Climate-driven instability will continue to affect the Arctic Ocean, atmosphere and terrestrial systems. Clearly, the primary strategy for mitigating risk from biogeochemical hazards must be to take action to slow permafrost thaw.
References
Mcguire, A. D. et al. Sensitivity of the carbon cycle in the Arctic to climate change. Ecol. Monogr. 79, 523–555 (2009). Details Arctic changes under RCP scenarios using a multi-model approach forecasting vegetation offsets of some carbon emissions.
Brandt, J. P. The extent of the North American boreal zone. Environ. Rev. 17, 101–161 (2009).
Chadburn, S. et al. Carbon stocks and fluxes in the high latitudes: using site-level data to evaluate Earth system models. Biogeosciences 14, 5143–5169 (2017).
Karjalainen, O. et al. Data descriptor: circumpolar permafrost maps and geohazard indices for near-future infrastructure risk assessments. Sci. Data 6, 190037 (2019).
Hjort, J. et al. Degrading permafrost puts Arctic infrastructure at risk by mid-century. Nat. Commun. 9, 5147 (2018).
Abramov, A., Vishnivetskaya, T. & Rivkina, E. Are permafrost microorganisms as old as permafrost? FEMS Microbiol. Ecol. 97, fiaa260 (2021).
Ricketts, M. P. et al. The effects of warming and soil chemistry on bacterial community structure in Arctic tundra soils. Soil Biol. Biochem. 148, 107882 (2020).
Hultman, J. et al. Multi-omics of permafrost, active layer and thermokarst bog soil microbiomes. Nature 521, 208–212 (2015).
Turetsky, M. R. et al. Carbon release through abrupt permafrost thaw. Nat. Geosci. 13, 138–143 (2020). Seminal paper that identifies abrupt permafrost thaw as an important mechanism in rapid Arctic change.
Nikrad, M. P., Kerkhof, L. J. & Aggblom, M. M. The subzero microbiome: microbial activity in frozen and thawing soils. FEMS Microbiol. Ecol. 92, fiw081 (2016).
Turetsky, M. R. et al. Permafrost collapse is accelerating carbon release. Nature 569, 32–24 (2019).
Wild, B. et al. Rivers across the Siberian Arctic unearth the patterns of carbon release from thawing permafrost. Proc. Natl Acad. Sci. USA 116, 10280–10285 (2019).
Anthony, K. W. et al. 21st-century modeled permafrost carbon emissions accelerated by abrupt thaw beneath lakes. Nat. Commun. 9, 3262 (2018).
Schaefer, K., Lantuit, H., Romanovsky, V. E., Schuur, E. A. G. & Witt, R. The impact of the permafrost carbon feedback on global climate. Environ. Res. Lett. 9, 085003 (2014).
Hong, E., Perkins, R. & Trainor, S. Thaw settlement hazard of permafrost related to climate warming in Alaska. Arctic 67, 93–103 (2014).
Trofimenko, Y. V., Evgenev, G. I. & Shashina, E. V. Functional loss risks of highways in permafrost areas due to climate change. Procedia Eng. 189, 258–264 (2017).
Wurzbacher, C., Nilsson, R. H., Rautio, M. & Peura, S. Poorly known microbial taxa dominate the microbiome of permafrost thaw ponds. ISME J. 11, 1938–1941 (2017).
Emerson, J. B. et al. Host-linked soil viral ecology along a permafrost thaw gradient. Nat. Microbiol. 3, 870–880 (2018).
Gross, M. Permafrost thaw releases problems. Curr. Biol. 29, R39–R41 (2019).
Walsh, M. G., De Smalen, A. W. & Mor, S. M. Climatic influence on anthrax suitability in warming northern latitudes. Sci. Rep. 8, 9269 (2018).
Zolkos, S. et al. Mercury export from Arctic great rivers. Environ. Sci. Technol. 54, 4140–4148 (2020).
Ewing, S. A. et al. Uranium isotopes and dissolved organic carbon in loess permafrost: modeling the age of ancient ice. Geochim. Cosmochim. Acta 152, 143–165 (2015).
Eriksson, M. On Weapons Plutonium in the Arctic Environment (Thule, Greenland). PhD thesis, Lund Univ. (2002).
Colgan, W. et al. The abandoned ice sheet base at Camp Century, Greenland, in a warming climate. Geophys. Res. Lett. 43, 8091–8096 (2016).
Anisimov, O., Kokorev, V. & Zhiltcova, Y. Arctic ecosystems and their services under changing climate: predictive-modeling assessment. Geogr. Rev. 107, 108–124 (2017).
Pelletier, M., Allard, M. & Levesque, E. Ecosystem changes across a gradient of permafrost degradation in subarctic Québec (Tasiapik Valley, Nunavik, Canada). Arct. Sci. 5, 1–26 (2019).
Perryman, C. R. et al. Heavy metals in the Arctic: distribution and enrichment of five metals in Alaskan soils. PLoS ONE 15, e0233297 (2020).
Gilichinsky, D. A. & Rivkina, E. M. Permafrost microbiology. Encycl. Earth Sci. Ser. 6, 726–732 (1995). Details the (at the time) emergent field of permafrost microbiology, extremophilic species and future prospects for emergent microbes.
