Genome-centric view of carbon processing in thawing permafrost.

As global temperatures rise, large amounts of carbon sequestered in permafrost are becoming available for microbial degradation. Accurate prediction of carbon gas emissions from thawing permafrost is limited by our understanding of these microbial communities. Here we use metagenomic sequencing of 214 samples from a permafrost thaw gradient to recover 1,529 metagenome-assembled genomes, including many from phyla with poor genomic representation. These genomes reflect the diversity of this complex ecosystem, with genus-level representatives for more than sixty per cent of the community. Meta-omic analysis revealed key populations involved in the degradation of organic matter, including bacteria whose genomes encode a previously undescribed fungal pathway for xylose degradation. Microbial and geochemical data highlight lineages that correlate with the production of greenhouse gases and indicate novel syntrophic relationships. Our findings link changing biogeochemistry to specific microbial lineages involved in carbon processing, and provide key information for predicting the effects of climate change on permafrost systems.

Coupling plant litter quantity to a novel metric for litter quality explains C storage changes in a thawing permafrost peatland.

Permafrost thaw is a major potential feedback source to climate change as it can drive the increased release of greenhouse gases carbon dioxide (CO2 ) and methane (CH4 ). This carbon release from the decomposition of thawing soil organic material can be mitigated by increased net primary productivity (NPP) caused by warming, increasing atmospheric CO2 , and plant community transition. However, the net effect on C storage also depends on how these plant community changes alter plant litter quantity, quality, and decomposition rates. Predicting decomposition rates based on litter quality remains challenging, but a promising new way forward is to incorporate measures of the energetic favorability to soil microbes of plant biomass decomposition. We asked how the variation in one such measure, the nominal oxidation state of carbon (NOSC), interacts with changing quantities of plant material inputs to influence the net C balance of a thawing permafrost peatland. We found: (1) Plant productivity (NPP) increased post-thaw, but instead of contributing to increased standing biomass, it increased plant biomass turnover via increased litter inputs to soil; (2) Plant litter thermodynamic favorability (NOSC) and decomposition rate both increased post-thaw, despite limited changes in bulk C:N ratios; (3) these increases caused the higher NPP to cycle more rapidly through both plants and soil, contributing to higher CO2 and CH4  fluxes from decomposition. Thus, the increased C-storage expected from higher productivity was limited and the high global warming potential of CH4 contributed a net positive warming effect. Although post-thaw peatlands are currently C sinks due to high NPP offsetting high CO2 release, this status is very sensitive to the plant community's litter input rate and quality. Integration of novel bioavailability metrics based on litter chemistry, including NOSC, into studies of ecosystem dynamics, is needed to improve the understanding of controls on arctic C stocks under continued ecosystem transition.

Permafrost thaw driven changes in hydrology and vegetation cover increase trace gas emissions and climate forcing in Stordalen Mire from 1970 to 2014.

Permafrost thaw increases active layer thickness, changes landscape hydrology and influences vegetation species composition. These changes alter belowground microbial and geochemical processes, affecting production, consumption and net emission rates of climate forcing trace gases. Net carbon dioxide (CO2) and methane (CH4) fluxes determine the radiative forcing contribution from these climate-sensitive ecosystems. Permafrost peatlands may be a mosaic of dry frozen hummocks, semi-thawed or perched sphagnum dominated areas, wet permafrost-free sedge dominated sites and open water ponds. We revisited estimates of climate forcing made for 1970 and 2000 for Stordalen Mire in northern Sweden and found the trend of increasing forcing continued into 2014. The Mire continued to transition from dry permafrost to sedge and open water areas, increasing by 100% and 35%, respectively, over the 45-year period, causing the net radiative forcing of Stordalen Mire to shift from negative to positive. This trend is driven by transitioning vegetation community composition, improved estimates of annual CO2 and CH4 exchange and a 22% increase in the IPCC's 100-year global warming potential (GWP_100) value for CH4. These results indicate that discontinuous permafrost ecosystems, while still remaining a net overall sink of C, can become a positive feedback to climate change on decadal timescales. This article is part of a discussion meeting issue 'Rising methane: is warming feeding warming? (part 2)'.

Methane dynamics regulated by microbial community response to permafrost thaw.

