, Volume 22, Issue 3, pp 447–459 | Cite as

Shifts of methanogenic communities in response to permafrost thaw results in rising methane emissions and soil property changes

  • Shiping WeiEmail author
  • Hongpeng Cui
  • Youhai Zhu
  • Zhenquan Lu
  • Shouji Pang
  • Shuai Zhang
  • Hailiang Dong
  • Xin SuEmail author
Original Paper


Permafrost thaw can bring negative consequences in terms of ecosystems, resulting in permafrost collapse, waterlogging, thermokarst lake development, and species composition changes. Little is known about how permafrost thaw influences microbial community shifts and their activities. Here, we show that the dominant archaeal community shifts from Methanomicrobiales to Methanosarcinales in response to the permafrost thaw, and the increase in methane emission is found to be associated with the methanogenic archaea, which rapidly bloom with nearly tenfold increase in total number. The mcrA gene clone libraries analyses indicate that Methanocellales/Rice Cluster I was predominant both in the original permafrost and in the thawed permafrost. However, only species belonging to Methanosarcinales showed higher transcriptional activities in the thawed permafrost, indicating a shift of methanogens from hydrogenotrophic to partly acetoclastic methane-generating metabolic processes. In addition, data also show the soil texture and features change as a result of microbial reproduction and activity induced by this permafrost thaw. Those data indicate that microbial ecology under warming permafrost has potential impacts on ecosystem and methane emissions.


Archaea community Methanogenic community Permafrost thaw Methane emission mcrA 



The authors acknowledge James Hurley at the University of Colorado for making a critical reading and revision of this paper. This research was supported by Funds of Oil and Gas Survey, China Geological Survey (GZH201400308 and GZH201400306).

Supplementary material

792_2018_1007_MOESM1_ESM.doc (934 kb)
Supplementary material 1 (DOC 934 kb)


