Microbial functional genes involved in nitrogen fixation, nitrification and denitrification in forest ecosystems

Soil Biology and Biochemistry

Volumn 75, Issue , 2014, Pages 11-25

  Levy Booth, David J ^a   Prescott, Cindy E ^a   Grayston, Susan J ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Denitrification; Forest; Functional genes; Nitrification; Nitrogen cycling; Nitrous oxide

Indexed keywords

AMMONIA; BACTERIA; CLIMATE CHANGE; DENITRIFICATION; DEPOSITION; ECOSYSTEMS; GENES; GREENHOUSE GASES; GROUNDWATER; METEOROLOGICAL PROBLEMS; NITRIFICATION; NITROGEN; NITROGEN FERTILIZERS; NITROGEN FIXATION; NITROGEN OXIDES; SOCIAL SCIENCES; SOILS; WATER POLLUTION;

AMMONIA OXIDIZING BACTERIA; ATMOSPHERIC DEPOSITIONS; FOREST; FUNCTIONAL GENES; NITRIFICATION AND DENITRIFICATION; NITRIFICATION-DENITRIFICATION; NITROGEN CYCLING; NITROUS OXIDE;

FORESTRY;

ABUNDANCE; ATMOSPHERIC DEPOSITION; CLIMATE CHANGE; COMMUNITY STRUCTURE; DENITRIFICATION; FOREST ECOSYSTEM; FOREST SOIL; GENE EXPRESSION; GREENHOUSE GAS; MICROBIAL ACTIVITY; MICROBIAL COMMUNITY; MOLECULAR ANALYSIS; NITROGEN CYCLE; NITROGEN FIXATION; PH; SOIL MICROORGANISM; STAND STRUCTURE;

AMMONIA; BACTERIA; DEPOSITION; ECOSYSTEMS; FERTILIZERS; FORESTRY; GENES; GREENHOUSE GASES; GROUND WATER; NITROGEN; NITROGEN OXIDES; NITROUS OXIDE; SOIL; WATER POLLUTION;

EUROPE; NORTH AMERICA;

EID: 84898976684     PISSN: 00380717     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.soilbio.2014.03.021     Document Type: Review

References (209)

1. Adair K.L., Schwartz E. Evidence that ammonia-oxidizing archaea are more abundant than ammonia-oxidizing bacteria in semiarid soils of northern Arizona, USA. Microbial Ecology 2008, 56:420-426.
2. Alvarez L., Bricio C., José Gómez M., Berenguer J. Lateral transfer of the denitrification pathway genes among thermus thermophilus strains. Applied and Environmental Microbiology February 15, 2011, 77:1352-1358.
3. 2-fixation and growth promotion in cedar colonized by an endophytic strain of Paenibacillus polymyxa. Biology and Fertility of Soils 2010, 49:235-239.
4. Anand R., Chanway C.P. Detection of GFP-labeled Paenibacillus polymyxa in autofluorescing pine seedling tissue. Biology and Fertility of Soils 2013, 49:111-118.
5. 2-fixation and seedling growth promotion of lodgepole pine by endophytic Paenibacillus polymyxa. Microbial Ecology 2013, 66:369-374.
6. Andert J., Börjesson G., Hallin S. Temporal changes in methane oxidizing and denitrifying communities and their activities in a drained peat soil. Wetlands 2012, 32:1047-1055.
7. Baalsrud K., Baalsrud K.S. Studies on Thiobacillus denitrificans. Archives of Microbiology 1954, 20:34-62.
8. Bäckman J.S.K., Hermansson A., Tebbe C.C., Lindgren P. Liming induces growth of a diverse flora of ammonia-oxidising bacteria in acid spruce forest soil as determined by SSCP and DGGE. Soil Biology and Biochemistry 2003, 35:1337-1347.
9. Ball P.N., MacKenzie M.D., DeLuca T.H., Montana W.E.H. Wildfire and charcoal enhance nitrification and ammonium-oxidizing bacterial abundance in dry montane forest soils. Journal of Environmental Quality 2010, 39:1243-1253.
10. Bárta J., Melichová T., Vaněk D., Picek T., Šantrůčková H. Effect of pH and dissolved organic matter on the abundance of nirK and nirS denitrifiers in spruce forest soil. Biogeochemistry 2010, 101:123-132.
11. Bartossek R., Nicol G.W., Lanzen A., Klenk H.P., Schleper C. Homologues of nitrite reductases in ammonia oxidizing archaea: diversity and genomic context. Environmental Microbiology 2010, 12:1075-1088.
12. Basiliko N., Khan A., Prescott C.E., Roy R., Grayston S.J. Soil greenhouse gas and nutrient dynamics in fertilized western Canadian plantation forests. Canadian Journal of Forest Research 2009, 39:1220-1235.
13. +, and CO oxidation by methanotrophs and nitrifiers. Microbiological Reviews 1989, 53:68-84.
14. x reductases in Agrobacterium tumefaciens: the inuence of nitrate, nitrite and oxygen availability. Environmental Microbiology 2008, 10:3070-3081.
15. Bergaust L., Mao Y., Bakken L.R., Frostegård Å. Denitri cation response patterns during the transition to anoxic respiration and posttranscriptional effects of suboptimal pH on nitrogen oxide reductase in Paracoccus denitri cans. Applied and Environmental Microbiology 2010, 76:6387-6396.
16. Bergmann D.F., Hooper A.B., Klotz M.G. Structure and sequence conservation of hao cluster genes autotrophic ammonia-oxidizing bacteria: evidence for their evolutionary history. Applied and Environmental Microbiology 2005, 71:5371-5382.
17. Billings S.A. Biogeochemistry: nitrous oxide in flux. Nature 2008, 456:888-889.
18. Bollag J.M., Tung G. Nitrous oxide release by soil fungi. Soil Biology and Biochemistry 1972, 4:271-276.
19. Bollmann A., Bär-Gilissen M.J., Laanbroek H.J. Growth at low ammonium concentrations and starvation response as potential factors involved in niche differentiation among ammonia-oxidizing bacteria. Applied and Environmental Microbiology 2002, 68:4751-4757.