Permafrost contains about 50% of the global soil carbon. It is thought that the thawing of permafrost can lead to a loss of soil carbon in the form of methane and carbon dioxide emissions. The magnitude of the resulting positive climate feedback of such greenhouse gas emissions is still unknown and may to a large extent depend on the poorly understood role of microbial community composition in regulating the metabolic processes that drive such ecosystem-scale greenhouse gas fluxes. Here we show that changes in vegetation and increasing methane emissions with permafrost thaw are associated with a switch from hydrogenotrophic to partly acetoclastic methanogenesis, resulting in a large shift in the δ(13)C signature (10-15‰) of emitted methane. We used a natural landscape gradient of permafrost thaw in northern Sweden as a model to investigate the role of microbial communities in regulating methane cycling, and to test whether a knowledge of community dynamics could improve predictions of carbon emissions under loss of permafrost. Abundance of the methanogen Candidatus 'Methanoflorens stordalenmirensis' is a key predictor of the shifts in methane isotopes, which in turn predicts the proportions of carbon emitted as methane and as carbon dioxide, an important factor for simulating the climate feedback associated with permafrost thaw in global models. By showing that the abundance of key microbial lineages can be used to predict atmospherically relevant patterns in methane isotopes and the proportion of carbon metabolized to methane during permafrost thaw, we establish a basis for scaling changing microbial communities to ecosystem isotope dynamics. Our findings indicate that microbial ecology may be important in ecosystem-scale responses to global change.

Partitioning of the net CO2 exchange using an automated chamber system reveals plant phenology as key control of production and respiration fluxes in a boreal peatland.

The net ecosystem CO2 exchange (NEE) drives the carbon (C) sink-source strength of northern peatlands. Since NEE represents a balance between various production and respiration fluxes, accurate predictions of its response to global changes require an in depth understanding of these underlying processes. Currently, however, detailed information of the temporal dynamics as well as the separate biotic and abiotic controls of the NEE component fluxes is lacking in peatland ecosystems. In this study, we address this knowledge gap by using an automated chamber system established across natural and trenching/vegetation removal plots to partition NEE into its production (i.e., gross and net primary production; GPP and NPP) and respiration (i.e., ecosystem, heterotrophic and autotrophic respiration; ER, Rh and Ra) fluxes in a boreal peatland in northern Sweden. Our results showed that daily NEE patterns were driven by GPP while variations in ER were governed by Ra rather than Rh. Moreover, we observed pronounced seasonal shifts in the Ra/Rh and above/belowground NPP ratios throughout the main phenological phases. Generalized linear model analysis revealed that the greenness index derived from digital images (as a proxy for plant phenology) was the strongest control of NEE, GPP and NPP while explaining considerable fractions also in the variations of ER and Ra. In addition, our data exposed greater temperature sensitivity of NPP compared to Rh resulting in enhanced C sequestration with increasing temperature. Overall, our study suggests that the temporal patterns in NEE and its component fluxes are tightly coupled to vegetation dynamics in boreal peatlands and thus challenges previous studies that commonly identify abiotic factors as key drivers. These findings further emphasize the need for integrating detailed information on plant phenology into process-based models to improve predictions of global change impacts on the peatland C cycle.

Microbial network, phylogenetic diversity and community membership in the active layer across a permafrost thaw gradient.

Biogenic production and release of methane (CH4 ) from thawing permafrost has the potential to be a strong source of radiative forcing. We investigated changes in the active layer microbial community of three sites representative of distinct permafrost thaw stages at a palsa mire in northern Sweden. The palsa site (intact permafrost and low radiative forcing signature) had a phylogenetically clustered community dominated by Acidobacteria and Proteobacteria. The bog (thawing permafrost and low radiative forcing signature) had lower alpha diversity and midrange phylogenetic clustering, characteristic of ecosystem disturbance affecting habitat filtering. Hydrogenotrophic methanogens and Acidobacteria dominated the bog shifting from palsa-like to fen-like at the waterline. The fen (no underlying permafrost, high radiative forcing signature) had the highest alpha, beta and phylogenetic diversity, was dominated by Proteobacteria and Euryarchaeota and was significantly enriched in methanogens. The Mire microbial network was modular with module cores consisting of clusters of Acidobacteria, Euryarchaeota or Xanthomonodales. Loss of underlying permafrost with associated hydrological shifts correlated to changes in microbial composition, alpha, beta and phylogenetic diversity associated with a higher radiative forcing signature. These results support the complex role of microbial interactions in mediating carbon budget changes and climate feedback in response to climate forcing.

Changes in peat chemistry associated with permafrost thaw increase greenhouse gas production.

