Sphagnum-dominated bogs are climatically impactful systems that exhibit two puzzling characteristics: CO₂:CH₄ ratios are greater than those predicted by electron balance models and C decomposition rates are enigmatically slow. We hypothesized that Maillard reactions partially explain both phenomena by increasing apparent CO₂ production via eliminative decarboxylation and sequestering bioavailable nitrogen (N). We tested this hypothesis using incubations of sterilized Maillard reactants, and live and sterilized bog peat. Consistent with our hypotheses, CO₂ production in the sterilized peat was equivalent to 8–13% of CO₂ production in unsterilized peat, and the increased formation of aromatic N compounds decreased N-availability. Numerous sterility assessments rule out biological contamination or extracellular enzyme activity as significant sources of this CO₂. These findings suggest a need for a reevaluation of the fixed CO₂:CH₄ production ratios commonly used in wetland biogeochemical models, which could be improved by incorporating abiotic sources of CO₂ production and N sequestration.

Microbes drive the biogeochemical cycles of earth systems, yet the long-standing goal of linking emerging genomic information, microbial traits, mechanistic ecosystem models, and projections under climate change has remained elusive despite a wealth of emerging genomic information. Here we developed a general genome-to-ecosystem (G2E) framework for integrating genome-inferred microbial kinetic traits into mechanistic models of terrestrial ecosystems and applied it at a well-studied Arctic wetland by benchmarking predictions against observed greenhouse gas emissions. We found variation in genome-inferred microbial kinetic traits resulted in large differences in simulated annual methane emissions, quantitatively demonstrating that the genomically observable variations in microbial capacity are consequential for ecosystem functioning. Applying microbial community-aggregated traits via genome relative-abundance-weighting gave better methane emissions predictions (i.e., up to 54% decrease in bias) compared to ignoring the observed abundances, highlighting the value of combined trait inferences and abundances. This work provides an example of integrating microbial functional trait-based genomics, mechanistic and pragmatic trait parameterizations of diverse microbial metabolisms, and mechanistic ecosystem modeling. The generalizable G2E framework will enable the use of abundant microbial metagenomics data to improve predictions of microbial interactions in many complex systems, including oceanic microbiomes.

Anaerobic incubations of peat have been widely used to explore soil processes, but this in vitro technique raises many questions as to how well it reproduces in situ conditions. To investigate this, we conducted 60–100 days (+25 days pre-incubation) anaerobic, temperature-controlled incubation experiments across a temperature range of 1–26°C on samples from bog and fen habitats, at two different depths (9–19and 25–35 cm). We observed exponential increases in CO2 and methane production with temperature in all conditions. We then compared field-based measurements of methane emission with modeled expectations by extrapolating incubation-determined methane production rates based on (a) soil temperature profiles, (b) the observed incubation temperature-methane production relationship, and (c) seasonal thaw depth from each site. The resulting incubation-extrapolated methane production agreed with measured emission rates within a factor of two at both sites and corresponded to 182 ± 54% and 59 ± 14% of the measured average yearly fluxes from the field for the bog and fen, respectively. The underestimation of fen methane fluxes may be due to the lack of living plant root-derived dissolved organic carbon inputs in incubations, a key process in fens. Conversely, the overestimation in bogs could be attributed to methane oxidation in the field, which is absent in anaerobic incubation conditions. Nonetheless incubations predicted greenhouse gas emissions from a northern peatland within a factor of two.

