Microbial competition in polar soils: A review of an understudied but potentially important control on productivity

Biology

Volumn 2, Issue 2, 2013, Pages 533-554

  Bell, Terrence H ^a,b   Callender, Katrina L ^a,b   Whyte, Lyle G ^a   Greer, Charles W ^b  

^a MCGILL UNIVERSITY   (Canada)

^b NATIONAL RESEARCH COUNCIL CANADA   (Canada)

Author keywords

Antarctic; Arctic; Bacteria; Biodegradation; Biogeochemistry; Competition; Fungi; Microbial communities; Soil

Indexed keywords

EID: 84901229596     PISSN: None     EISSN: 20797737     Source Type: Journal    
DOI: 10.3390/biology2020533     Document Type: Review

References (137)

1. Connell, J.H. The influence of interspecific competition and other factors on the distribution of the barnacle Chthamalus stellatus. Ecology 1961, 42, 710-723.
2. Huisman, J.; Weissing, F.J. Biodiversity of plankton by species oscillations and chaos. Nature 1999, 402, 407-410.
3. Van Nes, E.H.; Scheffer, M. Large species shifts triggered by small forces. Am. Nat. 2004, 164, 255-266.
4. Beninca, E.; Huisman, J.; Heerkloss, R.; Johnk, K.D.; Branco, P.; van Nes, E.H.; Scheffer, M.; Ellner, S.P. Chaos in a long-term experiment with a plankton community. Nature 2008, 451, 822-825.
5. Deslippe, J.R.; Hartmann, M.; Simard, S.W.; Mohn, W.W. Long-term warming alters the composition of arctic soil microbial communities. FEMS Microbiol. Ecol. 2012, 82, 303-315.
6. Yergeau, E.; Bokhorst, S.; Kang, S.; Zhou, J.Z.; Greer, C.W.; Aerts, R.; Kowalchuk, G.A. Shifts in soil microorganisms in response to warming are consistent across a range of antarctic environments. ISME J. 2012, 6, 692-702.
7. Barrett, L.G.; Bell, T.; Dwyer, G.; Bergelson, J. Cheating, trade-offs and the evolution of aggressiveness in a natural pathogen population. Ecol. Lett. 2011, 14, 1149-1157.
8. Kreth, J.; Merritt, J.; Shi, W.Y.; Qi, F.X. Competition and coexistence between Streptococcus mutans and Streptococcus sanguinis in the dental biofilm. J. Bacteriol. 2005, 187, 7193-7203.
9. Lopez-Garcia, S.L.; Vazquez, T.E.E.; Favelukes, G.; Lodeiro, A.R. Rhizobial position as a main determinant in the problem of competition for nodulation in soybean. Environ. Microbiol. 2002, 4, 216-224.
10. van Elsas, J.D.; Chiurazzi, M.; Mallon, C.A.; Elhottova, D.; Kristufek, V.; Salles, J.F. Microbial diversity determines the invasion of soil by a bacterial pathogen. Proc. Natl. Acad. Sci. USA 2012, 109, 1159-1164.
11. O'Brien, A.; Sharp, R.; Russell, N.J.; Roller, S. Antarctic bacteria inhibit growth of food-borne microorganisms at low temperatures. FEMS Microbiol. Ecol. 2004, 48, 157-167.
12. Bell, T.H.; Yergeau, E.; Juck, D.; Whyte, L.G.; Greer, C.W. Alteration of microbial community structure affects diesel degradation in an arctic soil. FEMS Microbiol. Ecol. 2013, in press.
13. Bullock, J.M.; Pywell, R.F.; Burke, M.J.W.; Walker, K.J. Restoration of biodiversity enhances agricultural production. Ecol. Lett. 2001, 4, 185-189.
14. Doherty, J.M.; Callaway, J.C.; Zedler, J.B. Diversity-function relationships changed in a long-term restoration experiment. Ecol. Appl. 2011, 21, 2143-2155.
