1932

Abstract

Permanently frozen soil, or permafrost, covers a large portion of the Earth's terrestrial surface and represents a unique environment for cold-adapted microorganisms. As permafrost thaws, previously protected organic matter becomes available for microbial degradation. Microbes that decompose soil carbon produce carbon dioxide and other greenhouse gases, contributing substantially to climate change. Next-generation sequencing and other -omics technologies offer opportunities to discover the mechanisms by which microbial communities regulate the loss of carbon and the emission of greenhouse gases from thawing permafrost regions. Analysis of nucleic acids and proteins taken directly from permafrost-associated soils has provided new insights into microbial communities and their functions in Arctic environments that are increasingly impacted by climate change. In this article we review current information from various molecular -omics studies on permafrost microbial ecology and explore the relevance of these insights to our current understanding of the dynamics of permafrost loss due to climate change.

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2016-06-29
2024-04-18
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Literature Cited

  1. Åkerman HJ, Johansson M. 2008. Thawing permafrost and thicker active layers in sub-arctic Sweden. Permafr. Periglac. Process. 19:3279–92 [Google Scholar]
  2. Allison SD. 2012. A trait-based approach for modelling microbial litter decomposition. Ecol. Lett. 15:91058–70 [Google Scholar]
  3. Allison SD, Martiny JBH. 2008. Resistance, resilience, and redundancy in microbial communities. PNAS 105:Suppl. 111512–19 [Google Scholar]
  4. Anthony KMWA, Anthony P, Grosse G, Chanton J. 2012. Geologic methane seeps along boundaries of Arctic permafrost thaw and melting glaciers. Nat. Geosci. 5:419–26 [Google Scholar]
  5. Ayala-Del-Río HL, Chain PS, Grzymski JJ, Ponder MA, Ivanova N. et al. 2010. The genome sequence of Psychrobacter arcticus 273-4, a psychroactive Siberian permafrost bacterium, reveals mechanisms for adaptation to low-temperature growth. Appl. Environ. Microbiol. 76:72304–12 [Google Scholar]
  6. Balázsi G, van Oudenaarden A, Collins JJ. 2011. Cellular decision making and biological noise: from microbes to mammals. Cell 144:6910–25 [Google Scholar]
  7. Bárcena TG, Yde JC, Finster KW. 2010. Methane flux and high-affinity methanotrophic diversity along the chronosequence of a receding glacier in Greenland. Ann. Glaciol. 51:5623–31 [Google Scholar]
  8. Behl RJ. 2011. Glacial demise and methane's rise. PNAS 108:155925–26 [Google Scholar]
  9. Bhattacharyya S, Cameron-Smith P, Bergmann D, Reagan M, Elliott S, Moridis G. 2012. Tropospheric impact of methane emissions from clathrates in the Arctic Region. Atmos. Chem. Phys. Discuss. 12:1026477–502 [Google Scholar]
  10. Bouskill NJ, Tang J, Riley WJ, Brodie EL. 2012. Trait-based representation of biological nitrification: model development, testing, and predicted community composition. Front. Microbiol. 3:364 [Google Scholar]
  11. Bridgham SD, Cadillo Quiroz H, Keller JK, Zhuang Q. 2013. Methane emissions from wetlands: biogeochemical, microbial, and modeling perspectives from local to global scales. Glob. Change Biol. 19:51325–46 [Google Scholar]
  12. Bridgham SD, Updegraff K, Pastor J. 1998. Carbon, nitrogen, and phosphorus mineralization in northern wetlands. Ecology 79:51545–61 [Google Scholar]
  13. Brown CT, Hug LA, Thomas BC, Sharon I, Castelle CJ. et al. 2015. Unusual biology across a group comprising more than 15% of domain Bacteria. Nature 523:7559208–11 [Google Scholar]