Northern peatlands are a globally significant source of methane (CH4), and emissions are projected to increase due to warming and permafrost loss. Understanding the microbial mechanisms behind patterns in CH4 production in peatlands will be key to predicting annual emissions changes, with stable carbon isotopes (δ13C-CH4) being a powerful tool for characterizing these drivers. Given that δ13C-CH4 is used in top-down atmospheric inversion models to partition sources, our ability to model CH4 production pathways and associated δ13C-CH4 values is critical. We sought to characterize the role of environmental conditions, including hydrologic and vegetation patterns associated with permafrost thaw, on δ13C-CH4 values from high-latitude peatlands. We measured porewater and emitted CH4 stable isotopes, pH, and vegetation composition from five boreal-Arctic peatlands. Porewater δ13C-CH4 was strongly associated with peatland type, with δ13C enriched values obtained from more minerotrophic fens (−61.2 ± 9.1‰) compared to permafrost-free bogs (−74.1 ± 9.4‰) and raised permafrost bogs (−81.6 ± 11.5‰). Variation in porewater δ13C-CH4 was best explained by sedge cover, CH4 concentration, and the interactive effect of peatland type and pH (r2 = 0.50, p < 0.001). Emitted δ13C-CH4 varied greatly but was positively correlated with porewater δ13C-CH4. We calculated a mixed atmospheric δ13C-CH4 value for northern peatlands of −65.3 ± 7‰ and show that this value is more sensitive to landscape drying than wetting under permafrost thaw scenarios. Our results suggest northern peatland δ13C-CH4 values are likely to shift in the future which has important implications for source partitioning in atmospheric inversion models.

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.

Quantifying the temperature sensitivity of methane (CH₄) production is crucial for predicting how wetland ecosystems will respond to climate warming. Typically, the temperature sensitivity (often quantified as a Q₁₀ value) is derived from laboratory incubation studies and then used in biogeochemical models. However, studies report wide variation in incubation-inferred Q₁₀ values, with a large portion of this variation remaining unexplained. Here we applied observations in a thawing permafrost peatland (Stordalen Mire) and a well-tested process-rich model (ecosys) to interpret incubation observations and investigate controls on inferred CH₄ production temperature sensitivity. We developed a field-storage-incubation modeling approach to mimic the full incubation sequence, including field sampling at a particular time in the growing season, refrigerated storage, and laboratory incubation, followed by model evaluation. We found that CH₄ production rates during incubation are regulated by substrate availability and active microbial biomass of key microbial functional groups, which are affected by soil storage duration and temperature. Seasonal variation in substrate availability and active microbial biomass of key microbial functional groups led to strong time-of-sampling impacts on CH₄ production. CH₄ production is higher with less perturbation post-sampling, i.e. shorter storage duration and lower storage temperature. We found a wide range of inferred Q₁₀ values (1.2–3.5), which we attribute to incubation temperatures, incubation duration, storage duration, and sampling time. We also show that Q₁₀ values of CH₄ production are controlled by interacting biological, biochemical, and physical processes, which cause the inferred Q₁₀ values to differ substantially from those of the component processes. Terrestrial ecosystem models that use a constant Q₁₀ value to represent temperature responses may therefore predict biased soil carbon cycling under future climate scenarios.

Aquatic networks contribute greenhouse gases and lateral carbon (C) export from catchments. The magnitudes of these fluxes exceed the global land C sink but are uncertain. Resolving this uncertainty is important for understanding climate feedbacks. We quantified vertical methane (CH₄) and carbon dioxide (CO₂) emissions from lakes and streams, and lateral export of dissolved inorganic and organic carbon from a hemiboreal catchment for 3 yr. Lateral C fluxes dominated the total aquatic C flux. All aquatic C fluxes were disproportionately contributed from spatially restricted areas and/or short-term events. Hence, consideration of local and episodic variability is vital. Temperature and runoff were the main temporal drivers for lake and stream C emissions, respectively. Whole-catchment aquatic C emissions scaled linearly with these drivers within timeframes of stable land-cover. Hence, temperature and runoff increase across Northern Hemisphere humid areas from climate change may yield proportional increases in aquatic C fluxes. 

