Climate change is already altering the landscape at high latitudes. Permafrost is thawing, the growing season is starting earlier, and, as a result, certain regions in the Arctic may be subjected to an increased incidence of freeze-thaw events. The potential release of carbon and nutrients from soil microbial cells that have been lysed by freeze-thaw transitions could have significant impacts on the overall carbon balance of arctic ecosystems, and therefore on atmospheric CO 2 concentrations. However, the impact of repeated freezing and thawing with the consequent growth and recrystallization of ice on microbial communities is still not well understood. Soil samples from three distinct sites, representing Canadian geographical low arctic, mid-arctic and high arctic soils were collected from Daring Lake, Alexandra Fjord and Cambridge Bay sampling sites, respectively. Laboratory-based experiments subjected the soils to multiple freeze-thaw cycles for 14 days based on field observations (0 °C to ？10 °C for 12 h and ？10 °C to 0 °C for 12 h) and the impact on the communities was assessed by phospholipid fatty acid (PLFA) methyl ester analysis and 16S ribosomal RNA gene sequencing. Both data sets indicated differences in composition and relative abundance between the three sites, as expected. However, there was also a strong variation within the two high latitude sites in the effects of the freeze-thaw treatment on individual PLFA and 16S-based phylotypes. These site-based heterogeneities suggest that the impact of climate change on soil microbial communities may not be predictable a priori; minor differential susceptibilities to freeze-thaw stress could lead to a “butterfly effect” as described by chaos theory, resulting in subsequent substantive differences in microbial assemblages. This perspectives article suggests that this is an unwelcome finding since it will make future predictions for the impact of on-going climate change on soil microbial communities in arctic regions all but impossible.
References
[1]
Olsson, P.Q.; Sturm, M.; Racine, C.H.; Romanovsky, V.; Liston, G.E. Five Stages of the Alaskan Arctic Cold Season with Ecosystem Implications. Arctic Antarct. Alp. Res. 2003, 35, 74–81, doi:10.1657/1523-0430(2003)035[0074:FSOTAA]2.0.CO;2.
Sulkava, P.; Huhta, V. Effects of Hard Frost and Freeze-Thaw Cycles on Decomposer Communities and N Mineralisation in Boreal Forest Soil. Appl. Soil Ecol. 2003, 22, 225–239, doi:10.1016/S0929-1393(02)00155-5.
[4]
Grogan, P.; Michelsen, A.; Ambus, P.; Jonasson, S. Freeze-Thaw Regime Effects on Carbon and Nitrogen Dynamics in Sub-Arctic Heath Tundra Mesocosms. Soil Biol. Biochem. 2004, 36, 641–654, doi:10.1016/j.soilbio.2003.12.007.
[5]
Yanai, Y.; Toyota, K.; Okazaki, M. Effects of Successive Soil Freeze-Thaw Cycles on Soil Microbial Biomass and Organic Matter Decomposition Potential of Soils. Soil Sci. Plant Nutr. 2004, 50, 821–829, doi:10.1080/00380768.2004.10408542.
[6]
Sharma, S.; Szele, Z.; Schilling, R.; Munch, J.C.; Schloter, M. Influence of Freeze-Thaw Stress on the Structure and Function of Microbial Communities and Denitrifying Populations in Soil. Appl. Environ. Microbiol. 2006, 72, 2148–2154.
[7]
Schimel, J.; Balser, T.C.; Wallenstein, M. Microbial Stress-Response Physiology and its Implications for Ecosystem Function. Ecology 2007, 88, 1386–1394, doi:10.1890/06-0219.
ACIA: Arctic Climate Impact Assessment; Cambridge University Press: Cambridge, UK, 2005; p. 1042.
[10]
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; Solomon, S., Qin, D., Manning, M., Chen, Z., Marquis, M., Averyt, K.B., Tignor, M., Miller, H.L., Eds.; Cambridge University Press: Cambridge, UK; New York, NY, USA, 2007.
[11]
Groffman, P.M.; Driscoll, C.T.; Fahey, T.J.; Hardy, J.P.; Fitzhugh, R.D.; Tierney, G.L. Colder Soils in a Warmer World: A Snow Manipulation Study in a Northern Hardwood Forest Ecosystem. Biogeochemistry 2001, 56, 135–150, doi:10.1023/A:1013039830323.
