Different Land Use Intensities in Grassland Ecosystems Drive Ecology of Microbial Communities Involved in Nitrogen Turnover in Soil

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Meyer, Annabel ^a   Focks, Andreas ^b   Radl, Viviane ^c   Keil, Daniel ^d   Welzl, Gerhard ^c   Schöning, Ingo ^e   Boch, Steffen ^f   Marhan, Sven ^d   Kandeler, Ellen ^d   Schloter, Michael ^c  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b WAGENINGEN UNIVERSITY   (Netherlands)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

^d UNIVERSITY OF HOHENHEIM   (Germany)

^e FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^f UNIVERSITY OF BERN   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; NITROGEN; ORGANIC NITROGEN;

AMMONIA OXIDIZER; AMOA AOA GENE; AMOA AOB GENE; ARTICLE; AZOSPIRILLUM; BACTERIAL GENE; BIODIVERSITY; CLIMATE; CONTROLLED STUDY; DENITRIFICATION; ECOSYSTEM; ENERGY RESOURCE; GENE DOSAGE; GENE FUNCTION; GRASSLAND; LAND USE; LAND USE INTENSITY; MICROBIAL ACTIVITY; MICROBIAL COMMUNITY; NIFH GENE; NIRK GENE; NIRS GENE; NITRIFICATION; NITROGEN AVAILABILITY; NITROGEN CYCLING; NITROGEN FIXATION; NITROGEN METABOLISM; NITROSOMONAS; NONHUMAN; PASTURE; PLANT COMMUNITY; PLANT GROWTH; POLYMERASE CHAIN REACTION; POPULATION ABUNDANCE; PSEUDOMONAS STUTZERI; QUANTITATIVE ANALYSIS; SOIL; SOIL TEXTURE;

AGRICULTURE; BACTERIA; BIODIVERSITY; DENITRIFICATION; ECOSYSTEM; GENES, BACTERIAL; NITRIFICATION; NITROGEN; NITROGEN CYCLE; POACEAE; SOIL; SOIL MICROBIOLOGY;

EID: 84883627945     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0073536     Document Type: Article

References (68)

