Significant and persistent impact of timber harvesting on soil microbial communities in Northern coniferous forests

ISME Journal

Volumn 6, Issue 12, 2012, Pages 2199-2218

  Hartmann, Martin ^a,f,g   Howes, Charles G ^a   Vaninsberghe, David ^a   Yu, Hang ^a,h   Bachar, Dipankar ^b,c   Christen, Richard ^b,c   Henrik Nilsson, Rolf ^d,e   Hallam, Steven J ^a   Mohn, William W ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b CNRS   (France)

^c UNIVERSITÉ CÔTE D'AZUR   (France)

^d UNIVERSITY OF GOTHENBURG   (Sweden)

^e UNIVERSITY OF TARTU   (Estonia)

^f AGROSCOPE RECKENHOLZ TÄNIKON RESEARCH STATION ART   (Switzerland)

^g SWISS FEDERAL RESEARCH INSTITUTE WSL   (Switzerland)

^h CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; FUNGAL DNA;

BIODIVERSITY; CONIFEROUS FOREST; DISTURBANCE; ECONOMIC DEVELOPMENT; ENERGY FLOW; FOREST ECOSYSTEM; FOREST MANAGEMENT; GENETIC MARKER; HOST-SYMBIONT INTERACTION; MICROBIAL COMMUNITY; SOIL MICROORGANISM; SOIL ORGANIC MATTER; STABILIZATION; SUSTAINABLE DEVELOPMENT; TAXONOMY; TIMBER HARVESTING;

ARTICLE; BACTERIUM; BIODIVERSITY; CANADA; CLASSIFICATION; CLUSTER ANALYSIS; CONIFER; DNA SEQUENCE; FORESTRY; FUNGUS; GENETIC MARKER; GENETICS; GROWTH, DEVELOPMENT AND AGING; MICROBIOLOGY; MULTIVARIATE ANALYSIS; TREE;

BACTERIA; BIODIVERSITY; BRITISH COLUMBIA; CLUSTER ANALYSIS; CONIFEROPHYTA; DNA, BACTERIAL; DNA, FUNGAL; FORESTRY; FUNGI; GENETIC MARKERS; MULTIVARIATE ANALYSIS; SEQUENCE ANALYSIS, DNA; SOIL MICROBIOLOGY; TREES;

BRITISH COLUMBIA; CANADA;

ACTINOBACTERIA; ACTINOBACTERIA (CLASS); ASCOMYCOTA; BACTERIA (MICROORGANISMS); FUNGI;

EID: 84871348772     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2012.84     Document Type: Article

References (120)