[12]
Kattsov, V.M.; K？llén, E.; Cattle, H.; Christensen, J.; Drange, H.; Hanssen-Bauer, I.; Jóhannesen, T.; Karol, I.; R？is？nen, J.; Svensson, G.; et al. Future Climate Change: Modeling and Scenarios for the Arctic. In Arctic Climate Impact Assessment; Cambridge University Press: New York, NY, USA, 2005; pp. 99–150.
[13]
Brooks, P.D.; Williams, M.W.; Schmidt, S.K. Inorganic Nitrogen and Microbial Biomass Dynamics Before and During Spring Snowmelt. Biogeochemistry 1998, 43, 1–15, doi:10.1023/A:1005947511910.
[14]
Schimel, J.P.; Clein, J.S. Microbial Response to Freeze-Thaw Cycles in Tundra and Taiga Soils. Soil Biol. Biochem. 1996, 28, 1061–1066, doi:10.1016/0038-0717(96)00083-1.
[15]
Larsen, K.S.; Jonasson, S.; Michelsen, A. Repeated Freeze-Thaw Cycles and Their Effects on Biological Processes in Two Arctic Ecosystem Types. Appl. Soil Ecol. 2002, 21, 187–195, doi:10.1016/S0929-1393(02)00093-8.
[16]
Larsen, K.S.; Grogan, P.; Jonasson, S.; Michelsen, A. Respiration and Microbial Dynamics in Two Subarctic Ecosystems During Winter and Spring Thaw: Effects of Increased Snow Depth. Arctic Antarct. Alp. Res. 2007, 39, 268–276, doi:10.1657/1523-0430(2007)39[268:RAMDIT]2.0.CO;2.
[17]
Christiansen, C.T.; Svendsen, S.H.; Schmidt, N.M.; Michelsen, A. High Arctic Heath Soil Respiration and Biogeochemical Dynamics During Summer and Autumn Freeze-in—Effects of Long-term Enhanced Water and Nutrient Supply. Glob. Change Biol. 2012, 18, 3224–3236, doi:10.1111/j.1365-2486.2012.02770.x.
[18]
Soulides, D.A.; Allison, F.E. Effect of Drying and Freezing Soils on Carbon Dioxide Production, Available Mineral Nutrients, Aggregation, and Bacterial Population. Soil Sci. 1961, 91, 291–298, doi:10.1097/00010694-196105000-00001.
[19]
Lipson, D.A.; Monson, R.K. Plant-Microbe Competition for Soil Amino Acids in the Alpine Tundra: Effects of Freeze-Thaw and Dry-Rewet Events. Oecologia 1998, 113, 406–414, doi:10.1007/s004420050393.
[20]
Buckeridge, K.M.; Cen, Y.-P.; Layzell, D.B.; Grogan, P. Soil Biogeochemistry During the Early Spring in Low Arctic Mesic Tundra and the Impacts of Deepened Snow and Enhanced Nitrogen Availability. Biogeochemistry 2010, 99, 127–141, doi:10.1007/s10533-009-9396-7.
[21]
M？nnist？, M.K.; Tiirola, M.; Haggblom, M.M. Effect of Freeze-Thaw Cycles on Bacterial Communities of Arctic Tundra Soil. Microb. Ecol. 2009, 58, 621–631.
[22]
Skogland, T.; Lomeland, S.; Goksoyr, J. Respiratory Burst after Freezing and Thawing of Soil—Experiments with Soil Bacteria. Soil Biol. Biochem. 1988, 20, 851–856, doi:10.1016/0038-0717(88)90092-2.
[23]
Herrmann, A.; Witter, E. Sources of C and N Contributing to the Flush in Mineralization upon Freeze-Thaw Cycles in Soils. Soil Biol. Biochem. 2002, 34, 1495–1505, doi:10.1016/S0038-0717(02)00121-9.
[24]
Shaver, G.R.; Chapin, F.S. Response to Fertilization by Various Plant-Growth Forms in an Alaskan Tundra—Nutrient Accumulation and Growth. Ecology 1980, 61, 662–675, doi:10.2307/1937432.
[25]
Jonasson, S.; Michelsen, A.; Schmidt, I.K. Coupling of Nutrient Cycling and Carbon Dynamics in the Arctic, Integration of Soil Microbial and Plant Processes. Appl. Soil Ecol. 1999, 11, 135–146, doi:10.1016/S0929-1393(98)00145-0.
[26]
Shaver, G.R.; Billings, W.D.; Chapin, F.S., III; Giblin, A.E.; Nadelhoffer, K.J.; Oechel, W.C.; Rastetter, E.B. Global Change and the Carbon Balance of Arctic Ecosystems. BioScience 1992, 42, 433–441, doi:10.2307/1311862.