1. Singh DK, (2008) Biodegradation and bioremediation of pesticide in soil: concept, method and recent developments. Indian Journal of Microbiology 48: 35-40.
2. Lillis L, Doyle E, Clipson N, (2009) Comparison of DNA- and RNA-based bacterial community structures in soil exposed to 2,4-dichlorophenol. Journal of Applied Microbiology 107: 1883-1893.
3. Sinha S, Chattopadhyay P, Pan I, Chatterjee S, Chanda P, et al. (2009) Microbial transformation of xenobiotics for environmental bioremediation. African Journal of Biotechnology 8: 6016-6027.
4. Ollivier J, Töwe S, Bannert A, Hai B, Kastl EM, et al. (2011) Nitrogen turnover in soil and global change. FEMS Microbiology Ecology 78: 3-16.
5. Dilly O, Blume HP, Sehy U, Jimenez M, Munch JC, (2003) Variation of stabilized, microbial and biologically active carbon and nitrogen in soil under contrasting land use and agricultural management practices. Chemosphere 52: 557-569.
6. Patra AK, Abbadie L, Clays-Josserand A, Degrange V, Grayston SJ, et al. (2006) Effects of management regime and plant species on the enzyme activity and genetic structure of N-fixing, denitrifying and nitrifying bacterial communities in grassland soils. Environmental Microbiology 8: 1005-1016.
7. Cookson WR, Osman M, Marschner P, Abaye DA, Clark I, et al. (2007) Controls on soil nitrogen cycling and microbial community composition across land use and incubation temperature. Soil Biology and Biochemistry 39: 744-756.
8. Robson TM, Lavorel S, Clement JC, Le Roux X, (2007) Neglect of mowing and manuring leads to slower nitrogen cycling in subalpine grasslands. Soil Biology & Biochemistry 39: 930-941.
9. Berthrong ST, Schadt CW, Pineiro G, Jackson RB, (2009) Afforestation alters the Composition of Functional Genes in Soil and Biogeochemical Processes in South American Grasslands. Applied and Environmental Microbiology 75: 6240-6248.
10. Cheneby D, Brauman A, Rabary B, Philippot L, (2009) Differential responses of nitrate reducer community size, structure, and activity to tillage systems. Applied and Environmental Microbiology 75: 3180-3186.
11. Vargas Gil S, Meriles J, Conforto C, Figoni G, Basanta M, et al. (2009) Field assessment of soil biological and chemical quality in response to crop management practices. World Journal of Microbiology and Biotechnology 25: 439-448.
12. Attard E, Poly F, Commeaux C, Laurent F, Terada A, et al. (2010) Shifts between Nitrospira- and Nitrobacter-like nitrite oxidizers underlie the response of soil potential nitrite oxidation to changes in tillage practices. Environmental Microbiology 12: 315-326.
13. Kaschuk G, Alberton O, Hungria M, (2009) Three decades of soil microbial biomass studies in Brazilian ecosystems: Lessons learned about soil quality and indications for improving sustainability. Soil Biology & Biochemistry 42: 1-13.
14. Hai B, Diallo NH, Sall S, Haesler F, Schauss K, et al. (2009) Quantification of key genes steering the microbial nitrogen cycle in the rhizosphere of sorghum cultivars in tropical agro-ecosystems. Applied and Environmental Microbiology 75: 1034-1043.
15. Thurston JM (1969) The effect of liming and fertilizers on the botanical composition of permanent grassland and the yield of hay. (Thurston JM ed.), 3-10. Blackwell, Oxford.
16. Kirkham FW, Mountford JO, Wilkins RJ, (1996) The effects of nitrogen, potassium and phosphorus addition on the vegetation of a Somerset peat moor under cutting management. Journal of Applied Ecology 33: 1013-1029.
17. Wedin DA, Tilman D, (1996) Influence of nitrogen loading and species composition on the carbon balance of grasslands. Science 274: 1720-1723.
18. O'Neill KM, Olson BE, Wallander R, Rolston MG, Seibert CE, (2010) Effects of Livestock Grazing on Grasshopper Abundance on a Native Rangeland in Montana. Environmental Entomology 39: 775-786.
19. Mills A, Adl MS, (2006) The effects of land use intensification on soil biodiversity in the pasture. Canadian Journal of Plant Science 86: 1339-1343.
20. Parfitt RL, Yeates GW, Ross DJ, Schon NL, Mackay AD, et al. (2010) Effect of fertilizer, herbicide and grazing management of pastures on plant and soil communities. Applied Soil Ecology 45: 175-186.
