Different roles of rhizosphere effect and long-term fertilization in the activity and community structure of ammonia oxidizers in a calcareous fluvo-aquic soil

Soil Biology and Biochemistry

Volumn 57, Issue , 2013, Pages 30-42

  Ai, Chao ^a   Liang, Guoqing ^a   Sun, Jingwen ^a   Wang, Xiubin ^a   He, Ping ^a   Zhou, Wei ^a  

^a INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

Ammonia oxidizing archaea; Ammonia oxidizing bacteria; Community structure; Long term fertilization; Population size; Potential nitrification activity; Rhizosphere

Indexed keywords

AMMONIA OXIDIZING BACTERIA; ARCHAEA; COMMUNITY STRUCTURES; LONG-TERM FERTILIZATION; POPULATION SIZES; POTENTIAL NITRIFICATION; RHIZOSPHERE;

AMMONIA; BACTERIA; DENITRIFICATION; ELECTROPHORESIS; MANURES; NITRIFICATION; NITROGEN FERTILIZERS; OXIDATION; POLYMERASE CHAIN REACTION; POPULATION STATISTICS; SOCIAL SCIENCES;

SOILS;

AMMONIA; CALCAREOUS SOIL; CHEMICAL COMPOSITION; CLUSTER ANALYSIS; COMMUNITY STRUCTURE; FERTILIZATION (REPRODUCTION); NITRIFICATION; POPULATION SIZE; RHIZOSPHERE; SOIL NITROGEN;

ARCHAEA; BACTERIA (MICROORGANISMS); NITROSOMONADALES; NITROSOSPIRA; TRITICUM AESTIVUM; ZEA MAYS;

EID: 84869878566     PISSN: 00380717     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.soilbio.2012.08.003     Document Type: Article

References (66)