Steven, B., Léveillé, R., Pollard, W. H. & Whyte, L. G. Microbial ecology and biodiversity in permafrost. Extremophiles 10, 259–267 (2006).
Voigt, C. et al. Warming of subarctic tundra increases emissions of all three important greenhouse gases—carbon dioxide, methane, and nitrous oxide. Glob. Change Biol. 23, 3121–3138 (2017).
Mackelprang, R., Saleska, S. R., Jacobsen, C. S., Jansson, J. K. & Taş, N. Permafrost meta-omics and climate change. Annu. Rev. Earth Planet. Sci. 44, 439–462 (2016).
Graham, D. E. et al. Microbes in thawing permafrost: the unknown variable in the climate change equation. ISME J. 6, 709–712 (2012).
Abbott, B. W. et al. Biomass offsets little or none of permafrost carbon release from soils, streams, and wildfire: an expert assessment. Environ. Res. Lett. 11, 034014 (2016).
Ren, J. et al. Biomagnification of persistent organic pollutants along a high-altitude aquatic food chain in the Tibetan Plateau: processes and mechanisms. Environ. Pollut. https://doi.org/10.1016/j.envpol.2016.10.019 (2016).
Dean, J. F. et al. Abundant pre-industrial carbon detected in Canadian Arctic headwaters: implications for the permafrost carbon feedback. Environ. Res. Lett. 13, 34024 (2018).
Jeffries, M. O., Overland, J. E. & Perovich, D. K. The Arctic shifts to a new normal. Phys. Today 66, 35–40 (2013).
El-Sayed, A. & Kamel, M. Future threat from the past. Environ. Sci. Pollut. Res. https://doi.org/10.1007/s11356-020-11234-9 (2020).
Houwenhuyse, S., Macke, E., Reyserhove, L., Bulteel, L. & Decaestecker, E. Back to the future in a petri dish: origin and impact of resurrected microbes in natural populations. Evol. Appl. 11, 29–41 (2018).
Miner, K. R. et al. Organochlorine pollutants within a polythermal glacier in the Interior Eastern Alaska Range. Water 10, 1157 (2018).
Li, F. et al. Arctic sea-ice loss intensifies aerosol transport to the Tibetan Plateau. Nat. Clim. Change 10, 1037–1044 (2020).
Eriksson, M., Lindahl, P., Roos, P., Dahlgaard, H. & Holm, E. U, Pu, and Am nuclear signatures of the thule hydrogen bomb debris. Environ. Sci. Technol. 42, 4717–4722 (2008).
Lind, O. C. et al. Characterization of U/Pu particles originating from the nuclear weapon accidents at Palomares, Spain, 1966 and Thule, Greenland, 1968. Sci. Total Environ. 376, 294–305 (2007).
Slemmons, K. E. H., Saros, J. E. & Simon, K. The influence of glacial meltwater on alpine aquatic ecosystems: a review. Environ. Sci. Process. Impacts 15, 1794 (2013).
Bidleman, T. F., Jantunen, L. M., Kurt-Karakus, P. B. & Wong, F. Chiral persistent organic pollutants as tracers of atmospheric sources and fate: review and prospects for investigating climate change influences. Atmos. Pollut. Res. 3, 371–382 (2012).
Chen, M. et al. Release of perfluoroalkyl substances from melting glacier of the Tibetan Plateau: insights into the impact of global warming on the cycling of emerging pollutants. J. Geophys. Res. Atmos. 124, 7442–7456 (2019).
Goodman, S. & Kertysova, K. The Nuclearisation of the Russian Arctic: New Reactors, New Risks (European Leadership Network, 2020); https://www.europeanleadershipnetwork.org/wp-content/uploads/2020/06/The-nuclearisation-of-the-Russian-Arctic-2.pdf
Byrne, S. et al. Persistent organochlorine pesticide exposure related to a formerly used defense site on St. Lawrence Island, Alaska: data from sentinel fish and human sera. Toxicol. Environ. Health 78, 37–54 (2015).
The National Academies of Sciences Understanding and Responding to Global Health Security Risks from Microbial Threats in the Arctic (National Academies Press, 2020); https://doi.org/10.17226/25887
Edwards, A. et al. Microbial genomics amidst the Arctic crisis. Microb. Genom. 6, e000375 (2020). Catalogues known genomic diversity, evolution dynamics and environment of Arctic microbes.
Botnen, S. S., Mundra, S., Kauserud, H. & Eidesen, P. B. Glacier retreat in the high Arctic: opportunity or threat for ectomycorrhizal diversity? FEMS Microbiol. Ecol. https://doi.org/10.1093/femsec/fiaa171 (2020).
Schuur, E. A. G. et al. Climate change and the permafrost carbon feedback. Nature 520, 171–179 (2015).
Ward, C. P., Nalven, S. G., Crump, B. C., Kling, G. W. & Cory, R. M. Photochemical alteration of organic carbon draining permafrost soils shifts microbial metabolic pathways and stimulates respiration. Nat. Commun. 8, 772 (2017).
Taş, N. et al. Landscape topography structures the soil microbiome in Arctic polygonal tundra. Nat. Commun. 9, 777 (2018).
Price, P. B. Microbial genesis, life and death in glacial ice. Can. J. Microbiol. 55, 1–11 (2009).