20. Booth M.S., Stark J.M., Rastetter E. Controls on nitrogen cycling in terrestrial ecosystems: a synthetic analysis of literature data. Ecological Monographs 2005, 75:139-157.
21. Bothe H., Jost G., Schloter M., Ward B.B., Witzel K.P. Molecular analysis of ammonia oxidation and denitrification in natural environments. FEMS Microbiology Reviews 2000, 24:673-690.
22. Boyle-Yarwood S.A., Bottomley P.J., Myrold D.D. Community composition of ammonia-oxidizing bacteria and archaea in soils under stands of red alder and Douglas r in Oregon. Environmental Microbiology 2008, 10:2956-2965.
23. Braker G., Fesefeld A., Witzel K.-P. Development of PCR primer systems for amplification of nitrite reductase genes (nirK and nirS) to detect denitrifying bacteria in environmental samples. Applied and Environmental Microbiology 1998, 64:3769-3775.
24. Braker G., Zhou J., Wu L., Devol A.H., Tiedje J.M. Nitrite reductase genes (nirK and nirS) as functional markers to investigate diversity of denitrifying bacteria in pacific northwest marine sediment communities. Applied and Environmental Microbiology 2000, 66:2096-2104.
25. Brockley R.P., Simpson D.G. Effects of Intensive Fertilization on the Foliar Nutrition and Growth of Young Lodgepole Pine Forests in the Interior of British Columbia 2004, Establishment and progress report, British Columbia Ministry of Forests Tech, Victoria, Rep. 018.
26. Bru D., Sarr A., Philippot L. Relative abundances of proteobacterial membrane-bound and periplasmic nitrate reductases in selected environments. Applied and Environmental Microbiology 2007, 5971-5974.
27. Bru D., Ramette R., Saby N.P.A., Dequiedt S., Ranjard L., Jolivet C., Arrouays D., Philippot L. Determinants of the distribution of nitrogen-cycling microbial communities at the landscape scale. The ISME Journal 2011, 5:532-542.
28. 2O from temperate forest. Journal of Geophysical Research 1992, 97:12851-12858.
29. Burton S.Q.A., Prosser J.I. Autotrophic ammonia oxidation at low pH through urea hydrolysis. Applied and Environmental Microbiology 2001, 67:2952-2957.
30. Cabello P., Roldán M.D., Moreno-Vivían C. Nitrate reduction and the nitrogen cycle in archaea. Microbiology 2004, 150:3527-3546.
31. Carlson C.A., Ingraham J.L. Comparison of denitrification by Pseudomonas stutzeri, Pseudomonas aeruginosa, and Paracoccus denitrificans. Applied and Environmental Microbiology 1983, 45:1247-1253.
32. Chain P., Lamerdin J., Larimer F., Regala W., Lao V., Land M., Hauser L., Hooper A., Klotz M., Norton J., Sayavedra-Soto L., Arciero D., Hommes N., Whittaker M., Arp D. Complete genome sequence of the ammonia-oxidizing bacterium and obligate chemolithoautotroph Nitrosomonas europaea. Journal of Bacteriology 2003, 185:2759-2773.
33. Chan Y.K., McCormick W.A., Watson R.J. Anew nos gene downstream from nosDFY is essential for dissimilatory reduction of nitrous oxide by rhizobium (sinorhizobium) meliloti. Microbiology 1997, 143:2817-2824.
34. 2O? A review. Global Change Biology 2007, 13:1-17.
35. Chen Z., Luo X., Hu R., Wu M., Wu J., Wei W. Impacts of long-term fertilization on the composition of denitrifier communities based on nitrite reductase analyses in a paddy soil. Microbial Ecology 2010, 60:850-861.
36. Chénier M.R., Beaumier D., Roy R., Driscoll B.T., Lawrence J.R., Greer C.W. Impact of seasonal variations and nutrient inputs on nitrogen cycling and degradation of hexadecane by replicated river biofilms. Applied and Environmental Microbiology 2003, 69:5170-5177.
37. 2) xation in natural ecosystems. Global Biogeochemical Cycles 1999, 13:623-645.
38. Clough T.J., Kelliher F.M., Sherlock R.R., Ford C.D. Lime and soil moisture effects on nitrous oxide and dinitrogen emissions from a pasture soil. Soil Science Society of America Journal 2004, 68:1600-1609.
39. Colliver B.B., Stephenson T. Production of nitrogen oxide and dinitrogen oxide by autotrophic nitrifiers. Biotechnology Advances 2000, 18:219-232.
40. Compton J.E., Watrud L.S., Porteous L.A., DeGrood S. Response of soil microbial biomass and community composition to chronic nitrogen additions at Harvard forest. Forest Ecology and Management 2004, 196:143-158.
41. 2O, and NO. Microbiology Reviews 1996, 60:609-640.
42. Cracknell P.C., Lousier J.D. Improving forest fertilization decision-making in British Columbia. Improving Forest fertilization Decision-Making in British Columbia: Proceedings of a Forest Fertilization Workshop, March 1988 1988, 293. Research Branch, Ministry of Forests, Victoria, British Columbia, Canada. J.D. Lousier, H. Brix, R. Brockley, R. Carter, V.G. Marshall (Eds.).
43. 2 emissions and denitrifier community size and activity. Applied and Environmental Microbiology March 15, 2010, 76:1870-1878.
44. Dalal R.C., Allen D.E. Greenhouse gas fluxes from natural ecosystems. Australian Journal of Botany 2008, 56:369-407.
45. Demanèche S., Philippot L., David M.M., Navarro E., Vogel T.M., Simonet P. Characterization of denitrification gene clusters of soil bacteria via a metagenomic approach. Applied and Environmental Microbiology 2009, 75:534-537.