[27]
Edwards, K.A.; Jefferies, R.L. Nitrogen uptake by Carex aquatilis during the winter-spring transition in a low Arctic wet meadow. J. Ecol. 2010, 98, 737–744, doi:10.1111/j.1365-2745.2010.01675.x.
[28]
Grogan, P.; Jonasson, S. Controls on Annual Nitrogen Cycling in the Understorey of a Sub-Arctic Birch Forest. Ecology 2003, 84, 202–218, doi:10.1890/0012-9658(2003)084[0202:COANCI]2.0.CO;2.
[29]
Larsen, K.S.; Michelsen, A.; Jonasson, S.; Beier, C.; Grogan, P. Nitrogen Uptake during Fall, Winter and Spring Differs among Plant Functional Groups in a Subarctic Heath Ecosystem. Ecosystems 2012, 15, 927–939.
[30]
Bottner, P. Response of Microbial Biomass to Alternate Moist and Dry Conditions in a Soil Incubated with C-14-labeled and N-15-labelled Plant-Material. Soil Biol. Biochem. 1985, 17, 329–337, doi:10.1016/0038-0717(85)90070-7.
[31]
Kieft, T.L.; Soroker, E.; Firestone, M.K. Microbial Biomass Response to a Rapid Increase in Water Potential When Dry soil is Wetted. Soil Biol. Biochem. 1987, 19, 119–126, doi:10.1016/0038-0717(87)90070-8.
[32]
Clein, J.S.; Schimel, J.P. Reduction in Microbial Activity in Birch Litter due to Drying and Rewetting Events. Soil Biol. Biochem. 1994, 26, 403–406, doi:10.1016/0038-0717(94)90290-9.
[33]
Fierer, N.; Schimel, J.P. A Proposed Mechanism for the Pulse in Carbon Dioxide Production Commonly Observed Following the Rapid Rewetting of a Dry Soil. Soil Sci. Soc. Am. J. 2003, 67, 798–805.
[34]
Franzluebbers, A.J.; Haney, R.L.; Honeycutt, C.W.; Schomberg, H.H.; Hons, F.M. Flush of Carbon Dioxide Following Rewetting of Dried Soil Relates to Active Organic Pools. Soil Sci. Soc. Am. J. 2000, 64, 613–623.
[35]
Jefferies, R.L.; Walker, N.A.; Edwards, K.A.; Dainty, J. Is the Decline of Soil Microbial Biomass in Late Winter Coupled to Changes in the Physical State of Cold Soils? Soil Biol. Biochem. 2010, 42, 129–135, doi:10.1016/j.soilbio.2009.10.008.
[36]
Kane, D.L.; Stein, J. Water-Movement into Seasonally Frozen Soils. Water Resour. Res. 1983, 19, 1547–1557, doi:10.1029/WR019i006p01547.
[37]
Marsh, P.; Woo, M.K. Wetting Front Advance and Freezing of Meltwater within a Snow Cover 1. Observations in the Canadian Arctic. Water Resour. Res. 1984, 20, 1853–1864, doi:10.1029/WR020i012p01853.
Mazur, P. Theoretical and Experimental Effects of Cooling and Warming Velocity on Survival of Frozen and Thawed Cells. Cryobiology 1966, 2, 181–192, doi:10.1016/S0011-2240(66)80165-7.
[40]
Mazur, P. Freezing of Living Cells: Mechanisms and Implications. Am. J. Physiol. 1984, 247, C125–C142.
[41]
Deal, P.H. Freeze-Thaw Behaviour of a Moderately Halophilic Bacterium as a Function of Salt Concentration. Cryobiology 1970, 7, 107–112, doi:10.1016/0011-2240(70)90005-2.
[42]
Mikan, C.J.; Schimel, J.P.; Doyle, A.P. Temperature Controls of Microbial Respiration in Arctic Tundra Soils Above and Below Freezing. Soil Biol. Biochem. 2002, 34, 1785–1795, doi:10.1016/S0038-0717(02)00168-2.
[43]
Panikov, N.S.; Flanagan, P.W.; Oechel, W.C.; Mastepanov, M.A.; Christensen, T.R. Microbial Activity in Soils Frozen to Below ？39 °C. Soil Biol. Biochem. 2006, 38, 785–794, doi:10.1016/j.soilbio.2005.07.004.