15. Fargione, J.; Tilman, D.; Dybzinski, R.; Lambers, J.H.; Clark, C.; Harpole, W.S.; Knops, J.M.H.; Reich, P.B.; Loreau, M. From selection to complementarity: Shifts in the causes of biodiversityproductivity relationships in a long-term biodiversity experiment. Proc. Roy. Soc. B 2007, 274, 871-876.
16. Foster, K.R.; Bell, T. Competition, not cooperation, dominates interactions among culturable microbial species. Curr. Biol. 2012, 22, 1845-1850.
17. Peter, H.; Beier, S.; Bertilsson, S.; Lindström, E.S.; Langenheder, S.; Tranvik, L.J. Functionspecific response to depletion of microbial diversity. ISME J. 2011, 5, 351-361.
18. Salles, J.F.; Poly, F.; Schmid, B.; Le Roux, X. Community niche predicts the functioning of denitrifying bacterial assemblages. Ecology 2009, 90, 3324-3332.
19. Strickland, M.S.; Lauber, C.; Fierer, N.; Bradford, M.A. Testing the functional significance of microbial community composition. Ecology 2009, 90, 441-451.
20. Degens, B.P. Decreases in microbial functional diversity do not result in corresponding changes in decomposition under different moisture conditions. Soil Biol. Biochem. 1998, 30, 1989-2000.
21. Griffiths, B.S.; Ritz, K.; Bardgett, R.D.; Cook, R.; Christensen, S.; Ekelund, F.; Sørensen, S.J.; Bååth, E.; Bloem, J.; de Ruiter, P.C.; et al. Ecosystem response of pasture soil communities to fumigation-induced microbial diversity reductions: An examination of the biodiversity-ecosystem function relationship. Oikos 2000, 90, 279-294.
22. Fournier, G.; Fournier, J.C. Effect of microbial competition on the survival and activity of 2,4-d-degrading Alcaligenes xylosoxidans subsp. Denitrificans added to soil. Lett. Appl. Microbiol. 1993, 16, 178-181.
23. Hibbing, M.E.; Fuqua, C.; Parsek, M.R.; Peterson, S.B. Bacterial competition: Surviving and thriving in the microbial jungle. Nat. Rev. Microbiol. 2010, 8, 15-25.
24. Little, A.E.F.; Robinson, C.J.; Peterson, S.B.; Raffa, K.E.; Handelsman, J. Rules of engagement: Interspecies interactions that regulate microbial communities. Annu. Rev. Microbiol. 2008, 62, 375-401.
25. Roesch, L.F.; Fulthorpe, R.R.; Riva, A.; Casella, G.; Hadwin, A.K.M.; Kent, A.D.; Daroub, S.H.; Camargo, F.A.O.; Farmerie, W.G.; Triplett, E.W. Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J. 2007, 1, 283-290.
26. Chu, H.Y.; 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. Microbiol. 2010, 12, 2998-3006.
27. Neufeld, J.D.; Mohn, W.W. Unexpectedly high bacterial diversity in arctic tundra relative to boreal forest soils, revealed by serial analysis of ribosomal sequence tags. Appl. Environ. Microb. 2005, 71, 5710-5718.
28. 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.
29. Prasad, S.; Manasa, P.; Buddhi, S.; Singh, S.M.; Shivaji, S. Antagonistic interaction networks among bacteria from a cold soil environment. FEMS Microbiol. Ecol. 2011, 78, 376-385.
30. Wong, C.M.V.L.; Tam, H.K.; Alias, S.A.; Gonzalez, M.; Gonzalez-Rocha, G.; Dominguez-Yevenes, M. Pseudomonas and pedobacter isolates from king george island inhibited the growth of foodborne pathogens. Pol. Polar Res. 2011, 32, 3-14.
31. Kotsyurbenko, O.R.; Glagolev, M.V.; Nozhevnikova, A.N.; Conrad, R. Competition between homoacetogenic bacteria and methanogenic archaea for hydrogen at low temperature. FEMS Microbiol. Ecol. 2001, 38, 153-159.
32. 15n]DNA-based stable isotope probing and pyrosequencing. Appl. Environ. Microb. 2011, 77, 4163-4171.