46. Di H.J., Cameron K.C., Shen J.P., Winefield C.S., O'Callaghan M., Bowatte S., He J.Z. Ammonia-oxidizing bacteria and archaea grow under contrasting soil nitrogen conditions. FEMS Microbiology Ecology 2010, 72:386-394.
47. Fierer N., Carney K., Horner-Devine M., Megonigal J. The biogeography of ammonia-oxidizing bacterial communities in soil. Microbial Ecology 2009, 58:435-445.
48. Francis C.A., Roberts K.J., Beman J.M., Santoro A.E., Oakley B.B. Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proceedings of the National Academy of Sciences USA 2005, 102:14683-14688.
49. Freedman Z., Eisenlord S.D., Zak D.R., Xue K., He Z., Zhou J. Towards a molecular understanding of N cycling in northern hardwood forests under future rates of N deposition. Soil Biology and Biochemistry 2013, 66:130-138.
50. Freitag T.E., Prosser J.I. Correlation of methane production and functional gene transcriptional activity in a peat soil. Applied and Environmental Microbiology 2009, 75:6679-6687.
51. Freitag T.E., Toet S., Ineson P., Prosser J.I. Links between methane flux and transcriptional activities of methanogens and methane oxidizers in a blanket peat bog. FEMS Microbiology Ecology 2010, 73:157-165.
52. Frey-Klett P., Garbaye J., Tarkka M. The mycorrhiza helper bacteria revisited. New Phytologist 2007, 176:22-36.
53. Frijlink M.J., Abee T., Laanbroek H.J., De Boer W., Konings W.N. The bioenergetics of ammonia and hydroxylamine oxidation in Nitrosomonas europaea at acid and alkaline pH. Archives of Microbiology 1992, 157:194-199.
54. Gans J., Wolinsky M., Dunbar J. Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science 2005, 309:1387-1390.
55. 2O sink. Global Change Biology 2009, 15:850-860.
56. Graham E.B., Wieder W.R., Leff J.W., Weintraub S.R., Townsend A.R., Cleveland C.C., Philippot L., Nemergut D.R. Do we need to understand microbial communities to predict ecosystem function? A comparison of statistical models of nitrogen cycling processes. Soil Biology and Biochemistry 2013, 10.1016/j.soilbio.2013.08.023.
57. Grayston S.J. Effects of forest fertilization on soil C sequestration and greenhouse gas emissions. Greenhouse-gas Budget of Soils Under Changing Climate and Land Use (BurnOut). Proceedings of the European Science Foundation Cost Action 639 Workshop, Vienna, Austria, April 2007 2007, 33-38. Federal Research and Training Centre for Forests, Natural Hazards and Landscape (BFW) Vienna, Austria. 110p. R. Jandl, M. Olsson (Eds.).
58. Green S.J., Prakash O., Gihring T.M., Akob D.M., Jasrotia P., Jardine P.M., Watson D.B., Brown S.D., Palumbo A.V., Kostka J.E. Denitrifying bacteria isolated from terrestrial subsurface sediments exposed to mixed-waste contamination. Applied and Environmental Microbiology 2010, 76:3244-3254.
59. Gubry-Rangin C., Hai B., Quince C., Engel M., Thomson B.C., James P., Schloter M., Griffiths R.I., Prosser J.I., Nicol G.W. Niche specialization of terrestrial archaeal ammonia oxidizers. Proceedings Of The National Academy Of Sciences USA 2011, 108:21206-21211.
60. Gundersen P., Christiansen J.R., Alberti G., Bruggemann N., Castaldi S., Gasche R., Kitzler B., Klemedtsson L., Lobo-do-Vale R., Moldan F., Rutting T., Schleppi P., Weslien P., Zechmeister-Boltenstern S. The response of methane and nitrous oxide uxes to forest change in Europe. Biogeosciences 2012, 9:3999-4012.
61. Hallam S.J., Mincer T.J., Schleper C., Preston C.M., Roberts K., Richardson P.M., DeLong E.F. Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine Crenarchaeota. PLoS Biology 2006, 4:521-536.
62. Hallin S., Lindgren P.-E. PCR detection of genes encoding nitrite reductase in denitrifying bacteria. Applied and Environmental Microbiology 1999, 65:1654-1657.
63. Hallin S., Jones C.M., Schloter M., Philippot L. Relationship between N-cycling communities and ecosystem functioning in a 50-year-old fertilization experiment. The ISME Journal 2009, 3:597-605.
64. Hayatsu M., Tago K., Saito M. Various players in the nitrogen cycle: diversity and functions of the microorganisms involved in nitrification and denitrification. Soil Science and Plant Nutrition 2008, 54:33-45.
65. He J.Z., Shen J.P., Zhang L.M., Zhu Y.G., Zheng Y.M., Xu M.G., Di H. Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices. Environmental Microbiology 2007, 9:2364-2374.
66. Henry S., Bru D., Stres B., Hallet S., Philippot L. Quantitative detection of the nosZ gene, encoding nitrous oxide reductase, and comparison of the abundances of 16S rRNA, narG, nirK, and nosZ genes in soils. Applied and Environmental Microbiology 2006, 72:5181-5189.
67. Heylen K., Gevers D., Vanparys B., Wittebolle L., Geets J., Boon N., De Vos P. The incidence of nirS and nirK and their genetic heterogeneity in cultivated denitrifiers. Environmental Microbiology 2006, 8:2012-21444.
68. Hoffman B.M., Lukoyanov D., Dean D.R., Seefeldt L.C. Nitrogenase: a draft mechanism. Accounts of Chemical Research 2013, 46:587-595.
69. Holmes A.J., Costello A., Lidstrom M.E., Murrell J.C. Evidence that participate methane monooxygenase and ammonia monooxygenase may be evolutionarily related. FEMS Microbiology Letters 1995, 132:203-208.
70. Holmes D.E., Bevin K.P., Lovley D.R. In situ expresion of nifD in Geobacteraceae in subsurface sediments. Applied and Environmental Microbiology 2004, 70:7251-7259.
71. Hooper D.U., Johnson L. Nitrogen limitation in dryland ecosystems: responses to geographical and temporal variation in precipitation. Biogeochemistry 1999, 46:247-293.