  14. Canadell JG, Kirschbaum MUF, Kurz WA, Sanz M-J, Schlamadinger B, Yamagata Y. 2007. Factoring out natural and indirect human effects on terrestrial carbon sources and sinks. Environ. Sci. Policy 10:4370–84 [Google Scholar]
  15. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA. et al. 2011. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. PNAS 108:Suppl. 14516–22 [Google Scholar]
  16. Chauhan A, Layton AC, Vishnivetskaya TA, Williams D, Pfiffner SM. et al. 2014. Metagenomes from thawing low-soil-organic-carbon mineral cryosols and permafrost of the Canadian high Arctic. Genome Announc. 2:6e01217–14 [Google Scholar]
  17. Chistoserdova L, Kalyuzhnaya MG, Lidstrom ME. 2009. The expanding world of methylotrophic metabolism. Annu. Rev. Microbiol. 63:1477–99 [Google Scholar]
  18. Chourey K, Jansson J, VerBerkmoes N, Shah M, Chavarria KL. et al. 2010. Direct cellular lysis/protein extraction protocol for soil metaproteomics. J. Proteome Res. 9:126615–22 [Google Scholar]
  19. Chu H, Fierer N, Lauber CL, Caporaso JG, Knight R, Grogan P. 2010. Soil bacterial diversity in the Arctic is not fundamentally different from that found in other biomes. Environ. Microbiol. 12:112998–3006 [Google Scholar]
  20. Collett TS, Dallimore SR. 2000. Permafrost-associated gas hydrate. Natural Gas Hydrate in Oceanic and Permafrost Environments 5 MD Max 43–60 Dordrecht, Neth: Springer [Google Scholar]
  21. Conrad R. 1999. Contribution of hydrogen to methane production and control of hydrogen concentrations in methanogenic soils and sediments. FEMS Microbiol. Ecol. 28:3193–202 [Google Scholar]
  22. Coolen MJL, Orsi WD. 2015. The transcriptional response of microbial communities in thawing Alaskan permafrost soils. Front. Microbiol. 6:197 [Google Scholar]
  23. Dmitriev VV, Suzina NE, Rusakova TG, Gilichinskii DA, Duda VI. 2001. Ultrastructural characteristics of natural forms of microorganisms isolated from permafrost grounds of Eastern Siberia by the method of low-temperature fractionation. Dokl. Biol. Sci. 378:1304–6 [Google Scholar]
  24. Duddleston KN, Kinney MA, Kiene RP, Hines ME. 2002. Anaerobic microbial biogeochemistry in a northern bog: acetate as a dominant metabolic end product. Glob. Biogeochem. Cycles 16:41063 [Google Scholar]
  25. Elberling B, Christiansen HH, Hansen BU. 2010. High nitrous oxide production from thawing permafrost. Nat. Geosci. 3:5332–35 [Google Scholar]
  26. Elberling B, Jakobsen BH, Berg P, Søndergaard J, Sigsgaard C. 2004. Influence of vegetation, temperature, and water content on soil carbon distribution and mineralization in four high Arctic soils. Arct. Antarct. Alp. Res. 36:4528–38 [Google Scholar]
  27. Elberling B, Michelsen A, Schädel C, Schuur EAG, Christiansen HH. et al. 2013. Long-term CO2 production following permafrost thaw. Nat. Clim. Change 3:10890–94 [Google Scholar]
  28. Elliott S, Reagan M, Moridis G, Smith PC. 2010. Geochemistry of clathrate-derived methane in Arctic ocean waters. Geophys. Res. Lett. 37:12L12607 [Google Scholar]
  29. Euskirchen ES, Bret-Harte MS, Scott GJ, Edgar C, Shaver GR. 2012. Seasonal patterns of carbon dioxide and water fluxes in three representative tundra ecosystems in northern Alaska. Ecosphere 3:14 [Google Scholar]
  30. Fierer N, Leff JW, Adams BJ, Nielsen UN, Bates ST. et al. 2012. Cross-biome metagenomic analyses of soil microbial communities and their functional attributes. PNAS 109:5221390–95 [Google Scholar]
  31. Friedlingstein P, Meinshausen M, Arora VK, Jones CD, Anav A. et al. 2014. Uncertainties in CMIP5 climate projections due to carbon cycle feedbacks. J. Clim. 27:2511–26 [Google Scholar]