  1. Allison SD, Treseder KK (2011) Climate changes feedbacks to microbial decomposition in boreal soils. Fungal Ecol 4:362–374CrossRefGoogle Scholar
  2. Anisimov OA, Nelson FE (1996) Permafrost distribution in the Northern Hemisphere under scenarios of climatic change. Glob Planet Change 14:59–72CrossRefGoogle Scholar
  3. Anthony KMW, Zimov SA, Grosse G, Jones MC, Anthony PM, Chapin FS III, Finlay JC, Mack MC, Davydov S, Frenzel P, Frolking S (2014) A shift of thermokarst lakes from carbon sources to sinks during the Holocene epoch. Nature 511:452–456CrossRefPubMedGoogle Scholar
  4. Barbier BA, Dziduch I, Liebner S, Ganzert L, Lantuit H, Pollard W, Wagner D (2012) Methane cycling communities in a permafrost-affected soil on Herschel Island, Western Canadian Arctic: active layer profiling of mcrA and pmoA genes. FEMS Microbiol Ecol 82:287–302CrossRefPubMedGoogle Scholar
  5. Chapin FS III, Sturm M, Serreze MC, McFadden JP, Key JR, Lloyd AH et al (2005) Role of land-surface changes in Arctic summer warming. Science 310:657–660CrossRefPubMedGoogle Scholar
  6. Christensen TR, Johansson T, Åkerman HJ, Mastepanov M (2004) Thawing sub-arctic permafrost: effects on vegetation and methane emissions. Geophys Res Lett 31:1–4CrossRefGoogle Scholar
  7. Conrad R, Erkel C, Liesack W (2006) Rice Cluster I methanogens, an important group of Archaea producing greenhouse gas in soil. Curr Opin Biotech 17:262–267CrossRefPubMedGoogle Scholar
  8. Coolen MJL, Orsi WD (2015) The transcriptional response of microbial communities in thawing Alaskan permafrost soils. Front Microbiol 6:1–14CrossRefGoogle Scholar
  9. Coolen MJL, van de Giessen J, Zhu EY, Wuchter C (2011) Bioavailability of soil organic matter and microbial community dynamics upon permafrost thaw. Environ Microbiol 13:2299–2314CrossRefPubMedGoogle Scholar
  10. DeLong EF (1992) Archaea in coastal marine environments. PNAS 89:5685–5689CrossRefPubMedPubMedCentralGoogle Scholar
  11. Deng J, Gu Y, Zhang J, Xue K, Qin Y, Yuan M, Yin H, He Z, Wu L, Schuur EAG, Tiedje JM, Zhou J (2015) Shifts of tundra bacterial and archaeal communities along a permafrost thaw gradient in Alaska. Mol Ecol 24:222–234CrossRefPubMedGoogle Scholar
  12. Ernakovich JG, Wallenstein MD (2015) Permafrost microbial community traits and functional diversity indicate low activity at in situ thaw temperatures. Soil Biol Biochem 87:78–89CrossRefGoogle Scholar
  13. Garcia JL, Ollivier B, Whitman WB (2006) The order Methanomicrobiales. Prokaryotes 3:208–230CrossRefGoogle Scholar
  14. Good IJ (1953) The population frequencies of species and estimation of population parameters. Biometrika 40:237–264CrossRefGoogle Scholar
  15. Graham DE, Wallenstein MD, Vishnivetskaya TA, Waldrop MP, Phelps TJ, Pfiffner SM et al (2012) Microbes in thawing permafrost: the unknown variable in the climate change equation. ISME J 6:709–712CrossRefPubMedGoogle Scholar
  16. Grosskopf R, Stubner S, Liesack W (1998) Novel euryarchaeotal lineages detected on rice roots and in the anoxic bulk soil of flooded rice microcosms. Appl Environ Microbiol 64:4983–4989PubMedCentralGoogle Scholar
  17. Hales BA, Edwards C, Ritchie DA, Hall G, Pickup RW, Saunders JR (1996) Isolation and identification of methanogen-specific DNA from blanket bog peat by PCR amplification and sequence analysis. Appl Environ Microbiol 62:668–675PubMedPubMedCentralGoogle Scholar
  18. Hallam SJ, Girguis PR, Preston CM, Richardson PM, DeLong EF (2003) Indentification of methyl coenzyme M reductase A (mcrA) genes associated with methane-oxidizing archaea. Appl Environ Microbiol 69:5483–5491CrossRefPubMedPubMedCentralGoogle Scholar
  19. Hultman J, Waldrop MP, Mackelprang R, David MM, McFarland J, Blazewicz SJ et al (2015) Multi-omics of permafrost, active layer and thermokarst bog soil microbiomes. Nature 521:208–212CrossRefPubMedGoogle Scholar
  20. Jansson JK, Tas N (2014) The microbial ecology of permafrost. Nat Rev Microbiol 12:414–425CrossRefPubMedGoogle Scholar
  21. Jin H, Wu J, Cheng G, Tomoko N, Sun G (1999) Methane emissions from wetlands on the Qinghai–Tibet Plateau. Chin Sci Bull 44:2282–2286CrossRefGoogle Scholar