72. Horz H.P., Barbrook A., Field C.B., Bohannan B.J. Ammonia-oxidizing bacteria respond to multifactorial global change. Proceedings of the National Academy of Science USA 2004, 101:15136-15141.
73. Humbert S., Tarnawski S., Fromin N., Mallet M.P., Aragno M., Zopfi J. Molecular detection of anammox bacteria in terrestrial ecosystems: distribution and diversity. The ISME Journal 2010, 4:450-454.
74. Humbert S., Zopfi J., Tarnawski S.-E. Abundance of anammox bacteria in different wetland soils. Environmental Microbiology Reports 2012, 4:484-490.
75. Hütsch B.W., Zhang S., Feng K., Yan F., Schubert S. Effect of pH on denitrification losses from different arable soils 2001, 92:962-963.
76. Hynes H.M., Germida J.J. Relationship between ammonia oxidizing bacteria and bioavailable nitrogen in harvested forest soils of central Alberta. Soil Biology and Biochemistry 2012, 46:18-25.
77. IPCC Climate Change 2007: the Physical Science Basis 2007, Cambridge University Press, Cambridge, UK.
78. Janssens I.A., Dieleman W., Luyssaert S., Subke J.-A., Reichstein M., Ceulemans R., Ciais P., Dolman A.J., Grace J., Matteucci G., Papale D., Piao S.L., Schulze E.D., Tang J., Law B.E. Reduction of forest soil respiration in response to nitrogen deposition. Nature Geoscience 2010, 3:315-322.
79. 2O emissions and carbon sequestration in a nitrogen-fertilized Douglas-fir stand. Journal of Geophysical Research-Biogeosciences 2008, 113. 10.1029/2008JG000764.
80. 2O flux dynamics in a nitrogen-fertilized Pacific Northwest Douglas-fir stand. Geoderma 2010, 157:118-125.
81. Jia Z., Conrad R. Bacteria rather than archaea dominate microbial ammonia oxidation in an agricultural soil. Environmental Microbiology 2009, 11:1658-1671.
82. Jiang Q.Q., Bakken L.R. Comparison of Nitrosospira strains isolated from terrestrial environments. FEMS Microbiology Ecology 1999, 30:171-186.
83. Johnson D.W., Curtis P.S. Effects of forest management on soil C and N storage: meta-analysis. Forest Ecology and Management 2001, 140:227-238.
84. Jones D.L., Shannon D., Murphy D.V., Farrar J. Role of dissolved organic nitrogen (DON) in soil N cycling in grassland soils. Soil Biology and Biochemistry 2004, 36:746-756.
85. Jones C.M., Stres B., Rosenquist M., Hallin S. Phylogenetic analysis of nitrite, nitric oxide, and nitrous oxide respiratory enzymes reveal a complex evolutionary history for denitri cation. Molecular Biology and Evolution 2008, 35:1955-1966.
86. Jordan F.L., Cantera J.J.L., Fenn M.E., Stein L.Y. Autotrophic ammonia-oxidizing bacteria contribute minimally to nitrification in a nitrogen-impacted forested ecosystem. Applied and Environmental Microbiology 2005, 71:197-206.
87. Jurgensen M.F., Graham R.T., Larsen M.J., Harvey A.E. Clear-cutting, woody residue removal, and nonsymbiotic nitrogen fixation in forest soils of the inland Pacific Northwest. Canadian Journal of Forest Research 1992, 22:1172-1178.
88. Kandeler E., Deiglamayr K., Tscherko D., Bru D., Philippot L. Abundance of narG, nirS, nirK, and nosZ Genes of denitrifying bacteria during primary successions of a glacier foreland. Applied and Environmental Microbiology 2006, 72:5957-5962.
89. Kandeler E., Brune T., Enowashi E., Dörr N., Guggenberger G., Lamersdorf N., Philippot L. Response of total and nitrate-dissimilating bacteria to reduced N deposition in a spruce forest soil profile. FEMS Microbiology Ecology 2009, 67:444-454.
90. Kirk J.L., Beaudette L.A., Hart M., Moutoglis P., Klironomos J.N., Lee H., Trevors J.T. Methods of studying soil microbial diversity. Journal of Microbiological Methods 2004, 58:169-188.
91. Knowles R. Denitrification. Microbiological Reviews 1982, 46:43-70.
92. Kobayashi M., Matsuo Y., Takimoto A., Suzuki S., Maruo F., Shoun H. Denitrification, a novel type of respiratory metabolism in fungal mitochondrion. The Journal of Biological Chemistry 1995, 271:16263-16267.
93. Koike I., Hattori A. Energy yield of denitrification: an estimate from growth yield in continuous cultures of Pseudomonas denitrificans under nitrate-, nitrite- and nitrous oxide-limited conditions. Journal of General Microbiology 1975, 88:11-19.
94. Könneke M., Bernhard A.E., De La Torre J.R., Walker C.B., Waterbury J.B., Stahl D.A. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 2005, 437:543-546.
95. 2O from soil: a revised approach to the dual-isotope labeling method. European Journal of Soil Science 2010, 61:759-772.
96. Kool D.M., Dolfing J., Wrage N., Van Groenigen J.W. Nitrifier denitrification as a distinct and significant source of nitrous oxide from soil. Soil Biology and Biochemistry 2011, 43:174-178.
97. Koops H.P., Möller U.C. The lithotrophic ammonia-oxidizing bacteria. The Prokaryotes 1992, 2625-2637. Springer Verlag, New York. A. Balows, H.G. Trüper, Dworkin, M.W. Harder, K.H. Schleifer (Eds.).
98. Kowalchuk G.A., Stephen J.R. Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annual Review of Microbiology 2001, 55:485-529.
99. Kuenen J.G. Anammox bacteria: from discovery to application. Nature Reviews Microbiology 2008, 6:320-326.
100. 2-fixation associated with wood decayed by some common fungi in western Montana. Canadian Journal of Forest Research 1978, 8:341-345.