  32. Friend AD, Lucht W, Rademacher TT, Keribin R, Betts R. et al. 2014. Carbon residence time dominates uncertainty in terrestrial vegetation responses to future climate and atmospheric CO2. PNAS 111:93280–85 [Google Scholar]
  33. Gilichinsky D, Vishnivetskaya T, Petrova M, Spirina E, Mamykin V, Rivkina E. 2008. Bacteria in the permafrost. Psychrophiles: From Biodiversity to Biotechnology R Margesin, F Schinner, J-C Marx, C Gerday 83–102 Berlin/Heidelberg: Springer [Google Scholar]
  34. Green JL, Bohannan BJM, Whitaker RJ. 2008. Microbial biogeography: from taxonomy to traits. Science 320:58791039–43 [Google Scholar]
  35. Hall EK, Neuhauser C, Cotner JB. 2008. Toward a mechanistic understanding of how natural bacterial communities respond to changes in temperature in aquatic ecosystems. ISME J 2:5471–81 [Google Scholar]
  36. Handelsman J, Rondon MR, Brady SF, Clardy J, Goodman RM. 1998. Molecular biological access to the chemistry of unknown soil microbes: a new frontier for natural products. Chem. Biol. 5:10R245–49 [Google Scholar]
  37. Hanemaaijer M, Röling WFM, Olivier BG, Khandelwal RA, Teusink B, Bruggeman FJ. 2015. Systems modeling approaches for microbial community studies: from metagenomics to inference of the community structure. Front. Microbiol. 6:213 [Google Scholar]
  38. Hansen AA, Herbert RA, Mikkelsen K, Jensen LL, Kristoffersen T. et al. 2007. Viability, diversity and composition of the bacterial community in a high Arctic permafrost soil from Spitsbergen, Northern Norway. Environ. Microbiol. 9:112870–84 [Google Scholar]
  39. Hayes DJ, Kicklighter DW, McGuire AD, Chen M, Zhuang Q. et al. 2014. The impacts of recent permafrost thaw on land-atmosphere greenhouse gas exchange. Environ. Res. Lett. 9:4045005 [Google Scholar]
  40. Hayes DJ, McGuire AD, Kicklighter DW. 2011. Is the northern high-latitude land-based CO2 sink weakening?. Glob. Biogeochem. Cycles 25:GB3018 [Google Scholar]
  41. Hines ME, Duddleston KN, Rooney Varga JN, Fields D, Chanton JP. 2008. Uncoupling of acetate degradation from methane formation in Alaskan wetlands: connections to vegetation distribution. Glob. Biogeochem. Cycles 22:2GB2017 [Google Scholar]
  42. Hinzman LD, Deal CJ, McGuire AD, Mernild SH, Polyakov IV, Walsh JE. 2013. Trajectory of the Arctic as an integrated system. Ecol. Appl. 23:81837–68 [Google Scholar]
  43. Hodgkins SB, Chanton JP, Langford LC, McCalley CK, Saleska SR. et al. 2015. Soil incubations reproduce field methane dynamics in a subarctic wetland. Biogeochemistry 126:1–2241–49 [Google Scholar]
  44. Hodgkins SB, Tfaily MM, McCalley CK, Logan TA, Crill PM. et al. 2014. Changes in peat chemistry associated with permafrost thaw increase greenhouse gas production. PNAS 111:165819–24 [Google Scholar]
  45. Hollesen J, Matthiesen H, Moller AJ, Elberling B. 2015. Permafrost thawing in organic Arctic soils accelerated by ground heat production. Nat. Clim. Change 5:574–78 [Google Scholar]
  46. Hultman J, Waldrop MP, Mackelprang R, David MM, McFarland J. et al. 2015. Multi-omics of permafrost, active layer and thermokarst bog soil microbiomes. Nature 521:7551208–12 [Google Scholar]
  47. Imelfort M, Parks D, Woodcroft BJ, Dennis P, Hugenholtz P, Tyson GW. 2014. GroopM: an automated tool for the recovery of population genomes from related metagenomes. PeerJ 2:e603 [Google Scholar]
  48. IPCC (Intergov. Panel Clim. Change) 2013. Near-term climate change: projections and predictability. Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change TF Stocker, D Qin, GK Plattner, M Tignor, SK Allen 953–1028 Cambridge, UK: Cambridge Univ. Press [Google Scholar]
