Skip to main content

Advertisement

SpringerLink
Log in

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

  • Original Paper
  • Published:
Extremophiles Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Allison SD, Treseder KK (2011) Climate changes feedbacks to microbial decomposition in boreal soils. Fungal Ecol 4:362–374

    Article  Google Scholar 

  • Anisimov OA, Nelson FE (1996) Permafrost distribution in the Northern Hemisphere under scenarios of climatic change. Glob Planet Change 14:59–72

    Article  Google Scholar 

  • 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 511:452–456

    Article  CAS  PubMed  Google Scholar 

  • 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 82:287–302

    Article  CAS  PubMed  Google Scholar 

  • 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 310:657–660

    Article  CAS  PubMed  Google Scholar 

  • Christensen TR, Johansson T, Åkerman HJ, Mastepanov M (2004) Thawing sub-arctic permafrost: effects on vegetation and methane emissions. Geophys Res Lett 31:1–4

    Article  Google Scholar 

  • Conrad R, Erkel C, Liesack W (2006) Rice Cluster I methanogens, an important group of Archaea producing greenhouse gas in soil. Curr Opin Biotech 17:262–267

    Article  CAS  PubMed  Google Scholar 

  • Coolen MJL, Orsi WD (2015) The transcriptional response of microbial communities in thawing Alaskan permafrost soils. Front Microbiol 6:1–14

    Article  Google Scholar 

  • 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 13:2299–2314

    Article  CAS  PubMed  Google Scholar 

  • DeLong EF (1992) Archaea in coastal marine environments. PNAS 89:5685–5689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 24:222–234

    Article  CAS  PubMed  Google Scholar 

  • Ernakovich JG, Wallenstein MD (2015) Permafrost microbial community traits and functional diversity indicate low activity at in situ thaw temperatures. Soil Biol Biochem 87:78–89

    Article  CAS  Google Scholar 

  • Garcia JL, Ollivier B, Whitman WB (2006) The order Methanomicrobiales. Prokaryotes 3:208–230

    Article  Google Scholar 

  • Good IJ (1953) The population frequencies of species and estimation of population parameters. Biometrika 40:237–264

    Article  Google Scholar 

  • 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 6:709–712

    Article  CAS  PubMed  Google Scholar 

  • 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 64:4983–4989

    CAS  PubMed Central  Google Scholar 

  • 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 62:668–675

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 69:5483–5491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 521:208–212

    Article  CAS  PubMed  Google Scholar 

  • Jansson JK, Tas N (2014) The microbial ecology of permafrost. Nat Rev Microbiol 12:414–425

    Article  CAS  PubMed  Google Scholar 

  • Jin H, Wu J, Cheng G, Tomoko N, Sun G (1999) Methane emissions from wetlands on the Qinghai–Tibet Plateau. Chin Sci Bull 44:2282–2286

    Article  CAS  Google Scholar 

  • Jin HJ, Li SX, Wang SL, Zhao L (2000) Impact of climatic change on permafrost and cold regions environment in China. Acta Geogr Sin 55:161–173

    Google Scholar 

  • 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):281–288

    Google Scholar 

  • Kendall MM, Boone AD (2006) The order Methanosarciales. Prokaryotes 3:244–256

    Article  Google Scholar 

  • Lawrence DM, Slater AG (2005) A projection of severe near-surface permafrost degradation during the 21st century. Geophys Res Lett 32:1–5

    Google Scholar 

  • 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 6:1–10

    Article  Google Scholar 

  • 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 148:3521–3530

    Article  CAS  PubMed  Google Scholar 

  • 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 2011:368–371

    Article  Google Scholar 

  • 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 514:478–481

    Article  CAS  PubMed  Google Scholar 

  • 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 79:523–555

    Article  Google Scholar 

  • 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 8:650–659

    Article  CAS  PubMed  Google Scholar 

  • Metje M, Frenzel P (2005) Effect of temperature on anaerobic ethanol oxidation and methanogenesis in acidic peat from a northern wetland. Appl Environ Microbiol 71:8191–8200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 5:3212

    Article  PubMed  Google Scholar 

  • 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 64:240–247

    Article  CAS  PubMed  Google Scholar 

  • 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 5:787–797

    Article  CAS  PubMed  Google Scholar 

  • 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 32:303–315

    Article  Google Scholar 

  • 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 61:1–15

    Article  CAS  PubMed  Google Scholar 

  • 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 58:926–936

    Article  Google Scholar 

  • Schloss PD, Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71:1501–1506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 75:7537–7541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 58:701–714

    Article  Google Scholar 

  • 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 459:556–559

    Article  CAS  PubMed  Google Scholar 

  • 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 303:353–356

    Article  CAS  PubMed  Google Scholar 

  • Steven B, Leveille R, Pollard WH, Whyte LG (2006) Microbial ecology and biodiversity in permafrost. Extremophiles 10:259–267

    Article  PubMed  Google Scholar 

  • 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 10:3388–3403

    Article  CAS  PubMed  Google Scholar 

  • Sturn M, Racine C, Tape K (2001) Climate change: increasing shrub abundance in the Arctic. Nature 411:546–547

    Article  Google Scholar 

  • Takai K, Horikoshi K (2000) Rapid detection and quantification of members of the archaeal community by quantitative PCR using fluorogenic probes. Appl Environ Microbiol 66:5066–5072

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 30:283–287

    Article  Google Scholar 

  • Wagner D (2008) Microbial communities and processes in Arctic permafrost environments. In: Dion P, Nautiyal CS (eds) Microbiology of extreme soils. Springer, Berlin, pp 133–154

    Chapter  Google Scholar 

  • 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 14:173–185

    Article  Google Scholar 

  • 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 291:207–217

    Article  CAS  Google Scholar 

  • 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 59:72–90

    Article  Google Scholar 

  • 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)

  • Woo MK (1992) Impacts of climatic variability and change on Canadian wetlands. Can Water Resour J 17:63–69

    Article  Google Scholar 

  • 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 103:31–44

    Article  Google Scholar 

  • Yang ZP, Ou YH, Xu XL, Zhao L, Song MH, Zhou CP (2010b) Effects of permafrost degradation on ecosystem. Acta Ecol Sin 30:33–39

    Article  Google Scholar 

  • 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 23:132–154

    Article  Google Scholar 

  • Zimov SA, Schuur EAG, Chapin FS (2006) Permafrost and the global carbon budget. Science 312:1612–1613

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

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).

Author information

Authors and Affiliations

  1. State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, Beijing, 100083, China

    Shiping Wei, Hongpeng Cui, Hailiang Dong & Xin Su

  2. School of Marine Sciences, China University of Geosciences, Beijing, 100083, China

    Shiping Wei & Xin Su

  3. Oil and Gas Survey, Geological Survey, Beijing, 100029, China

    Youhai Zhu, Zhenquan Lu, Shouji Pang & Shuai Zhang

Authors
  1. Shiping Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hongpeng Cui
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Youhai Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhenquan Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shouji Pang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Shuai Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hailiang Dong
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Xin Su
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Shiping Wei or Xin Su.

Additional information

Communicated by A. Oren.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 934 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wei, S., Cui, H., Zhu, Y. et al. Shifts of methanogenic communities in response to permafrost thaw results in rising methane emissions and soil property changes. Extremophiles 22, 447–459 (2018). https://doi.org/10.1007/s00792-018-1007-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00792-018-1007-x

Keywords

Search

Navigation