Methane dynamics regulated by microbial community response to permafrost thaw. 4,5,16 . The net effect is that the high methane-emitting fen contributes 7 55 times the greenhouse impact per unit area as the palsa. This thaw progression is also associated 56 with an increase in overall organic matter lability, including a decrease in C:N and an increase in 57 humification rates 9 . We hypothesized, consistent with previous studies of in situ bog and fen 58 systems [17][18][19] , that thaw progression also facilitates a shift from hydrogenotrophic to acetoclastic 59 CH 4 production. 60We used the distinct isotopic signatures of different microbial CH 4 production and 61 consumption pathways to directly relate changes in CH 4 dynamics across the thaw gradient to 62 underlying changes in the microbial community. Methane produced by hydrogenotrophic 63 methanogens generally has lower 13 C and higher D ( 13 C = -110 to -60‰ and D = -250 to -64 170‰) relative to that produced by acetoclastic methanogens ( 13 C = -60 to -50‰ and D = -400 65 to -250‰) 19,20 . If methanotrophic microbes then oxidize CH 4 , lighter molecules are 66 preferentially consumed, leaving the remaining CH 4 13 C-and D-enriched relative to the original 67 CH 4 pool (see expected patterns in Extended Data Fig 1) 19 . Greater fractionation is associated with hydrogenotrophic methanogenesis, and was 85 found in the thawing Sphagnum site (average C = 1.053 ± 0.002). Significantly less 86 fractionation (p=0.002) associated with more acetoclastic production or with consumption by 87 oxidation was found in the fully thawed Eriophorum porewater (average C = 1.046 ± 0.001). 88Here, increases in acetoclastic production, not oxidation, best explain isotopic shifts because 89 lower C and higher 13 C-CH 4 are accompanied by significantly lower D-CH 4 (Extended Data 90 Fig. 1, p< 0.001) 19 . This is consistent with the pattern of isotopes in CH 4 emissions as well as 91 incubations of Stordalen peat 9 and studies showing bog-to-fen shifts from hydrogenotrophic to 92 acetoclastic methanogenesis [17][18][19] . 93The CH 4 flux and isotope results provide compelling but indirect evidence for changes in 94 CH 4 -cycling microbial communities with permafrost thaw. These microbiological changes could 95 be shifts in activity of particular community members or changes in community composition. We 96 examined the role of community composition through 16S rRNA gene amplicon sequencing. All 97 known methanogens belong to a small number of archaeal lineages within the Euryarchaeota 23 . 98As expected, the shift from CH 4 -neutral intact permafrost palsa to CH 4 -emitting wetland 99 corresponded to a substantial increase in the relative abundance of methanogenic archaeal 100 lineages (Fig. 1c, Extended Data Table 2,3). In the aerobic palsa and surface Sphagnum habitats, 101 methanogens were found in low relative abundance (average <0.6%), while the anaerobic 102 environments of the Eriophorum and deeper (below the water table) Sphagnum habitats harbored 10...
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.
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 (CH 4 ) vs. carbon dioxide (CO 2 ) 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 CH 4 and CO 2 production potentials, higher relative CH 4 /CO 2 ratios, and a shift in CH 4 production pathway from CO 2 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 CH 4 . This impact of permafrost thaw on organic matter chemistry could intensify the predicted climate feedbacks of increasing temperatures, permafrost carbon mobilization, and hydrologic changes.H igh-latitude soils in the Northern Hemisphere contain an estimated 1,400-1,850 petagrams (Pg) of carbon, of which ∼277 Pg is in peatlands within the permafrost zone (1, 2). This quantity of 277 Pg represents over one-third of the carbon stock in the atmosphere (ca. 800 Pg) (3). The fate of this carbon in a warming climate-i.e., the responses of net carbon balance and CH 4 emissions-is important in predicting climate feedbacks of permafrost thaw. Although northern peatlands are currently a net carbon sink, and have been since the end of the last glaciation, they are a net source of CH 4 (4, 5), emitting 0.046-0.09 Pg of carbon as CH 4 per year (4, 6, 7). Due to CH 4 's disproportionate global warming potential (33× CO 2 for 1 kg CH 4 vs. 1 kg CO 2 at a 100-y timescale) (8), this is equivalent to 6-12% of annual fossil fuel emissions of CO 2 (8.7 Pg of C) (9). The thaw of permafrost peatlands may alter their CH 4 and CO 2 emissions due to mobilization of formerly frozen carbon, higher temperatures, altered redox conditions, and evolving organic matter chemistry. Changes in carbon emissions, and in CH 4 emission in particular, could have potentially significant climate impacts. CH 4 is produced by two primary mechanisms (10-12),...