  49. Jafarov EE, Marchenko SS, Romanovsky VE. 2012. Numerical modeling of permafrost dynamics in Alaska using a high spatial resolution dataset. Cryosphere Discuss. 6:189–124 [Google Scholar]
  50. Jansson JK, Taş N. 2014. The microbial ecology of permafrost. Nat. Rev. Microbiol. 12:6414–25 [Google Scholar]
  51. Johansson T, Malmer N, Crill PM, Fridborg T, Åkerman JH. et al. 2006. Decadal vegetation changes in a northern peatland, greenhouse gas fluxes and net radiative forcing. Glob. Change Biol. 12:122352–69 [Google Scholar]
  52. Johnstone JF, Hollingsworth TN, Chapin FS III, Mack MC. 2010. Changes in fire regime break the legacy lock on successional trajectories in Alaskan boreal forest. Glob. Change Biol. 16:41281–95 [Google Scholar]
  53. Jørgensen CJ, Johansen KML, Westergaard-Nielsen A, Elberling B. 2015. Net regional methane sink in High Arctic soils of northeast Greenland. Nat. Geosci. 8:120–23 [Google Scholar]
  54. Kasischke ES, Turetsky MR. 2006. Recent changes in the fire regime across the North American boreal region: spatial and temporal patterns of burning across Canada and Alaska. Geophys. Res. Lett. 33:9L09703 [Google Scholar]
  55. Keller JK, Bridgham SD. 2007. Pathways of anaerobic carbon cycling across an ombrotrophic-minerotrophic peatland gradient. Limnol. Oceanogr. 52:196–107 [Google Scholar]
  56. Kennedy M, Mrofka D, von der Borch C. 2008. Snowball Earth termination by destabilization of equatorial permafrost methane clathrate. Nature 453:7195642–45 [Google Scholar]
  57. Khalil MAK, Rasmussen RA. 1989. Climate-induced feedbacks for the global cycles of methane and nitrous oxide. Tellus B 41B:5554–59 [Google Scholar]
  58. Khvorostyanov DV, Krinner G, Ciais P, Heimann M, Zimov SA. 2008. Vulnerability of permafrost carbon to global warming. Part I: model description and role of heat generated by organic matter decomposition. Tellus B 60:2250–64 [Google Scholar]
  59. Knittel K, Boetius A. 2009. Anaerobic oxidation of methane: progress with an unknown process. Annu. Rev. Microbiol. 63:1311–34 [Google Scholar]
  60. Knowlton C, Veerapaneni R, D'Elia T, Rogers SO. 2013. Microbial analyses of ancient ice core sections from Greenland and Antarctica. Biology 2:1206–32 [Google Scholar]
  61. Kolb S. 2009. Aerobic methanol-oxidizing Bacteria in soil. FEMS Microbiol. Lett. 300:11–10 [Google Scholar]
  62. Koven CD, Riley WJ, Subin ZM, Tang JY, Torn MS. et al. 2013. The effect of vertically resolved soil biogeochemistry and alternate soil C and N models on C dynamics of CLM4. Biogeosciences 10:117109–31 [Google Scholar]
  63. Kvenvolden KA, Lorenson TD. 1993. Methane in permafrost: preliminary results from coring at Fairbanks, Alaska. Chemosphere 26:1–4609–16 [Google Scholar]
  64. Lantuit H, Overduin PP, Couture N, Wetterich S, Aré F. et al. 2011. The Arctic Coastal Dynamics Database: a new classification scheme and statistics on Arctic permafrost coastlines. Estuaries Coasts 35:2383–400 [Google Scholar]
  65. Lau MCY, Stackhouse BT, Layton AC, Chauhan A, Vishnivetskaya TA. et al. 2015. An active atmospheric methane sink in high Arctic mineral cryosols. ISME J 9:1880–91 [Google Scholar]
  66. Lauber CL, Hamady M, Knight R, Fierer N. 2009. Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl. Environ. Microbiol. 75:155111–20 [Google Scholar]
  67. Lawrence DM, Oleson KW, Flanner MG, Thornton PE, Swenson SC. et al. 2011. Parameterization improvements and functional and structural advances in Version 4 of the Community Land Model. J. Adv. Model. Earth Syst. 3:1M03001 [Google Scholar]
  68. Lee H, Schuur EAG, Inglett KS, Lavoie M, Chanton JP. 2012. The rate of permafrost carbon release under aerobic and anaerobic conditions and its potential effects on climate. Glob. Change Biol. 18:2515–27 [Google Scholar]