1. Allison SD, Martiny JBH. (2008). Resistance, resilience, and redundancy in microbial communities. Proc Natl Acad Sci USA 105: 11512-11519.
2. Allmér J, Stenlid J, Dahlberg A. (2009). Logging-residue extraction does not reduce the diversity of litter-layer saprotrophic fungi in three Swedish coniferous stands after 25 years. Can J Forest Res 39: 1737-1748.
3. Amann RI, Ludwig W, Schleifer KH. (1995). Phylogenetic identification and in-situ detection of individual microbial-cells without cultivation. Microbiol Rev 59: 143-169.
4. Anderson MJ. (2001). A new method for non-parametric multivariate analysis of variance. Aust J Ecol 26: 32-46.
5. Anderson MJ, Willis TJ. (2003). Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84: 511-525.
6. Anderson MJ. (2006). Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62: 245-253.
7. Attiwill PM, Weston CJ. (2008). Environmental interactions: forest soils. In: Evans J (ed). The Forests Handbook, An Overview of Forest Science. Wiley-Blackwell: Oxford, UK, pp 157-187.
8. Axelrood PE, Chow ML, Arnold CS, Lu K, McDermott JM, Davies J. (2002a). Cultivation-dependent characterization of bacterial diversity from British Columbia forest soils subjected to disturbance. Can J Microbiol 48: 643-654.
9. Axelrood PE, Chow ML, Radomski CC, McDermott JM, Davies J. (2002b). Molecular characterization of bacterial diversity from British Columbia forest soils subjected to disturbance. Can J Microbiol 48: 655-674.
10. Bååth E, Frostegård Å , Pennanen T, Fritze H. (1995). Microbial community structure and pH response in relation to soil organic matter quality in wood-ash fertilized, clear-cut or burned coniferous forest soils. Soil Biol Biochem 27: 229-240.
11. Bååth E, Anderson TH. (2003). Comparison of soil fungal/ bacterial ratios in a pH gradient using physiological and PLFA-based techniques. Soil Biol Biochem 35: 955-963.
12. Baldrian P, Kolarik M, Stursova M, Kopecky J, Valaskova V, Vetrovsky T et al. (2012). Active and total microbial communities in forest soil are largely different and highly stratified during decomposition. ISME J 6: 248-258.
13. Ballard TM. (2000). Impacts of forest management on northern forest soils. Forest Ecol Manag 133: 37-42.
14. Barengo N, Sieber TN, Holdenrieder O. (2000). Diversity of endophytic mycobiota in leaves and twigs of pubescent birch (Betula pubescens). Sydowia 52: 305-320.
15. Barrios E. (2007). Soil biota, ecosystem services and land productivity. Ecol Econ 64: 269-285.
16. Battigelli JP, Spence JR, Langor DW, Berch SM. (2004). Short-term impact of forest soil compaction and organic matter removal on soil mesofauna density and oribatid mite diversity. Can J Forest Res 34: 1136-1149.
17. Belser LW. (1979). Population ecology of nitrifying bacteria. Annu Rev Microbiol 33: 309-333.
18. Benjamini Y, Hochberg Y. (1995). Controlling the false discovery rate - a practical and powerful approach to multiple testing. J Roy Stat Soc B Met 57: 289-300.
19. Berch S, Morris D, Malcolm J. (2011). Intensive forest biomass harvesting and biodiversity in Canada: a summary of relevant issues. Forest Chron 87: 478-487.
20. Bonan GB. (2008). Forests and climate change: forcings, feedbacks, and the climate benefits of forests. Science 320: 1444-1449.
21. Bouxin G. (2005). Ginkgo, a multivariate analysis package. J Veg Sci 16: 355-359.
22. Bowman J. (2006). The methanotrophs - the families Methylococcaceae and Methylocystaceae. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds). The Prokaryotes. Springer: New York, pp 266-289.
23. Bray JR, Curtis JT. (1957). An ordination of the upland forest communities of southern Wisconsin. Ecol Monogr 27: 325-349.
24. Brockett BFT, Prescott CE, Grayston SJ. (2012). Soil moisture is the major factor influencing microbial community structure and enzyme activities across seven biogeoclimatic zones in western Canada. Soil Biol Biochem 44: 9-20.
25. Bruns TD, Bidartondo MI, Taylor DL. (2002). Host specificity in ectomycorrhizal communities: what do the exceptions tell us? Integr Comp Biol 42: 352-359.
26. Busse MD, Beattie SE, Powers RF, Sanchez FG, Tiarks AE. (2006). Microbial community responses in forest mineral soil to compaction, organic matter removal, and vegetation control. Can J Forest Res 36: 577-588.
