Fungi mediate nitrous oxide production but not ammonia oxidation in aridland soils of the southwestern US

Soil Biology and Biochemistry

Volumn 63, Issue , 2013, Pages 24-36

  Marusenko, Yevgeniy ^a   Huber, David P ^a,b   Hall, Sharon J ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

^b Nucl Eng Idaho State University   (United States)

Author keywords

Denitrification; Fungi; Nitrification; Nitrogen cycling; Nitrous oxide (N2O); Urbanization

Indexed keywords

AUTOTROPHIC BACTERIA; IRRIGATION AND FERTILIZERS; NITRIFICATION AND DENITRIFICATION; NITROGEN CYCLING; NITROUS OXIDE; NITROUS OXIDE PRODUCTION; POTENTIAL NITRIFICATION; URBANIZATION;

ACETYLENE; AMMONIA; BACTERIA; BIOCIDES; DENITRIFICATION; LIGHTING; NITRIFICATION; NITROGEN; NITROGEN OXIDES; OXIDATION; SOIL MOISTURE; URBAN GROWTH;

FUNGI;

AMMONIA; ARID REGION; CHEMOAUTOTROPHY; DENITRIFICATION; FUNGUS; GROWTH RATE; NITROGEN CYCLE; NITROUS OXIDE; OXIDATION; PROKARYOTE; SOIL FERTILITY; SOIL MICROORGANISM; SURVIVAL; URBANIZATION;

SONORAN DESERT; UNITED STATES;

ARCHAEA; BACTERIA (MICROORGANISMS); FUNGI; POACEAE; PROKARYOTA;

EID: 84876487326     PISSN: 00380717     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.soilbio.2013.03.018     Document Type: Article

References (108)