Stordalen Mire is a peatland in the discontinuous permafrost zone in arctic Sweden that exhibits a habitat gradient from permafrost palsa, to Sphagnum bog underlain by permafrost, to Eriophorum-dominated fully thawed fen. We used three independent approaches to evaluate the annual, multi-decadal, and millennial apparent carbon accumulation rates (aCAR) across this gradient: seven years of direct semi-continuous measurement of CO₂ and CH₄ exchange, and 21 core profiles for ²¹⁰Pb and ¹⁴C peat dating. Year-round chamber measurements indicated net carbon balance of −13 ± 8, −49 ± 15, and −91 ± 43 g C m⁻² y⁻¹ for the years 2012–2018 in palsa, bog, and fen, respectively. Methane emission offset 2%, 7%, and 17% of the CO₂ uptake rate across this gradient. Recent aCAR indicates higher C accumulation rates in surface peats in the palsa and bog compared to current CO₂ fluxes, but these assessments are more similar in the fen. aCAR increased from low millennial-scale levels (17–29 g C m⁻² y⁻¹) to moderate aCAR of the past century (72–81 g C m⁻² y⁻¹) to higher recent aCAR of 90–147 g C m⁻² y⁻¹. Recent permafrost collapse, greater inundation and vegetation response has made the landscape a stronger CO₂ sink, but this CO₂ sink is increasingly offset by rising CH₄ emissions, dominated by modern carbon as determined by ¹⁴C. The higher CH₄ emissions result in higher net CO_2-equivalent emissions, indicating that radiative forcing of this mire and similar permafrost ecosystems will exert a warming influence on future climate.

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 in northern peatlands is likely to create a positive feedback to climate change, as microbes transform soil carbon (C) into carbon dioxide (CO₂) or methane (CH₄). While the microbiome's encoded C-processing potential changes with thaw, the impact on substrate utilization and gas emissions is less well characterized. We therefore examined microbial C-cycling dynamics from a partially thawed Sphagnum-dominated bog to a fully thawed sedge-dominated fen in Stordalen Mire (68.35°N, 19.05°E), Sweden. We profiled C substrate utilization diversity and extent by Biolog Ecoplates™, then tested substrate-specific hypotheses by targeted additions (of glucose, the short chain fatty acids (SCFAs) acetate and butyrate, and the organic acids galacturonic acid and p-hydroxybenzoic acid, all at field-relevant concentrations) under anaerobic conditions at 15 °C. In parallel we characterized microbiomes (via 16S rRNA amplicon sequencing and quantitative polymerase chain reaction) and C gas emissions. The fen exhibited a higher substrate use diversity and faster rate of overall substrate utilization than in the bog, based on Biolog Ecoplate™ incubations. Simple glucose additions (akin to a positive control) to peat microcosms fueled fermentation as expected (reflected in enriched fermenter lineages, their inferred metabolisms, and CO₂ production), but also showed potential priming of anaerobic phenol degradation in the bog. Addition of SCFAs to bog and fen produced the least change in lineages and in CO₂, and modest suppression of CH₄ primarily in the fen, attributed to inhibition. Addition of both organic acids greatly increased the CO₂:CH₄ ratio in the deep peats but had distinct individual gas dynamics and impacts on microbiota. Both organic acids appeared to act as both C source and as a microbial inhibitor, with galacturonic acid also likely playing a role in electron transfer or acceptance. Collectively, these results support the importance of aboveground-belowground linkages - and in particular the role of Sphagnum spp.- in supplying substrates and inhibitors that drive microbiome assembly and C processing in these dynamically changing systems. In addition, they highlight an important temporal dynamic: responses on the short time scale of incubations (which would reflect transition conditions in the field) differ from those evident at the longer scales of habitat transition, in ways consequential to C gas emissions. In the short term, substrate addition response reflected microbiome legacy (e.g., bog communities were slower to process C and better tolerated inhibitors than fen communities) but led to little overall increase in C gas production (and a high skew to CO₂). At the longer time scale of bog and fen thaw stages (which are used to represent these systems in models) the concomitant shifts in plants, hydrology and microbiota attenuate microbiome legacy impacts on substrate processing and C gas emissions over time. As habitat transition areas expand under accelerating change, we hypothesize an increased role of microbiome legacy in the landscape overall, leading to a lag in the increase of CH₄ emissions expected from fen expansion.