101. Laughlin R.J., Stevens R.J. Evidence for fungal dominance of denitrification and codenitrification in a grassland soil. Soil Science Society of America Journal 2002, 66:1540-1548.
102. Laverman A., Speksnijder A., Braster M., Kowalchuk G., Verhoef H., van Verseveld H. Spatiotemporal stability of an ammonia-oxidizing community in a nitrogen-saturated forest soil. Microbial Ecology 2001, 42:35-45.
103. LeBauer D.S., Tresender K.K. Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 2008, 89:371-379.
104. Leckie S. Methods of microbial community profiling and their application to forest soils. Forest Ecology and Management 2005, 220:88-106.
105. Lehtovirta L.E., Prosser J.I., Nicol G.W. Soil pH regulates the abundance and diversity of group 1.1c crenarchaeota. - FEMS Microbiology Ecology 2009, 70:367-376.
106. Lehtovirta-Morley L.E., Stoecker K., Vilcinskas A., Prosser J.I., Nicol G.W. Cultivation of an obligate acidophilic ammonia oxidizer from a nitrifying acid soil. Proceedings of the National Academy of Sciences USA 2011, 108:15892-15897.
107. Leininger S., Urich T., Schloter M., Schwark L., Qi J., Nicol G.W., Prosser J.I., Schuster S.C., Schleper C. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 2006, 442:806-809.
108. Levy-Booth D.J., Winder R.S. Quantification of nitrogen reductase and nitrite reductase genes in soil of thinned and clear-cut Douglas-fir stands by using real-time PCR. Applied and Environmental Microbiology 2010, 76:7116-7125.
109. Li C., Hung L. Nitrogen-fixing (acetylene-reducing) bacteria associated with ectomycorrhizae of douglas-fir. Plant and Soil 1987, 98:425-428.
110. 2 production as affected by soil pH. FEMS Microbiology Ecology 2010, 72:407-417.
111. 2. Soil Biology and Biochemistry 2012, 46:163-171.
112. Long A., Heitman J., Tobias C., Philips R., Song B. Co-occuring anammox, denitrification and codenitrification in agricultural soils. Applied and Environmental Microbiology 2013, 79:168-179.
113. López-Gutiérrez J.C., Henry S., Hallet S., Martin-Laurent F., Catroux G., Philippot L. Quantification of a novel group of nitrate-reducing bacteria in the environment by real-time PCR. Journal of Microbiology Methods 2004, 57:399-407.
114. Lu L., Jia Z. Urease gene-containing Archaea dominate autotrophic ammonia oxidation in two acid soils. Environmental Microbiology 2013, 15:1795-1809.
115. Martens-Habbena W., Berube P.M., Urakawa H., de la Torre J.R., Stahl D.A. Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature 2009, 461:976-979.
116. Martikainen P.J. Nitrous oxide emission associated with autotrophic ammonium oxidation in acid coniferous forest soil. Applied and Environmental Microbiology 1985, 50:1519-1525.
117. Matson P., Gower S., Volkmann C., Billow C., Grier C. Soil nitrogen cycling and nitrous oxide flux in a rocky mountain Douglas-fir forest: effects of fertilization, irrigation and carbon addition. Biogeochemistry 1992, 18:101-117.
118. McGill B.J., Enquist B.J., Weiher E., Westoby M. Rebuilding community ecology from functional traits. Trends in Ecology and Evolution 2006, 21:178-185.
119. Mertens J., Broos K., Wakelin S.A., Kowalchuk G.A., Springael D., Smolders E. Bacteria, not archaea, restore nitrification in a zinc-contaminated soil. The ISME Journal 2009, 3:916-923.
120. Morales S.E., Cosart T., Holben W.E. Bacterial gene abundances as indicators of greenhouse gas emission in soils. The ISME Journal 2010, 4:799-808.
121. Murugapiran S.K., Huntemann M., Wei C., Han J., Detter J.C., Han C., Erkkila T.H., Teshima H., Chen A., Kyrpides N., Mavrommatis K., Markowitz V., Szeto E., Ivanova N., Pagani I., Pati A., Goodwin L., Peters L., Pitluck S., Lam J., McDonald A.I., Dodsworth J.A., Woyke T., Hedlund B.P. Thermus oshimai JL-2 and T.thermophilus JL-18 genome analysis illuminates pathways for carbon, nitrogen, and sulfur cycling. Standards of Genome Sciences 2013, 7:449-468.
122. Myrold D.D., Zeglin L.H., Jansson J.K. The potential of metagenomic approaches for understanding soil microbial processes. Soil Science Society of America Journal 2014, 78:3-10.
123. Nakahara K., Tanimoto T., Hatano K., Usuda K., Shoun H. Cytochrome P-450 55A1 (P-450dNIR) acts as nitric oxide reductase employing NADH as the direct electron donor. The Journal of Biological Chemistry 1993, 268:8350-8355.
124. Nicol G.W., Leininger S., Schleper C., Prosser J.I. The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Microbial Ecology 2008, 10:2966-2978.
125. Nicolaisen M.H., Bælum J., Jacobsen C.S., Sørensen J. Transcription dynamics of the functional tfdA gene during MCPA herbicide degradation by Cupriavidus necator AEO106 (pRO101) in agricultural soil. Environmental Microbiology 2008, 10:571-579.
126. Norton J.M., Alzerreca J.J., Suwa Y., Klotz M.G. Diversity of ammonia monooxygenase operon in autotrophic ammonia-oxidizing bacteria. Archives of Microbiology 2002, 177:139-149.
127. Nugroho R., Röling W., Laverman A., Verhoef H. Low nitrification rates in acid scots pine forest soils are due to pH-related factors. Microbial Ecology 2007, 53:89-97.
128. 15N tracer studies of the primary nitrite maximum. Journal of Marine Research 1981, 39:203-226.
129. Onodera Y., Nakagawa T., Takahashi R., Tokuyama T. Seasonal change in vertical distribution of ammonia-oxidizing archaea and bacteria and their nitrification in temperate forest soil. Microbes and Environments 2010, 25:28-35.