Niederberger, T. D. et al. Microbial characterization of a subzero, hypersaline methane seep in the Canadian high Arctic. ISME J. 4, 1326–1339 (2010).
Malavin, S., Shmakova, L., Claverie, J. M. & Rivkina, E. Frozen Zoo: a collection of permafrost samples containing viable protists and their viruses. Biodivers. Data J. 8, e51586 (2020).
Gilichinsky, D., Rivkina, E., Shcherbakova, V., Laurinavichuis, K. & Tiedje, J. Supercooled water brines within permafrost—an unknown ecological niche for microorganisms: a model for astrobiology. Astrobiology 3, 331–341 (2003).
Legendre, M. et al. Thirty-thousand-year-old distant relative of giant icosahedral DNA viruses with a pandoravirus morphology. Proc. Natl Acad. Sci. USA 111, 4274–4279 (2014).
Legendre, M. et al. In-depth study of Mollivirus sibericum, a new 30,000-yold giant virus infecting Acanthamoeba. Proc. Natl Acad. Sci. USA 112, E5327–E5335 (2015).
MacKelprang, R. et al. Metagenomic analysis of a permafrost microbial community reveals a rapid response to thaw. Nature 480, 368–371 (2011). Uses deep metagenomic sequencing to map the impacts of thaw on the Arctic microbial community structure and genomics.
Mühlemann, B. et al. Diverse variola virus (smallpox) strains were widespread in northern Europe in the Viking age. Science 369, eaaw8977 (2020).
Ng, T. F. F. et al. Preservation of viral genomes in 700-y-old caribou feces from a subarctic ice patch. Proc. Natl Acad. Sci. USA 111, 16842–16847 (2014).
Shmakova, L. et al. A living bdelloid rotifer from 24,000-year-old Arctic permafrost. Curr. Biol. 31, PR712–R713 (2021).
Siliakus, M. F., van der Oost, J. & Kengen, S. W. M. Adaptations of archaeal and bacterial membranes to variations in temperature, pH and pressure. Extremophiles 21, 651–670 (2017).
Edwards, A. Coming in from the cold: potential microbial threats from the terrestrial cryosphere. Front. Earth Sci. 3, 12 (2015).
Mackelprang, R. et al. Microbial survival strategies in ancient permafrost: insights from metagenomics. ISME J. 11, 2305–2318 (2017).
Bale, N. J. et al. Fatty acid and hopanoid adaption to cold in the methanotroph Methylovulum psychrotolerans. Front. Microbiol. 10, 589 (2019).
Johnson, S. S. et al. Ancient bacteria show evidence of DNA repair. Proc. Natl Acad. Sci. USA 104, 14401–14405 (2007).
Ji, M. et al. Atmospheric trace gases support primary production in Antarctic desert surface soil. Nature 552, 400–403 (2017).
Burkert, A., Douglas, T. A., Waldrop, M. P. & Mackelprang, R. Changes in the active, dead, and dormant microbial community structure across a Pleistocene permafrost chronosequence. Appl. Environ. Microbiol. 85, e02646–18 (2019).
Colangelo-Lillis, J., Eicken, H., Carpenter, S. D. & Deming, J. W. Evidence for marine origin and microbial-viral habitability of subzero hypersaline aqueous inclusions within permafrost near Barrow, Alaska. FEMS Microbiol. Ecol. 92, fiw053 (2016).
Boetius, A., Anesio, A. M., Deming, J. W., Mikucki, J. A. & Rapp, J. Z. Microbial ecology of the cryosphere: sea ice and glacial habitats. Nat. Rev. Microbiol. 13, 677–690 (2015).
Zhong, Z.-P. et al. Viral ecogenomics of Arctic cryopeg brine and sea ice. mSystems https://doi.org/10.1128/mSystems.00246-20 (2020).
Bay, S. K. et al. Trace gas oxidizers are widespread and active members of soil microbial communities. Nat. Microbiol. 6, 246–256 (2021).
Aslam, S. N., Huber, C., Asimakopoulos, A. G., Steinnes, E. & Mikkelsen, Ø. Trace elements and polychlorinated biphenyls (PCBs) in terrestrial compartments of Svalbard, Norwegian Arctic. Sci. Total Environ. 685, 1127–1138 (2019).
Winiger, P. et al. Source apportionment of circum-Arctic atmospheric black carbon from isotopes and modeling. Sci. Adv. 5, eaau8052 (2019).
Villa, S., Migliorati, S., Monti, G. S., Holoubek, I. & Vighi, M. Risk of POP mixtures on the Arctic food chain. Environ. Toxicol. Chem. 36, 1181–1192 (2017).
Ma, J., Hung, H., Tian, C. & Kallenborn, R. Revolatilization of persistent organic pollutants in the Arctic induced by climate change. Nat. Clim. Change 1, 255–260 (2011).
Ji, X., Abakumov, E. & Polyakov, V. Assessments of pollution status and human health risk of heavy metals in permafrost-affected soils and lichens: a case-study in Yamal Peninsula, Russia Arctic. Hum. Ecol. Risk Assess. 25, 2142–2159 (2019).
Mu, C. et al. Carbon and mercury export from the Arctic rivers and response to permafrost degradation. Water Res. 161, 54–60 (2019).