[44]
Casanueva, A.; Tuffin, M.; Cary, C.; Cowan, D.A. Molecular Adaptations to Psychrophily: The Impact of “Omic” Technologies. Trends Microbiol. 2010, 18, 374–381, doi:10.1016/j.tim.2010.05.002.
[45]
Wilson, S.L.; Walker, V.K. Selection of Low-Temperature Resistance in Bacteria and Potential Applications. Environ. Technol. 2010, 31, 943–956, doi:10.1080/09593331003782417.
[46]
Oquist, M.G.; Sparrman, T.; Klemedtsson, L.; Drotz, S.H.; Grip, H.; Schleucher, J.; Nilsson, M. Water Availability Controls Microbial Temperature Responses in Frozen Soil CO2 Production. Glob. Change Biol. 2009, 15, 2715–2722, doi:10.1111/j.1365-2486.2009.01898.x.
[47]
Tilston, E.L.; Sparrman, T.; Oquist, M.G. Unfrozen Water Content Moderates Temperature Dependence of Sub-Zero Microbial Respiration. Soil Biol. Biochem. 2010, 42, 1396–1407, doi:10.1016/j.soilbio.2010.04.018.
[48]
Clein, J.S.; Schimel, J.P. Microbial Activity of Tundra and Taiga Soils at Subzero Temperatures. Soil Biol. Biochem. 1995, 27, 1231–1234, doi:10.1016/0038-0717(95)00044-F.
[49]
Schimel, J.P.; Mikan, C. Changing Microbial Substrate Use in Arctic Tundra Soils through a Freeze-Thaw Cycle. Soil Biol. Biochem. 2005, 37, 1411–1418, doi:10.1016/j.soilbio.2004.12.011.
[50]
Michaelson, G.J.; Ping, C.L. Soil Organic Carbon and CO2 Respiration at Subzero Temperature in Soils of Arctic Alaska. J. Geophys. Res. Atmos. 2003, 108, D2.
[51]
Schimel, J.P.; Bilbrough, C.; Welker, J.A. Increased Snow Depth Affects Microbial Activity and Nitrogen Mineralization in Two Arctic Tundra Communities. Soil Biol. Biochem. 2004, 36, 217–227, doi:10.1016/j.soilbio.2003.09.008.
[52]
Walker, V.K.; Palmer, G.R.; Voordouw, G. Freeze-Thaw Tolerance and Clues to the Winter Survival of a Soil Community. Appl. Environ. Microb. 2006, 72, 1784–1792, doi:10.1128/AEM.72.3.1784-1792.2006.
[53]
McMahon, S.K.; Wallenstein, M.D.; Schimel, J.P. A Cross-Seasonal Comparison of Active and Total Bacterial Community Composition in Arctic Tundra Soil Using Bromodeoxyuridine Labeling. Soil Biol. Biochem. 2011, 43, 287–295.
[54]
Monson, R.K.; Lipson, D.L.; Burns, S.P.; Turnipseed, A.A.; Delany, A.C.; Williams, M.W.; Schmidt, S.K. Winter Forest Soil Respiration Controlled by Climate and Microbial Community Composition. Nature 2006, 439, 711–714.
Lipson, D.A.; Schmidt, S.K. Seasonal Changes in an Alpine Soil Bacterial Community in the Colorado Rocky Mountains. Appl. Environ. Microb. 2004, 70, 2867–2879, doi:10.1128/AEM.70.5.2867-2879.2004.
[57]
Lipson, D.A.; Schadt, C.W.; Schmidt, S.K. Changes in Soil Microbial Community Structure and Function in an Alpine Dry Meadow Following Spring Snow Melt. Microb. Ecol. 2002, 43, 307–314, doi:10.1007/s00248-001-1057-x.
[58]
Henry, G. Climate Change and Soil Freezing Dynamics: Historical Trends and Projected Changes. Clim. Change 2008, 87, 421–434.
[59]
Chu, H.Y.; Neufeld, J.D.; Walker, V.K.; Grogan, P. The Influence of Vegetation Type on the Dominant Soil Bacteria, Archaea, and Fungi in a Low Arctic Tundra Landscape. Soil Sci. Soc. Am. J. 2011, 75, 1756–1765.
[60]
Chu, H.; Fierer, N.; Lauber, C.L.; Caporaso, J.G.; Knight, R.; Grogan, P. Soil Bacterial Diversity in the Arctic is not Fundamentally Different from that Found in Other Biomes. Environ. Microb. 2010, 12, 2998–3006, doi:10.1111/j.1462-2920.2010.02277.x.