33. Siciliano, S.D.; Ma, W.K.; Ferguson, S.; Farrell, R.E. Nitrifier dominance of arctic soil nitrous oxide emissions arises due to fungal competition with denitrifiers for nitrate. Soil Biol. Biochem. 2009, 41, 1104-1110.
34. Steven, B.; Niederberger, T.D.; Bottos, E.M.; Dyen, M.R.; Whyte, L.G. Development of a sensitive radiorespiration method for detecting microbial activity at subzero temperatures. J. Microbiol. Methods 2007, 71, 275-280.
35. D'Amico, S.; Collins, T.; Marx, J.C.; Feller, G.; Gerday, C. Psychrophilic microorganisms: Challenges for life. EMBO Rep. 2006, 7, 385-389.
36. Fierer, N.; Jackson, R.B. The diversity and biogeography of soil bacterial communities. Proc. Natl. Acad. Sci. USA 2006, 103, 626-631.
37. Yergeau, E.; Schoondermark-Stolk, S.A.; Brodie, E.L.; Dejean, S.; DeSantis, T.Z.; Goncalves, O.; Piceno, Y.M.; Andersen, G.L.; Kowalchuk, G.A. Environmental microarray analyses of antarctic soil microbial communities. ISME J. 2009, 3, 340-351.
38. Chong, C.W.; Pearce, D.A.; Convey, P.; Tan, I.K.P. The identification of environmental parameters which could influence soil bacterial community composition on the antarctic peninsula: A statistical approach. Antarct Sci. 2012, 24, 249-258.
39. Mannisto, M.K.; Tiirola, M.; Haggblom, M.M. Bacterial communities in arctic fjelds of finnish lapland are stable but highly ph-dependent. FEMS Microbiol. Ecol. 2007, 59, 452-465.
40. Ganzert, L.; Lipski, A.; Hubberten, H.W.; Wagner, D. The impact of different soil parameters on the community structure of dominant bacteria from nine different soils located on livingston island, south shetland archipelago, antarctica. FEMS Microbiol. Ecol. 2011, 76, 476-491.
41. Bell, T.H.; Yergeau, E.; Maynard, C.; Juck, D.; Whyte, L.G.; Greer, C.W. Predictable bacterial composition and hydrocarbon degradation in arctic soils following diesel and nutrient disturbance. ISME J. 2013, doi:10.1038/ismej.2013.1031.
42. Dennis, P.G.; Rushton, S.P.; Newsham, K.K.; Lauducina, V.A.; Ord, V.J.; Daniell, T.J.; O'Donnell, A.G.; Hopkins, D.W. Soil fungal community composition does not alter along a latitudinal gradient through the maritime and sub-antarctic. Fungal Ecol. 2012, 5, 403-408.
43. Fujimura, K.E.; Egger, K.N. Host plant and environment influence community assembly of high arctic root-associated fungal communities. Fungal Ecol. 2012, 5, 409-418.
44. Arenz, B.E.; Blanchette, R.A. Distribution and abundance of soil fungi in antarctica at sites on the peninsula, ross sea region and mcmurdo dry valleys. Soil Biol. Biochem. 2011, 43, 308-315.
45. Powell, S.M.; Bowman, J.P.; Ferguson, S.H.; Snape, I. The importance of soil characteristics to the structure of alkane-degrading bacterial communities on sub-antarctic macquarie island. Soil Biol. Biochem. 2010, 42, 2012-2021.
46. Ramirez, K.S.; Craine, J.M.; Fierer, N. Consistent effects of nitrogen amendments on soil microbial communities and processes across biomes. Glob. Change Biol. 2012, 18, 1918-1927.
47. Campbell, B.J.; Polson, S.W.; Hanson, T.E.; Mack, M.C.; Schuur, E.A.G. The effect of nutrient deposition on bacterial communities in arctic tundra soil. Environ. Microbiol. 2010, 12, 1842-1854.
48. Urcelay, C.; Bret-Harte, M.S.; Diaz, S.; Chapin, F.S. Mycorrhizal colonization mediated by species interactions in arctic tundra. Oecologia 2003, 137, 399-404.