Brown, T. M., Macdonald, R. W., Muir, D. C. G. & Letcher, R. J. The distribution and trends of persistent organic pollutants and mercury in marine mammals from Canada’s eastern Arctic. Sci. Total Environ. 618, 500–517 (2018).
Ferrario, C., Finizio, A. & Villa, S. Legacy and emerging contaminants in meltwater of three alpine glaciers. Sci. Total Environ. 574, 350–357 (2017).
Miner, K. R., Bogdal, C., Pavlova, P. A., Steinlin, C. & Kreutz, K. J. Quantitative screening level assessment of human risk from PCB in glacial meltwater: Silvretta Glacier, Swiss Alps. Ecotoxicol. Environ. Saf. 166, 251–258 (2018).
Octaviani, M., Stemmler, I., Lammel, G. & Graf, H. F. Atmospheric transport of persistent organic pollutants to and from the Arctic under present-day and future climate. Environ. Sci. Technol. 49, 3593–3602 (2015).
Nielsen, S. P., Iosjpe, M. & Strand, P. Collective doses to man from dumping of radioactive waste in the Arctic seas. Sci. Total Environ. 202, 135–146 (1997).
Eickmeyer, D. C. et al. Interactions of polychlorinated biphenyls and organochlorine pesticides with sedimentary organic matter of retrogressive thaw slump-affected lakes in the tundra uplands adjacent to the Mackenzie Delta, NT, Canada. J. Geophys. Res. G Biogeosci. 121, 411–421 (2016).
St Pierre, K. A. et al. Unprecedented increases in total and methyl mercury concentrations downstream of retrogressive thaw slumps in the western Canadian Arctic. Environ. Sci. Technol. 52, 14099–14109 (2018).
Birnbaum, L. S. When environmental chemicals act like uncontrolled medicine. Trends Endocrinol. Metab. 24, 321–323 (2013).
Potapowicz, J., Szumińska, D., Szopińska, M. & Polkowska, Ż. The influence of global climate change on the environmental fate of anthropogenic pollution released from the permafrost: part I. Case study of Antarctica. Sci. Total Environ. 651, 1534–1548 (2019).
Kim, K.-S. et al. Associations of organochlorine pesticides and polychlorinated biphenyls in visceral vs. subcutaneous adipose tissue with type 2 diabetes and insulin resistance. Chemosphere 94, 151–157 (2014).
Knutsen, H. K. et al. Risk to human health related to the presence of perfluorooctane sulfonic acid and perfluorooctanoic acid in food. EFSA J. 16, e05194 (2018).
Iszatt, N. et al. Prenatal and postnatal exposure to persistent organic pollutants and infant growth: a pooled analysis of seven European birth cohorts. Environ. Health Perspect. 123, 730–736 (2015).
Nadal, M., Marquès, M., Mari, M. & Domingo, J. L. Climate change and environmental concentrations of POPs: a review. Environ. Res. 143, 177–185 (2015).
Toxicological Profile for Lead (Agency for Toxic Substances and Disease Registry, 2020); https://www.atsdr.cdc.gov/toxprofiles/tp13.pdf
Toxicological Profile for Mercury (Agency for Toxic Substances and Disease Registry, 1999); https://www.atsdr.cdc.gov/ToxProfiles/tp46.pdf
Toxicological Profile for Cadmium (Agency for Toxic Substances and Disease Registry, 2012); https://www.atsdr.cdc.gov/toxprofiles/tp5.pdf
Halbach, K., Mikkelsen, Ø., Berg, T. & Steinnes, E. The presence of mercury and other trace metals in surface soils in the Norwegian Arctic. Chemosphere 188, 567–574 (2017).
Miner, K. R. et al. Legacy organochlorine pollutants in glacial watersheds: a review. Environ. Sci. Process. Impacts 19, 1474–1483 (2017).
Jamieson, H. E. The legacy of arsenic contamination from mining and processing refractory gold ore at Giant Mine, Yellowknife, Northwest Territories, Canada. Rev. Mineral. Geochem. 79, 533–551 (2014).
Tolvanen, A. et al. Mining in the Arctic environment—a review from ecological, socioeconomic and legal perspectives. J. Environ. Manag. 233, 832–844 (2019).
Liu, X., Jiang, S., Zhang, P. & Xu, L. Effect of recent climate change on Arctic Pb pollution: a comparative study of historical records in lake and peat sediments. Environ. Pollut. 160, 161–168 (2012).
Antcibor, I. et al. Trace metal distribution in pristine permafrost-affected soils of the Lena River delta and its hinterland, northern Siberia, Russia. Biogeosciences 11, 1–15 (2014).
Lim, A. G. et al. A revised pan-Arctic permafrost soil Hg pool based on western Siberian peat Hg and carbon observations. Biogeosciences 17, 3083–3097 (2020).
Schuster, P. F. et al. Permafrost stores a globally significant amount of mercury. Geophys. Res. Lett. 45, 1463–1471 (2018).
Schaefer, K. et al. Potential impacts of mercury released from thawing permafrost. Nat. Commun. 11, 4650 (2020). Estimates future releases of mercury from the permafrost from present to 2300, under RCP scenarios.
Jiskra, M. E., Sonke, J., Agnan, Y., Helmig, D. & Obrist, D. Insights from mercury stable isotopes on terrestrial-atmosphere exchange of Hg(0) in the Arctic tundra. Biogeosciences 16, 4051–4064 (2019).