[61]
Labine, C. Meteorology and Climatology of the Alexandra Fjord Lowland. In Ecology of a Polar Oasis, Alexandra Fiord, Ellesmere Island, Canada; Svoboda, J., Freedman, B., Eds.; Captus University Publications: Toronto, Canada, 1994; pp. 23–39.
[62]
Rayback, S.A.; Henry, G.H.R. Reconstruction of Summer Temperature for a Canadian High Arctic Site from Retrospective Analysis of the Dwarf Shrub, Cassiope tetragona. Arctic Antarct. Alp. Res. 2006, 38, 228–238, doi:10.1657/1523-0430(2006)38[228:ROSTFA]2.0.CO;2.
[63]
Sasser, M. Identification of Bacteria by Gas Chromatography of Cellular Fatty Acids; MIDI Technical note #101: Newark, DE, USA, 1990. revised 2001.
[64]
Klose, S.; Acosta-Martinez, V.; Ajwa, H.A. Microbial Community Composition and Enzyme Activities in a Sandy Loam Soil after Fumigation with Methyl Bromide or Alternative Biocides. Soil Biol. Biochem. 2006, 38, 1243–1254, doi:10.1016/j.soilbio.2005.09.025.
[65]
Kumar, N.; Shah, V.; Walker, V.K. Perturbation of an Arctic Soil Microbial Community by Metal Nanoparticles. J. Hazard. Mater. 2011, 190, 816–822, doi:10.1016/j.jhazmat.2011.04.005.
[66]
Dowd, S.E.; Callaway, T.R.; Wolcott, R.D.; Sun, Y.; McKeehan, T.; Hagevoort, R.G.; Edrington, T.S. Evaluation of the Bacterial Diversity in the Feces of Cattle Using 16S rDNA Bacterial Tag-Encoded FLX Amplicon Pyrosequencing (bTEFAP). BMC Microbiol. 2008, 8, 125, doi:10.1186/1471-2180-8-125.
[67]
Ishak, H.D.; Plowes, R.; Sen, R.; Kellner, K.; Meyer, E.; Estrada, D.A.; Dowd, S.E.; Mueller, U.G. Bacterial Diversity in Solenopsis invicta and Solenopsis geminata Ant Colonies Characterized by 16S amplicon 454 Pyrosequencing. Microb. Ecol. 2011, 61, 821–831.
[68]
Research and Testing Laboratory. Available online: http://www.researchandtesting.com/ (accessed on 17 December 2012).
[69]
Gontcharova, V.; Youn, E.; Wolcott, R.D.; Hollister, E.B.; Gentry, T.J.; Dowd, S.E. Black Box Chimera Check (B2C2): A Windows-Based Software for Batch Depletion of Chimeras from Bacterial 16S rRNA Gene Datasets. Open Microbiol. J. 2010, 4, 47–52, doi:10.2174/1874285801004010047.
[70]
Bailey, M.T.; Dowd, S.E.; Parry, N.M.; Galley, J.D.; Schauer, D.B.; Lyte, M. Stressor Exposure Disrupts Commensal Microbial Populations in the Intestines and Leads to Increased Colonization by Citrobacter rodentium. Infect. Immun. 2010, 78, 1509–1519, doi:10.1128/IAI.00862-09.
Cole, J.R.; Wang, Q.; Cardenas, E.; Fish, J.; Chai, B.; Farris, R.J.; Kulam-Syed-Mohideen, A.S.; McGarrell, D.M.; Marsh, T.; Garrity, G.M.; et al. The Ribosomal Database Project: Improved Alignments and New Tools for rRNA Analysis. Nucleic Acids Res. 2009, 37, D141–D145.
[73]
Suutari, M.; Laakso, S. Microbial Fatty-Acids and Thermal Adaptation. Crit. Rev. Microbiol. 1994, 20, 129–137.
[74]
Singleton, D.R.; Furlong, M.A.; Peacock, A.D.; White, D.C.; Coleman, D.C.; Whitman, W.B. Solirubrobacter pauli gen. nov., sp. nov., A Mesophilic Bacterium within the Rubrobacteridae Related to Common Soil Clones. Int. J. Syst. Evol. Microbiol. 2003, 53, 485–490, doi:10.1099/ijs.0.02438-0.