49. Robinson, C.H.; Saunders, P.W.; Madan, N.J.; Pryce-Miller, E.J.; Pentecost, A. Does nitrogen deposition affect soil microfungal diversity and soil n and p dynamics in a high arctic ecosystem? Glob. Change Biol. 2004, 10, 1065-1079.
50. Stomeo, F.; Makhalanyane, T.P.; Valverde, A.; Pointing, S.B.; Stevens, M.I.; Cary, C.S.; Tuffin, M.I.; Cowan, D.A. Abiotic factors influence microbial diversity in permanently cold soil horizons of a maritime-associated antarctic dry valley. FEMS Microbiol. Ecol. 2012, 82, 326-340.
51. Hoj, L.; Rusten, M.; Haugen, L.E.; Olsen, R.A.; Torsvik, V.L. Effects of water regime on archaeal community composition in arctic soils. Environ. Microbiol. 2006, 8, 984-996.
52. Fell, J.W.; Scorzetti, G.; Connell, L.; Craig, S. Biodiversity of micro-eukaryotes in antarctic dry valley soils with <5% soil moisture. Soil Biol. Biochem. 2006, 38, 3107-3119.
53. Bridge, P.D.; Newsham, K.K. Soil fungal community composition at mars oasis, a southern maritime antarctic site, assessed by pcr amplification and cloning. Fungal Ecol. 2009, 2, 66-74.
54. Liebner, S.; Harder, J.; Wagner, D. Bacterial diversity and community structure in polygonal tundra soils from samoylov island, lena delta, siberia. Int. Microbiol. 2008, 11, 195-202.
55. Aislabie, J.M.; Jordan, S.; Barker, G.M. Relation between soil classification and bacterial diversity in soils of the ross sea region, antarctica. Geoderma 2008, 144, 9-20.
56. Tosi, S.; Onofri, S.; Brusoni, M.; Zucconi, L.; Vishniac, H. Response of antarctic soil fungal assemblages to experimental warming and reduction of uv radiation. Polar Biol. 2005, 28, 470-482.
57. Feller, G.; Gerday, C. Psychrophilic enzymes: Hot topics in cold adaptation. Nat. Rev. Microbiol. 2003, 1, 200-208.
58. Cavicchioli, R. Cold-adapted archaea. Nat. Rev. Microbiol. 2006, 4, 331-343.
59. Harder, W.; Veldkamp, H. Competition of marine psychrophilic bacteria at low temperatures. Antonie Van Leeuwenhoek 1971, 37, 51-63.
60. Nedwell, D.B.; Rutter, M. Influence of temperature on growth rate and competition between two psychrotolerant antarctic bacteria: Low temperature diminishes affinity for substrate uptake. Appl. Environ. Microb. 1994, 60, 1984-1992.
61. Knoblauch, C.; Jorgensen, B.B. Effect of temperature on sulphate reduction, growth rate and growth yield in five psychrophilic sulphate-reducing bacteria from arctic sediments. Environ. Microbiol. 1999, 1, 457-467.
62. Margesin, R. Effect of temperature on growth parameters of psychrophilic bacteria and yeasts. Extremophiles 2009, 13, 257-262.
63. Hillebrand, H. On the generality of the latitudinal diversity gradient. Am. Nat. 2004, 163, 192-211.
64. Hogg, I.D.; Cary, S.C.; Convey, P.; Newsham, K.K.; O'Donnell, A.G.; Adams, B.J.; Aislabie, J.; Frati, F.; Stevens, M.I.; Wall, D.H. Biotic interactions in antarctic terrestrial ecosystems: Are they a factor? Soil Biol. Biochem. 2006, 38, 3035-3040.
65. Teixeira, L.C.R.S.; 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.
66. Allen, B.; Willner, D.; Oechel, W.C.; Lipson, D. Top-down control of microbial activity and biomass in an arctic soil ecosystem. Environ. Microbiol. 2010, 12, 642-648.
67. Newsham, K.K.; Rolf, J.; Pearce, D.A.; Strachan, R.J. Differing preferences of antarctic soil nematodes for microbial prey. Eur. J. Soil Biol. 2004, 40, 1-8.
