Chapter 9 : Microbial Carbon Cycling in Permafrost

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Terrestrial and submarine permafrost is identified as one of the most vulnerable carbon pools on Earth. In some areas, permafrost comprises upwards of 80% ice in the form of large features, such as massive ice sheets many kilometers in length; or on smaller scales, such as ice wedges and ice lenses, and as ice that fills soil pore space. Residual pockets of seawater, from the subsidence of the polar ocean, exist as saturated, salt-rich permafrost environments known as salt lenses or cryopegs. All of these permafrost features sustain microbial communities that contribute to carbon cycling in polar regions. The way in which gas is released from permafrost, i.e., the rate and pathway, determines the ratio of methane and carbon dioxide emitted to the atmosphere. This chapter describes the different carbon pools, carbon fluxes, and freeze-thaw stresses related to microbial activities. It then examines methane-cycling communities in Arctic active-layer and permafrost environments. The fast recovery of the microbial activity during spring suggests that carbon mineralization in thawing Arctic sediment may rapidly respond to warming, resulting in substantial changes in microbial carbon cycling and growth of microbial populations. Environmental sequences from the Laptev Sea coast consist of four specific permafrost clusters. It was hypothesized that these clusters comprise methanogenic with a specific physiological potential to survive under harsh environmental conditions. A first study on submarine permafrost of the Laptev Sea shelf demonstrated that intact DNA was extractable from late Pleistocene permafrost deposits with an age of up to 111,000 years.

Citation: Vishnivetskaya T, Liebner S, Wilhelm R, Wagner D. 2012. Microbial Carbon Cycling in Permafrost, p 183-200. In Miller R, Whyte L (ed), Polar Microbiology: Life in a Deep Freeze. ASM Press, Washington, DC. doi: 10.1128/9781555817183.ch9

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Restriction Fragment Length Polymorphism
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1. Anisimov, O.,, and S. Reneva. 2006. Permafrost and changing climate: the Russian perspective. Ambio 35:169175.
2. Aselmann, I.,, and J. Crutzen. 1989. Global distribution of natural freshwater wetlands and rice paddies, their net primary productivity, seasonality and possible methane emissions. J. Atmos. Chem. 8:307358.
3. Belova, S. E.,, T. A. Pankratov,, and S. N. Dedysh. 2006. Bacteria of the genus Burkholderia as a typical component of the microbial community of sphagnum peat bogs. Microbiology 75:9096.
4. Berestovskaia, I.,, A. M. Lysenko,, T. P. Turova,, and L. V. Vasil’eva. 2006. A psychrotolerant Caulobacter sp. from Russian polar tundra soil. Mikrobiologiia 75:377382. (In Russian.)
5. Berestovskaya, Y. Y.,, L. V. Vasil’eva,, O. V. Chestnykh,, and G. A. Zavarzin. 2002. Methanotrophs of the psychrophilic microbial community of the Russian Arctic tundra. Microbiology 71:460466.
6. Biasi, C.,, O. Rusalimova,, H. Meyer,, C. Kaiser,, W. Wanek,, P. Barsukov,, H. Junger,, and A. Richter. 2005. Temperature-dependent shift from labile to recalcitrant carbon sources of arctic heterotrophs. Rapid Commun. Mass Spectrom. 19:14011408.
7. Boetius, A.,, K. Ravenschlag,, C. J. Schubert,, D. Rickert,, F. Widdel,, A. Gieseke,, R. Amann,, B. B. Jørgensen,, U. Witte,, and O. Pfannkuche. 2000. A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature 407:623626.
8. Bölter, M.,, N. Soethe,, R. Horn,, and C. Uhlig. 2005. Seasonal development of microbial activity in soils of northern Norway. Pedosphere 15:716727.
9. Bowman, J. P., 1999. The methanotrophs—the families Methylococcaceae and Methylocystaceae . In M. Dworkin (ed.), The Prokaryotes. Springer-Verlag, New York, NY.
10. Buckeridge, K. M.,, Y. P. Cen,, D. B. Layzell,, and P. Grogan. 2010. Soil biogeochemistry during the early spring in low arctic mesic tundra and the impacts of deepened snow and enhanced nitrogen availability. Biogeochemistry 99:127141.
11. Camill, P. 1999. Patterns of boreal permafrost peatland vegetation across environmental gradients sensitive to climate warming. Can. J. Bot. 77:721733.