27. Canadell JG, Raupach MR. (2008). Managing forests for climate change mitigation. Science 320: 1456-1457.
28. Chatterjee A, Vance GF, Pendall E, Stahl PD. (2008). Timber harvesting alters soil carbon mineralization and microbial community structure in coniferous forests. Soil Biol Biochem 40: 1901-1907.
29. Chow ML, Radomski CC, McDermott JM, Davies J, Axelrood PE. (2002). Molecular characterization of bacterial diversity in lodgepole pine (Pinus contorta) rhizosphere soils from British Columbia forest soils differing in disturbance and geographic source. FEMS Microbiol Ecol 42: 347-357.
30. Clarke KR. (1993). Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18: 117-143.
31. Clarke KR, Gorley RN. (2006). PRIMER v6: User Manual/ Tutorial, 6 edn. PRIMER-E: Plymouth.
32. 2 concentrations to forest soil compaction at the Long-term Soil Productivity sites in central British Columbia. Can J Soil Sci 80: 625-632.
33. De Cáceres M, Legendre P. (2009). Associations between species and groups of sites: indices and statistical inference. Ecology 90: 3566-3574.
34. De Cáceres M, Legendre P, Moretti M. (2010). Improving indicator species analysis by combining groups of sites. Oikos 119: 1674-1684.
35. Derringer G, Suich R. (1980). Simultaneous optimization of several response variables. J Qual Technol 12: 214-219.
36. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K et al. (2006). Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72: 5069-5072.
37. Díaz S, Fargione J, Chapin FS III, Tilman D. (2006). Biodiversity loss threatens human well-being. PLoS Biol 4: e277.
38. Dighton J, White JF, Oudemans P. (2005). The Fungal Community: Its Organization and Role in the Ecosystem. CRC Press: New York, USA.
39. Dominati E, Patterson M, Mackay A. (2010). A framework for classifying and quantifying the natural capital and ecosystem services of soils. Ecol Econ 69: 1858-1868.
40. Fahey TJ, Woodbury PB, Battles JJ, Goodale CL, Hamburg SP, Ollinger SV et al. (2010). Forest carbon storage: ecology, management, and policy. Front Ecol Environ 8: 245-252.
41. Fierer N, Schimel JP, Holden PA. (2003). Variations in microbial community composition through two soil depth profiles. Soil Biol Biochem 35: 167-176.
42. Frey B, Niklaus PA, Kremer J, Luscher P, Zimmermann S. (2011). Heavy machinery traffic impacts methane emission, abundance of methanogens and community structure in oxic forest soils. Appl Environ Microbiol 77: 6060-6068.
43. Good IJ. (1953). The population frequencies of species and the estimation of population parameters. Biometrika 40: 237-264.
44. Gower JC. (2005). Principal coordinates analysis. Encycl Biostat. John Wiley & Sons, Ltd: Oxford, UK. http://dx.doi.org/10.1002/0470011815. b2a13070.
45. Greacen EL, Sands R. (1980). Compaction of forest soils - a review. Aust J Soil Res 18: 163-189.
46. Grigal DF. (2000). Effects of extensive forest management on soil productivity. Forest Ecol Manag 138: 167-185.
47. Hannam KD, Quideau SA, Kishchuk BE. (2006). Forest floor microbial communities in relation to stand composition and timber harvesting in northern Alberta. Soil Biol Biochem 38: 2565-2575.
48. Hartmann M, Lee S, Hallam SJ, Mohn WW. (2009). Bacterial, archaeal and eukaryal community structures throughout soil horizons of harvested and naturally disturbed forest stands. Environ Microbiol 11: 3045-3062.
49. Hartmann M, Howes CG, Abarenkov K, Mohn WW, Nilsson RH. (2010). V-Xtractor: An open-source, high-throughput software tool to identify and extract hypervariable regions of small subunit (16S/18S) ribosomal RNA gene sequences. J Microbiol Methods 83: 250-253.
50. Holcomb RW. (1996). The Long-Term Soil Productivity study in British Columbia. FRDA report 256. Canadian Forest Service and British Columbia Ministry of Forests: Victoria, BC, Canada.
51. Hope GD. (2006). Establishment of long-term soil productivity studies on acidic soils in the interior douglas-fir zone. LTSP Research Note. British Columbia Ministry of Forests and Range: Victoria BC, Canada, p 4.