68. Williamson, L.L.; Borlee, B.R.; Schloss, P.D.; Guan, C.H.; Allen, H.K.; Handelsman, J. Intracellular screen to identify metagenomic clones that induce or inhibit a quorum-sensing biosensor. Appl. Environ. Microb. 2005, 71, 6335-6344.
69. Deming, J.W. Psychrophiles and polar regions. Curr. Opin. Microbiol. 2002, 5, 301-309.
70. Lifshitz, R.; Kloepper, J.W.; Scher, F.M.; Tipping, E.M.; Laliberte, M. Nitrogen-fixing pseudomonads isolated from roots of plants grown in the canadian high arctic. Appl. Environ. Microb. 1986, 51, 251-255.
71. D'Costa, V.M.; King, C.E.; Kalan, L.; Morar, M.; Sung, W.W.L.; Schwarz, C.; Froese, D.; Zazula, G.; Calmels, F.; Debruyne, R.; et al. Antibiotic resistance is ancient. Nature 2011, 477, 457-461.
72. Ma, Y.F.; Wang, L.; Shao, Z.Z. Pseudomonas, the dominant polycyclic aromatic hydrocarbondegrading bacteria isolated from antarctic soils and the role of large plasmids in horizontal gene transfer. Environ. Microbiol. 2006, 8, 455-465.
73. Martinez-Rosales, C.; Fullana, N.; Musto, H.; Castro-Sowinski, S. Antarctic DNA moving forward: Genomic plasticity and biotechnological potential. FEMS Microbiol. Lett. 2012, 331, 1-9.
74. Fujiyoshi, M.; Yoshitake, S.; Watanabe, K.; Murota, K.; Tsuchiya, Y.; Uchida, M.; Nakatsubo, T. Successional changes in ectomycorrhizal fungi associated with the polar willow salix polaris in a deglaciated area in the high arctic, svalbard. Polar Biol. 2011, 34, 667-673.
75. Sundqvist, M.K.; Giesler, R.; Graae, B.J.; Wallander, H.; Fogelberg, E.; Wardle, D.A. Interactive effects of vegetation type and elevation on aboveground and belowground properties in a subarctic tundra. Oikos 2011, 120, 128-142.
76. Deslippe, J.R.; Simard, S.W. Below-ground carbon transfer among betula nana may increase with warming in arctic tundra. New Phytol. 2011, 192, 689-698.
77. 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.
78. Reed, H.E.; Martiny, J.B.H. Testing the functional significance of microbial composition in natural communities. FEMS Microbiol. Ecol. 2007, 62, 161-170.
79. Singh, B.K.; Bardgett, R.D.; Smith, P.; Reay, D.S. Microorganisms and climate change: Terrestrial feedbacks and mitigation options. Nat. Rev. Microbiol. 2010, 8, 779-790.
80. Wagner, D.; Liebner, S. Global warming and carbon dynamics in permafrost soils: Methane production and oxidation. In Permafrost Soils; Margesin, R., Ed.; Springer Berlin Heidelberg: Berlin, Heidelberg, Germany, 2009; pp. 219-236.
81. Wagner, D.; Gattinger, A.; Embacher, A.; Pfeiffer, E.M.; Schloter, M.; Lipski, A. Methanogenic activity and biomass in holocene permafrost deposits of the lena delta, siberian arctic and its implication for the global methane budge. Glob. Change Biol. 2007, 13, 1089-1099.
82. Ho, A.; Luke, C.; Frenzel, P. Recovery of methanotrophs from disturbance: Population dynamics, evenness and functioning. ISME J. 2011, 5, 750-758.
83. Martineau, C.; Whyte, L.G.; Greer, C.W. Stable isotope probing analysis of the diversity and activity of methanotrophic bacteria in soils from the canadian high arctic. Appl. Environ. Microb. 2010, 76, 5773-5784.
84. Achtnich, C.; Bak, F.; Conrad, R. Competition for electron donors among nitrate reducers, ferric iron reducers, sulfate reducers, and methanogens in anoxic paddy soil. Biol. Fertil. Soils 1995, 19, 65-72.