12. Chan, O. C.,, P. Claus,, P. Casper,, A. Ulrich,, T. Lueders,, and R. Conrad. 2005. Vertical distribution of the methanogenic archaeal community in Lake Dagow sediment. Environ. Microbiol. 7:11391149.
13. Clemmensen, K. E.,, P. L. Sorensen,, A. Michelsen,, S. Jonasson,, and L. Ström. 2008. Site-dependent N uptake from N-form mixtures by arctic plants, soil microbes and ectomycorrhizal fungi. Oecologia 155:771783.
14. Conrad, R. 2005. Quantification of methanogenic pathways using stable carbonisotopic signatures: a review and a proposal. Organ. Geochem. 36:739752.
15. D'Amico, S.,, T. Collins,, J.-C. Marx,, G. Feller,, and C. Gerday. 2006. Psychrophilic microorganisms: challenges for life. EMBO Rep. 7:385389.
16. Dedysh, S. N.,, Y. Y. Berestovskaya,, L. V. Vasylieva,, S. E. Belova,, V. N. Khmelenina,, N. E. Suzina,, Y. A. Trotsenko,, W. Liesack,, and G. A. Zavarzin. 2004. Methylocella tundrae sp nov., a novel methanotrophic bacterium from acidic tundra peatlands. Int. J. Syst. Evol. Microbiol. 54:151156.
17. Denman, K. L.,, G. Brasseur,, A. Chidthaisong,, P. Ciais,, P. M. Cox,, R. E. Dickinson,, D. Hauglustaine,, C. Heinze,, E. Holland,, D. Jacob,, U. Lohmann,, S. Ramachandran,, P. L. Da Silva Dias,, S. C. Wofsy,, and X. Zhang. 2007. Couplings between changes in the climate system and biogeochemistry. In IPCC, Climate Change 2007: the Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change . Cambridge University Press, Cambridge, United Kingdom, and New York, NY.
18. Dobrovolskaya, T. G.,, L. V. Lysak,, and D. G. Zvyagintsev. 1996. Soils and microbial diversity. Euras. Soil Sci. 29:630634.
19. Dunfield, P. F.,, A. Yuryev,, P. Senin,, A. V. Smirnova,, M. S. Stott,, S. Hou,, B. Ly,, J. H. Saw,, Z. Zhou,, Y. Ren,, J. Wang,, B. W. Mountain,, M. A. Crowe,, T. M. Weatherby,, P. L. E. Bodelier,, W. Liesack,, L. Feng,, L. Wang,, and M. Alam. 2007. Methane oxidation by an extremely acidophilic bacterium of the phylum Verrucomicrobia. Nature 450:879882.
20. Eskelinen, A.,, S. Stark,, and M. Männistö. 2009. Links between plant community composition, soil organic matter quality and microbial communities in contrasting tundra habitats. Oecologia 161:113123.
21. Eugster, W.,, W. R. Rouse,, R. A. Pielke,, J. P. McFadden,, D. D. Baldocchi,, T. G. F. Kittel,, F. S. Chapin III,, G. Liston,, P. L. Vidale,, E. Vaganov,, and S. Chambers. 2000. Land-atmosphere energy exchange in Arctic tundra and boreal forest: available data and feedbacks to climate. Global Change Biol. 6:84115.
22. Eugster, W.,, J. P. McFadden,, and F. S. Chapin. 2005. Differences in surface roughness, energy, and CO2 fluxes in two moist tundra vegetation types, Kuparuk watershed, Alaska, USA. Arct. Antarct. Alpine Res. 37:6167.
23. Franzmann, P. D.,, N. Springer,, W. Ludwig,, E. Conway de Macario,, and M. Rohde. 1992. A methanogenic archaeon from Ace Lake, Antarctica: Methanococcoides burtonii sp. nov. Syst. Appl. Microbiol. 15:573581.
24. Franzmann, P. D.,, Y. Liu,, D. L. Balkwill,, H. C. Aldrich,, E. Conway de Macario,, and D. R. Boone. 1997. Methanogenium frigidium sp. nov., a psychrophilic, H2-using methanogen from Ace Lake, Antarctica. Int. J. Sys. Bacteriol. 47:10681072.
25. Ganzert, L.,, G. Jurgens,, U. Münster,, and D. Wagner. 2007. Methanogenic communities in permafrost-affected soils of the Laptev Sea coast, Siberian Arctic, characterized by 16S rRNA gene fingerprints. FEMS Microbiol. Ecol. 59:476488.