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. Allen M.F. Mycorrhizal fungi: highways for water and nutrients in arid soils. Vadose Zone Journal 2007, 6:291-297.
3. Allen M.F. Water dynamics of mycorrhizas in arid soils. Fungi in Biogeochemical Cycles 2006, 74-97. Cambridge University Press, New York. G.M. Gadd (Ed.).
4. Austin A., Yahdjian L., Stark J., Belnap J., Porporato A., Norton U., Ravetta D., Schaeffer S. Water pulses and biogeochemical cycles in arid and semiarid ecosystems. Oecologia 2004, 141:221-235.
5. Bang C., Faeth S.H., Sabo J.L. Control of arthropod abundance, richness, and composition in a heterogeneous desert city. Ecological Monographs 2012, 82:85-100.
6. Bang C., Sabo J.L., Faeth S.H. Reduced wind speed improves plant growth in a desert city. Plos One 2010, 5:e11061.
7. Bates S.T., Nash T.H., Garcia-Pichel F. Patterns of diversity for fungal assemblages of biological soil crusts from the southwestern United States. Mycologia 2012, 104:353-361.
8. Belnap J., Hawkes C.V., Firestone M.K. Boundaries in miniature: two examples from soil. BioScience 2003, 53:739-749.
9. Belnap J., Lange O.L. Biological Soil Crusts: Structure, Function and Management. Ecological Studies 2001, vol. 150. Springer-Verlag, Berlin.
10. Blackwell M. The fungi: 1, 2, 3, ... 5,1 million species?. Biodiversity Special Issue, American Journal of Botany 2011, 98:426-438.
11. Bremer D.J. Nitrous oxide fluxes in turfgrass: effects of nitrogen fertilization rates and types. Journal of Environmental Quality 2006, 35:1678-1685.
12. Briggs J.M., Schaafsma H., Trenkov D. Woody vegetation expansion in a desert grassland: prehistoric human impact?. Journal of Arid Environments 2007, 69:458-472.
13. Brown J.H., Valone T.J., Curtin C.G. Reorganization of an arid ecosystem in response to recent climate change. Proceedings of the National Academy of Sciences USA 1997, 94:9729-9733.
14. Buyantuyev A., Wu J. Urban heat islands and landscape heterogeneity: linking spatiotemporal variations in surface temperatures to land-cover and socioeconomic patterns. Landscape Ecology 2010, 25:17-33.
15. Camargo J.A., Alonso A. Ecological and toxicological effects of inorganic nitrogen pollution in aquatic ecosystems: a global assessment. Environment International 2006, 32:831-849.
16. - production in a forest and an agricultural soil. Biology and Fertility of Soils 1998, 27:27-34.
17. Collins S.L., Sinsabaugh R.L., Crenshaw C., Green L., Porras-Alfaro A., Stursova M., Zeglin L.H. Pulse dynamics and microbial processes in aridland ecosystems. Journal of Ecology 2008, 96:413-420.
18. Cousins J., Hope D., Gries C., Stutz J. Preliminary assessment of arbuscular mycorrhizal fungal diversity and community structure in an urban ecosystem. Mycorrhiza 2003, 13:319-326.
19. Crenshaw C.L., Lauber C., Sinsabaugh R.L., Stavely L.K. Fungal control of nitrous oxide production in semiarid grassland. Biogeochemistry 2008, 87:17-27.
20. Davies R., Hall S.J. Direct and indirect effects of urbanization on soil and plant nutrients in desert ecosystems of the Phoenix metropolitan area, Arizona (USA). Urban Ecosystems 2010, 13:295-317.
21. Egerton-Warburton L.M., Johnson N.C., Allen E.B. Mycorrhizal community dynamics following nitrogen fertilization: a cross-site test in five grasslands. Ecological Monographs 2007, 77:527-544.
22. Faeth S., Warren P., Shochat E., Marussich W. Trophic dynamics in urban communities. Bioscience 2005, 55:399-407.
23. Firestone M.K., Firestone R.B., Tiedje J.M. Nitrous oxide from soil denitrification: factors controlling its biological production. Science 1980, 208:749-751.
24. Frey S.D., Elliott E.T., Paustian K. Bacterial and fungal abundance and biomass in conventional and no-tillage agroecosystems along two climatic gradients. Soil Biology and Biochemistry 1999, 31:573-585.
25. Fu B.J., Zhang Q.J., Chen L.D., Zhao W.W., Gulinck H., Liu G.B., Yang Q.K., Zhu Y.G. Temporal change in land use and its relationship to slope degree and soil type in a small catchment on the Loess Plateau of China. Catena 2006, 65:41-48.
26. Green L.E., Porras-Alfaro A., Sinsabaugh R.L. Translocation of nitrogen and carbon integrates biotic crust and grass production in desert grassland. Journal of Ecology 2008, 96:1076-1085.
27. Groffman P.M., Pouyat R.V., Cadenasso M.L., Zipperer W.C., Szlavecz K., Yesilonis I.C., Band L.E., Brush G.S. Land use context and natural soil controls on plant community composition and soil nitrogen and carbon dynamics in urban and rural forests. Forest Ecology and Management 2006, 236:177-192.
28. 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.