Blais, J. M. et al. Arctic seabirds transport marine-derived contaminants. Science 309, 445 (2005).
Brimble, S. K. et al. High Arctic ponds receiving biotransported nutrients from a nearby seabird colony are also subject to potentially toxic loadings of arsenic, cadmium, and zinc. Environ. Toxicol. Chem. 28, 2426–2433 (2009).
Michelutti, N. et al. Trophic position influences the efficacy of seabirds as metal biovectors. Proc. Natl Acad. Sci. USA 107, 10543–10548 (2010).
Mallory, M. L. & Braune, B. M. Tracking contaminants in seabirds of Arctic Canada: temporal and spatial insights. Mar. Pollut. Bull. 64, 1475–1484 (2012).
Lehnherr, I. Methylmercury biogeochemistry: a review with special reference to Arctic aquatic ecosystems. Environ. Rev. 22, 229–243 (2014).
Steinlin, C. et al. A temperate alpine glacier as a reservoir of polychlorinated biphenyls: model results of incorporation, transport, and release. Environ. Sci. Technol. 50, 5572–5579 (2016).
Pavlova, P. A., Schmid, P., Zennegg, M., Bogdal, C. & Schwikowski, M. Trace analysis of hydrophobic micropollutants in aqueous samples using capillary traps. Chemosphere 106, 51–56 (2014).
Blais, J. M. et al. Melting glaciers: a major source of persistent organochlorines to subalpine Bow Lake in Banff National Park, Canada. Ambio 30, 410–415 (2001).
Lafrenière, M. J., Blais, J. M., Sharp, M. J. & Schindler, D. W. Organochlorine pesticide and polychlorinated biphenyl concentrations in snow, snowmelt, and runoff at Bow Lake, Alberta. Environ. Sci. Technol. 40, 4909–4915 (2006).
Elliott, J. E. et al. Factors influencing legacy pollutant accumulation in alpine osprey: biology, topography, or melting glaciers? Environ. Sci. Technol. 46, 9681–9689 (2012).
Walters, D. M. et al. Trophic magnification of organic chemicals: a global synthesis. Environ. Sci. Technol. 50, 4650–4658 (2016).
Miner, K. R., Wayant, N. & Ward, H. Preventing chemical release in hurricanes. Science 362, 166 (2018).
Quadroni, S. & Bettinetti, R. Health risk assessment for the consumption of fresh and preserved fish (Alosa agone) from Lago di Como (northern Italy). Environ. Res. 156, 571–578 (2017).
Mangano, M. C., Sarà, G. & Corsolini, S. Monitoring of persistent organic pollutants in the polar regions: knowledge gaps & gluts through evidence mapping. Chemosphere 172, 37–45 (2017).
Villa, S., Vighi, M., Maggi, V., Finizio, A. & Bolzacchini, E. Historical trends of organochlorine pesticides in an alpine glacier. J. Atmos. Chem. 46, 295–311 (2003).
Garmash, O. et al. Deposition history of polychlorinated biphenyls to the Lomonosovfonna glacier, Svalbard: a 209 congener analysis. Environ. Sci. Technol. 47, 12064–12072 (2013).
Bizzotto, E. C., Villa, S., Vaj, C. & Vighi, M. Comparison of glacial and non-glacial-fed streams to evaluate the loading of persistent organic pollutants through seasonal snow/ice melt. Chemosphere 74, 924–930 (2009).
Villa, S., Negrelli, C., Finizio, A., Flora, O. & Vighi, M. Organochlorine compounds in ice melt water from Italian alpine rivers. Ecotoxicol. Environ. Saf. 63, 84–90 (2006).
Miner, K. R. et al. A screening-level approach to quantifying risk from glacial release of organochlorine pollutants in the Alaskan Arctic. J. Expo. Sci. Environ. Epidemiol. 29, 293–301 (2018). Develops the first human risk assessment of glacially stored pollutants in the Arctic.
Czub, G. & McLachlan, M. S. A food chain model to predict the levels of lipophilic organic contaminants in humans. Environ. Toxicol. Chem. 23, 2356–2366 (2004).
Wang, X., Gong, P., Wang, C., Ren, J. & Yao, T. A review of current knowledge and future prospects regarding persistent organic pollutants over the Tibetan Plateau. Sci. Total Environ. 573, 139–154 (2016).
Desforges, J. P. et al. Predicting global killer whale population collapse from PCB pollution. Science 361, 1373–1376 (2018).
Macdonald, R. W. et al. Contaminants in the Canadian Arctic: 5 years of progress in understanding sources, occurrence and pathways. Sci. Total Environ. 254, 93–234 (2000).
Pavlova, P. A. et al. Polychlorinated biphenyls in a temperate alpine glacier: 1. Effect of percolating meltwater on their distribution in glacier ice. Environ. Sci. Technol. 49, 14085–14091 (2015).
Wania, F., Westgate, J. N., Technol, E. S. & Asap, A. On the mechanism of mountain cold-trapping of organic chemicals. Environ. Sci. Technol. 42, 9092–9098 (2008).
Strand, P. & Cooke, A. Environmental Radioactivity in the Arctic (Scientific Committee of the Environmental Radioactivity in the Arctic, 1995).