  69. Lehmann J, Joseph S. 2009. Biochar for Environmental Management: Science and Technology. Abingdon, UK: Routledge
  70. Liebner S, Rublack K, Stuehrmann T, Wagner D. 2008. Diversity of aerobic methanotrophic bacteria in a permafrost active layer soil of the Lena Delta, Siberia. Microb. Ecol. 57:125–35 [Google Scholar]
  71. Lipson DA, Haggerty JM, Srinivas A, Raab TK, Sathe S, Dinsdale EA. 2013. Metagenomic insights into anaerobic metabolism along an Arctic peat soil profile. PLOS ONE 8:5e64659 [Google Scholar]
  72. Lunt DJ, Ridgwell A, Sluijs A, Zachos J, Hunter S, Haywood A. 2011. A model for orbital pacing of methane hydrate destabilization during the Palaeogene. Nat. Geosci. 4:11775–78 [Google Scholar]
  73. Mackelprang R, Waldrop MP, DeAngelis KM, David MM, Chavarria KL. et al. 2011. Metagenomic analysis of a permafrost microbial community reveals a rapid response to thaw. Nature 480:7377368–71 [Google Scholar]
  74. Manzoni S, Porporato A. 2009. Soil carbon and nitrogen mineralization: theory and models across scales. Soil Biol. Biochem. 41:71355–79 [Google Scholar]
  75. Maslin M, Owen M, Betts R, Day S, Dunkley Jones T, Ridgwell A. 2010. Gas hydrates: past and future geohazard?. Philos. Trans. R. Soc. A 368:2369–93 [Google Scholar]
  76. Matthiesen H, Jensen JB, Gregory D, Hollesen J, Elberling B. 2014. Degradation of archaeological wood under freezing and thawing conditions: effects of permafrost and climate change. Archaeometry 56:3479–95 [Google Scholar]
  77. McCalley CK, Woodcroft BJ, Hodgkins SB, Wehr RA, Kim E-H. et al. 2014. Methane dynamics regulated by microbial community response to permafrost thaw. Nature 514:7523478–81 [Google Scholar]
  78. McGill BJ, Enquist BJ, Weiher E, Westoby M. 2006. Rebuilding community ecology from functional traits. Trends Ecol. Evol. 21:4178–85 [Google Scholar]
  79. McGuire AD, Anderson LG, Christensen TR. 2009. Sensitivity of the carbon cycle in the Arctic to climate change. Biogeosciences 79:4523–55 [Google Scholar]
  80. Megonigal JP, Hines ME, Visscher PT. 2003. Anaerobic metabolism: linkages to trace gases and aerobic processes. Treatise on Geochemistry 8 Biogeochemistry HD Holland, KK Turekian 317–424 Amsterdam, Neth: Elsevier [Google Scholar]
  81. Melton JR, Wania R, Hodson EL, Poulter B, Ringeval B. et al. 2013. Present state of global wetland extent and wetland methane modelling: conclusions from a model intercomparison project (WETCHIMP). Biogeosciences 10:2753–88 [Google Scholar]
  82. Meng L, Paudel R, Hess PGM, Mahowald NM. 2015. Seasonal and interannual variability in wetland methane emissions simulated by CLM4Me′ and CAM-chem and comparisons to observations of concentrations. Biogeosciences 12:134029–49 [Google Scholar]
  83. Mondav R, Woodcroft BJ, Kim E-H, McCalley CK, Hodgkins SB. et al. 2014. Discovery of a novel methanogen prevalent in thawing permafrost. Nat. Commun. 5:3212 [Google Scholar]
  84. Montzka SA, Dlugokencky EJ, Butler JH. 2011. Non-CO2 greenhouse gases and climate change. Nature 476:735843–50 [Google Scholar]
  85. Mykytczuk NCS, Foote SJ, Omelon CR, Southam G, Greer CW, Whyte LG. 2013. Bacterial growth at −15°C; molecular insights from the permafrost bacterium Planococcus halocryophilus Or1. ISME J 7:61211–26 [Google Scholar]
  86. Myrold DD, Zeglin LH, Jansson JK. 2014. The potential of metagenomic approaches for understanding soil microbial processes. Soil Sci. Soc. Am. J. 78:13–10 [Google Scholar]