1. Agogué H., Brink M., Dinasquet J., Herndl G.J. Major gradients in putatively nitrifying and non-nitrifying Archaea in the deep North Atlantic. Nature 2008, 456:788-791.
2. Ai C., Liang G., Sun J., Wang X., Zhou W. Responses of extracellular enzyme activities and microbial community in both the rhizosphere and bulk soil to long-term fertilization practices in a fluvo-aquic soil. Geoderma 2012, 173-174:330-338.
3. Avrahami S., Conrad R. Patterns of community change among ammonia oxidizers in meadow soils upon long-term incubation at different temperatures. Applied and Environmental Microbiology 2003, 69:6152-6164.
4. Cavagnaro T., Jackson L., Hristova K., Scow K. Short-term population dynamics of ammonia oxidizing bacteria in an agricultural soil. Applied Soil Ecology 2008, 40:13-18.
5. Chen X.P., Zhu Y.G., Xia Y., Shen J.P., He J.Z. Ammonia-oxidizing archaea: important players in paddy rhizosphere soil?. Environmental Microbiology 2008, 10:1978-1987.
6. Cheng W., Johnson D., Fu S. Rhizosphere effects on decomposition: controls of plant species, phenology, and fertilization. Soil Science Society of America Journal 2003, 67:1418-1427.
7. Chu H., Fujii T., Morimoto S., Lin X., Yagi K. Population size and specific nitrification potential of soil ammonia-oxidizing bacteria under long-term fertilizer management. Soil Biology and Biochemistry 2008, 40:1960-1963.
8. Chu H., Fujii T., Morimoto S., Lin X., Yagi K., Hu J., Zhang J. Community structure of ammonia-oxidizing bacteria under long-term application of mineral fertilizer and organic manure in a sandy loam soil. Applied and Environmental Microbiology 2007, 73:485-491.
9. Coci M., Nicol G., Pilloni G., Schmid M., Kamst-van Agterveld M., Bodelier P., Laanbroek H. Quantitative assessment of ammonia-oxidizing bacterial communities in the epiphyton of submerged macrophytes in shallow lakes. Applied and Environmental Microbiology 2010, 76:1813-1821.
10. De Boer W., Kowalchuk G. Nitrification in acid soils: micro-organisms and mechanisms. Soil Biology and Biochemistry 2001, 33:853-866.
11. Di H., Cameron K., Shen J., Winefield C., O'Callaghan M., Bowatte S., He J. Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nature Geoscience 2009, 2:621-624.
12. Fan F., Yang Q., Li Z., Wei D., Cui X.a., Liang Y. Impacts of organic and inorganic fertilizers on nitrification in a cold climate soil are linked to the bacterial ammonia oxidizer community. Microbial Ecology 2011, 62:982-990.
13. Fan F., Zhang F., Lu Y. Linking plant identity and interspecific competition to soil nitrogen cycling through ammonia oxidizer communities. Soil Biology and Biochemistry 2011, 43:46-54.
14. Fierer N., Carney K.M., Horner-Devine M.C., Megonigal J.P. The biogeography of ammonia-oxidizing bacterial communities in soil. Microbial Ecology 2009, 58:435-445.
15. Fontaine S., Barot S. Size and functional diversity of microbe populations control plant persistence and long-term soil carbon accumulation. Ecology Letters 2005, 8:1075-1087.
16. Francis C.A., Beman J.M., Kuypers M.M.M. New processes and players in the nitrogen cycle: the microbial ecology of anaerobic and archaeal ammonia oxidation. The ISME Journal 2007, 1:19-27.
17. Frijlink M.J., Abee T., Laanbroek H.J., 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.
18. Glaser K., Hackl E., Inselsbacher E., Strauss J., Wanek W., Zechmeister-Boltenstern S., Sessitsch A. Dynamics of ammonia-oxidizing communities in barley-planted bulk soil and rhizosphere following nitrate and ammonium fertilizer amendment. FEMS Microbiology Ecology 2010, 74:575-591.
19. Gubry-Rangin C., Nicol G.W., Prosser J.I. Archaea rather than bacteria control nitrification in two agricultural acidic soils. FEMS Microbiology Ecology 2010, 74:566-574.
20. Hallam S.J., Konstantinidis K.T., Putnam N., Schleper C., Watanabe Y., Sugahara J., Preston C., De La Torre J., Richardson P.M., DeLong E.F. Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum. Proceedings of the National Academy of Sciences 2006, 103:18296-18301.
21. Hart S.C., Stark J.M., Davidson E.A., Firestone M.K. Nitrogen mineralization, immobilisation and nitrification. Methods of Soil Analysis. Part 2. Microbial and Biogeochemical Properties 1994, 985-1018. Soil Science Society of America, Madison. R.W. Weaver, J.S. Angle, P.S. Bottomley (Eds.).