85. Stibal, M.; Wadham, J.L.; Lis, G.P.; Telling, J.; Pancost, R.D.; Dubnick, A.; Sharp, M.J.; Lawson, E.C.; Butler, C.E.H.; Hasan, F.; et al. Methanogenic potential of arctic and antarctic subglacial environments with contrasting organic carbon sources. Glob. Change Biol. 2012, 18, 3332-3345.
86. IPCC. Climate Change 2007: The Physical Science Basis; Cambridge University Press: Cambridge, UK, 2007.
87. Wrage, N.; Velthof, G.L.; van Beusichem, M.L.; Oenema, O. Role of nitrifier denitrification in the production of nitrous oxide. Soil Biol. Biochem. 2001, 33, 1723-1732.
88. Fierer, N.; Bradford, M.A.; Jackson, R.B. Toward an ecological classification of soil bacteria. Ecology 2007, 88, 1354-1364.
89. Tarnocai, C.; Canadell, J.G.; Schuur, E.A.G.; Kuhry, P.; Mazhitova, G.; Zimov, S. Soil organic carbon pools in the northern circumpolar permafrost region. Glob. Biogeochem. Cycles 2009, 23, doi: 10.1029/2008GB003327.
90. Tveit, A.; Schwacke, R.; Svenning, M.M.; Urich, T. Organic carbon transformations in high-arctic peat soil: Key functions and microorganisms. ISME J. 2013, 7, 299-311.
91. Meidute, S.; Demoling, F.; Bååth, E. Antagonistic and synergistic effects of fungal and bacterial growth in soil after adding different carbon and nitrogen sources. Soil Biol. Biochem. 2008, 40, 2334-2343.
92. Zak, D.R.; Kling, G.W. Microbial community composition and function across an arctic tundra landscape. Ecology 2006, 87, 1659-1670.
93. Greer, C.W.; Whyte, L.G.; Niederberger, T.D. Microbial communities in hydrocarbon-contaminated temperate, tropical, alpine, and polar soils. In Handbook of Hydrocarbon and Lipid Microbiology; Timmis, K.N., Ed.; Springer Berlin Heidelberg: Berlin, Germany; Heidelberg, Germany, 2010; pp. 2313-2328.
94. Aislabie, J.; Saul, D.J.; Foght, J.M. Bioremediation of hydrocarbon-contaminated polar soils. Extremophiles 2006, 10, 171-179.
95. Ciric, L.; Philp, J.C.; Whiteley, A.S. Hydrocarbon utilization within a diesel-degrading bacterial consortium. FEMS Microbiol. Lett. 2010, 303, 116-122.
96. Sorkhoh, N.A.; Ghannoum, M.A.; Ibrahim, A.S.; Stretton, R.J.; Radwan, S.S. Crude-oil and hydrocarbon-degrading strains of rhodococcus-rhodochrous isolated from soil and marine environments in kuwait. Environ. Pollut. 1990, 65, 1-17.
97. Whyte, L.G.; Hawari, J.; Zhou, E.; Bourbonnière, L.; Inniss, W.E.; Greer, C.W. Biodegradation of variable-chain-length alkanes at low temperatures by a psychrotrophic rhodococcus sp. Appl. Environ. Microb. 1998, 64, 2578-2584.
98. Yergeau, E.; Sanschagrin, S.; Beaumier, D.; Greer, C.W. Metagenomic analysis of the bioremediation of diesel-contaminated canadian high arctic soils. PLoS One 2012, 7, e30058.
99. Beschta, R.L.; Ripple, W.J. Large predators and trophic cascades in terrestrial ecosystems of the western united states. Biol. Conserv. 2009, 142, 2401-2414.
100. Falkowski, P.; Scholes, R.J.; Boyle, E.; Canadell, J.; Canfield, D.; Elser, J.; Gruber, N.; Hibbard, K.; Hogberg, P.; Linder, S.; et al. The global carbon cycle: A test of our knowledge of earth as a system. Science 2000, 290, 291-296.
101. 15n in symbiotic fungi and plants estimates nitrogen and carbon flux rates in arctic tundra. Ecology 2006, 87, 816-822.
102. 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.