  87. Neumann RB, Blazewicz SJ, Conaway CH, Turetsky MR, Waldrop MP. 2016. Modeling CH4 and CO2 cycling using porewater stable isotopes in a thermokarst bog in Interior Alaska: results from three conceptual reaction networks. Biogeochemistry 127:157–87 [Google Scholar]
  88. Nicora CD, Anderson BJ, Callister SJ, Norbeck AD, Purvine SO. et al. 2013. Amino acid treatment enhances protein recovery from sediment and soils for metaproteomic studies. Proteomics 13:18–192776–85 [Google Scholar]
  89. Nossov DR, Torre Jorgenson M, Kielland K, Kanevskiy MZ. 2013. Edaphic and microclimatic controls over permafrost response to fire in interior Alaska. Environ. Res. Lett. 8:3035013 [Google Scholar]
  90. Nozhevnikova AN, Simankova MV, Parshina SN, Kotsyurbenko OR. 2001. Temperature characteristics of methanogenic archaea and acetogenic bacteria isolated from cold environments. Water Sci. Technol. 44:841–48 [Google Scholar]
  91. Oechel WC, Laskowski CA, Burba G, Gioli B, Kalhori AAM. 2014. Annual patterns and budget of CO2 flux in an Arctic tussock tundra ecosystem. J. Geophys. Res. Biogeosci. 119:3323–39 [Google Scholar]
  92. Op den Camp HJM, Islam T, Stott MB, Harhangi HR, Hynes A. et al. 2009. Environmental, genomic and taxonomic perspectives on methanotrophic Verrucomicrobia. Environ. Microbiol. Rep. 1:5293–306 [Google Scholar]
  93. Pan C, Banfield JF. 2014. Quantitative metaproteomics: functional insights into microbial communities. Methods Mol. Biol. 1096:231–40 [Google Scholar]
  94. Panikov NS. 2009. Microbial activity in frozen soils. Permafrost Soils R Margesin 119–47 Berlin/Heidelberg: Springer [Google Scholar]
  95. Price ND, Reed JL, Palsson . 2004. Genome-scale models of microbial cells: evaluating the consequences of constraints. Nat. Rev. Microbiol. 2:11886–97 [Google Scholar]
  96. Pries CH, Schuur E. 2013. Thawing permafrost increases old soil and autotrophic respiration in tundra: partitioning ecosystem respiration using δ13C and Δ14C. Glob. Change Biol. 19:2649–61 [Google Scholar]
  97. Qian H, Joseph R, Zeng N. 2010. Enhanced terrestrial carbon uptake in the Northern High Latitudes in the 21st century from the Coupled Carbon Cycle Climate Model Intercomparison Project model projections. Glob. Change Biol. 16:2641–56 [Google Scholar]
  98. Rasmussen RA, Khalil MAK, Moraes F. 1993. Permafrost methane content: 1. Experimental data from sites in northern Alaska. Chemosphere 26:1–4591–94 [Google Scholar]
  99. Riley WJ, Subin ZM, Lawrence DM. 2011. Barriers to predicting changes in global terrestrial methane fluxes: analyses using CLM4Me, a methane biogeochemistry model integrated in CESM. Biogeosciences 8:1925–53 [Google Scholar]
  100. Riseborough D, Shiklomanov N, Etzelmüller B, Gruber S, Marchenko S. 2008. Recent advances in permafrost modelling. Permafr. Periglac. Process. 19:2137–56 [Google Scholar]
  101. Rivkina EM, Friedmann EI, McKay CP, Gilichinsky DA. 2000. Metabolic activity of permafrost bacteria below the freezing point. Appl. Environ. Microbiol. 66:83230–33 [Google Scholar]
  102. Rivkina EM, Gilichinsky D, Wagener S, Tiedje J, McGrath J. 1998. Biogeochemical activity of anaerobic microorganisms from buried permafrost sediments. Geomicrobiol. J. 15:3187–93 [Google Scholar]
  103. Rivkina EM, Laurinavichus KS, Gilichinsky DA, Shcherbakova VA. 2002. Methane generation in permafrost sediments. Dokl. Biol. Sci. 383:1179–81 [Google Scholar]
  104. Rivkina EM, Shcherbakova V, Laurinavichius K, Petrovskaya L, Krivushin K. et al. 2007. Biogeochemistry of methane and methanogenic archaea in permafrost. FEMS Microbiol. Ecol. 61:11–15 [Google Scholar]