Wright, S. M. et al. Spatial variation in the vulnerability of Norwegian Arctic counties to radiocaesium deposition. Sci. Total Environ. 202, 173–184 (1997).
Mitchell, P. I., León Vintró, L., Dahlgaard, H., Gascó, C. & Sánchez-Cabeza, J. A. Perturbation in the 240Pu/239Pu global fallout ratio in local sediments following the nuclear accidents at Thule (Greenland) and Palomares (Spain). Sci. Total Environ. 202, 147–153 (1997).
Khalturin, V. I., Rautian, T. G., Richards, P. G. & Leith, W. S. A review of nuclear testing by the Soviet Union at Novaya Zemlya, 1955–1990. Sci. Glob. Secur. 13, 1–42 (2005). Reviews the Novaya Zemlya nuclear testing site history, nuclear releases and posits environmental distribution.
Travkina, A. V. et al. Monitoring the environmental contamination of Kara Sea and shallow bays of Novaya Zemlya. J. Radioanal. Nucl. Chem. 311, 1673–1680 (2017).
Skorve, J. The environment of the nuclear test sites on Novaya Zemlya. Sci. Total Environ. 202, 167–172 (1997).
Sarkisov, A. A. The question of clean-up of radioactive contamination in the Arctic region. Her. Russ. Acad. Sci. 89, 7–22 (2019).
Pogrebov, V. B., Fokin, S. I., Galtsova, V. V. & Ivanov, G. I. Benthic communities as influenced by nuclear testing and radioactive waste disposal off Novaya Zemlya in the Russian Arctic. Mar. Pollut. Bull. 35, 333–339 (1997).
Miroshnikov, A. Y. et al. Radioecological investigations on the northern Novaya Zemlya Archipelago. Oceanology 57, 204–214 (2017).
Salbu, B. et al. Radioactive contamination from dumped nuclear waste in the Kara Sea—results from the joint Russian-Norwegian expeditions in 1992-1994. Sci. Total Environ. 202, 185–198 (1997).
Oughton, D. H., Børretzen, P., Salbu, B. & Tronstad, E. Mobilisation of 137Cs and 90Sr from sediments: potential sources to Arctic waters. Sci. Total Environ. 202, 155–165 (1997).
Faria, S. H., Weikusat, I. & Azuma, N. The microstructure of polar ice. Part I: highlights from ice core research. J. Struct. Geol. 61, 2–20 (2014).
Karlsson, N. B. et al. Ice-penetrating radar survey of the subsurface debris field at Camp Century, Greenland. Cold Reg. Sci. Technol. 165, 102788 (2019). The most recent ice-penetrating radar survey of Camp Century, Greenland, characterizing the location and concentration of wastes.
Vandecrux, B., Colgan, W. T., Solgaard, A., Steffensen, J. P. & Karlsson, N. B. Firn evolution at Camp Century, Greenland: 1966-2100. Front. Earth Sci. 9, 578978 (2021).
Vila, E., Hornero-Méndez, D., Azziz, G., Lareo, C. & Saravia, V. Carotenoids from heterotrophic bacteria isolated from Fildes Peninsula, King George Island, Antarctica. Biotechnol. Rep. 21, e00306 (2019).
Chaudhary, D. K., Kim, D. U., Kim, D. & Kim, J. Flavobacterium petrolei sp. nov., a novel psychrophilic, diesel-degrading bacterium isolated from oil-contaminated Arctic soil. Sci. Rep. 9, 4134 (2019).
de Gouw, J. A. et al. Daily satellite observations of methane from oil and gas production regions in the United States. Sci. Rep. 10, 1379 (2020).
Girardot, F. et al. Bacterial diversity on an abandoned, industrial wasteland contaminated by polychlorinated biphenyls, dioxins, furans and trace metals. Sci. Total Environ. 748, 141242 (2020).
Price, P. B. Microbial life in glacial ice and implications for a cold origin of life. FEMS Microbiol. Ecol. 59, 217–231 (2007).
Schütte, U. M. E. et al. Effect of permafrost thaw on plant and soil fungal community in a boreal forest: does fungal community change mediate plant productivity response? J. Ecol. 107, 1737–1752 (2019).
Jensen, P. E., Hennessy, T. W. & Kallenborn, R. Water, sanitation, pollution, and health in the Arctic. Environ. Sci. Pollut. Res. 25, 32827–32830 (2018).
Ewing, S. A. et al. Long-term anoxia and release of ancient, labile carbon upon thaw of Pleistocene permafrost. Geophys. Res. Lett. 42, 10730–10738 (2015).
Elder, C. D. et al. Seasonal sources of whole-lake CH4 and CO2 emissions from interior Alaskan thermokarst lakes. J. Geophys. Res. Biogeosci. 124, 1209–1229 (2019).
Jansen, E. et al. Past perspectives on the present era of abrupt Arctic climate change. Nat. Clim. Change 10, 714–721 (2020).
Nellier, Y.-M. et al. Mass budget in two high altitude lakes reveals their role as atmospheric PCB sinks. Sci. Total Environ. 511, 203–213 (2015).
Garnett, J. et al. Mechanistic insight into the uptake and fate of persistent organic pollutants in sea ice. Environ. Sci. Technol. 53, 6757–6764 (2019).