[75]
Kim, M.K.; Na, J.R.; Lee, T.H.; Im, W.T.; Soung, N.K.; Yang, D.C. Solirubrobacter soli sp. nov., Isolated from Soil of a Ginseng Field. Int. J. Syst. Evol. Microbiol. 2007, 57, 1453–1455, doi:10.1099/ijs.0.64715-0.
[76]
Paulino-Lima, I.G.; Azua-Bustos, A.; Vicu？a, R.; González-Silva, C.; Salas, L.; Teixeira, L.; Rosado, A.; da Costa Leitao, A.A.; Lage, C. Isolation of UVC-tolerant Bacteria from the Hyperarid Atacama Desert, Chile. Microb. Ecol. 2012, doi:10.1007/s00248-012-0121-z.
[77]
Collins, D.; Luxton, T.; Kumar, N.; Shah, S.; Walker, V.K.; Shah, V. Assessing the Impact of Copper and Zinc Oxide Nanoparticles on Soil: A Field Study. PLoS One 2012, 7, e42663.
[78]
Mackey, B.M. Lethal and Sublethal Effects of Refrigeration, Freezing and Freeze-Drying on Micro-Organisms. Soc. Appl. Bacteriol. Symp. Ser. 1984, 12, 45–75.
[79]
Xu, H.; Griffith, M.; Patten, C.L.; Glick, B.R. Isolation and Characterization of an Antifreeze Protein with Ice Nucleation Activity from the Plant Growth Promoting Rhizobacterium Pseudomonas putida GR12-2. Can. J. Microbiol. 1998, 44, 64–73.
[80]
Raymond, J.A.; Fritsen, C.H. Semipurification and Ice Recrystallization Inhibition Activity of Ice-active Substances Associated with Antarctic Photosynthetic Organisms. Cryobiology 2001, 43, 63–70, doi:10.1006/cryo.2001.2341.
[81]
Gilbert, J.A.; Hill, P.J.; Dodd, C.E.R.; Laybourn-Parry, J. Demonstration of Antifreeze Protein Activity in Antarctic Lake Bacteria. Microbiology 2004, 150, 171–180, doi:10.1099/mic.0.26610-0.
[82]
Wilson, S.L.; Frazer, C.; Cumming, B.F.; Nuin, P.A.S.; Walker, V.K. Cross-tolerance between Osmotic and Freeze-Thaw Stress in Microbial Assemblages from Temperate Lakes. FEMS Microbiol. Ecol. 2012, 82, 405–415.
[83]
Yergeau, E.; Kowalchuk, G.A. Responses of Antarctic Soil Microbial Communities and Associated Functions to Temperature and Freeze-Thaw Cycle Frequency. Environ. Microbiol. 2008, 10, 2223–2235, doi:10.1111/j.1462-2920.2008.01644.x.
[84]
Teixeira, L.; Peixoto, R.S.; Cury, J.C.; Sul, W.J.; Pellizari, V.H.; Tiedje, J.; Rosado, A.S. Bacterial Diversity in Rhizosphere Soil from Antarctic Vascular Plants of Admiralty Bay, Maritime Antarctica. ISME J. 2010, 4, 989–1001, doi:10.1038/ismej.2010.35.
Deslippe, J.R.; Egger, K.N.; Henry, G.H.R. Impacts of Warming and Fertilization on Nitrogen-Fixing Microbial Communities in the Canadian High Arctic. FEMS Microbiol. Ecol. 2005, 53, 41–50.
[87]
Whitman, W.B.; Coleman, D.C.; Wiebe, W.J. Prokaryotes: The Unseen Majority. Proc. Natl. Acad. Sci. USA 1998, 95, 6578–6583, doi:10.1073/pnas.95.12.6578.
[88]
Walker, J.K.M.; Egger, K.N.; Henry, G.H.R. Long-Term Experimental Warming Alters Nitrogen-Cycling Communities but Site factors Remain the Primary Drivers of Community Structure in High Arctic Tundra Soils. ISME J. 2008, 2, 982–995, doi:10.1038/ismej.2008.52.
Schimel, J.P.; Gulledge, J. Microbial Community Structure and Global Trace Gases. Glob. Change Biol. 1998, 4, 745–758, doi:10.1046/j.1365-2486.1998.00195.x.
[91]
Banerjee, S.; Siciliano, S.D. Evidence of High Microbial Abundance and Spatial Dependency in Three Arctic Soil Ecosystems. Soil Sci. Soc. Am. J. 2011, 75, 2227–2232.