103. Nordin, A.; Schmidt, I.K.; Shaver, G.R. Nitrogen uptake by arctic soil microbes and plants in relation to soil nitrogen supply. Ecology 2004, 85, 955-962.
104. Schmidt, I.K.; Michelsen, A.; Jonasson, S. Effects of labile soil carbon on nutrient partitioning between an arctic graminoid and microbes. Oecologia 1997, 112, 557-565.
105. Hodge, A.; Robinson, D.; Fitter, A. Are microorganisms more effective than plants at competing for nitrogen? Trends Plant Sci. 2000, 5, 304-308.
106. Buckeridge, K.M.; Jefferies, R.L. Vegetation loss alters soil nitrogen dynamics in an arctic salt marsh. J. Ecol. 2007, 95, 283-293.
107. Clemmensen, K.E.; Sorensen, P.L.; Michelsen, A.; Jonasson, S.; Strom, L. Site-dependent n uptake from n-form mixtures by arctic plants, soil microbes and ectomycorrhizal fungi. Oecologia 2008, 155, 771-783.
108. Edwards, K.A.; McCulloch, J.; Kershaw, G.P.; Jefferies, R.L. Soil microbial and nutrient dynamics in a wet arctic sedge meadow in late winter and early spring. Soil Biol. Biochem. 2006, 38, 2843-2851.
109. Hill, P.W.; Farrar, J.; Roberts, P.; Farrell, M.; Grant, H.; Newsham, K.K.; Hopkins, D.W.; Bardgett, R.D.; Jones, D.L. Vascular plant success in a warming antarctic may be due to efficient nitrogen acquisition. Nat. Clim. Change 2011, 1, 50-53.
110. Henry, H.A.L.; Jefferies, R.L. Plant amino acid uptake, soluble n turnover and microbial n capture in soils of a grazed arctic salt marsh. J. Ecol. 2003, 91, 627-636.
111. Chapin, F.S.; Moilanen, L.; Kielland, K. Preferential use of organic nitrogen for growth by a nonmycorrhizal arctic sedge. Nature 1993, 361, 150-153.
112. Vitousek, P.M.; Howarth, R.W. Nitrogen limitation on land and in the sea: How can it occur. Biogeochemistry 1991, 13, 87-115.
113. Vitousek, P.M.; Aber, J.D.; Howarth, R.W.; Likens, G.E.; Matson, P.A.; Schindler, D.W.; Schlesinger, W.H.; Tilman, D. Human alteration of the global nitrogen cycle: Sources and consequences. Ecol. Appl. 1997, 7, 737-750.
114. Imsenecki, A.A.; Popova, L.S.; Kirillova, N.F. Effect of nitrogen source on growth of arthrobacter simplex and its biosynthesis of cholinesterase. Mikrobiologiâ 1976, 45, 614-619.
115. Rice, C.W.; Tiedje, J.M. Regulation of nitrate assimilation by ammonium in soils and in isolated soil microorganisms. Soil Biol. Biochem. 1989, 21, 597-602.
116. Recous, S.; Mary, B.; Faurie, G. Microbial immobilization of ammonium and nitrate in cultivated soils. Soil Biol. Biochem. 1990, 22, 913-922.
117. Hill, P.W.; Farrell, M.; Roberts, P.; Farrar, J.; Grant, H.; Newsham, K.K.; Hopkins, D.W.; Bardgett, R.D.; Jones, D.L. Soil-and enantiomer-specific metabolism of amino acids and their peptides by antarctic soil microorganisms. Soil Biol. Biochem. 2011, 43, 2410-2416.
118. Fierer, N.; Lauber, C.L.; Ramirez, K.S.; Zaneveld, J.; Bradford, M.A.; Knight, R. Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. ISME J. 2012, 6, 1007-1017.
119. Powell, S.M.; Ferguson, S.H.; Snape, I.; Siciliano, S.D. Fertilization stimulates anaerobic fuel degradation of antarctic soils by denitrifying microorganisms. Environ. Sci. Technol. 2006, 40, 2011-2017.
120. Roy, R.; Greer, C.W. Hexadecane mineralization and denitrification in two diesel fuel-contaminated soils. FEMS Microbiol. Ecol. 2000, 32, 17-23.
