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Methane Dynamics Regulated by Microbial Community Response to Permafrost Thaw

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Methane Dynamics Regulated by Microbial Community Response to Permafrost Thaw LETTER doi:10.1038/nature13798 Methane dynamics regulated by microbial community response to permafrost thaw Carmody K. McCalley1{, Ben J. Woodcroft2, Suzanne B. Hodgkins3, Richard A. Wehr1, Eun-Hae Kim4, Rhiannon Mondav2{, Patrick M. Crill5, Jeffrey P. Chanton3, Virginia I. Rich4, Gene W. Tyson2 & Scott R. Saleska1 Permafrost contains about 50% of the global soil carbon1. It is thought with previous studies of in situ bog and fen systems17–19, that thaw that the thawing of permafrost can lead to a loss of soil carbon in the progression also facilitates a shift from hydrogenotrophic to acetoclas- 2,3 form of methane and carbon dioxide emissions . The magnitude of tic CH4 production. the resulting positive climate feedback of such greenhouse gas emis- We used the distinct isotopic signatures of different microbial CH4 3 sions is still unknown and may to a large extent depend on the poorly production and consumption pathways to directly relate changes in CH4 understood role of microbial community composition in regulating dynamics across the thaw gradient to underlying changes in the micro- the metabolic processes that drive such ecosystem-scale greenhouse bial community. Methane produced by hydrogenotrophic methanogens gas fluxes. Here we show that changes in vegetation and increasing generally has lower d13C and higher dD(d13C 52110% to 260% and methane emissions with permafrost thaw are associated with a switch dD 52250%to 2170%) relative to that produced by acetoclastic metha- from hydrogenotrophic to partly acetoclastic methanogenesis, result- nogens (d13C 5260% to 250% and dD 52400% to 2250%)19,20. 13 inginalargeshiftinthed C signature (10–15%) of emitted methane. If methanotrophic microbes then oxidize CH4, lighter molecules are 13 We used a natural landscape gradient of permafrost thaw in northern preferentially consumed, leaving the remaining CH4 enriched in C 4,5 Sweden as a model to investigate the role of microbial communit- and D relative to the original CH4 pool (expected patterns are shown in ies in regulating methane cycling, and to test whether a knowledge of Extended Data Fig. 1)19,20. community dynamics could improvepredictions of carbon emissions High-temporal-resolution measurements of the magnitude and iso- under loss of permafrost. Abundance of the methanogen Candidatus topic composition of CH4 emissions, using a quantum cascade laser spec- ‘Methanoflorens stordalenmirensis’6 is a key predictor of the shifts in trometer (Aerodyne Research Inc.) connected to autochambers, showed 13 methane isotopes, which in turn predicts the proportions of carbon that CH4 emissions and their C content increased with thaw. Average emitted as methane and as carbon dioxide, an important factor for CH4 fluxes increased from effectively zero at the intact permafrost palsa 22 21 simulating the climate feedback associated with permafrost thaw in site to 1.46 6 0.37 mg CH4 m h (all errors are reported as s.e.m.) at the 3,7 22 21 global models . By showing that the abundance of key microbial thawing Sphagnum site, and to 8.75 6 0.50 mg CH4 m h at the fully lineages can be used to predict atmospherically relevant patterns in thawed Eriophorum site (Fig. 1a; P , 0.001). The average d13C of emit- methane isotopes and the proportion of carbon metabolized to meth- ted CH4 also increased significantly, from 279.6 6 0.9% in the Sphagnum ane during permafrost thaw, we establish a basis for scaling changing site to 266.3 6 1.6% in the Eriophorum site (Fig. 1b; P 5 0.03). This microbial communities to ecosystem isotope dynamics. Our findings consistent 10–15% divergence between sites was maintained through 13 indicate that microbial ecology may be important in ecosystem-scale the growing season but overlain by parallel fluctuations in d C-CH4, responses to global change. suggesting that weather patterns exerted a common influence over the Multiple factors—including hydrology, vegetation, organic matter chem- magnitude of isotopic fractionation. Porewater CH4 isotopes showed a istry, pH and soil microclimate—are affected by permafrost loss5,8,9. similar pattern, with Eriophorum site porewater d13Cabout10% higher Together these factors regulate microbial metabolisms that release car- than that of Sphagnum (July and August; Fig. 1b and Extended Data 10–12 13 bon dioxide (CO2) and methane (CH4) from thawing permafrost Table 1). Porewater CH4 was C-enriched by 5–20% relative to emitted and are the basis for Earth-system model predictions of future CH4 CH4, as expected, as a result of diffusive fractionation (Methods, equa- emissions7,13,14. However, the role of microbial community composition tion (2))18,21. in regulating the metabolic processes that drive ecosystem-scale fluxes The apparent fractionation factor for carbon in porewater CH4 rela- is unknown. tive to CO2, aC (Methods, equation (2), and Extended Data Table 1), is 22 At our study site in Stordalen mire, as in other thawing permafrost a related index of changes in CH4 production . Greater fractionation is peatlands8,15, permafrost loss causes hydrological and vegetation shifts: associated with hydrogenotrophic methanogenesis and was found in well-drained permafrost-supported palsas collapse into partly thawed the thawing Sphagnum site (aC 5 1.053 6 0.002). Significantly less frac- bogs dominated by moss (Sphagnum spp.) and fully thawed fens domi- tionation (P 5 0.002) associated with more acetoclastic production or nated by sedges (such as Eriophorum angustifolium)4. Between 1970 and with consumption by oxidation was found in the fully thawed Eriophorum 4 2000, 10% of Stordalen’s palsa habitat thawed into such wetlands . This porewater (aC 5 1.046 6 0.001). Here, increases in acetoclastic produc- transition drives an appreciable global warming impact because CO2- tion, not oxidation, best explain isotopic shifts because lower aC and higher 13 emitting palsa is converted to bogs and fens, which take up CO2 but emit d C-CH4 are accompanied by significantly lower dD-CH4 (Extended 3 4,5,16 19 CH4 (a more potent greenhouse gas ) . The net effect is that the high- Data Fig. 1; P,0.001) . This is consistent with the pattern of isotopes in CH4 methane-emitting fen contributes sevenfold as much greenhouse impact emissions, in incubations ofStordalen peat9 and in studies showing bog- per unit area as the palsa. This thaw progression is also associated with to-fen shifts from hydrogenotrophic to acetoclastic methanogenesis17–19. an increase in overall organic matter lability, including a decrease in C:N The CH4 flux and isotope results provide compelling but indirect evid- 9 ratio and an increase in humification rates . We speculated, consistent ence for changes in CH4-cycling microbial communities with permafrost 1Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85721, USA. 2Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, University of Queensland, Brisbane 4072, Queensland, Australia. 3Department of Earth, Ocean and Atmospheric Science, Florida State University, Tallahassee, Florida 32306, USA. 4Department of Soil, Water and Environmental Science, University of Arizona, Tucson, Arizona 85721, USA. 5Department of Geological Sciences, Stockholm University, Stockholm 106 91, Sweden. {Present addresses: Earth Systems Research Center, University of New Hampshire, Durham, New Hampshire 03824, USA (C.K.M.); Department of Ecology and Genetics, Uppsala University, Uppsala 75 236, Sweden (R.M.). 478 | NATURE | VOL 514 | 23 OCTOBER 2014 ©2014 Macmillan Publishers Limited. All rights reserved LETTER RESEARCH a Eriophorum (fully thawed) Flux Porewater c Acetoclastic (obligate) 25 Acetoclastic (facultative) ) Sphagnum (intermediate thaw) Flux Porewater Hydrogenotrophic –1 Palsa (intact permafrost) Flux Other Archaea h 20 Bacteria –2 m 4 Palsa 15 10 flux (mg CH 4 5 Sphagnum (aerobic) CH 0 Permafrost thaw b –50 –60 Sphagnum (anaerobic) (‰) 4 –70 C-CH 13 δ –80 Eriophorum –90 11 July 31 July 20 August 9 September 29 September 2011 13 Figure 1 | Increases in the magnitude and d C signature of CH4 during by taxonomic identity assigned from 16S rRNA amplicon sequencing (n 5 3). permafrost thaw track shifts in methanogen communities. a, Average daily For the intermediate-thaw Sphagnum site, aerobic communities were 13 CH4 emissions (error bars represent s.e.m.; n 5 2–3). b, d C composition sampled above the water table; anaerobic communities were sampled below of emitted and porewater CH4 (error bars represent s.e.m.; flux n 5 2–3, the water table. porewater n 5 6–9). c, Relative abundance of methanogenic groups as inferred thaw. These microbiological changes could be shifts in activity of par- thaw, a novel observation at the ecosystem scale. The early successional ticular community members or changes in community composition. We hydrogenotroph ‘M. stordalenmirensis’6 dominates methanogenic meta- examined the role of community composition through 16S rRNA gene bolism in the early stages of thaw, followed by the subsequent emergence amplicon sequencing. All known methanogens belong to a small number of a more diverse methanogen community, including obligate acetoclas- of archaeal lineages within the Euryarchaeota23. As expected, the shift tic methanogens. This microbial succession provides direct evidence from CH4-neutral intact permafrost palsa to CH4-emitting wetland cor- for how changes in ecosystem structure during permafrost thaw (plant responded to a substantial increase in the relative abundance of metha- succession and increases
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