Kortenkamp, A. & Faust, M. Regulate to reduce chemical mixture risk. Science 361, 224–226 (2018).
Kirchgeorg, T. et al. Seasonal accumulation of persistent organic pollutants on a high altitude glacier in the eastern Alps. Environ. Pollut. 218, 804–812 (2016).
Weil, T. et al. Legal immigrants: invasion of alien microbial communities during winter occurring desert dust storms. Microbiome 5, 32 (2017).
Li, J. et al. Evidence for persistent organic pollutants released from melting glacier in the central Tibetan Plateau, China. Environ. Pollut. 220, 178–185 (2017).
Walvoord, M. A., Voss, C. I., Ebel, B. A. & Minsley, B. J. Development of perennial thaw zones in boreal hillslopes enhances potential mobilization of permafrost carbon. Environ. Res. Lett. 14, 015003 (2019).
Mogrovejo, D. C. et al. Prevalence of antimicrobial resistance and hemolytic phenotypes in culturable Arctic bacteria. Front. Microbiol. 11, 570 (2020).
Friedman, C. L. & Selin, N. E. Long-range atmospheric transport of polycyclic aromatic hydrocarbons: a global 3-D model analysis including evaluation of Arctic sources. Environ. Sci. Technol. 46, 9501–9510 (2012).
Myers-Smith, I. H. et al. Complexity revealed in the greening of the Arctic. Nat. Clim. Change 10, 106–117 (2020).
Vonk, J. E. et al. Reviews and syntheses: effects of permafrost thaw on Arctic aquatic ecosystems. Biogeosciences 12, 7129–7167 (2015).
MacInnis, J. J. et al. Fate and transport of perfluoroalkyl substances from snowpacks into a lake in the high Arctic of Canada. Environ. Sci. Technol. 53, 10753–10762 (2019).
Yeung, L. W. Y. et al. Vertical profiles, sources, and transport of PFASs in the Arctic Ocean. Environ. Sci. Technol. 51, 6735–6744 (2017).
Colatriano, D. et al. Genomic evidence for the degradation of terrestrial organic matter by pelagic Arctic Ocean Chloroflexi bacteria. Commun. Biol. 1, 90 (2018).
Commane, R. et al. Carbon dioxide sources from Alaska driven by increasing early winter respiration from Arctic tundra. Proc. Natl Acad. Sci. USA 114, 5361–5366 (2017).
Hartmann, M. et al. Variation of ice nucleating particles in the European Arctic over the last centuries. Geophys. Res. Lett. https://doi.org/10.1029/2019GL082311 (2019).
Murray, B. J., Carslaw, K. S. & Field, P. R. Opinion: cloud-phase climate feedback and the importance of ice-nucleating particles. Atmos. Chem. Phys. 21, 665–679 (2021).
Joyce, R. E. et al. Biological ice-nucleating particles deposited year-round in subtropical precipitation. Appl. Environ. Microbiol. 85, e01567-19 (2019).
Yumashev, D., van Hussen, K., Gille, J. & Whiteman, G. Towards a balanced view of Arctic shipping: estimating economic impacts of emissions from increased traffic on the Northern Sea Route. Clim. Change 143, 143–155 (2017).
Ramage, J. et al. Population living on permafrost in the Arctic. Popul. Environ. https://doi.org/10.1007/s11111-020-00370-6 (2021).
Bartsch, A., Pointner, G., Ingeman-Nielsen, T. & Lu, W. Towards circumpolar mapping of Arctic settlements and infrastructure based on Sentinel-1 and Sentinel-2. Remote Sens. 12, 2368 (2020).
Dewailly, E. Canadian Inuit and the Arctic dilemma. Oceanography 19, 88–89 (2006).
Plaza, C. et al. Direct observation of permafrost degradation and rapid soil carbon loss in tundra. Nat. Geosci. 12, 627–631 (2019).
Kashuba, E. et al. Ancient permafrost staphylococci carry antibiotic resistance genes. Microb. Ecol. Health Dis. https://doi.org/10.1080/16512235.2017.1345574 (2017).
Dcosta, V. M. et al. Antibiotic resistance is ancient. Nature 477, 457–461 (2011).
Perron, G. G. et al. Functional characterization of bacteria isolated from ancient Arctic soil exposes diverse resistance mechanisms to modern antibiotics. PLoS ONE 10, e0069533 (2015).
Gilichinsky, D. et al. in Psychrophiles: From Biodiversity to Biotechnology (eds Margesin, R. et al.) 83–102 (Springer-Verlag, 2008).
Forsberg, K. J. et al. The shared antibiotic resistome of soil bacteria and human pathogens. Science 337, 1107–1111 (2012).
Woodcroft, B. J. et al. Genome-centric view of carbon processing in thawing permafrost. Nature 560, 49–54 (2018).
Taubenberger, J. K. et al. Reconstruction of the 1918 influenza virus: unexpected rewards from the past. mBio 3, e00201–12 (2012).
Jordan, D., Tumpey, T. & Jester, B. The Deadliest Flu: The Complete Story of the Discovery and Reconstruction of the 1918 Pandemic Virus (US Center for Disease Control, 2019).
Tumpey, T. M. et al. Characterization of the reconstructed 1918 Spanish influenza pandemic virus. Science 310, 77–80 (2005).