130. Palmer K., Drake H.L., Horn M.A. Genome-derived criteria for assigning environmental narG and nosZ sequences to operational taxonomic units of nitrate reducers. Applied and Environmental Microbiology August 1, 2009, 75:5170-5174.
131. 2O emission pattern from acidic peat soils in arctic tundra. The ISME Journal 2012, 6:1058-1077.
132. 2O-metabolizing palsa peat. Applied and Environmental Microbiology 2012, 78:5584-5596.
133. Pang P.C., Cho C.M. Oxygen consumption and denitrification activity of a conifer forest soil profile. Soil Science Society of America Journal 1984, 48:393-399.
134. Paul L.R., Chapman B.K., Chanway C.P. Nitrogen fixation associated with Suillus tomentosus tuberculate ectomycorrhizae on Pinus contorta var. latifolia. Annals of Botany 2007, 99:1101-1109.
135. 15N tracer and pool dilution techniques. Biogeochemistry 1999, 44:135-150.
136. Penton C.R., Johnson T.A., Quensen J.F., Iwai S., Cole J.R., Tiedje J.M. Functional genes to assess nitrogen cycling and aromatic hydrocarbon degradation: primers and processing matter. Frontiers in Microbiology 2013, 4:1-17.
137. Pester M., Rattei T., Flechl S., Gröngröft A., Richter A., Overmann J., Reinhold-Hirek B., Loy A., Wagner M. amoA-based consensus phylogeny of ammonia-oxidizing archaea and deep sequencing of amoA genes from soils of four different geographic regions. Environmental Microbiology 2012, 14:525-539.
138. Petersen D.G., Blazewicz S.J., Firestone M., Herman D.J., Turetsky M., Waldrop M. Abundance of microbial genes associated with nitrogen cycling as indices of biogeochemical process rates across a vegetation gradient in Alaska. Environmental Microbiology 2012, 14:993-1008.
139. Philippot L. Denitrifying genes in bacterial and archaeal genomes. Biochimica Biophysica Acta 2002, 1577:355-376.
140. 2 fixation by archaea and bacteria in an agricultural soil. Proceedings of the National Academy of Sciences 2011, 108:4170-4175.
141. Prosser J.I., Nicol G.W. Relative contributions of archaea and bacteria to aerobic ammonia oxidation in the environment. Environmental Microbiology 2008, 10:2931-2941.
142. Prosser J.I., Nicol G.W. Archaeal and bacterial ammonia oxidisers in soil: the quest for niche specialisation and differentiation. Trends in Microbiology 2012, 20:523-531.
143. Purkhold U., Pommerening-Röser A., Juretschko S., Schmid M.C., Koops H., Wagner M. Phylogeny of all recognized species of ammonia oxidizers based on comparative 16S rRNA and amoA sequence analysis: implications for molecular diversity surveys. Applied and Environmental Microbiology 2000, 66:5368-5382.
144. Rasche F., Knapp D., Kaiser C., Koranda M., Kitzler B., Zechmeister-Boltenstern S., Richter A., Sessitsch A. Seasonality and resource availability control bacterial and archaeal communities in soils of a temperate beech forest. The ISME Journal 2011, 5:389-402.
145. 2O): the dominant ozone-depleting substance emitted in the 21st century. Science 2009, 326:123-125.
146. Rich J.J., Heichen R.S., Bottomley P.J., Cromack K., Myrold D.D. Community composition and functioning of denitrifying bacteria from adjacent meadow and forest soils. Applied and Environmental Microbiology 2003, 69:5974-5982.
147. 2O from the nitrogen cycle - could enzyme regulation hold the key?. Trends in Biotechnology 2009, 27:388-397.
148. Richarson D.J. Bacterial respiration: a exible process for a changing environment. Microbiology 2000, 146:551-571.
149. Roesch L.F., Fulthorpe R.R., Riva A., Casella G., Hadwin A.K., Kent A.D., Daroub S.H., Camargo F.A.O., Farmerie W.G., Triplett E.W. Pyrosequencing enumerates and contrasts soil microbial diversity. ISME Journal 2007, 1:283-290.
150. Rooney D.C., Kennedy N.M., Gleeson D.B., Clipson N.J.W. Response of ammonia-oxidising bacterial communities to nitrogen, lime and plant species in upland grassland soil. Applied and Environmental Soil Science 2010, 2010. 10.1155/2010/319721.
151. 2-fixing, and total-community bacteria by terminal restriction fragment length polymorphism analysis using multiple restriction enzymes. Applied and Environmental Microbiology 2005, 71:2026-2035.
152. Rösch C., Mergel A., Bothe H. Biodiversity of denitrifying and dinitrogen-fixing bacteria in an acid forest soil. Applied and Environmental Microbiology 2002, 68:3818-3829.
153. Rotthauwe J.-H., Witzel K.-P., Liesack W. The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Applied and Environmental Microbiology 1997, 63:4704-4712.
154. 2O emission hotspots along a natural pH gradient in organic forest soil. Biology and Fertility of Soils 2013, 49:714-721.
155. Saad O.A.L.O., Conrad R. Adaptation to temperature of nitric oxide-producing nitrate-reducing bacterial populations in soil. Systematic and Applied Microbiology 1993, 16:120-125.
156. Schleper C., Nicol G.W. Ammonia-oxidising archaea - physiology, ecology and evolution. Advances in Microbial Physiology 2010, 57:1-41.
157. Schleper C., Jurgen G., Jonusscheit M. Genomic studies of uncultivated archaea. Nature Reviews Microbiology 2005, 3:479-488.
158. Schmidt I., van Spanning R.J.M., Jetten M.S.M. Denitrification and ammonia oxidation by Nitrosomonas europaea wild-type, and NirK- and NorB-deficient mutants. Microbiology 2004, 150:4107-4114.