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.
In arid environments such as deserts, nitrogen is often the most limiting nutrient for biological activity. The majority of the ecosystem nitrogen flux is typically thought to be driven by production and loss of reactive nitrogen species by microorganisms in the soil. We found that high soil-surface temperatures (greater than 50 degrees C), driven by solar radiation, are the primary cause of nitrogen loss in Mojave Desert soils. This abiotic pathway not only enables the balancing of arid ecosystem nitrogen budgets, but also changes our view of global nitrogen cycling and the predicted impact of climate change and increased temperatures on nitrogen bioavailability.
Isotopic data provide powerful constraints on regional and global methane emissions and their source profiles. However, inverse modeling of spatially resolved methane flux is currently constrained by a lack of information on the variability of source isotopic signatures. In this study, isotopic signatures of emissions in the Fennoscandian Arctic have been determined in chambers over wetland, in the air 0.3 to 3 m above the wetland surface and by aircraft sampling from 100 m above wetlands up to the stratosphere. Overall, the methane flux to atmosphere has a coherent δ 13 C isotopic signature of À71 ± 1‰, measured in situ on the ground in wetlands. This is in close agreement with δ 13 C isotopic signatures of local and regional methane increments measured by aircraft campaigns flying through air masses containing elevated methane mole fractions. In contrast, results from wetlands in Canadian boreal forest farther south gave isotopic signatures of À67 ± 1‰. Wetland emissions dominate the local methane source measured over the European Arctic in summer. Chamber measurements demonstrate a highly variable methane flux and isotopic signature, but the results from air sampling within wetland areas show that emissions mix rapidly immediately above the wetland surface and methane emissions reaching the wider atmosphere do indeed have strongly coherent C isotope signatures. The study suggests that for boreal wetlands (>60°N) global and regional modeling can use an isotopic signature of À71‰ to apportion sources more accurately, but there is much need for further measurements over other wetlands regions to verify this.
Emissions of reactive N compounds produced during terrestrial N cycling can be an important N loss pathway from ecosystems. Most measurements of this process focus on NO and N(2)O efflux; however, in alkaline soils such as those in the Mojave Desert, NH(3) production can be an important component of N gas loss. We investigated patterns of NO and NH(3) emissions in the Mojave Desert and identified seasonal changes in temperature, precipitation and spatial heterogeneity in soil nutrients as primary controllers of soil efflux. Across all seasons, NH(3) dominated reactive N gas emissions with fluxes ranging from 0.9 to 10 ng N m(-2) s(-1) as compared to NO fluxes of 0.08-1.9 ng N m(-2) s(-1). Fluxes were higher in April and July than in October; however, a fall precipitation event yielded large increases in both NO and NH(3) efflux. To explore the mechanisms driving field observations, we combined NO and NH(3) soil flux measurements with laboratory manipulations of temperature, water and nutrient conditions. These experiments showed a large transient NH(3) pulse (~70-100 ng N m(-2) s(-1)) following water addition, presumably driven by an increase in soil NH(4) (+) concentrations. This was followed by an increase in NO production, with maximum NO flux rates of 34 ng N m(-2) s(-1). Our study suggests that immediately following water addition NH(3) volatilization proceeds at high rates due to the absence of microbial competition for NH(4) (+); during this period N gas loss is insensitive to changes in temperature and soil nutrients. Subsequently, NO emission increases and rates of both NO and NH(3) emission are sensitive to temperature and nutrient constraints on microbial activity. Addition of labile C reduces gaseous N losses, presumably by increasing microbial immobilization, whereas addition of NO(3) (-) stimulates NO and NH(3) efflux.
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