26. Gilichinsky, D. A., 2002. Permafrost, p. 23672385. In G. Bitton (ed.) Encyclopedia of Environmental Microbiology . John Wiley and Sons, New York, NY.
27. Gilichinsky, D. A.,, V. S. Soina,, and M. A. Petrova. 1993. Cryoprotective properties of water in the Earth cryollitosphere and its role in exobiology. Orig. Life Evol. Biosph. 23:6575.
28. Gilichinsky, D.,, T. Vishnivetskaya,, M. Petrova,, E. Spirina,, V. Mamykin,, and E. Rivkina,. 2008. Bacteria in permafrost, p. 83102. In R. Margesin,, F. Schinner,, J.-C. Marx,, and C. Gerday (ed.), Psychrophiles: from Biodiversity to Biotechnology . Springer, Berlin, Germany.
29. Gorham, E. 1991. Northern peatlands: role in the carbon cycle and probable responses to climatic warming. Ecol. Appl. 1:182195.
30. Gough, L.,, G. R. Shaver,, J. Carroll,, D. L. Royer,, and J. A. Laundre. 2000. Vascular plant species richness in Alaskan arctic tundra: the importance of soil pH. J. Ecol. 88:5466.
31. Graef, C.,, A. G. Hestnes,, M. M. Svenning,, and P. Frenzel. 2011. The active methanotrophic community in a wetland from the High Arctic. Environ. Microbiol. Rep. 3:466472.
32. Grosse, G.,, L. Schirrmeister,, and T. J. Malthus. 2006. Application of Landsat-7 satellite data and a DEM for the quantification of thermokarst-affected terrain types in the periglacial Lena-Anabar coastal lowland. Polar Res. 25:5167.
33. Grosskopf, R.,, S. Stubner,, and W. Liesack. 1998. Novel euryarchaeotal lineages detected on rice roots and in the anoxic bulk soil of flooded rice microcosms. Appl. Environ. Microbiol. 64:49834989.
34. Guggenberger, G.,, W. Zech,, and H.-R. Schulten. 1994. Formation and mobilization pathways of dissolved organic matter: evidence from chemical structural studies of organic matter fractions in acid forest floor solutions. Org. Geochem. 21:5166.
35. Hales, B. A.,, C. Edwards,, D. A. Ritchie,, G. Hall,, R. W. Pickup,, and J. R. Saunders. 1996. Isolation and identification of methanogen-specific DNA from blanket bog peat by PCR amplification and sequence analysis. Appl. Environ. Microbiol. 62:668675.
36. Hansen, A. A.,, R. A. Herbert,, K. Mikkelsen,, L. L. Jensen,, T. Kristoffersen,, J. M. Tiedje,, B. A. Lomstein,, and K. W. Finster. 2007. Viability, diversity and composition of the bacterial community in a high Arctic permafrost soil from Spitsbergen, Northern Norway. Environ. Microbiol. 9:28702884.
37. Hedderich, R.,, and W. Whitman,. 2006. Physiology and biochemistry of the methane-producing archaea, p. 10501079. In M. Dworkin,, S. Falkow,, E. Rosenberg,, K.-H. Schleifer,, and E. Stackebrandt (ed.), The Prokaryotes: a Handbook on the Biology of Bacteria , 3rd ed., vol. 2. Springer, New York, NY.
38. Hobbie, S. E.,, and L. Gough. 2004. Litter decomposition in moist acidic and non-acidic tundra with different glacial histories. Oecologia 140:113124.
39. Hobbie, J. E.,, E. A. Hobbie,, H. Drossman,, M. Conte,, J. C. Weber,, J. Shamhart,, and M. Weinrobe. 2009. Mycorrhizal fungi supply nitrogen to host plants in Arctic tundra and boreal forests: 15N is the key signal. Can. J. Microbiol. 55:8494.
40. Høj, L.,, R. A. Olsen,, and V. L. Torsvik. 2005. Archaeal communities in High Arctic wetlands at Spitsbergen, Norway (78°N) as characterised by 16S rRNA gene fingerprinting. FEMS Microbiol. Ecol. 53:89101.
41. Høj, L.,, M. Rusten,, L. E. Haugen,, R. A. Olsen,, and V. L. Torsvik. 2006. Effects of water regime on archaeal community composition in Arctic soils. Environ. Microbiol. 8:984996.
42. IPCC. 2007. Climate Change 2007: the Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change . Cambridge University Press, Cambridge, United Kingdom, and New York, NY.