159. Sharma S., Radl V., Hai B., Kloos K., Mrkonjic Fuka M., Engel M., Schauss K., Schloter M. Quantification of functional genes from procaryotes in soil by PCR. Journal of Microbiological Methods 2007, 68:445-452.
160. Shaw L.J., Nicol G.W., Smith Z., Fear J., Prosser J.I., Baggs E.M. Nitrosopsira spp. can produce nitrous oxide via a nitrifier denitrification pathway. Environmental Microbiology 2006, 8:214-222.
161. Shoun H., Kim D.H., Uchiyama H., Sugiyama J. Denitrification by fungi. FEMS Microbiology Letters 1992, 73:277-281.
162. Silver W.L., Herman D.J., Firestone M.K. Dissimilatory nitrate reduction to ammonium in upland tropical forest soil. Ecology 2001, 82:2410-2416.
163. 2 emission from temperate pine forest soil. Soil Biology and Biochemistry 1995, 27:1401-1408.
164. Smethurst P.J. Forest fertilization: trends in knowledge and practice compared to agriculture. Plant and Soil 2010, 335:83-100.
165. Smith C.J., Osborn A.M. Advantanges and limitations of quantitative PCR (Q-PCR)-based approaches in microbial ecology. FEMS Microbiology Ecology 2009, 67:6-20.
166. Spiegelman D., Whissell G., Greer C.W. Asurvey of the methods for the characterization of microbial consortia and communities. Canadian Journal of Microbiology 2005, 51:355-386.
167. Stephen J.R., Kowalchuk G.A., Bruns M.-V., McCaig A.E., Phillips C.J., Embley T.M., Prosser J.I. Analysis of β-subgroup proteobacterial ammonia oxidizer populations in soil by denaturing gradient gel electrophoresis analysis and hierarchical phylogenetic probing. Applied and Environmental Microbiology 1998, 64:2958-2965.
168. Stephen J.R., Chang Y.J., Macnaughton S.J., Kowalchuk G.A., Leung K.T., Flemming C.A., White D.C. Effect of toxic metals on indigenous soil β-subgroup proteobacterium ammonia oxidizer community structure and protection against toxicity by inoculated metal-resistant bacteria. Applied and Environmental Microbiology 1999, 65:95-101.
169. Strous M., Pelletier E., Mangenot S., Rattei T., Lehner A., Taylor M.W., Horn M., Daims H., Bartol-Mavel D., Wincker P., Barbe V., Fonknechten N., Vallenet D., Segurens B., Schenowitz-Truong C., Médigue C., Collingro A., Snel B., Dutilh B.E., Op den Camp H.J., van der Drift C., Cirpus I., van de Pas-Schoonen K.T., Harhangi H.R., van Niftrik L., Schmid M., Keltjens J., van de Vossenberg J., Kartal B., Meier H., Frishman D., Huynen M.A., Mewes H.W., Weissenbach J., Jetten M.S., Wagner M., Le Paslier D. Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature 2006, 440:790-794.
170. 2O emissions and nirK abundance. Biology and Fertility of Soils 2009, 45:855-863.
171. Szukics U., Abell G., Hödl V., Mitter B., Sessitsch A., Hackl E., Zechmeister-Boltenstern S. Nitrifiers and denitrifiers respond rapidly to changed moisture and increasing temperature in a pristine forest soil. FEMS Microbiology Ecology 2010, 72:395-406.
172. Szukics U., Hackl E., Zechmeister-Boltenstern S., Sessitsch A. Rapid and dissimilar response of ammonia oxidizing archaea and bacteria to nitrogen and water amendment in two temperate forest soils. Microbiological Research 2012, 167:103-109.
173. Tavares P., Pereira A.S., Moura J.J.G., Moura I. Metalloenzymes of the denitrification pathway. Journal of Inorganic Biochemistry 2006, 1000:2087-2100.
174. Temme K., Zhao D., Voigt C.A. Refactoring the nitrogen fixation gene cluster from klebsiella oxytoca. Proceedings of the National Academy of Sciences 2012, 109:7085-7090.
175. Thomsen J.K., Geest T., Cox R.P. Mass-spectrometric studies of the effect of pH on the accumulation of intermediates in denitri cation by Paracoccus denitri cans. Applied and Environmental Microbiology 1994, 60:536-541.
176. Tiedje J.M. Ecology of denitrification and dissimilatory nitrate reduction to ammonium. Biology of Anaerobic Microorganisms 1988, 179-244.
177. Torsvik V., Goksoyr J., Daae F.L. High diversity in DNA of soil bacteria. Applied and Environmental 1990, 56:782-787.
178. Torsvik V., Øvreås L., Thingstad T.F. Prokaryotic Diversity-Magnitude, dynamics, and controlling factors. Science 2002, 296:1064-1066.
179. Tourna M., Freitag T.E., Nicol G.W., Prosser J.I. Growth, activity and temperature responses of ammonia-oxidizing archaea and bacteria in soil microcosms. Environmental Microbiology 2008, 10:1357-1364.
180. Tourna M., Freitag T.E., Posser J.I. Stable isotope probing analysis of interactions between ammonia oxidizers. Applied and Environmental Microbiology 2010, 76:2468-2477.
181. Tourna M., Stieglmeier M., Spang A., Konneke M., Schintlmeister A., Urich T., Engel M., Schloter M., Wagner M., Richer A., Schleper C. Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proceedings Of The National Academy Of Sciences USA 2011, 20:8420-8425.
182. Treusch A.H., Leininger S., Kietzin A., Schuster S.C., Klenk H.P., Schleper C. Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling. Environmental Microbiology 2005, 7:1985-1995.
183. Uchimura H., Enjoji H., Seki T., Taguchi A., Takaya N., Shoun H. Nitrate reductase-formate dehydrogenase couple involved in the fungal denitrification by Fusarium oxysporum. The Journal of Biochemistry 2002, 131:579-586.
184. 2-fixing bacterial diversity detected in rice roots by molecular evolutionary analysis of nifH gene sequences. Journal of Bacteriology 1995, 177:1414-1417.