22. He J., Shen J., Zhang L., Zhu Y., Zheng Y., Xu M., 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.
23. Herman D., Jaeger K., Schwartz C., Firestone E. Root influence on nitrogen mineralization and nitrification in rhizosphere soil. Soil Science Society of America Journal 2006, 70:1504-1511.
24. Hermansson A., Lindgren P.E. Quantification of ammonia-oxidizing bacteria in arable soil by real-time PCR. Applied and Environmental Microbiology 2001, 67:972-976.
25. Herrmann M., Saunders A.M., Schramm A. Archaea dominate the ammonia-oxidizing community in the rhizosphere of the freshwater macrophyte Littorella uniflora. Applied and Environmental Microbiology 2008, 74:3279-3283.
26. Hussain Q., Liu Y., Jin Z., Zhang A., Pan G., Li L., Crowley D., Zhang X., Song X., Cui L. Temporal dynamics of ammonia oxidizer (amoA) and denitrifier (nirK) communities in the rhizosphere of a rice ecosystem from Tai Lake region, China. Applied Soil Ecology 2011, 48:210-218.
27. Innerebner G., Knapp B., Vasara T., Romantschuk M., Insam H. Traceability of ammonia-oxidizing bacteria in compost-treated soils. Soil Biology and Biochemistry 2006, 38:1092-1100.
28. Jia Z., Conrad R. Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil. Environmental Microbiology 2009, 11:1658-1671.
29. Könneke M., Bernhard A.E., José R., Walker C.B., Waterbury J.B., Stahl D.A. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 2005, 437:543-546.
30. Kirk G., Kronzucker H. The potential for nitrification and nitrate uptake in the rhizosphere of wetland plants: a modelling study. Annals of Botany 2005, 96:639-646.
31. Kleineidam K., Kosmrlj K., Kublik S., Palmer I., Pfab H., Ruser R., Fiedler S., Schloter M. Influence of the nitrification inhibitor 3, 4-dimethylpyrazole phosphate (DMPP) on ammonia-oxidizing bacteria and archaea in rhizosphere and bulk soil. Chemosphere 2011, 84:182-186.
32. Kowalchuk G.A., Stephen J.R. Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annual Reviews in Microbiology 2001, 55:485-529.
33. Kowalchuk G.A., Stephen J.R., De Boer W., Prosser J.I., Embley T.M., Woldendorp J.W. Analysis of ammonia-oxidizing bacteria of the beta subdivision of the class Proteobacteria in coastal sand dunes by denaturing gradient gel electrophoresis and sequencing of PCR-amplified 16S ribosomal DNA fragments. Applied and Environmental Microbiology 1997, 63:1489-1497.
34. Kowalchuk G.A., Stienstra A.W., Heilig G.H.J., Stephen J.R., Woldendorp J.W. Molecular analysis of ammonia-oxidising bacteria in soil of successional grasslands of the Drentsche A (The Netherlands). FEMS Microbiology Ecology 2000, 31:207-215.
35. Kuzyakov Y. Review: factors affecting rhizosphere priming effects. Journal of Plant Nutrition and Soil Science 2002, 165:382-396.
36. Leininger S., Urich T., Schloter M., Schwark L., Qi J., Nicol G., Prosser J., Schuster S., Schleper C. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 2006, 442:806-809.
37. Liljeroth E., Kuikman P., Veen J.A. Carbon translocation to the rhizosphere of maize and wheat and influence on the turnover of native soil organic matter at different soil nitrogen levels. Plant and Soil 1994, 161:233-240.
38. Malchair S., De Boeck H.J., Lemmens C.M.H.M., Merckx R., Nijs I., Ceulemans R., Carnol M. Do climate warming and plant species richness affect potential nitrification, basal respiration and ammonia-oxidizing bacteria in experimental grasslands?. Soil Biology and Biochemistry 2010, 42:1944-1951.
39. Muyzer G., de Waal E.C., Uitterlinden A.G. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Applied and Environmental Microbiology 1993, 59:695-700.
40. Neumann G., Römheld V. Root-induced changes in the availability of nutrients in the rhizosphere. Plant Roots: the Hidden Half 2002, 617-649. Marcel Dekker, Inc., New York. third ed. Y. Waisel, A. Eshel, U. Kafkafi (Eds.).
41. 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. Environmental Microbiology 2008, 10:2966-2978.
42. Park B.J., Park S.J., Yoon D.N., Schouten S., Damsté J.S.S., Rhee S.K. Cultivation of autotrophic ammonia-oxidizing archaea from marine sediments in coculture with sulfur-oxidizing bacteria. Applied and Environmental Microbiology 2010, 76:7575-7587.
43. Phillips C.J., Harris D., Dollhopf S.L., Gross K.L., Prosser J.I., Paul E.A. Effects of agronomic treatments on structure and function of ammonia-oxidizing communities. Applied and Environmental Microbiology 2000, 66:5410-5418.