  22. Jin HJ, Li SX, Wang SL, Zhao L (2000) Impact of climatic change on permafrost and cold regions environment in China. Acta Geogr Sin 55:161–173Google Scholar
  23. Kang X (1996) The features of climate change in the Qinghai–Tibetan Plateau region in the past 40 years. J Glaciol Geocryol 18(Suppl. 1):281–288Google Scholar
  24. Kendall MM, Boone AD (2006) The order Methanosarciales. Prokaryotes 3:244–256CrossRefGoogle Scholar
  25. Lawrence DM, Slater AG (2005) A projection of severe near-surface permafrost degradation during the 21st century. Geophys Res Lett 32:1–5Google Scholar
  26. Liebner S, Ganzert L, Kiss A, Yang S, Wagner D, Svenning MM (2015) Shifts in methanogenic community composition and methane fluxes along the degradation of discontinuous permafrost. Front Microbiol 6:1–10CrossRefGoogle Scholar
  27. Luton PE, Wayne JM, Sharp RJ, Riley PW (2002) The mcrA gene as an alternative to 16S rRNA in the phylogenetic analysis of methanogen population in landfill. Microbiology 148:3521–3530CrossRefPubMedGoogle Scholar
  28. Mackelprang R, Waldrop MP, DeAngelis KM, David MM, Chavarria KL, Blazewicz SJ, Rubin EM, Jansson JK (2011) Metagenomic analysis of a permafrost microbial community reveals a rapid response to thaw. Nature 2011:368–371CrossRefGoogle Scholar
  29. McCalley CK, Woodcroroft BJ, Hodgkins SB, Wehr RA, Kim EH, Mondav R, Crill PM, Chanton JP, Rich VI, Tyson GW, Saleska SR (2014) Methane dynamics regulated by microbial community response to permafrost thaw. Nature 514:478–481CrossRefPubMedGoogle Scholar
  30. McGuire AD, Anderson LG, Christensen TR, Dallimore S, Guo L, Hayes DL, Heimann M, Lorenson TD, Macdonald RW, Roulet N (2009) Sensitivity of the carbon cycle in the Arctic to climate change. Ecol Monogr 79:523–555CrossRefGoogle Scholar
  31. Meng J, Xu J, Qin D, He Y, Xiao X, Wang F (2014) Genetic and functional properties of uncultivated MCG archaea assessed by metagenome and gene expression analysis. ISME J 8:650–659CrossRefPubMedGoogle Scholar
  32. Metje M, Frenzel P (2005) Effect of temperature on anaerobic ethanol oxidation and methanogenesis in acidic peat from a northern wetland. Appl Environ Microbiol 71:8191–8200CrossRefPubMedPubMedCentralGoogle Scholar
  33. Mondav R, Woodcroft B, Kim EH, McCalley CK, Hodgkins SB, Crill PM et al (2014) Discovery of a novel methanogen prevalent in thawing permafrost. Nat Commun 5:3212CrossRefPubMedGoogle Scholar
  34. Nunoura T, Oida H, Miyazaki J, Miyashita A, Imachi H, Takai K (2008) Quantification of mcrA by fluorescent PCR in methanogenic and methanotrophic microbial communities. FEMS Microbiol Ecol 64:240–247CrossRefPubMedGoogle Scholar
  35. Ochsenreiter T, Selezi D, Quaiser A, Bonch-Osmolovskaya L, Schleper C (2003) Diversity and abundance of Crenarchaeota in terrestrial habitats studied by 16S RNA surveys and real time PCR. Environ Microbiol 5:787–797CrossRefPubMedGoogle Scholar
  36. Osterkamp TE, Viereck L, Shur Y, Jorgensons MT, Racine C, Doyle A, Boone RD (2000) Observations of thermokarst and its impact on boreal forests in Alaska, USA. Arct Antarct Alp Res 32:303–315CrossRefGoogle Scholar
  37. Rivkina E, Shcherbakova V, Laurinavichius K, Petrovskaya L, Krivushin K, Kraev G, Pecheritsina S, Gilichinsky D (2007) Biogeochemistry of methane and methanogenic archaea in permafrost. FEMS Microbiol Ecol 61:1–15CrossRefPubMedGoogle Scholar
  38. Sakai S, Imachi H, Hanada S, Ohashi A, Harada H, Kamagata Y (2008) Methanocella paludicola gen. nov., sp. nov., a methane-producing archaeon, the first isolate of the lineage ‘Rice Cluster I’, and proposal of the new archaeal order Methanocellales ord. nov. Int J Syst Evol Microbiol 58:926–936CrossRefGoogle Scholar
  39. Schloss PD, Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71:1501–1506CrossRefPubMedPubMedCentralGoogle Scholar
  40. Schloss PD, Westcott SI, Ryabin T, Hall JR, Hartmann M, Hollister EB et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541CrossRefPubMedPubMedCentralGoogle Scholar