  105. Roden EE, Wetzel RG. 1996. Organic carbon oxidation and suppression of methane production by microbial Fe(III) oxide reduction in vegetated and unvegetated freshwater wetland sediments. Limnol. Oceanogr. 41:81733–48 [Google Scholar]
  106. Rodrigues DF, Ivanova N, He Z, Huebner M, Zhou J, Tiedje JM. 2008. Architecture of thermal adaptation in an Exiguobacterium sibiricum strain isolated from 3 million year old permafrost: a genome and transcriptome approach. BMC Genom 9:1547 [Google Scholar]
  107. Rodrigues DF, Tiedje JM. 2008. Coping with our cold planet. Appl. Environ. Microbiol. 74:61677–86 [Google Scholar]
  108. Romanovsky VE, Smith SL, Christiansen HH. 2010. Permafrost thermal state in the polar Northern Hemisphere during the international polar year 2007–2009: a synthesis. Permafr. Periglac. Process. 21:2106–16 [Google Scholar]
  109. Schuur EAG, Bockheim J, Canadell JG, Euskirchen E, Field CB. et al. 2008. Vulnerability of permafrost carbon to climate change: implications for the global carbon cycle. BioScience 58:8701–14 [Google Scholar]
  110. Schuur EAG, McGuire AD, Schädel C, Grosse G, Harden JW. et al. 2015. Climate change and the permafrost carbon feedback. Nature 520:7546171–79 [Google Scholar]
  111. Sitch S, Smith B, Prentice IC, Arneth A, Bondeau A. et al. 2003. Evaluation of ecosystem dynamics, plant geography and terrestrial carbon cycling in the LPJ dynamic global vegetation model. Glob. Change Biol. 9:2161–85 [Google Scholar]
  112. Smith SL, Romanovsky VE, Lewkowicz AG, Burn CR, Allard M. et al. 2010. Thermal state of permafrost in North America: a contribution to the international polar year. Permafr. Periglac. Process. 21:2117–35 [Google Scholar]
  113. Steven B, Briggs G, McKay CP, Pollard WH, Greer CW, Whyte LG. 2007. Characterization of the microbial diversity in a permafrost sample from the Canadian high Arctic using culture-dependent and culture-independent methods. FEMS Microbiol. Ecol. 59:2513–23 [Google Scholar]
  114. Subin ZM, Koven CD, Riley WJ, Torn MS, Lawrence DM, Swenson SC. 2012. Effects of soil moisture on the responses of soil temperatures to climate change in cold regions. J. Clim. 26:3139–58 [Google Scholar]
  115. Tarnocai C, Canadell JG, Schuur EAG, Kuhry P, Mazhitova G, Zimov S. 2009. Soil organic carbon pools in the northern circumpolar permafrost region. Glob. Biogeochem. Cycles 23:2GB2023 [Google Scholar]
  116. Taş N, Prestat E, McFarland JW, Wickland KP, Knight R. et al. 2014. Impact of fire on active layer and permafrost microbial communities and metagenomes in an upland Alaskan boreal forest. ISME J. 8:91904–19 [Google Scholar]
  117. Thonicke K, Spessa A, Prentice IC, Harrison SP. 2010. The influence of vegetation, fire spread and fire behaviour on biomass burning and trace gas emissions: results from a process-based model. Biogeosciences 7:61991–2011 [Google Scholar]
  118. Tian H, Xu X, Liu M, Ren W, Zhang C. et al. 2010. Spatial and temporal patterns of CH4 and N2O fluxes in terrestrial ecosystems of North America during 1979–2008: application of a global biogeochemistry model. Biogeosciences 7:92673–94 [Google Scholar]
  119. Todd-Brown KEO, Hopkins FM, Kivlin SN, Talbot JM, Allison SD. 2012. A framework for representing microbial decomposition in coupled climate models. Biogeochemistry 109:1–319–33 [Google Scholar]
  120. Tringe SG, Hugenholtz P. 2008. A renaissance for the pioneering 16S rRNA gene. Curr. Opin. Microbiol. 11:5442–46 [Google Scholar]
  121. Tveit AT, Schwacke R, Svenning MM, Urich T. 2012. Organic carbon transformations in high-Arctic peat soils: key functions and microorganisms. ISME J. 7:2299–311 [Google Scholar]