44. Prosser J. Autotrophic nitrification in bacteria. Advances in Microbial Physiology 1990, 30:125-181.
45. Rovira A. Plant root exudates. The Botanical Review 1969, 35:35-57.
46. Sørensen J. The rhizosphere as a habitat for soil microorganisms. Modern Soil Microbiology 1997, 21-45. Marcel Dekker, New York. J.D. van Elsas, J.T. Trevors, E.M.K. Wellington (Eds.).
47. Schauss K., Focks A., Leininger S., Kotzerke A., Heuer H., Thiele-Bruhn S., Sharma S., Wilke B.M., Matthies M., Smalla K. Dynamics and functional relevance of ammonia-oxidizing archaea in two agricultural soils. Environmental Microbiology 2009, 11:446-456.
48. Shen J., Zhang L., Zhu Y., Zhang J., He J. Abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea communities of an alkaline sandy loam. Environmental Microbiology 2008, 10:1601-1611.
49. Stephen J.R., McCaig A.E., Smith Z., Prosser J.I., Embley T.M. Molecular diversity of soil and marine 16S rRNA gene sequences related to beta-subgroup ammonia-oxidizing bacteria. Applied and Environmental Microbiology 1996, 62:4147-4154.
50. Subbarao G., Ito O., Sahrawat K., Berry W., Nakahara K., Ishikawa T., Watanabe T., Suenaga K., Rondon M., Rao I. Scope and strategies for regulation of nitrification in agricultural systems-challenges and opportunities. Critical Reviews in Plant Sciences 2006, 25:303-335.
51. Subbarao G., Rondon M., Ito O., Ishikawa T., Rao I., Nakahara K., Lascano C., Berry W. Biological nitrification inhibition (BNI) - is it a widespread phenomenon?. Plant and Soil 2007, 294:5-18.
52. Tamura K., Dudley J., Nei M., Kumar S. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 2007, 24:1596-1599.
53. 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.
54. 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. Environmental genome shotgun sequencing of the Sargasso Sea. Science 2004, 304:66-74.
55. Verhamme D.T., Prosser J.I., Nicol G.W. Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. The ISME Journal 2011, 5:1067-1071.
56. Walker C., De La Torre J., Klotz M., Urakawa H., Pinel N., Arp D., Brochier-Armanet C., Chain P., Chan P., Gollabgir A. Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proceedings of the National Academy of Sciences 2010, 107:8818-8823.
57. Wang S., Wang Y., Feng X., Zhai L., Zhu G. Quantitative analyses of ammonia-oxidizing Archaea and bacteria in the sediments of four nitrogen-rich wetlands in China. Applied Microbiology and Biotechnology 2011, 90:779-787.
58. Wang Y., Ke X., Wu L., Lu Y. Community composition of ammonia-oxidizing bacteria and archaea in rice field soil as affected by nitrogen fertilization. Systematic and Applied Microbiology 2009, 32:27-36.
59. Wessén E., Nyberg K., Jansson J.K., Hallin S. Responses of bacterial and archaeal ammonia oxidizers to soil organic and fertilizer amendments under long-term management. Applied Soil Ecology 2010, 45:193-200.
60. White C.S. Monoterpenes: their effects on ecosystem nutrient cycling. Journal of Chemical Ecology 1994, 20:1381-1406.
61. Wu Y., Lu L., Wang B., Lin J., Cai Z., Yan X., Jia Z. Long-term field fertilization significantly alters community structure of ammonia-oxidizing bacteria rather than archaea in a paddy soil. Soil Science Society of America Journal 2011, 75:1405-1413.
62. Xue D., Gao Y., Yao H., Huang C. Nitrification potentials of Chinese tea orchard soils and their adjacent wasteland and forest soils. Journal of Environmental Sciences 2009, 21:1225-1229.
63. Yao H., Gao Y., Nicol G.W., Campbell C.D., Prosser J.I., Zhang L., Han W., Singh B.K. Links between ammonia oxidizer community structure, abundance, and nitrification potential in acidic soils. Applied and Environmental Microbiology 2011, 77:4618-4625.
64. Zhang B., Sun B., Ji M., Liu H., Liu X. Quantification and comparison of ammonia-oxidizing bacterial communities in MBRs treating various types of wastewater. Bioresource Technology 2010, 101:3054-3059.
65. Zhang L.M., Hu H.W., Shen J.P., He J.Z. Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils. The ISME Journal 2011, 10.1038/ismej.2011.168.
66. Zhang L.M., Offre P.R., He J.Z., Verhamme D.T., Nicol G.W., Prosser J.I. Autotrophic ammonia oxidation by soil thaumarchaea. Proceedings of the National Academy of Sciences 2010, 107:17240-17245.