Carbon release due to permafrost thaw represents a potentially major positive climate change feedback. The magnitude of carbon loss and the proportion lost as methane (CH4) vs. carbon dioxide (CO2) depend on factors including temperature, mobilization of previously frozen carbon, hydrology, and changes in organic matter chemistry associated with environmental responses to thaw. While the first three of these effects are relatively well understood, the effect of organic matter chemistry remains largely unstudied. To address this gap, we examined the biogeochemistry of peat and dissolved organic matter (DOM) along a ∼40-y permafrost thaw progression from recently- to fully thawed sites in Stordalen Mire (68.35°N, 19.05°E), a thawing peat plateau in northern Sweden. Thaw-induced subsidence and the resulting inundation along this progression led to succession in vegetation types accompanied by an evolution in organic matter chemistry. Peat C/N ratios decreased whereas humification rates increased, and DOM shifted toward lower molecular weight compounds with lower aromaticity, lower organic oxygen content, and more abundant microbially produced compounds. Corresponding changes in decomposition along this gradient included increasing CH4 and CO2 production potentials, higher relative CH4/CO2 ratios, and a shift in CH4 production pathway from CO2 reduction to acetate cleavage. These results imply that subsidence and thermokarst-associated increases in organic matter lability cause shifts in biogeochemical processes toward faster decomposition with an increasing proportion of carbon released as CH4. This impact of permafrost thaw on organic matter chemistry could intensify the predicted climate feedbacks of increasing temperatures, permafrost carbon mobilization, and hydrologic changes.

Methylotrophy in the Mire: direct and indirect routes for methane production in thawing permafrost.

While wetlands are major sources of biogenic methane (CH4), our understanding of resident microbial metabolism is incomplete, which compromises the prediction of CH4 emissions under ongoing climate change. Here, we employed genome-resolved multi-omics to expand our understanding of methanogenesis in the thawing permafrost peatland of Stordalen Mire in Arctic Sweden. In quadrupling the genomic representation of the site's methanogens and examining their encoded metabolism, we revealed that nearly 20% of the metagenome-assembled genomes (MAGs) encoded the potential for methylotrophic methanogenesis. Further, 27% of the transcriptionally active methanogens expressed methylotrophic genes; for Methanosarcinales and Methanobacteriales MAGs, these data indicated the use of methylated oxygen compounds (e.g., methanol), while for Methanomassiliicoccales, they primarily implicated methyl sulfides and methylamines. In addition to methanogenic methylotrophy, >1,700 bacterial MAGs across 19 phyla encoded anaerobic methylotrophic potential, with expression across 12 phyla. Metabolomic analyses revealed the presence of diverse methylated compounds in the Mire, including some known methylotrophic substrates. Active methylotrophy was observed across all stages of a permafrost thaw gradient in Stordalen, with the most frozen non-methanogenic palsa found to host bacterial methylotrophy and the partially thawed bog and fully thawed fen seen to house both methanogenic and bacterial methylotrophic activities. Methanogenesis across increasing permafrost thaw is thus revised from the sole dominance of hydrogenotrophic production and the appearance of acetoclastic at full thaw to consider the co-occurrence of methylotrophy throughout. Collectively, these findings indicate that methanogenic and bacterial methylotrophy may be an important and previously underappreciated component of carbon cycling and emissions in these rapidly changing wetland habitats.IMPORTANCEWetlands are the biggest natural source of atmospheric methane (CH4) emissions, yet we have an incomplete understanding of the suite of microbial metabolism that results in CH4 formation. Specifically, methanogenesis from methylated compounds is excluded from all ecosystem models used to predict wetland contributions to the global CH4 budget. Though recent studies have shown methylotrophic methanogenesis to be active across wetlands, the broad climatic importance of the metabolism remains critically understudied. Further, some methylotrophic bacteria are known to produce methanogenic by-products like acetate, increasing the complexity of the microbial methylotrophic metabolic network. Prior studies of Stordalen Mire have suggested that methylotrophic methanogenesis is irrelevant in situ and have not emphasized the bacterial capacity for metabolism, both of which we countered in this study. The importance of our findings lies in the significant advancement toward unraveling the broader impact of methylotrophs in wetland methanogenesis and, consequently, their contribution to the terrestrial global carbon cycle.

Diverse sediment microbiota shape methane emission temperature sensitivity in Arctic lakes.