43. Jeanthon, C.,, S. L’Haridon,, N. Pradel,, and D. Prieur. 1999. Rapid identification of hyperthermophilic methanococci isolated from deep-sea hydrothermal vents. Int. J. Syst. Bacteriol. 49:591594.
44. Jonasson, S.,, J. Castro,, and A. Michelsen. 2004. Litter, warming and plants affect respiration and allocation of soil microbial and plant C, N and P in arctic mesocosms. Soil Biol. Biochem. 36:11291139.
45. Jones, A.,, V. Stolbovoy,, C. Tarnocai,, G. Broll,, O. Spaargaren,, and L. Montanarella (ed.). 2010. Soil Atlas of the Northern Circumpolar Region . European Commission, Publications Office of the European Communities, Luxembourg.
46. Jurgens, G.,, F. O. Glöckner,, R. Amann,, A. Saano,, L. Montonen,, M. Likolammi,, and U. Münster. 2000. Identification of novel Archaea in bacterioplankton of a boreal forest lake by phylogenetic analysis and fluorescent in situ hybridization. FEMS Microbiol. Ecol. 34:4556.
47. Kaiser, K.,, G. Guggenberger,, L. Haumeier,, and W. Zech. 2001. Seasonal variations in the chemical composition of dissolved organic matter in organic forest floor layer leachates of old-growth Scots pine (Pinus sylvestris L.) and European beech (Fagus sylvatica L.) stand in northeastern Bavaria, Germany. Biogeochemistry 55:103143.
48. Kaluzhnaya, M. G.,, V. A. Makutina,, T. G. Rusakova,, D. V. Nikitin,, V. N. Khmelenina,, V. V. Dmitriev,, and Y. A. Trotsenko. 2002. Methanotrophic communities in the soils of the Russian northern taiga and subarctic tundra. Microbiology 71:223227.
49. Keough, B. P.,, T. M. Schmidt,, and R. E. Hicks. 2003. Archaeal nucleic acids in picoplankton from great lakes on three continents. Microb. Ecol. 46:238248.
50. Khmelenina, V. N.,, V. A. Makutina,, M. G. Kaluzhnaya,, E. M. Rivkina,, D. A. Gilichinsky,, and Y. A. Trotsenko. 2002. Discovery of viable methanotrophic bacteria in permafrost sediments of northeast Siberia. Dokl. Biol. Sci. 384:235237.
51. Knorr, W.,, I. C. Prentice,, J. I. House,, and E. A. Holland. 2005. Long-term sensitivity of soil carbon turnover to warming. Nature 433:298301.
52. Kobabe, S.,, D. Wagner,, and E. M. Pfeiffer. 2004. Characterisation of microbial community composition of a Siberian tundra soil by fluorescence in situ hybridisation. FEMS Microbiol. Ecol. 50:1323.
53. Koch, K.,, C. Knoblauch,, and D. Wagner. 2009. Methanogenic community composition and anaerobic carbon turnover in submarine permafrost sediments of the Siberian Laptev Sea. Environ. Microbiol. 11:657668.
54. Kotelnikova, S.,, A. J. L. Macario,, and K. Pedersen. 1998. Methanobacterium subterraneum sp. nov., a new alkaliphilic, eurythermic and halotolerant methanogen isolated from deep granitic groundwater. Int. J. Syst. Bacteriol. 48:357367.
55. Kreyling, J.,, C. Beierkuhnlein,, and A. Jentsch. 2010. Effects of soil freeze-thaw cycles differ between experimental plant communities. Basic Appl. Ecol. 11:6575.
56. Krivushin, K. V.,, V. A. Shcherbakova,, L. E. Petrovskaya,, and E. M. Rivkina. 2010. Methanobacterium veterum sp. nov., from ancient Siberian permafrost. Int. J. Sys. Evol. Microbiol. 60:455459.
57. Lee, H.,, E. A. G. Schuur,, and J. G. Vogel. 2010. Soil CO2 production in upland tundra where permafrost is thawing. J. Geophys. Res. 115:G01009.
58. Liebner, S.,, K. Rublack,, T. Stuehrmann,, and D. Wagner. 2008. Diversity of aerobic methanotrophic bacteria in a permafrost soil of the Lena Delta, Siberia. Microb. Ecol. 57:2535.
59. Liebner, S.,, and D. Wagner. 2007. Abundance, distribution and potential activity of methane oxidizing bacteria in permafrost soils from the Lena Delta, Siberia. Environ. Microbiol. 9:107117.