  41. Schuur EAG, Bockheim J, Canadell JG, Euskirchen E, Field CB, Goryachkin SV et al (2008) Vulnerability of permafrost carbon to climate change: implications for the global carbon cycle. Bioscience 58:701–714CrossRefGoogle Scholar
  42. Schuur EAG, Vogel JG, Crummer KG, Lee H, Sickman JO, Osterkamp TE (2009) The effect of permafrost thaw on old carbon release and net carbon exchange from tundra. Nature 459:556–559CrossRefPubMedGoogle Scholar
  43. Smith LC, MacDonald GM, Velichko AA, Beilman WD, Borisova OK, Frey KE, Kremenetski KV, Sheng Y (2004) Siberian peatlands: a net carbon sink and global methane source since the early Holocene. Science 303:353–356CrossRefPubMedGoogle Scholar
  44. Steven B, Leveille R, Pollard WH, Whyte LG (2006) Microbial ecology and biodiversity in permafrost. Extremophiles 10:259–267CrossRefPubMedGoogle Scholar
  45. Steven B, Wayne HP, Charles WG, Lyle GW (2008) Microbial diversity and activity through a permafrost/ground ice core profile from the Canadian high Arctic. Environ Microbiol 10:3388–3403CrossRefPubMedGoogle Scholar
  46. Sturn M, Racine C, Tape K (2001) Climate change: increasing shrub abundance in the Arctic. Nature 411:546–547CrossRefGoogle Scholar
  47. Takai K, Horikoshi K (2000) Rapid detection and quantification of members of the archaeal community by quantitative PCR using fluorogenic probes. Appl Environ Microbiol 66:5066–5072CrossRefPubMedPubMedCentralGoogle Scholar
  48. Vitt DH, Halsey LA, Zoltai SC (2000) The changing landscape of Canada’s western boreal forest: the current dynamics of permafrost. Can J For Res 30:283–287CrossRefGoogle Scholar
  49. Wagner D (2008) Microbial communities and processes in Arctic permafrost environments. In: Dion P, Nautiyal CS (eds) Microbiology of extreme soils. Springer, Berlin, pp 133–154CrossRefGoogle Scholar
  50. Wagner D, Kobabe S, Pfeiffer EM, Hubberten HW (2003) Microbial controls on methane fluxes from a polygonal tundra of the Lena Delta, Siberia. Permafr Periglac 14:173–185CrossRefGoogle Scholar
  51. Wang G, Qian J, Cheng G, Lai Y (2002) Soil organic carbon pool of grassland soils on the Qinghai–Tibetan Plateau and its global implication. Sci Total Environ 291:207–217CrossRefGoogle Scholar
  52. Wang P, Huang X, Pang S, Zhu Y, Lu Z, Zhuang S, Liu H, Yang K, Li B (2014) Geochemical dynamics of the gas hydrate system in the Qilian Mountain permafrost, Qinghai, Northwest China. Mar Petrol Geol 59:72–90CrossRefGoogle Scholar
  53. Wei S, Cui H, He H, Hu F, Su X, Zhu Y (2014) Diversity and distribution of Archaea community along a stratigraphic permafrost profile from Qinghai–Tibetan Plateau, China. Archaea 2014. (Article ID240817)Google Scholar
  54. Woo MK (1992) Impacts of climatic variability and change on Canadian wetlands. Can Water Resour J 17:63–69CrossRefGoogle Scholar
  55. Yang M, Nelson FE, Shiklomanov NI, Guo D, Wan G (2010a) Permafrost degradation and its environmental effects on the Tibetan Plateau: a review of recent research. Earth Sci Rev 103:31–44CrossRefGoogle Scholar
  56. Yang ZP, Ou YH, Xu XL, Zhao L, Song MH, Zhou CP (2010b) Effects of permafrost degradation on ecosystem. Acta Ecol Sin 30:33–39CrossRefGoogle Scholar
  57. Zhang T, Barry RG, Knowles K, Heginbottom JA, Brown J (1999) Statistic and characteristics of permafrost and ground-ice distribution in the Northern Hemisphere. Polar Geogr 23:132–154CrossRefGoogle Scholar
  58. Zimov SA, Schuur EAG, Chapin FS (2006) Permafrost and the global carbon budget. Science 312:1612–1613CrossRefPubMedGoogle Scholar

Copyright information

© Springer Japan KK, part of Springer Nature 2018

Authors and Affiliations

  • Shiping Wei
    • 1
    • 2
    Email author
  • Hongpeng Cui
    • 1
  • Youhai Zhu
    • 3
  • Zhenquan Lu
    • 3
  • Shouji Pang
    • 3
  • Shuai Zhang
    • 3
  • Hailiang Dong
    • 1
  • Xin Su
    • 1
    • 2
    Email author
  1. 1.State Key Laboratory of Biogeology and Environmental GeologyChina University of GeosciencesBeijingChina
  2. 2.School of Marine SciencesChina University of GeosciencesBeijingChina
  3. 3.Oil and Gas Survey, Geological SurveyBeijingChina

Personalised recommendations