52. Jeraldo P, Chia N, Goldenfeld N. (2011). On the suitability of short reads of 16S rRNA for phylogeny-based analyses in environmental surveys. Environ Microbiol 13: 3000-3009.
53. Jones MD, Durall DM, Cairney JWG. (2003). Ectomycorrhizal fungal communities in young forest stands regenerating after clearcut logging. New Phytol 157: 399-422.
54. Josefsson T, Olsson J, Östlund L. (2010). Linking forest history and conservation efforts: long-term impact of low-intensity timber harvest on forest structure and wood-inhabiting fungi in northern Sweden. Biol Conserv 143: 1803-1811.
55. Jurgensen MF, Harvey AE, Graham RT, Page-Dumroese DS, Tonn JR, Larsen MJ et al. (1997). Impacts of timber harvesting on soil organic matter, nitrogen, productivity, and health of Inland Northwest forests. Forest Sci 43: 234-251.
56. Käll L, Storey JD, Noble WS. (2009). Qvality: nonparametric estimation of q-values and posterior error probabilities. Bioinformatics 25: 964-966.
57. Keenan RJ, Kimmins JP. (1993). The ecological effects of clear-cutting. Environ Rev 1: 121-144.
58. Kirby R. (2005). Actinomycetes and lignin degradation. In: Laskin AI, Bennett JW, Gadd GM, Sariaslani S (eds). Adv Appl Microbiol. Elsevier Academic Press Inc: San Diego, USA, pp 125-168.
59. Kirschbaum MUF. (2003). To sink or burn? A discussion of the potential contributions of forests to greenhouse gas balances through storing carbon or providing biofuels. Biomass Bioenerg 24: 297-310.
60. Kozlowski TT. (1999). Soil compaction and growth of woody plants. Scan J Forest Res 14: 596-619.
61. Kramer C, Gleixner G. (2008). Soil organic matter in soil depth profiles: distinct carbon preferences of microbial groups during carbon transformation. Soil Biol Biochem 40: 425-433.
62. Kranabetter JM, Chapman BK. (1999). Effects of forest soil compaction and organic matter removal on leaf litter decomposition in central British Columbia. Can J Soil Sci 79: 543-550.
63. Kranabetter JM, Sanborn P, Chapman WK, Dubé S. (2006). The contrasting response to soil disturbance between lodgepole pine and hybrid white spruce in subboreal forests. Soil Sci Soc Am J 70: 1591-1599.
64. Kretzer AM, King ZR, Bai S. (2009). Bacterial communities associated with tuberculate ectomycorrhizae of Rhizopogon spp. Mycorrhiza 19: 277-282.
65. Lane DJ. (1991). 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds). Nucleic Acid Techniques in Bacterial Systematics. John Wiley and Sons: Chichester, NY, pp 115-175.
66. Letunic I, Bork P. (2011). Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res 39: W475-W478.
67. Levenshtein V. (1966). Binary codes capable of correcting deletions, insertions, and reversals. Soviet Physics Doklady 10: 707-710.
68. Li Q, Allen HL, Wilson CA. (2003). Nitrogen mineralization dynamics following the establishment of a loblolly pine plantation. Can J Forest Res 33: 364-374.
69. Li QC, Allen HL, Wollum AG. (2004). Microbial biomass and bacterial functional diversity in forest soils: effects of organic matter removal, compaction, and vegetation control. Soil Biol Biochem 36: 571-579.
70. Lovie P. (2005). Coefficient of variation. Encyc Stat Behav Sci. John Wiley & Sons, Ltd: Oxford, UK. http://dx.doi.org/10.1002/0470013192.bsa107.
71. Margulies M, Egholm M, Altman W, Attiya S, Bader J, Bemben L et al. (2005). Genome sequencing in microfabricated high-density picolitre reactors. Nature 437: 376-380.
72. Mariani L, Chang SX, Kabzems R. (2006). Effects of tree harvesting, forest floor removal, and compaction on soil microbial biomass, microbial respiration, and N availability in a boreal aspen forest in British Columbia. Soil Biol Biochem 38: 1734-1744.
73. Marshall VG. (2000). Impacts of forest harvesting on biological processes in northern forest soils. Forest Ecol Manag 133: 43-60.
74. McCarthy AJ, Williams ST. (1992). Actinomycetes as agents of biodegradation in the environment - a review. Gene 115: 189-192.
75. Michel HM, Williams MA. (2011). Soil habitat and horizon properties impact bacterial diversity and composition. Soil Sci Soc Am J 75: 1440-1448.
76. Miles L, Kapos V. (2008). Reducing greenhouse gas emissions from deforestation and forest degradation: global land-use implications. Science 320: 1454-1455.