60. Liebner, S.,, J. Zeyer,, D. Wagner,, C. Schubert,, E.-M. Pfeiffer,, and C. Knoblauch. 2011. Methane oxidation associated with submerged brown mosses reduces methane emissions from Siberian polygonal tundra. J. Ecol. 99:914922.
61. Lin, C.,, L. Raskin,, and D. A. Stahl. 1997. Microbial community structure in gastrointestinal tracts of domestic animals: comparative analyses using rRNA-targeted oligonucleotide probes. FEMS Microbiol. Ecol. 22:281294.
62. Lomans, B. P.,, R. Maas,, R. Luderer,, H. J. M. Op den Camp,, A. Pol,, C. van der Drift,, and G. D. Vogels. 1999. Isolation and characterization of Methanomethylovorans hollandica gen. nov., sp. nov., isolated from freshwater sediment, a methylotrophic methanogen able to grow on dimethyl sulfide and methanethiol. Appl. Environ. Microbiol. 65:36413650.
63. Mangelsdorf, K.,, E. Finsel,, S. Liebner,, and D. Wagner. 2009. Temperature adaptation of microbial communities in different horizons of Siberian permafrost-affected soils from the Lena Delta. Chem. Erde 69:169182.
64. Männistö, M. K.,, and M. M. Häggblom. 2006. Characterization of psychrotolerant heterotrophic bacteria from Finnish Lapland. Syst. Appl. Microbiol. 29:229243.
65. Männistö, M. K.,, M. Tiirola,, and M. M. Häggblom. 2009. Effect of freeze-thaw cycles on bacterial communities of Arctic tundra soil. Microb. Ecol. 58:621631.
66. Martineau, C.,, L. G. Whyte,, and C. W. Greer. 2010. Stable isotope analysis of the diversity and activity of methanotrophic bacteria in soils from the Canadian high Arctic. Appl. Environ. Microbiol. 76:57735784.
67. Mathrani, I. M.,, and D. R. Boone. 1985. Isolation and characterization of a moderately halophilic methanogen from a solar saltern. Appl. Environ. Microbiol. 50:140143.
68. Metje, M.,, and P. Frenzel. 2007. Methanogenesis and methanogenic pathways in a peat from subarctic permafrost. Environ. Microbiol. 9:954964.
69. Morozova, D.,, D. Möhlmann,, and D. Wagner. 2007. Survival of methanogenic archaea from Siberian permafrost under simulated Martian thermal conditions. Orig. Life Evol. Biosph. 37:189200.
70. Morozova, D.,, and D. Wagner. 2007. Stress response of methanogenic archaea from Siberian permafrost compared to methanogens from nonpermafrost habitats. FEMS Microbiol. Ecol. 61:1625.
71. Muhr, J.,, W. Borken,, and E. Matzner. 2009. Effects of soil frost on soil respiration and its radiocarbon signature in a Norway spruce forest soil. Glob. Change Biol. 15:782793.
72. Nelson, D. M.,, A. J. Glawe,, D. P. Labeda,, I. K. Cann,, and R. I. Mackie. 2009. Paenibacillus tundrae sp. nov. and Paenibacillus xylanexedens sp. nov., psychrotolerant, xylan-degrading bacteria from Alaskan tundra. Int. J. Syst. Evol. Microbiol. 59:17081714.
73. Neufeld, J. D.,, and W. W. Mohn. 2005. Unexpectedly high bacterial diversity in Arctic tundra relative to boreal forest soils, revealed by serial analysis of ribosomal sequence tags. Appl. Environ. Microbiol. 71:57105718.
74. Ochsenreiter, T.,, D. Selezi,, A. Quaiser,, L. Bonch-Osmolovskaya,, and C. Schleper. 2003. Diversity and abundance of Crenarchaeota in terrestrial habitats studied by 16S RNA surveys and real time PCR. Environ. Microbiol. 5:787797.
75. Oechel, W. C.,, S. J. Hastings,, M. Jenkins,, G. Riechers,, N. E. Grulke,, and G. L. Vourlitis. 1993. Recent change of arctic tundra ecosystems from a net carbon sink to a source. Nature 361:520526.
76. Oechel, W. C.,, and G. L. Vourlitis. 1994. The effects of climate charge on land-atmosphere feedbacks in arctic tundra regions. Trends Ecol. Evol. 9:324329.
77. Oechel, W. C.,, G. L. Vourlitis,, S. J. Hastings,, R. C. Zulueta,, L. Hinzman,, and D. Kane. 2000. Acclimation of ecosystem CO2 exchange in the Alaskan Arctic in response to decadal climate warming. Nature 406:978981.