  122. Tveit AT, Urich T, Frenzel P, Svenning MM. 2015. Metabolic and trophic interactions modulate methane production by Arctic peat microbiota in response to warming. PNAS 112:19E2507–16 [Google Scholar]
  123. Tyson GW, Chapman J, Hugenholtz P, Allen EE, Ram RJ. et al. 2004. Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428:697837–43 [Google Scholar]
  124. Updegraff K, Bridgham SD, Pastor J, Weishampel P, Harth C. 2001. Response of CO2 and CH4 emissions in peatlands to warming and water-table manipulation. Ecol. Appl. 11:2311–26 [Google Scholar]
  125. Varin T, Lovejoy C, Jungblut AD, Vincent WF, Corbeil J. 2012. Metagenomic analysis of stress genes in microbial mat communities from Antarctica and the High Arctic. Appl. Environ. Microbiol. 78:2549–59 [Google Scholar]
  126. Vatsurina A, Badrutdinova D, Schumann P, Spring S, Vainshtein M. 2008. Desulfosporosinus hippei sp. nov., a mesophilic sulfate-reducing bacterium isolated from permafrost. Int. J. Syst. Evol. Microbiol. 58:Pt. 51228–32 [Google Scholar]
  127. Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D. et al. 2004. Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:566766–74 [Google Scholar]
  128. Wadham JL, Arndt S, Tulaczyk S, Stibal M, Tranter M. et al. 2012. Potential methane reservoirs beneath Antarctica. Nature 488:7413633–37 [Google Scholar]
  129. Wagner D. 2008. Microbial communities and processes in Arctic permafrost environments. Microbiology of Extreme Soils P Dion, CS Nautiyal 133–54 Berlin/Heidelberg: Springer [Google Scholar]
  130. Waldrop MP, Wickland KP, White R III, Berhe AA, Harden JW, Romanovsky VE. 2010. Molecular investigations into a globally important carbon pool: permafrost-protected carbon in Alaskan soils. Glob. Change Biol.162543–54
  131. Wania R, Melton JR, Hodson EL, Poulter B, Ringeval B. et al. 2013. Present state of global wetland extent and wetland methane modelling: methodology of a model inter-comparison project (WETCHIMP). Geosci. Model. Dev. 6:3617–41 [Google Scholar]
  132. Whiting GJ, Chanton JP. 1993. Primary production control of methane emission from wetlands. Nature 364:6440794–95 [Google Scholar]
  133. Wieder WR, Bonan GB, Allison SD. 2013. Global soil carbon projections are improved by modelling microbial processes. Nat. Clim. Change 3:10909–12 [Google Scholar]
  134. Willerslev E, Hansen AJ, Ronn R, Brand TB, Barnes I. et al. 2004. Long-term persistence of bacterial DNA. Curr. Biol. 14:1R9–10 [Google Scholar]
  135. Woese CR, Fox GE. 1977. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. PNAS 74:115088–90 [Google Scholar]
  136. Ye R, Jin Q, Bohannan B, Keller JK, McAllister SA, Bridgham SD. 2012. pH controls over anaerobic carbon mineralization, the efficiency of methane production, and methanogenic pathways in peatlands across an ombrotrophic-minerotrophic gradient. Soil Biol. Biochem. 54:36–47 [Google Scholar]
  137. Yergeau E, Hogues HE, Whyte LG, Greer CW. 2010. The functional potential of high Arctic permafrost revealed by metagenomic sequencing, qPCR and microarray analyses. ISME J 4:91206–14 [Google Scholar]
  138. Zhang C, Stapleton RD, Zhou J, Palumbo AV, Phelps TJ. 1999. Iron reduction by psychrotrophic enrichment cultures. FEMS Microbiol. Ecol. 30:4367–71 [Google Scholar]
  139. Zhang D-C, Brouchkov A, Griva G, Schinner F, Margesin R. 2013a. Isolation and characterization of bacteria from ancient Siberian permafrost sediment. Biology 2:185–106 [Google Scholar]
  140. Zhang Y, Wang X, Fraser R, Olthof I, Chen W. et al. 2013b. Modelling and mapping climate change impacts on permafrost at high spatial resolution for an Arctic region with complex terrain. Cryosphere 7:41121–37 [Google Scholar]
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