21. Postma-Blaauw MB, de Goede RGM, Bloem J, Faber JH, Brussaard L, (2010) Soil biota community structure and abundance under agricultural intensification and extensification. Ecology 91: 460-473.
22. Fischer M, Bossdorf O, Gockel S, et al. (2010) Implementing large-scale and long-term functional biodiversity research: The Biodiversity Exploratories. Basic and Applied Ecology 11: 473-485.
23. Grime JP, (1977) Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. The American Naturalist 111: 1169-1194.
24. Ellenberg H., Weber H.E., Düll R., Wirth V. (2001) Zeigerwerte von Pflanzen in Mitteleuropa. Institute for Phytogeography, University of Göttingen, Göttingen.
25. Houba V, Novozamsky I, Huybregts A, van der Lee J, (1986) Comparison of soil extractions by 0.01 M CaCl2, by EUF and by some conventional procedures. Plant and Soil 96: 433-437.
26. Hoffmann H, Schloter M, Wilke BM, (2007) Gradients of potential microbial nitrification rates in soil aggregates; Biology and Fertility of Soils. 44: 411-413.
27. Tiedje JM (1988) Ecology of denitrification and dissimilatory nitrate reduction to ammonium. John Wiley and Sons, New York.
28. Šimek M, Hopkins DW, (1999) Regulation of potential denitrification by soil pH in long-term fertilized arable soils. Biology and Fertility of Soils 30: 41-4.
29. Tilman (1987) Secondary succession of pattern of plants dominate experimental nitrogen gradients. Ecological Monographies 57: 1898-1914.
30. Scott D, Shay J, (1990) Competition, Fire, and Nutients in a Mixed-Grass Prairie. Ecology 71: 1959-1967.
31. Jacquemyn H, Brys R, Hermy M, (2003) Short-term effects of different management regimes on the response of calcareous grassland vegetation to increased nitrogen. Biological Conservation 111: 137-147.
32. Maurer K, Weyand A, Fischer M, et al. (2006) Old cultural traditions, in addition to land use and topography, are shaping plant diversity of grasslands in the Alps.Biological Conservation. 110: 438-446.
33. Klimek S, Richter G, Kemmermann A, Hofmann M, Isselstein J, (2007) Plant species richness and composition in managed grasslands: the relative importance of field management and environmental factors. Biological. Conservation 134: 559-570.
34. Gough L, Osenberg CW, Gross C, Collins S, (2000) Fertilization effects on species density and primary productivity in herbaceous plant communities. Oikos 89: 428-439.
35. Le Roux X, Bardy M, Loiseau P, Louault F, (2003) Stimulation of soil nitrification and denitrification by grazing in grasslands: do changes in plant species composition matter? Oecologia 137: 417-425.
36. Le Roux X, Poly F, Currey P, et al. (2008) Effects of aboveground grazing on coupling among nitrifier activity, abundance and community structure. ISME Journal 2: 221-232.
37. Gubry-Rangin C, Hai B, Quince C, Engel M, Thomson BC, et al. (2011) Niche specialization of terrestrial archaeal ammonia oxidizers; PNAS. 108: 21206-21211.
38. Tourna M, Stieglmeier M, Spang A, Koenneke M, Schintlmeister A, et al. (2011) Nitrosophaera vinnensis, an ammonia oxidizing archaeaon from soil; PNAS 108, 8420-8425.
39. Subbarao GV, Nakahara K, Hurtado MP, Ono H, Morata DE, et al. (2009) Evidence for biological nitrification inhibition in Brachiaria pastures. Proceedings of the National Academy of Sciences (USA) 106: 7302-1730.
40. Leininger S, Urich T, Schloter M, et al. (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442: 806-809.
41. Babic KH, Schauss K, Hai B, Sikora S, Redzepovic S, et al. (2008) Influence of different Sinorhizobium meliloti inocula on abundance of genes involved in nitrogen transformations in the rhizosphere of alfalfa (Medicago sativa L.). Environmental Microbiology 10: 2922-2930.
42. Di HJ, Cameron KC, Shen JP, He JZ, Winefield CS, (2009) A lysimeter study of nitrate leaching from grazed grassland as affected by a nitrification inhibitor, dicyandiamide, and relationships with ammonia oxidizing bacteria and archaea. Soil Use and Management 25: 454-461.
43. Jia ZJ, Conrad R, (2009) Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil. Environmental Microbiology 11: 1658-1671.