78. Oelbermann, M.,, M. English,, and S. L. Schiff. 2008. Evaluating carbon dynamics and microbial activity in arctic soils under warmer temperatures. Can. J. Soil Sci. 88:3144.
79. Omelchenko, M. B.,, L. V. Vasieleva,, G. A. Zavarzin,, N. D. Savelieva,, A. M. Lysenko,, L. L. Mityushina,, V. N. Khmelenina,, and Y. A. Trotsenko. 1996. A novel psychrophilic methanotroph of the genus Methylobacter . Microbiology 65:339343.
80. Osterkamp, T. E., 2001. Subsea permafrost, p. 29022912. In J. H. Steele,, S. A. Thorpe,, and K. K. Turekian (ed.), Encyclopedia of Ocean Sciences . Academic Press, San Diego, CA.
81. Parinkina, O. M. 1989. Microflora of tundra soils: ecological geographical features and productivity. Nauka, Leningrad, Russia.
82. Pol, A.,, K. Heijmans,, H. R. Harhangi,, D. Tedesco,, M. S. M. Jetten,, and H. J. M. Op den Camp. 2007. Methanotrophy below pH 1 by a new Verrucomicrobia species. Nature 450:874878.
83. Post, W. M.,, W. R. Emanuel,, P. J. Zinke,, and A. G. Stangenberger. 1982. Soil carbon pools and world life zones. Nature 298:156159.
84. Raghoebarsing, A. A.,, A. Pol,, K. T. van de Pas-Schoonen,, A. J. P. Smolders,, K. F. Ettwig,, W. I. C. Rijpstra,, S. Schouten,, J. S. Sinninghe Damsté,, H. J. M. Op den Camp,, M. S. M. Jetten,, and M. Strous. 2006. A microbialconsortium couples anaerobic methane oxidation to dentrification. Nature 440:918921.
85. Ramakrishnan, B.,, T. Lueders,, P. F. Dunfield,, R. Conrad,, and M. W. Friedrich. 2001. Archaeal community structures in rice soils from different geographical regions before and after initiation of methane production. FEMS Microbiol. Ecol. 37:175186.
86. Rinnan, R.,, A. Michelsen,, E. Bååth,, and S. Jonasson. 2007. Fifteen years of climate change manipulations alter soil microbial communities in a subarctic heath ecosystem. Glob. Change Biol. 13:2839.
87. Rinnan, R.,, S. Stark,, and A. Tolvanen. 2009. Response of vegetation and soil microbial communities to warming and simulated herbivory in a subarctic heath. J. Ecol. 97:788800.
88. Rivkina, E. M.,, D. Gilichinsky,, S. Wagener,, J. Tiedje,, and J. McGrath. 1998. Biochemical activity of anaerobic microorganisms from buried permafrost sediments. Geomicrobiology 15:187193.
89. Russell, N. J. 2000. Cold shock and cold acclimation in cold-adapted bacteria. Mol. Integr. Physiol. 126:130134.
90. Sawicka, J. E.,, A. Robador,, C. Hubert,, B. B. Jorgensen,, and V. Bruchert. 2010. Effects of freeze-thaw cycles on anaerobic microbial processes in an Arctic intertidal mud flat. ISME J. 4:585594.
91. Schink, B.,, and A. J. M. Stams,. 2006. Syntrophism among prokaryotes, p. 309335. In M. Dworkin,, S. Falkow,, E. Rosenberg,, K.-H. Schleifer,, and E. Stackebrandt (ed.), The Prokaryotes: a Handbook on the Biology of Bacteria , 3rd ed., vol. 2. Springer, New York, NY.
92. Schuur, E. A. G.,, J. Bockheim,, J. C. Canadell,, E. Euskirchen,, C. B. Field,, S. V. Goryachkin,, S. Hagemann,, P. Kuhry,, P. M. Lafleur,, H. Lee,, G. Mazhitova,, F. E. Nelson,, A. Rinke,, V. E. Romanovsky,, N. Shiklomanov,, C. Tarnocai,, S. Venevsky,, J. G. Vogel,, and S. A. Zimov. 2008. Vulnerability of permafrost carbon to climate change: implications for the global carbon cycle. BioScience 58:701714.
93. Shlimon, A. G.,, M. W. Friedrich,, H. Niemann,, N. B. Ramsing,, and K. Finster. 2004. Methanobacterium aarhusense sp. nov., a novel methanogen isolated from a marine sediment (Aarhus Bay, Denmark). Int. J. Syst. Evol. Microbiol. 54:759763.
