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Methane dynamics regulated by microbial community response to permafrost thaw

Abstract

Permafrost contains about 50% of the global soil carbon1. It is thought that the thawing of permafrost can lead to a loss of soil carbon in the form of methane and carbon dioxide emissions2,3. The magnitude of the resulting positive climate feedback of such greenhouse gas emissions is still unknown3 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 δ13C signature (10–15‰) of emitted methane. We used a natural landscape gradient of permafrost thaw in northern Sweden4,5 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 stordalenmirensis6 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 models3,7. 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.

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Figure 1: Increases in the magnitude and δ13C signature of CH4 during permafrost thaw track shifts in methanogen communities.
Figure 2: Correlation between αC and both Candidatus ‘Methanoflorens stordalenmirensis’ and the anaerobic CH4:CO2 production ratio.
Figure 3: Simulated effect of CH4 from different methanogen communities in thawing permafrost on atmospheric δ13C-CH4 in a box model of the atmosphere.

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Sequence Read Archive

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Amplicon sequencing data are deposited in the NCBI Sequence Read Archive with accession number SRP042265.

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Acknowledgements

We thank the Abisko Scientific Research Station for infrastructure and logistical support; T. Logan and N. Rakos for their assistance in the field; and S. Wofsy and S. Frolking for feedback on a draft of this paper. This work was supported by the US Department of Energy Office of Biological and Environmental Research (award DE-SC0004632), and by the University of Arizona Technology and Research Initiative Fund, through the Water, Environmental and Energy Solutions Initiative. R.M. was supported by an Australian Postgraduate Award Scholarship.

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Authors and Affiliations

Authors

Contributions

S.R.S., V.I.R., P.M.C., J.C. and G.W.T. designed the study. C.K.M., S.B.H., R.A.W., P.M.C., J.C. and S.R.S. designed and/or performed flux/porewater/isotope measurements and laboratory incubations. C.K.M., B.J.W., R.M., E.-H.K., S.R.S., V.I.R. and G.W.T. designed and/or performed analyses integrating bioinformatics and biogeochemistry. C.K.M., V.I.R. and S.R.S. wrote the paper in consultation with B.J.W., S.B.H., J.C., P.M.C., E.-H.K., R.M. and G.W.T.

Corresponding authors

Correspondence to Carmody K. McCalley or Scott R. Saleska.

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Extended data figures and tables

Extended Data Figure 1 Expected and observed relationships between the δD and δ13C content of porewater CH4.

The thick grey arrow shows the expected pattern in H and C isotopes of CH4 when variations are caused by shifts between acetoclastic (lower right) and hydrogenotrophic (upper left) production. The thin black arrows pointing to the upper right indicate the expected pattern in H and C isotopes of CH4 when variations are caused by changes in CH4 oxidation19. The points are observed isotopic compositions of samples collected between July and October 2011 at the partly thawed Sphagnum and fully thawed Eriophorum sites; site averages are shown with error bars (error bars represent s.e.m.; n = 13 (Sphagnum) and 20 (Eriophorum)). Although the scatter allows for some variation in both production and oxidation, the average Eriophorum porewater CH4 had significantly more 13C and less D relative to Sphagnum porewater (Hotelling’s T2 test, P = 0.0001, n = 33), indicating that the overall inter-site isotopic differences were due mostly to differences in the CH4 production pathway rather than to differences in CH4 oxidation. Additionally, in August there was a significant negative relationship between δ13C-CH4 and δD-CH4 of porewater samples collected across sites (dashed line, linear regression, R2 = 0.5, P < 0.02, n = 12). Note that on the vertical axis δD-H2O has been subtracted from δD-CH4 to correct for the effect of δD exchange between H2O and CH4 (refs 203850).

Source data

Extended Data Figure 2 Simulations, using high and low temperature and C release scenarios, of the effect of CH4 release from thawing permafrost on atmospheric δ13C-CH4.

a, Scenarios of permafrost C release due to thaw (red bounding lines, high temperature; orange bounding lines, low temperature; the range in each case is defined by high and low C release scenarios). b, Impact on atmospheric methane mixing ratios (assuming that 2.3% of released C is emitted as methane). c, Impact of the high climate change scenario on atmospheric methane isotopes, assuming Eriophorum-like emissions (blue bounding lines, δ13C ≈ −65‰), or assuming Sphagnum-like emissions (green bounding lines, δ13C ≈ −80‰). d, As in c, except for the low climate change scenario. In c and d, dotted horizontal lines indicate the detection limit for CH4 isotopes28.

Extended Data Table 1 Summary of porewater chemistry, average (s.e.m.), n = 3
Extended Data Table 2 Relative abundance, taxonomic classification and predicted methanogenic pathway of the dominant methanogen operational taxonomic units (OTUs)
Extended Data Table 3 Relative abundance of methanogen functional groups within the Archaea
Extended Data Table 4 Results of linear regression analysis for predicting αC from the relative abundances of methanogenic pathways, dominant methanogenic lineages and environmental variables (n = 41)
Extended Data Table 5 Results of stepwise multiple regression analysis for predicting αC from relative abundances of methanogenic lineages and environmental variables
Extended Data Table 6 Estimate of the relative contribution of hydrogenotrophic production to annual CH4 emission at Stordalen mire
Extended Data Table 7 Small-subunit rRNA gene amplicon multiplex identifiers (MIDs) used for each sample
Extended Data Table 8 Results of stepwise multiple regression analysis for predicting δ13C-CH4 from relative abundances of methanogenic lineages and environmental variables (model 1), the relative abundance of ‘M. stordalenmirensis’ from environmental variables (model 2), and αC from environmental variables (model 3)

Supplementary information

Supplementary Data

Operational taxonomic unit (OTU) table from 16S rRNA gene amplicon analysis. Each row represents an OTU. The first set of columns show the number of that 16S rRNA gene amplicon found in each sample. The rightmost columns show the taxonomy of that OTU predicted with BLAST. The samples presented in this study represent a subset of a larger sampling campaign (eg. Mondav et al 2014) therefore not all OTU's identified in the larger sample-set are present in this table. (XLS 9134 kb)

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McCalley, C., Woodcroft, B., Hodgkins, S. et al. Methane dynamics regulated by microbial community response to permafrost thaw. Nature 514, 478–481 (2014). https://doi.org/10.1038/nature13798

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