Northern post-glacial lakes are significant, increasing sources of atmospheric carbon through ebullition (bubbling) of microbially-produced methane (CH4) from sediments. Ebullitive CH4 flux correlates strongly with temperature, reflecting that solar radiation drives emissions. However, here we show that the slope of the temperature-CH4 flux relationship differs spatially across two post-glacial lakes in Sweden. We compared these CH4 emission patterns with sediment microbial (metagenomic and amplicon), isotopic, and geochemical data. The temperature-associated increase in CH4 emissions was greater in lake middles-where methanogens were more abundant-than edges, and sediment communities were distinct between edges and middles. Microbial abundances, including those of CH4-cycling microorganisms and syntrophs, were predictive of porewater CH4 concentrations. Results suggest that deeper lake regions, which currently emit less CH4 than shallower edges, could add substantially to CH4 emissions in a warmer Arctic and that CH4 emission predictions may be improved by accounting for spatial variations in sediment microbiota.

Bimodal diel pattern in peatland ecosystem respiration rebuts uniform temperature response.

Accurate projections of climate change impacts on the vast carbon stores of northern peatlands require detailed knowledge of ecosystem respiration (ER) and its heterotrophic (Rh) and autotrophic (Ra) components. Currently, however, standard flux measurement techniques, i.e. eddy covariance and manual chambers, generate empirical ER data during only night- or daytime, respectively, which are extrapolated to the daily scale based on the paradigm that assumes a uniform diel temperature response. Here, using continuous autochamber measurements, we demonstrate a distinct bimodal pattern in diel peatland ER which contrasts the unimodal pattern inherent to the classical assumption. This feature results from divergent temperature dependencies of day- and nighttime ER due to varying contributions from Rh and Ra. We further find that disregarding these bimodal dynamics causes significant bias in ER estimates across multiple temporal scales. This calls for improved process-based understanding of ER to advance our ability to simulate peatland carbon cycle-climate feedbacks.

Shipborne eddy covariance observations of methane fluxes constrain Arctic sea emissions.

We demonstrate direct eddy covariance (EC) observations of methane (CH4) fluxes between the sea and atmosphere from an icebreaker in the eastern Arctic Ocean. EC-derived CH4 emissions averaged 4.58, 1.74, and 0.14 mg m-2 day-1 in the Laptev, East Siberian, and Chukchi seas, respectively, corresponding to annual sea-wide fluxes of 0.83, 0.62, and 0.03 Tg year-1. These EC results answer concerns that previous diffusive emission estimates, which excluded bubbling, may underestimate total emissions. We assert that bubbling dominates sea-air CH4 fluxes in only small constrained areas: A ~100-m2 area of the East Siberian Sea showed sea-air CH4 fluxes exceeding 600 mg m-2 day-1; in a similarly sized area of the Laptev Sea, peak CH4 fluxes were ~170 mg m-2 day-1. Calculating additional emissions below the noise level of our EC system suggests total ESAS CH4 emissions of 3.02 Tg year-1, closely matching an earlier diffusive emission estimate of 2.9 Tg year-1.

Methanotrophy across a natural permafrost thaw environment.

The fate of carbon sequestered in permafrost is a key concern for future global warming as this large carbon stock is rapidly becoming a net methane source due to widespread thaw. Methane release from permafrost is moderated by methanotrophs, which oxidise 20-60% of this methane before emission to the atmosphere. Despite the importance of methanotrophs to carbon cycling, these microorganisms are under-characterised and have not been studied across a natural permafrost thaw gradient. Here, we examine methanotroph communities from the active layer of a permafrost thaw gradient in Stordalen Mire (Abisko, Sweden) spanning three years, analysing 188 metagenomes and 24 metatranscriptomes paired with in situ biogeochemical data. Methanotroph community composition and activity varied significantly as thaw progressed from intact permafrost palsa, to partially thawed bog and fully thawed fen. Thirteen methanotroph population genomes were recovered, including two novel genomes belonging to the uncultivated upland soil cluster alpha (USCα) group and a novel potentially methanotrophic Hyphomicrobiaceae. Combined analysis of porewater δ13C-CH4 isotopes and methanotroph abundances showed methane oxidation was greatest below the oxic-anoxic interface in the bog. These results detail the direct effect of thaw on autochthonous methanotroph communities, and their consequent changes in population structure, activity and methane moderation potential.

Host-linked soil viral ecology along a permafrost thaw gradient.