94. Sjögersten, S.,, and P. A. Wookey. 2009. The impact of climate change on ecosystem carbon dynamics at the Scandinavian mountain birch forest-tundra heath ecotone. Ambio 38:210.
95. Steven, B.,, G. Briggs,, C. P. McKay,, W. H. Pollard,, C. W. Greer,, and L. G. Whyte. 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. 59:513523.
96. Steven, B.,, R. Léveillé,, W. H. Pollard,, and L. G. Whyte. 2006. Microbial ecology and biodiversity in permafrost. Extremophiles 10:259267.
97. Steven, B.,, W. H. Pollard,, C. W. Greer,, and L. G. Whyte. 2008. Microbial diversity and activity through a permafrost/ground ice core profile from the Canadian high Arctic. Environ. Microbiol. 10:33883403.
98. Ström, L.,, and T. R. Christensen. 2007. Below ground carbon turnover and greenhouse gas exchanges in a sub-arctic wetland. Soil Biol. Biochem. 39:16891698.
99. Tarnocai, C. 2006. The effect of climate change on carbon in Canadian peatlands. Glob. Planet. Change 53:222232.
100. Tarnocai, C.,, J. G. Canadell,, E. A. G. Schuur,, P. Kuhry,, G. Mazhitova,, and S. Zimov. 2009. Soil organic carbon pools in the northern circumpolar permafrost region. Glob. Biogeochem. Cycles 23:GB2023.
101. Trotsenko, Y. A.,, and V. N. Khmelenina. 2005. Aerobic methanotrophic bacteria of cold ecosystems. FEMS Microbiol. Ecol. 53:1526.
102. Trumbore, S. E.,, O. A. Chadwick,, and R. Amundson. 1996. Rapid exchange between soil carbon and atmospheric carbon dioxide driven by temperature change. Science 272:393396.
103. Vasilyeva, L. V.,, M. V. Omelchenko,, Y. Y. Berestovskaya,, A. M. Lysenko,, W. R. Abraham,, S. N. Dedysh,, and G. A. Zavarzin. 2006. Asticcacaulis benevestitus sp. nov., a psychrotolerant, dimorphic, prosthecate bacterium from tundra wetland soil. Int. J. Syst. Evol. Microbiol. 56:20832088.
104. Vishnivetskaya, T.,, S. Kathariou,, J. McGrath,, D. Gilichinsky,, and J. M. Tiedje. 2000. Low-temperature recovery strategies for the isolation of bacteria from ancient permafrost sediments. Extremophiles 4:165173.
105. Vorobyova, E.,, V. Soina,, M. Gorlenko,, N. Minkovskaya,, N. Zalinova,, A. Mamukelashvili,, D. Gilichinsky,, E. Rivkina,, and T. Vishnivetskaya. 1997. The deep cold biosphere: facts and hypothesis. FEMS Microbiol. Rev. 20:277290.
106. Wagner, D., 2008. Microbial communities and processes in Arctic permafrost environments, p. 133154. In P. Dion, and C. S. Nautiyal (ed.) Microbiology of Extreme Soils . Springer, Berlin, Germany.
107. Wagner, D.,, A. Gattinger,, A. Embacher,, E. M. Pfeiffer,, M. Schloter,, and A. Lipski. 2007. Methanogenic activity and biomass in Holocene permafrost deposits of the Lena Delta, Siberian Arctic and its implication for the global methane budget. Glob. Change Biol. 13:10891099.
108. Wagner, D.,, S. Kobabe,, and S. Liebner. 2009. Bacterial community structure and carbon turnover in permafrost-affected soils of the Lena Delta, northeastern Siberia. Can. J. Microbiol. 55:7383.
109. Wagner, D.,, S. Kobabe,, E. M. Pfeiffer,, and H.-W. Hubberten. 2003. Microbial controls on methane fluxes from a polygonal tundra of the Lena Delta, Siberia. Permafrost Periglacial Processes 14:173185.
110. Wagner, D.,, and S. Liebner,. 2009. Global warming and carbon dynamics in permafrost soils: methane production and oxidation, p. 219236. In R. Margesin (ed.), Permafrost Soils . Springer, Berlin, Germany.
111. Wagner, D.,, A. Lipski,, A. Embacher,, and A. Gattinger. 2005. Methane fluxes in extreme permafrost habitats of the Lena Delta: effects of microbial community structure and organic matter quality. Environ. Microbiol. 7:15821592.