29. Hall S.J., Ahmed B., Ortiz P., Davies R., Sponseller R.A., Grimm N.B. Urbanization alters soil microbial functioning in the Sonoran Desert. Ecosystems 2009, 12:654-671.
30. 2O and NO emissions from an arid, urban ecosystem. Journal of Geophysical Research-Biogeosciences 2008, 113.
31. Hall S.J., Sponseller R.A., Grimm N.B., Huber D., Kaye J.P., Clark C., Collins S.L. Ecosystem response to nutrient enrichment across an urban airshed in the Sonoran Desert. Ecological Applications 2011, 21:640-660.
32. Hammer Ø., Harper D.A., Ryan P.D. PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 2001, 4:1-9.
33. Hart S.C., Stark J.M., Davidson E.A., Firestone M.K. Nitrogen mineralisation, immobilisation, and nitrification. Methods of Soil Analysis. Part 2. Microbiological and Chemical Properties 1994, 985-1018. Soil Science Society of America, Madison, WI. R.W. Weaver, J.S. Angle, P.S. Bottomley (Eds.).
34. 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.
35. Herold M.B., Baggs E.M., Daniell T.J. Fungal and bacterial denitrification are differently affected by long-term pH amendment and cultivation or arable soil. Soil Biology and Biochemistry 2012, 54:25-35.
36. 2. Journal of Geophysical Research 2011, 116:G02001.
37. Jung M.Y., Park S.J., Min D., Kim J.S., Rijpstra W.I.C., Sinninghe Damsté J.S., Kim G.J., Madsen E.L., Rhee S.K. Enrichment and characterization of an autotrophic ammonia-oxidizing archaeon of mesophilic crenarchaeal group I.1a from an agricultural soil. Applied and Environmental Microbiology 2011, 77:8635-8647.
38. Kaye J.P., Eckert S.E., Gonzales D.A., Allen J.O., Hall S.J., Sponseller R.A., Grimm N.B. Decomposition of urban atmospheric carbon in Sonoran Desert soils. Urban Ecosystems 2011, 14:737-754.
39. Kaye J.P., McCulley R.L., Burke I.C. Carbon fluxes, nitrogen cycling, and soil microbial communities in adjacent urban, native and agricultural ecosystems. Global Change Biology 2005, 11:575-587.
40. Kaye J.P., Burke I., Mosier A., Guerschman J. Methane and nitrous oxide fluxes from urban soils to the atmosphere. Ecological Applications 2004, 14:975-981.
41. Klotz M.G., Stein L.Y. Nitrifier genomics and evolution of the N-cycle. FEMS Microbiology Letters 2008, 278:146-156.
42. Konneke 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.
43. Kramer P.J., Boyer J.S. Water Relations of Plants and Soils 1995, 84-114. Academic Press, San Diego.
44. Kuenen J.G., Robertson L.A. Combined nitrification-denitrification processes. FEMS Microbiology Reviews 1994, 15:109-117.
45. 2O emissions and gross N transformations related to fungi and bacteria in a grassland soil. Applied Soil Ecology 2009, 42:25-30.
46. Laughlin R., Stevens R. Evidence for fungal dominance of denitrification and codenitrification in a grassland soil. Soil Science Society of America Journal 2002, 66:1540-1548.
47. 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.
48. Lennon J.T., Aanderud Z.T., Lehmkuhl B.K., Schoolmaster D.R. Mapping the niche space of soil microorganisms using taxonomy and traits. Ecology 2012, 93:1867-1879.
49. Linn D.M., Doran J.W. Effect of water-filled pore space on carbon dioxide and nitrous oxide production in tilled and nontilled soils. Soil Science Society of America Journal 1984, 48:1267-1272.
50. Lohse K.A., Hope D., Sponseller R., Allen J.O., Grimm N.B. Atmospheric deposition of carbon and nutrients across an arid metropolitan area. Science of the Total Environment 2008, 402:95-105.
51. Lorenz K., Lal R. Biogeochemical C and N cycles in urban soils. Environment International 2009, 35:1-8.
52. Ma W.K., Farrell R.E., Siciliano S.D. Soil formate regulates the fungal nitrous oxide emission pathway. Applied and Environmental Microbiology 2008, 74:6690-6696.
53. MacMahon J.A. Warm deserts. North American Terrestrial Vegetation 2000, 285-322. Cambridge University Press, New York. second ed. M.G. Barbour, W.D. Billings (Eds.).
54. Maestre F.T., Bowker M.A., Cantón Y., Castillo-Monroy A.P., Cortina J., Escolar C., Escudero A., Lázaro R., Martínez I. Ecology and functional roles of biological soil crusts in semi-arid ecosystems of Spain. Journal of Arid Environments 2011, 75:1282-1291.
55. Martin C.A. Landscape sustainability in a Sonoran Desert city. Cities and the Environment 2008, 1:1-16.
56. Marusenko, Y., Bates, S.T., Anderson, I., Johnson, S.L., Soule, T., Garcia-Pichel, F. Ammonia oxidizing archaea and bacteria are structured by geography in biological soil crusts across North American arid lands. Ecological Processes, in press.
57. McCrackin M.L., Harms T.K., Grimm N.B., Hall S.J., Kaye J.P. Responses of soil microorganisms to resource availability in urban, desert soils. Biogeochemistry 2008, 87:143-155.