Climate change threatens to release abundant carbon that is sequestered at high latitudes, but the constraints on microbial metabolisms that mediate the release of methane and carbon dioxide are poorly understood1-7. The role of viruses, which are known to affect microbial dynamics, metabolism and biogeochemistry in the oceans8-10, remains largely unexplored in soil. Here, we aimed to investigate how viruses influence microbial ecology and carbon metabolism in peatland soils along a permafrost thaw gradient in Sweden. We recovered 1,907 viral populations (genomes and large genome fragments) from 197 bulk soil and size-fractionated metagenomes, 58% of which were detected in metatranscriptomes and presumed to be active. In silico predictions linked 35% of the viruses to microbial host populations, highlighting likely viral predators of key carbon-cycling microorganisms, including methanogens and methanotrophs. Lineage-specific virus/host ratios varied, suggesting that viral infection dynamics may differentially impact microbial responses to a changing climate. Virus-encoded glycoside hydrolases, including an endomannanase with confirmed functional activity, indicated that viruses influence complex carbon degradation and that viral abundances were significant predictors of methane dynamics. These findings suggest that viruses may impact ecosystem function in climate-critical, terrestrial habitats and identify multiple potential viral contributions to soil carbon cycling.

Discovery of a novel methanogen prevalent in thawing permafrost.

Thawing permafrost promotes microbial degradation of cryo-sequestered and new carbon leading to the biogenic production of methane, creating a positive feedback to climate change. Here we determine microbial community composition along a permafrost thaw gradient in northern Sweden. Partially thawed sites were frequently dominated by a single archaeal phylotype, Candidatus 'Methanoflorens stordalenmirensis' gen. nov. sp. nov., belonging to the uncultivated lineage 'Rice Cluster II' (Candidatus 'Methanoflorentaceae' fam. nov.). Metagenomic sequencing led to the recovery of its near-complete genome, revealing the genes necessary for hydrogenotrophic methanogenesis. These genes are highly expressed and methane carbon isotope data are consistent with hydrogenotrophic production of methane in the partially thawed site. In addition to permafrost wetlands, 'Methanoflorentaceae' are widespread in high methane-flux habitats suggesting that this lineage is both prevalent and a major contributor to global methane production. In thawing permafrost, Candidatus 'M. stordalenmirensis' appears to be a key mediator of methane-based positive feedback to climate warming.

Environmental and physical controls on northern terrestrial methane emissions across permafrost zones.

Methane (CH4 ) emissions from the northern high-latitude region represent potentially significant biogeochemical feedbacks to the climate system. We compiled a database of growing-season CH4 emissions from terrestrial ecosystems located across permafrost zones, including 303 sites described in 65 studies. Data on environmental and physical variables, including permafrost conditions, were used to assess controls on CH4 emissions. Water table position, soil temperature, and vegetation composition strongly influenced emissions and had interacting effects. Sites with a dense sedge cover had higher emissions than other sites at comparable water table positions, and this was an effect that was more pronounced at low soil temperatures. Sensitivity analysis suggested that CH4 emissions from ecosystems where the water table on average is at or above the soil surface (wet tundra, fen underlain by permafrost, and littoral ecosystems) are more sensitive to variability in soil temperature than drier ecosystems (palsa dry tundra, bog, and fen), whereas the latter ecosystems conversely are relatively more sensitive to changes of the water table position. Sites with near-surface permafrost had lower CH4 fluxes than sites without permafrost at comparable water table positions, a difference that was explained by lower soil temperatures. Neither the active layer depth nor the organic soil layer depth was related to CH4 emissions. Permafrost thaw in lowland regions is often associated with increased soil moisture, higher soil temperatures, and increased sedge cover. In our database, lowland thermokarst sites generally had higher emissions than adjacent sites with intact permafrost, but emissions from thermokarst sites were not statistically higher than emissions from permafrost-free sites with comparable environmental conditions. Overall, these results suggest that future changes to terrestrial high-latitude CH4 emissions will be more proximately related to changes in moisture, soil temperature, and vegetation composition than to increased availability of organic matter following permafrost thaw.

Freshwater methane emissions offset the continental carbon sink.

Inland waters (lakes, reservoirs, streams, and rivers) are often substantial methane (CH(4)) sources in the terrestrial landscape. They are, however, not yet well integrated in global greenhouse gas (GHG) budgets. Data from 474 freshwater ecosystems and the most recent global water area estimates indicate that freshwaters emit at least 103 teragrams of CH(4) year(-1), corresponding to 0.65 petagrams of C as carbon dioxide (CO(2)) equivalents year(-1), offsetting 25% of the estimated land carbon sink. Thus, the continental GHG sink may be considerably overestimated, and freshwaters need to be recognized as important in the global carbon cycle.