185. Van Miegroet H., Jandl R. Are Nitrogen-fertilized Forest soils sinks or sources of carbon?. Enviromental Monitoring and Assessment 2007, 128:121-131.
186. Venter J.C., Remington K., Heidelberg J.F., Halpern A.L., Rusch D., Eisen J.A., Wu D., Paulsen I., Nelson K.E., Nelson W., Fouts D., Levy S., Knap A.E., Lomas M.W., Nealson K., White O., Peterson J., Hoffman J., Parsons R., Baden-Tillson H., Pfannkoch C., Rogers Y.H., Smith H.O. Environmental genome shotgun sequencing of the Sargasso sea. Science 2004, 304:66-74.
187. Verhagen F.J.M., Laanbroek H.J. Competition for ammonium between nitrifying and heterotrophic bacteria in duel energy-limited chemostats. Applied and Environmental Microbiology 1991, 57:3255-3263.
188. Vitousek P.M., Howarth R.W. Nitrogen limitation on land and in the sea: how can it occur?. Biogeochemistry 1991, 13:87-115.
189. Vitousek P.M., Aber J.D., Howarth R.W., Likens G.E., Matson P.M., Schindler D.W., Schlesinger W.H., Tilman D.G. Human alteration of the global nitrogen cycle: sources and consequences. Ecological Applications 1997, 7:737-750.
190. Vitousek P.M., Cassman K., Cleveland C., Crews T., Field C.B., Grimm N.B., Howarth R.W., Marino R., Martinelli L., Rastetter E.B., Sprent J.I. Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 2002, 57:1-45.
191. Walker C.B., de la Torre J.R., Klotz M.G., Urakawa H., Pinel N., Arp D.J., Brochier-Armanet C., Chain P.S.G., Chan P.P., Gollabgir A. Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proceeding of the National Academy of Sciences USA 2010, 107:8818-8823.
192. Wallenstein M.D., McNulty S., Fernandez I.J., Boggs J., Schlesinger W.H. Nitrogen fertilization decreases forest soil fungal and bacterial biomass in three long-term experiments. Forest Ecology and Management 2006, 222:459-468.
193. Wallenstein M.D., Peterjohn W.T., Schlesinger W.H. Nfertilization effects on denitrification and N cycling in an aggrading forest. Ecological Applications 2006, 16:2168-2176.
194. Wallenstein M.D., Myrold D.D., Firestone M., Voyten M. Environmental controls on denitrifying communities and denitrification rates: insights from molecular methods. Ecological Applications 2006, 16:2143-2152.
195. Wang Q., Quensen J.F., Fish J.A., Lee T.K., Sun Y., Tiedje J.M., Cole J.R. Ecological patterns of nifH genes in four terrestrial climatic zones explored with targeted metagenomics using FrameBot, a new informatics tool. MBIO 2013, 4. e00592-13.
196. Webster G., Embley T.M., Prosser J.I. Grassland management regimens reduce small-scale heterogeneity and species diversity of β-proteobacterial ammonia oxidizer populations. Applied and Environmental Microbiology 2002, 68:20-30.
197. Webster G., Embley T.M., Freitag T.E., Smith Z., Prosser J.I. Links between ammonia oxidizer species composition, functional diversity and nitrification kinetics in grassland soils. Environmental Microbiology 2005, 7:676-684.
198. Wertz S., Dandie C.E., Goyer C., Trevors J.T., Patten C.L. Diversity of nirK denitrifying genes and transcripts in an agricultural soil. Applied and Environmental Microbiology 2009, 75:7365-7377.
199. Wertz S., Leigh A.K.K., Grayston S.J. Effects of long-term fertilization of forest soils on potential nitrification and on the abundance and community structure of ammonia oxidizers and nitrite oxidizers. FEMS Microbiology Ecology 2012, 79:142-154.
200. Widmer F., Shaffer B.T., Porteous L.A., Seidler R.J. Analysis of nifH gene pool complexity in soil and litter at a Douglas fir forest site in the Oregon cascade mountain range. Applied and Environmental Microbiology 1999, 65:374-380.
201. Wrage N., Velthof G.L., van Beusichem M.L., Oenema O. Role of nitri er denitri cation in the production of nitrous oxide. Soil Biology and Biochemistry 2001, 33:1723-1732.
202. Yeager C.M., Northup D.E., Grow C.C., Barns S.M., Kuske C.R. Changes in nitrogen-fixing and ammonia-oxidizing bacterial communities in soil of a mixed conifer forest after wildfire. Applied and Environmental Microbiology 2005, 71:2713-2722.
203. Yergeau E., Kang S., He Z., Zhou J., Kowalchuk G.A. Functional microarray analysis of nitrogen and carbon cycling genes across an Antarctic latitudinal transect. The ISME Journal 2007, 1:163-179.
204. Yin S.X., Chen D., Chen L.M., Edis R. Dissimilatory nitrate reduction to ammonium and responsible microorganisms in two Chinese and Australian paddy soils. Soil Biology and Biochemistry 2002, 34:1131-1137.
205. Yool A., Martin A.P., Fernandez C., Clark D.R. The significance of nitrification for oceanic new production. Nature 2007, 447:999-1002.
206. Zani S., Mellon M.T., Collier J.L., Zehr J.P. Expression of nifH genes in natural microbial assemblages in Lake George, New York, detected by reverse transcriptase PCR. Applied and Environmental Microbiology 2000, 66:3119-3124.
207. Zeglin L.H., Taylor A.E., Myrold D.D., Bottomley P.J. Bacterial and archaeal amoA gene distribution covaries with soil nitrification properties across a range of land uses. Environmental Microbiology Reports 2011, 3:717-726.
208. Zhu G., Wang S., Wang Y., Wang C., Risgaard-Petersen N., Jetten M.S.M., Yin C. Anaerobic ammonia oxidation in a fertilized paddy soil. The ISME Journal 2011, 5:1905-1912.
209. 2O and NO under low oxygen availability. Proceedings of the National Academy of Science USA 2013, doi:10.10731219993110.