112. Walker, M. D.,, C. H. Wahren,, R. D. Hollister,, G. H. Henry,, L. E. Ahlquist,, J. M. Alatalo,, M. S. Bret-Harte,, M. P. Calef,, T. V. Callaghan,, A. B. Carroll,, H. E. Epstein,, I. S. Jonsdottir,, J. A. Klein,, B. Magnusson,, U. Molau,, S. F. Oberbauer,, S. P. Rewa,, C. H. Robinson,, G. R. Shaver,, K. N. Suding,, C. C. Thompson,, A. Tolvanen,, O. Totland,, P. L. Turner,, C. E. Tweedie,, P. J. Webber,, and P. A. Wookey. 2006a. Plant community responses to experimental warming across the tundra biome. Proc. Natl. Acad. Sci. USA 103:13421346.
113. Walker, V. K.,, G. R. Palmer,, and G. Voordouw. 2006b. Freeze-thaw tolerance and clues to the winter survival of a soil community. Appl. Environ. Microbiol. 72:17841792.
114. Wartiainen, I.,, A. G. Hestnes,, I. R. McDonald,, and M. M. Svenning. 2006a. Methylobacter tundripaludum sp. nov., a novel methanotrophic bacterium from Arctic wetland soil, Svalbard, Norway (78° N). Int. J. Syst. Evol. Microbiol. 56:109113.
115. Wartiainen, I.,, A. G. Hestnes,, I. R. McDonald,, and M. M. Svenning. 2006b. Methylocystis rosea sp. nov., a novel methanotrophic bacterium from Arctic wetland soil, Svalbard, Norway (78° N). Int. J. Syst. Evol. Microbiol. 56:541547.
116. Wartiainen, I.,, A. G. Hestnes,, and M. M. Svenning. 2003. Methanotrophic diversity in high arctic wetlands on the islands of Svalbard (Norway)—denaturing gradient gel electrophoresis analysis of soil DNA and enrichment cultures. Can. J. Microbiol. 49:602612.
117. Whitman, W. B.,, D. C. Coleman,, and W. J. Wiebe. 1998. Prokaryotes: the unseen majority. Proc. Natl. Acad. Sci. USA 95:65786583.
118. Wuebbles, J.,, and K. Hayhoe. 2002. Atmospheric methane and global change. Earth Sci. Rev. 57:177210.
119. Yergeau, E.,, H. Hogues,, L. G. Whyte,, and C. W. Greer. 2010. The functional potential of highArctic permafrost revealed by metagenomic sequencing, qPCR, and microarray analyses. ISME J. 4:12061214.
120. Zak, D. R.,, and G. W. Kling. 2006. Microbial community composition and function across an arctic tundra landscape. Ecology 87:16591670.
121. Zhang, T.,, R. G. Barry,, K. Knowles,, J. A. Heginbotton,, and J. Brown. 1999. Statistics and characteristics of permafrost and ground-ice distribution in the Northern Hemisphere. Polar Geogr. 23:132154.
122. Zhou, J.,, M. E. Davey,, J. B. Figueras,, E. Rivkina,, D. Gilichinsky,, and J. M. Tiedje. 1997. Phylogenetic diversity of a bacterial community determined from Siberian tundra soil DNA. Microbiology 143:39133919.
123. Zimov, S. A.,, E. A. G. Schuur,, and F. S. Chapin III. 2006. Permafrost and the global carbon budget. Science 312:16121613.


Generic image for table

Taxonomy of all previously described methanogenic

The references cited in the table may be found in the (http://www.bacterio.cict.fr/index.html).

Citation: Vishnivetskaya T, Liebner S, Wilhelm R, Wagner D. 2012. Microbial Carbon Cycling in Permafrost, p 183-200. In Miller R, Whyte L (ed), Polar Microbiology: Life in a Deep Freeze. ASM Press, Washington, DC. doi: 10.1128/9781555817183.ch9
Generic image for table

Taxonomy of methane-oxidizing

The references cited in the table may be found in the ( http://www.bacterio.cict.fr/index.html).

Citation: Vishnivetskaya T, Liebner S, Wilhelm R, Wagner D. 2012. Microbial Carbon Cycling in Permafrost, p 183-200. In Miller R, Whyte L (ed), Polar Microbiology: Life in a Deep Freeze. ASM Press, Washington, DC. doi: 10.1128/9781555817183.ch9

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