77. Mummey DL, Clarke JT, Cole CA, O'Connor BG, Gannon JE, Ramsey PW. (2010). Spatial analysis reveals differences in soil microbial community interactions between adjacent coniferous forest and clearcut ecosystems. Soil Biol Biochem 42: 1138-1147.
78. Nacke H, Thürmer A, Wollherr A, Will C, Hodac L, Herold N et al. (2011). Pyrosequencing-based assessment of bacterial community structure along different management types in German forest and grassland soils. PLoS One 6: e17000.
79. Needleman SB, Wunsch CD. (1970). A general method applicable to search for similarities in amino acid sequence of 2 proteins. J Mol Biol 48: 443-453.
80. Nilsson RH, Bok G, Ryberg M, Kristiansson E, Hallenberg N. (2009a). A software pipeline for processing and identification of fungal ITS sequences. Source Code Biol Med 4: 1.
81. Nilsson RH, Ryberg M, Abarenkov K, Sjokvist E, Kristiansson E. (2009b). The ITS region as a target for characterization of fungal communities using emerging sequencing technologies. FEMS Microbiol Lett 296: 97-101.
82. Nilsson RH, Veldre V, Hartmann M, Unterseher M, Amend A, Bergsten J et al. (2010). An open source software package for automated extraction of ITS1 and ITS2 from fungal ITS sequences for use in high-throughput community assays and molecular ecology. Fungal Ecol 3: 284-287.
83. Nordén B, Ryberg M, Götmark F, Olausson B. (2004). Relative importance of coarse and fine woody debris for the diversity of wood-inhabiting fungi in temperate broadleaf forests. Biol Conserv 117: 1-10.
84. Normile D. (2010). Saving forests to save biodiversity. Science 329: 1278-1280.
85. Page-Dumroese DS, Jurgensen MF, Tiarks AE, Ponder F, Sanchez FG, Fleming RL et al. (2006). Soil physical property changes at the North American Long-Term Soil Productivity study sites: 1 and 5 years after compaction. Can J Forest Res 36: 551-564.
86. Paul LR, Chapman BK, Chanway CP. (2007). Nitrogen fixation associated with Suillus tomentosus tuberculate ectomycorrhizae on Pinus contorta var. latifolia. Ann Bot 99: 1101-1109.
87. Ponder F, Tadros M. (2002). Phospholipid fatty acids in forest soil four years after organic matter removal and soil compaction. Appl Soil Ecol 19: 173-182.
88. Ponder F, Fleming RL, Berch S, Busse MD, Elioff JD, Hazlett PW et al. (2012). Effects of organic matter removal, soil compaction and vegetation control on 10th year biomass and foliar nutrition: LTSP continentwide comparisons. Forest Ecol Manag 278: 35-54.
89. Powers RF. (1999). On the sustainable productivity of planted forests. New Forest 17: 263-306.
90. Powers RF, Scott DA, Sanchez FG, Voldseth RA, Page- Dumroese D, Elioff JD et al. (2005). The North American long-term soil productivity experiment: findings from the first decade of research. Forest Ecol Manag 220: 31-50.
91. Powers RF. (2006). Long-term soil productivity: genesis of the concept and principles behind the program. Can J Forest Res 36: 519-528.
92. Quince C, Lanzen A, Curtis TP, Davenport RJ, Hall N, Head IM et al. (2009). Accurate determination of microbial diversity from 454 pyrosequencing data. Nat Methods 6: 639-641.
93. Sanborn P, Kranabetter JM, Chapman BK. (2000). Nutrient removals in woody biomass: preliminary estimates from the sub-boreal spruce long-term soil productivity study. LTSP Research Note. Brisith Columbia Ministry of Forests and Range: Victoria BC, Canada, p 6.
94. Sanchez FG, Scott DA, Ludovici KH. (2006a). Negligible effects of severe organic matter removal and soil compaction on loblolly pine growth over 10 years. Forest Ecol Manag 227: 145-154.
95. Sanchez FG, Tiarks AE, Kranabetter JM, Page-Dumroese DS, Powers RF, Sanborn PT et al. (2006b). Effects of organic matter removal and soil compaction on fifthyear mineral soil carbon and nitrogen contents for sites across the United States and Canada. Can J Forest Res 36: 565-576.
96. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB et al. (2009). Introducing mothur: opensource, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75: 7537-7541.
97. Schnurr-Pütz S, Bååth E, Guggenberger G, Drake HL, Kusel K. (2006). Compaction of forest soil by logging machinery favours occurrence of prokaryotes. FEMS Microbiol Ecol 58: 503-516.