121. Callaghan, T.V.; Bjorn, L.O.; Chernov, Y.; Chapin, T.; Christensen, T.R.; Huntley, B.; Ims, R.A.; Johansson, M.; Jolly, D.; Jonasson, S.; et al. Biodiversity, distributions and adaptations of arctic species in the context of environmental change. AMBIO 2004, 33, 404-417.
122. Allison, S.D.; Martiny, J.B.H. Resistance, resilience, and redundancy in microbial communities. Proc. Natl. Acad. Sci. USA 2008, 105, 11512-11519.
123. Lawrence, D.; Fiegna, F.; Behrends, V.; Bundy, J.G.; Phillimore, A.B.; Bell, T.; Barraclough, T.G. Species interactions alter evolutionary responses to a novel environment. PLoS Biol. 2012, 10, e1001330.
124. Olsson, P.A.; Eriksen, B.E.; Dahlberg, A. Colonization by arbuscular mycorrhizal and fine endophytic fungi in herbaceous vegetation in the canadian high arctic. Can. J. Bot. 2004, 82, 1547-1556.
125. Schmidt, I.K.; Jonasson, S.; Shaver, G.R.; Michelsen, A.; Nordin, A. Mineralization and distribution of nutrients in plants and microbes in four arctic ecosystems: Responses to warming. Plant Soil 2002, 242, 93-106.
126. Lamb, E.G.; Han, S.; Lanoil, B.D.; Henry, G.H.R.; Brummell, M.E.; Banerjee, S.; Siciliano, S.D. A high arctic soil ecosystem resists long-term environmental manipulations. Glob. Change Biol. 2011, 17, 3187-3194.
127. Barbéran, A.; Bates, S.T.; Casamayor, E.O.; Fierer, N. Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME J. 2012, 6, 343-351.
128. Pan, C.L.; Fischer, C.R.; Hyatt, D.; Bowen, B.P.; Hettich, R.L.; Banfield, J.F. Quantitative tracking of isotope flows in proteomes of microbial communities. Mol. Cell. Proteomics 2011, 10, M110.006049.
129. Griffiths, B.S.; Kuan, H.L.; Ritz, K.; Glover, L.A.; McCaig, A.E.; Fenwick, C. The relationship between microbial community structure and functional stability, tested experimentally in an upland pasture soil. Microb. Ecol. 2004, 47, 104-113.
130. Deni, J.; Penninckx, M.J. Nitrification and autotrophic nitrifying bacteria in a hydrocarbonpolluted soil. Appl. Environ. Microb. 1999, 65, 4008-4013.
131. Powell, S.J.; Prosser, J.I. Inhibition of ammonium oxidation by nitrapyrin in soil and liquid culture. Appl. Environ. Microb. 1986, 52, 782-787.
132. Bremner, J.M.; McCarty, G.W.; Yeomans, J.C.; Chai, H.S. Effects of phosphoroamides on nitrification, denitrification, and mineralization of organic nitrogen in soil. Commun. Soil Sci. Plant 1986, 17, 369-384.
133. Myrold, D.D.; Posavatz, N.R. Potential importance of bacteria and fungi in nitrate assimilation in soil. Soil Biol. Biochem. 2007, 39, 1737-1743.
134. Bremner, J.M.; Yeomans, J.C. Effects of nitrification inhibitors on denitrification of nitrate in soil. Biol. Fertil. Soils 1986, 2, 173-179.
135. Yeomans, J.C.; Bremner, J.M. Effects of urease inhibitors on denitrification in soil. Commun. Soil Sci. Plant 1986, 17, 63-73.
136. Winfrey, M.R.; Ward, D.M. Substrates for sulfate reduction and methane production in intertidal sediments. Appl. Environ. Microb. 1983, 45, 193-199.
137. Shen, N.; Ko, J.H.; Xiao, G.P.; Wesolowski, D.; Shan, G.; Geller, B.; Izadjoo, M.; Altman, S. Inactivation of expression of several genes in a variety of bacterial species by egs technology. Proc. Natl. Acad. Sci. USA 2009, 106, 8163-8168.