58. 2O production by heterotrophic N transformations in a semiarid soil. Applied Soil Ecology 2006, 32:253-263.
59. McLain J.E.T., Martens D.A. Nitrous oxide flux from soil amino acid mineralization. Soil Biology and Biochemistry 2005, 37:289-299.
60. Mosier A. Acetylene inhibition of ammonium oxidation in soil. Soil Biology and Biochemistry 1980, 12:443-444.
61. Mulder A., Vandegraaf A.A., Robertson L.A., Kuenen J.G. Anaerobic ammonium oxidation discovered in a denitrifying fluidized-bed reactor. FEMS Microbiology Ecology 1995, 16:177-183.
62. Mummey D.L., Smith J.L., Bolton H. Nitrous oxide flux from a shrub-steppe ecosystem: sources and regulation. Soil Biology and Biochemistry 1994, 26:279-286.
63. Review of Phoenix, AZ in 2009 2009, NOAA (National Oceanic and Atmospheric Administration), National Weather Service. http://www.wrh.noaa.gov/psr/pns/2010/January/Brief1.php.
64. Offre P., Prosser J.I., Nicol G.W. Growth of ammonia-oxidizing archaea is inhibited by acetylene. FEMS Microbiology Ecology 2009, 70:99-108.
65. Ojima D.S., Tieszen L., Chuluun T., Belnap J., Dodd J., Chen Z. Factors influencing production systems of the Mongolian steppe: potential global change impacts on semi-arid ecosystems. People and Rangelands: Building the Future: Proceedings of the VI International Rangeland Congress, Australia 1999, 264-265. D. Eldridge, D. Freudenberger (Eds.).
66. Palmer M.W. Putting things in even better order: the advantages of canonical correspondence analysis. Ecology 1993, 74:2215-2230.
67. Parker S.S., Schimel J.P. Soil nitrogen availability and transformations differ between the summer and the growing season in California grassland. Applied Soil Ecology 2011, 48:185-192.
68. Pennington D.D., Collins S.L. Response of an aridland ecosystem to interannual climate variability and prolonged drought. Landscape Ecology 2007, 22:897-910.
69. Peterjohn W.T., Schlesinger W.H. Factors controlling denitrification in a Chihuahuan Desert ecosystem. Soil Science Society of America Journal 1991, 55:1694-1701.
70. Porras-Alfaro A., Herrera J., Natvig D.O., Lipinski K., Sinsabaugh R.L. Diversity and distribution of soil fungal communities in a semiarid grassland. Mycologia 2011, 103:10-21.
71. Porras-Alfaro A., Herrera J., Sinsabaugh R.L., Odenbach K.J., Lowrey T., Natvig D.O. Novel root fungal consortium associated with a dominant desert grass. Applied and Environmental Microbiology 2008, 74:2805-2813.
72. Porras-Alfaro A., Herrera J., Natvig D.O., Sinsabaugh R.L. Effect of long-term nitrogen fertilization on mycorrhizal fungi associated with a dominant grass in a semiarid grassland. Plant and Soil 2007, 296:65-75.
73. Prendergast-Miller M.T., Baggs E.M., Johnson D. Nitrous oxide production by the ectomycorrhizal fungi Paxillus involutus and Tylospora fibrillosa. FEMS Microbiology Letters 2011, 316(1):31-35.
74. Prosser J.I. Autotrophic nitrification in bacteria. Advances in Microbial Physiology 1989, 30:125-181.
75. Raciti S.M., Burgin A.J., Groffman P.M., Lewis D., Fahey T.J. Denitrification in suburban lawn soils. Journal of Environmental Quality 2011, 40:1932-1940.
76. Raciti S.M., Groffman P.M., Jenkins J.C., Pouyat R.V., Fahey T.J., Pickett S.T.A., Cadenasso M.L. Nitrate production and availability in residential soils. Ecological Applications 2011, 21:2357-2366.
77. Rasche M.E., Ferry J.G. Molecular biology of methanogens and Archaea. The Encyclopedia of Molecular Biology and Molecular Medicine 1996, Weinheim, New York, pp. 66-78. R.A. Meyers (Ed.).
78. Reynolds J.F., Kemp P.R., Ogle K., Fernández R.J. Modifying the 'pulse-reserve' paradigm for deserts of North America: precipitation pulses, soil water, and plant responses. Oecologia 2004, 141:194-210.
79. Rousk J., Demoling L.A., Bahr A., Bååth E. Examining the fungal and bacterial niche overlap using selective inhibitors in soil. FEMS Microbiology Ecology 2008, 63:350-358.
80. Safriel U., Adeel Z., Niemeijer D., Puigdefabregas J., White R., Lal R., Winslow M., Ziedler J., Prince S., Archer E., King C. Dryland systems. Ecosystems and Human Well-being. Findings of the Conditions and Trends Working Group of the Millennium Ecosystem Assessment 2005, 623-662. Island Press, Washington, D.C. R. Hassan, R.J. Scholes, N. Ash (Eds.).
81. 2O produced by marine ammonia-oxidizing archaea. Science 2011, 333:1282-1285.
82. Seo D.C., DeLaune R.D. Fungal and bacterial mediated denitrification in wetlands: influence of sediment redox condition. Water Research 2010, 44:2441-2450.
83. Schimel J.P., Firestone M.K., Killham K.S. Identification of heterotrophic nitrification in a Sierran forest soil. Applied and Environmental Microbiology 1984, 48:802-806.