98. Shestak CJ, Busse MD. (2005). Compaction alters physical but not biological indices of soil health. Soil Sci Soc Am J 69: 236-246.
99. Simard SW, Jones MD, Durall DM, Hope GD, Stathers RJ, Sorensen NS et al. (2003). Chemical and mechanical site preparation: effects on Pinus contorta growth, physiology, and microsite quality on grassy, steep forest sites in British Columbia. Can J Forest Res 33: 1495-1515.
100. Simard SW. (2009). Response diversity of ectomycorrhizas in forest succession following disturbance. In: Azcón-Aguilar C, Barea JM, Gianinazzi S, Gianinazzi-Pearson V (eds). Mycorrhizas - Functional Processes and Ecological Impact. Springer: Heidelberg, Germany, pp 1-19.
101. Simpson EH. (1949). Measurement of diversity. Nature 163: 688.
102. Singh BK, Bardgett RD, Smith P, Reay DS. (2010). Microorganisms and climate change: terrestrial feedbacks and mitigation options. Nat Rev Microbiol 8: 779-790.
103. Staddon WJ, Duchesne LC, Trevors JT. (1999). The role of microbial indicators of soil quality in ecological forest management. Forest Chron 75: 81-86.
104. Sundquist A, Bigdeli S, Jalili R, Druzin M, Waller S, Pullen K et al. (2007). Bacterial flora-typing with targeted, chip-based pyrosequencing. BMC Microbiol 7: 108.
105. Tan X, Chang SX, Kabzems R. (2008). Soil compaction and forest floor removal reduced microbial biomass and enzyme activities in a boreal aspen forest soil. Biol Fert Soils 44: 471-479.
106. Tedersoo L, May TW, Smith ME. (2010a). Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20: 217-263.
107. Tedersoo L, Nilsson RH, Abarenkov K, Jairus T, Sadam A, Saar I et al. (2010b). 454 pyrosequencing and Sanger sequencing of tropical mycorrhizal fungi provide similar results but reveal substantial methodological biases. New Phytol 188: 291-301.
108. Turnbaugh P, Quince C, Faith J, McHardy A, Yatsunenko T, Niazi F et al. (2010). Organismal, genetic, and transcriptional variation in the deeply sequenced gut microbiomes of identical twins. Proc Natl Acad Sci USA 107: 7503-7508.
109. Verschuyl J, Riffell S, Miller D, Wigley TB. (2011). Biodiversity response to intensive biomass production from forest thinning in North American forests - a meta-analysis. Forest Ecol Manag 261: 221-232.
110. von Wilpert K, Schäffer J. (2006). Ecological effects of soil compaction and initial recovery dynamics: a preliminary study. Eur J Forest Res 125: 129-138.
111. Vucetich JA, Waite TA, Qvarnemark L, Ibargüen S. (2000). Review: Population variability and extinction risk. Conserv Biol 14: 1704-1714.
112. Walmsley JD, Jones DL, Reynolds B, Price MH, Healey JR. (2009). Whole tree harvesting can reduce second rotation forest productivity. Forest Ecol Manag 257: 1104-1111.
113. Wang Q, Garrity GM, Tiedje JM, Cole JR. (2007). Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73: 5261-5267.
114. Wei X, Liu W, Waterhouse J, Armleder M. (2000). Simulations on impacts of different management strategies on long-term site productivity in lodgepole pine forests of the central interior of British Columbia. Forest Ecol Manag 133: 217-229.
115. White TJ, Bruns T, Lee S, Taylor J. (1990). Amplification and direct sequencing of fungal ribosomal RNA for phylogenetics. In: Innis MA, Gelfand DH, Sninsko JJ, White TJ (eds) PCR Protocols: a Guide to Methods and Applications. Academic Press: San Diego, pp 315-322.
116. Will C, Thurmer A, Wollherr A, Nacke H, Herold N, Schrumpf M et al. (2010). Horizon-specific bacterial community composition of german grassland soils, as revealed by pyrosequencing-based analysis of 16S rRNA genes. Appl Environ Microbiol 76: 6751-6759.
117. Worrell R, Hampson A. (1997). The influence of some forest operations on the sustainable management of forest soils - A review. Forestry 70: 61-85.
118. Wright DA, Killham K, Glover LA, Prosser JI. (1995). Role of pore size location in determining bacterial activity during predation by protozoa in soil. Appl Environ Microbiol 61: 3537-3543.
119. Zehr JP, Jenkins BD, Short SM, Steward GF. (2003). Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environ Microbiol 5: 539-554.
120. Zumft W. (1997). Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61: 533-616.