Revich, B., Tokarevich, N. & Parkinson, A. J. Climate change and zoonotic infections in the Russian Arctic. Int. J. Circumpolar Health 71, 18792 (2012).
Waits, A., Emelyanova, A., Oksanen, A., Abass, K. & Rautio, A. Human infectious diseases and the changing climate in the Arctic. Environ. Int. 121, 703–713 (2018).
Hueffer, K., Drown, D., Romanovsky, V. & Hennessy, T. Factors contributing to anthrax outbreaks in the circumpolar north. Ecohealth 17, 174–180 (2020).
Springer, Y. P. et al. Novel Orthopoxvirus infection in an Alaska resident. Clin. Infect. Dis. 64, 1737–1741 (2017).
Mackay, D. Multimedia Environmental Models (CRC Press, 2001).
Mackay, D., Celsie, A. K. D., Powell, D. E. & Parnis, J. M. Bioconcentration, bioaccumulation, biomagnification and trophic magnification: a modelling perspective. Environ. Sci. Process. Impacts 20, 72–85 (2018).
Vizcaino, E., Grimalt, J. O., Fernandez-Somoano, A. & Tardon, A. Transport of persistent organic pollutants across the human placenta. Environ. Int. 65, 107–115 (2014).
Costa, O. et al. First-trimester maternal concentrations of polyfluoroalkyl substances and fetal growth throughout pregnancy. Environ. Int. https://doi.org/10.1016/j.envint.2019.05.024 (2019).
Adetona, O. et al. Concentrations of select persistent organic pollutants across pregnancy trimesters in maternal and in cord serum in Trujillo, Peru. Chemosphere 91, 1426–1433 (2013).
Toxicological Profile for Plutonium (Agency for Toxic Substances and Disease Registry, 2010); https://www.atsdr.cdc.gov/toxprofiles/tp143.pdf
Toxicological Profile for Cesium (Agency for Toxic Substances and Disease Registry, 2004); https://www.atsdr.cdc.gov/toxprofiles/tp157.pdf
Serikova, S. et al. High carbon emissions from thermokarst lakes of western Siberia. Nat. Commun. 10, 1552 (2019).
Swingedouw, D. et al. Early warning from space for a few key tipping points in physical, biological, and social-ecological systems. Surv. Geophys. https://doi.org/10.1007/s10712-020-09604-6 (2020).
Lewkowicz, A. G. & Way, R. G. Extremes of summer climate trigger thousands of thermokarst landslides in a high Arctic environment. Nat. Commun. 10, 1329 (2019).
Tank, S. E. et al. Landscape matters: predicting the biogeochemical effects of permafrost thaw on aquatic networks with a state factor approach. Permafr. Periglac. Process. https://doi.org/10.1002/ppp.2057 (2020).
Feng, J. et al. Warming-induced permafrost thaw exacerbates tundra soil carbon decomposition mediated by microbial community. Microbiome 8, 3 (2020).
Stein, A. F. et al. NOAA’s HYSPLIT atmospheric transport and dispersion modeling system. Bull. Am. Meteorol. Soc. 96, 2059–2077 (2015).
Donald, D. B. et al. Delayed deposition of organochlorine pesticides at a temperate glacier. Environ. Sci. Technol. 33, 1794–1798 (1999).
Hermanson, M. H. et al. Current-use and legacy pesticide history in the Austfonna ice cap, Svalbard, Norway. Environ. Sci. Technol. 39, 8163–8169 (2005).
Salvadó, J. A., Sobek, A., Carrizo, D. & Gustafsson, Ö. Observation-based assessment of PBDE loads in Arctic ocean waters. Environ. Sci. Technol. 50, 2236–2245 (2016).
Vecchiato, M. et al. The great acceleration of fragrances and PAHs archived in an ice core from Elbrus, Caucasus. Sci. Rep. 10, 10661 (2020).
Miteva, V., Teacher, C., Sowers, T. & Brenchley, J. Comparison of the microbial diversity at different depths of the GISP2 Greenland ice core in relationship to deposition climates. Environ. Microbiol. 11, 640–656 (2009).
Acknowledgements
A portion of this work was carried out at the Jet Propulsion Laboratory, California Institute of Technology, under a contract with the National Aeronautics and Space Administration (80NM0018D0004). This work is a part of both the NASA-ESA Arctic Methane and Permafrost Challenge (AMPAC) and the NASA Arctic-Boreal Vulnerability Experiment (ABoVE). Research on microbial liberation from frozen Arctic environments is supported by UKRI grant NE/S001034/1 to A.E.
Author information
Authors and Affiliations
Contributions
All of the authors contributed to writing and revising this paper.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Peer review information Nature Climate Change thanks Ianina Altshuler, Lauren Thompson and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Miner, K.R., D’Andrilli, J., Mackelprang, R. et al. Emergent biogeochemical risks from Arctic permafrost degradation. Nat. Clim. Chang. 11, 809–819 (2021). https://doi.org/10.1038/s41558-021-01162-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41558-021-01162-y
Further reading
-
Permafrost carbon emissions in a changing Arctic
Nature Reviews Earth & Environment (2022)
-
Carbon Emission Risk and Governance
International Journal of Disaster Risk Science (2022)