84. Schlesinger W.H., Raikes J.A., Hartley A.E., Cross A.F. On the spatial pattern of soil nutrients in desert ecosystems. Ecology 1996, 7:364-374.
85. Seitzinger S., Harrison J.A., Bohlke J.K., Bouwman A.F., Lowrance R., Peterson B., Tobias C., Van Drecht G. Denitrification across landscapes and waterscapes: a synthesis. Ecological Applications 2006, 16:2064-2090.
86. Shoun H., Kim D.H., Uchiyama H., Sugiyama J. Denitrification by fungi. FEMS Microbiology Letters 1992, 94:277-281.
87. Shoun H., Fushinobu S., Jiang L., Kim S.W., Wakagi T. Fungal denitrification and nitric oxide reductase cytochrome P450nor. Philosophical Transactions of the Royal Society B 2012, 367:1186-1194.
88. Singh B.K., Bardgett R.D., Smith P., Reay D.S. Microorganisms and climate change: terrestrial feedbacks and mitigation options. Nature Reviews Microbiology 2010, 8:779-790.
89. Smith A., Koper N., Francis C., Fahrig L. Confronting collinearity: comparing methods for disentangling the effects of habitat loss and fragmentation. Landscape Ecology 2009, 24:1271-1285.
90. Smith K., Thomson P., Clayton H., McTaggart I., Conen F. Effects of temperature, water content and nitrogen fertilisation on emissions of nitrous oxide by soils. Atmospheric Environment 1998, 32:3301-3309.
91. Spielmann K., Schaafsma H., Hall S.J., Kruse-Peeples M., Briggs J. Legacies on the landscape: the enduring effects of long-term human ecosystem interactions. Changing Histories, Landscapes, and Perspectives: the 20th Anniversary Southwest Symposium 2011, 199-217. University Press of Colorado, Boulder. M. Nelson, C. Strawhacker (Eds.).
92. Sponseller R.A., Hall S.J., Huber D.P., Grimm N.B., Kaye J.P., Clark C.M., Collins S.L. Variation in monsoon precipitation drives spatial and temporal patterns of Larrea tridentata growth in the Sonoran Desert. Functional Ecology 2012, 26:750-758.
93. 2 flux in a Sonoran Desert ecosystem. Global Change Biology 2007, 13:426-436.
94. Stark J.M. Shaker speeds for aerobic soil slurry incubations. Communications in Soil Science & Plant Analysis 1996, 27:2625-2631.
95. Strauss S.L., Day T.A., Garcia-Pichel F. Nitrogen cycling in desert biological soil crusts across biogeographic regions in the southwestern United States. Biogeochemistry 2012, 108:171-182.
96. Strickland M.S., Rousk J. Considering fungal: bacterial dominance in soils-methods, controls, and ecosystem implications. Soil Biology and Biochemistry 2010, 42:1385-1395.
97. Stursova M., Crenshaw C., Sinsabaugh R. Microbial responses to long-term N deposition in a semiarid grassland. Microbial Ecology 2006, 51:90-98.
98. Sullivan B.W., Selmants P.C., Hart S.C. New evidence that high potential nitrification rates occur in soils during dry seasons: are microbial communities metabolically active during dry seasons?. Soil Biology and Biochemistry 2012, 53:28-31.
99. 2O production by fungal denitrification. Rapid Communications in Mass Spectrometry 2008, 22:3989-3996.
100. Taylor A.E., Zeglin L.H., Dooley S., Myrold D.D., Bottomley P.J. Evidence for different contributions of archaea and bacteria to the ammonia-oxidizing potential of diverse Oregon soils. Applied and Environmental Microbiology 2010, 76:7691-7698.
101. Tourna M., Stieglmeier M., Spang A., Könneke M., Schintlmeister A., Urich T., Engel M., Schloter M., Wagner M., Richter A., Schleper C. Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proceedings of the National Academy of Sciences USA 2011, 108:8420-8425.
102. Trujillo J.E. Seasonality and Ecosystem Response in Two Prehistoric Agricultural Regions of Central Arizona 2011, Master of Science thesis, ProQuest Publication 1490595. School of Life Sciences, Arizona State University, Tempe.
103. Veresoglou S.D., Chen B.D., Rillig M.C. Arbuscular mycorrhiza and soil nitrogen cycling. Soil Biology and Biochemistry 2012, 46:53-62.
104. Warren A., Sud Y.C., Rozanov B. The future of deserts. Journal of Arid Environments 1996, 32:75-89.
105. Weisblum B., Davies J. Antibiotic inhibitors of the bacterial ribosome. Bacteriological Reviews 1968, 32:493-528.
106. Wrage N., Velthof G.L., van Beusichem M.L., Oenema O. Role of nitrifier denitrification in the production of nitrous oxide. Soil Biology and Biochemistry 2001, 33:1723-1732.
107. Historical Climate Information 1985, WRCC (Western Regional Climate Center), National Oceanic and Atmospheric Administration. http://www.wrcc.dri.edu/narratives/arizona, third ed.
108. Zhou Z.M., Takaya N., Shoun H. Multi-energy metabolic mechanisms of the fungus Fusarium oxysporum in low oxygen environments. Bioscience Biotechnology and Biochemistry 2010, 74:2431-2437.