44. Mertens J, Broos K, Wakelin SA, Kowalchuk GA, Springael D, et al. (2009) Bacteria, not archaea, restore nitrification in a zinc-contaminated soil. ISME Journal 3: 916-923.
45. Offre P, Prosser JI, Nicol GW, (2009) Growth of ammonia-oxidizing archaea in soil microcosms is inhibited by acetylene. FEMS Microbiology Ecology 70: 99-108.
46. Schauss K, Focks A, Leininger S, Kotzerke A, Heuer H, et al. (2009) Dynamics and functional relevance of ammonia-oxidizing archaea in two agricultural soils. Environmental Microbiology 11: 446-456.
47. Drew MC, Lynch JM (1980) Soil anaerobiosis, microorganisms, and root function. Annual Review of Phytopathology 18.
48. Zausig JR, Stepniewski W, Horn R, (1993) Oxygen Concentration and redox potential Gradients in Unsaturated Model Soil Aggregates. Soil Science Society of America Journal 57: 908-916.
49. Vinther FP, Eiland F, Lind AM, Elsgaard L, (1999) Microbial biomass and numbers of denitrifiers related to macropore channels in agricultural and forest soils. Soil Biology and Biochemistry 31: 603-611.
50. Henry S, Baudoin E, Lopez-Gutierrez JC, Martin-Laurent F, Brauman A, et al. (2004) Quantification of denitrifying bacteria in soils by nirK gene targeted real-time PCR. Journal of Microbiological Methods 59: 327-335.
51. Henry S, Bru D, Stres B, Hallet S, Philippot L, (2006) 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 72: 5181-5189.
52. Dandie CE, Burton DL, Zebarth BJ, Henderson SL, Trevors JT, et al. (2008) Changes in Bacterial Denitrifier Community Abundance over Time in an Agricultural Field and Their Relationship with Denitrification Activity. Applied and Environmental Microbiology 74: 5997-6005.
53. Hallin S, Jones CM, Schloter M, Philippot L, (2009) Relationship between N-cycling communities and ecosystem functioning in a 50-year-old fertilization experiment. ISME Journal 3: 597-605.
54. Sharma S, Aneja MK, Mayer J, Munch JC, Schloter M, (2005) Diversity of transcripts of nitrite reductase genes (nirK and nirS) in rhizospheres of grain legumes. Applied and Environmental Microbiology 71: 2001-2007.
55. Sharma S, Szele Z, Schilling R, Munch JC, Schloter M, (2006) Influence of freeze-thaw stress on the structure and function of microbial communities and denitrifying populations in Soil. Applied and Environmental Microbiology 72: 2148-2154.
56. Enwall K, Philippot L, Hallin S, (2005) Activity and composition of the denitrifying bacterial community respond differently to long-term fertilization. Applied and Environmental Microbiology 71: 8335-8343.
57. Philippot L, Hallin S, (2005) Finding the missing link between diversity and activity using denitrifying bacteria as a model functional community. Current Opinion in Microbiology 8: 234-239.
58. Bremer C, Braker G, Matthies D, Reuter A, Engels C, et al. (2007) Impact of plant functional group, plant species, and sampling time on the composition of nirK-type denitrifier communities in soil. Applied and Environmental Microbiology 73: 6876-6884.
59. Mounier E, Hallet S, Chèneby D, et al. (2004) Influence of maize mucilage on the diversity and activity of the denitrifying community. Environmental Microbiology 6: 301-312.
60. Henry S, Texier S, Hallet S, et al. (2008) Disentangling the rhizosphere effect on nitrate reducers and denitrifiers: insight into the role of root exudates. Environmental Microbiology 10: 3082-3092.
61. Myrold DD, Bottomley PJ (2007) Biological N inputs. (Paul EA, eds.), 365-388. Elsivier, Burlington.
62. Brankatsch R, Töwe S, Kleineidam K, Zeyer J, Schloter M, (2011) Abundances and potential activities of nitrogen cycling microbial communities along a glacier chronosequence; The ISME Journal. 5: 1025-1037.
63. Hou F, Nan Z, Xiao J, Chang S, (2002) [Characteristics of vegetation, soil, and their coupling of degraded grasslands]. Ying Yong Sheng Tai Xue Bao 13: 915-922.
64. Patra AK, Abbadie L, Clays-Josserand A, et al. (2005) Effects of grazing on microbial functional groups involved in soil N dynamics. Ecological Monographs 75: 65-80.
65. Rösch C, Mergel A, Bothe H, (2002) Biodiversity of denitrifying and dinitrogen-fixing bacteria in an acid forest soil. Applied Environmental Microbiology. 68: 3818-3829.
66. Rotthauwe JH, Witzel KP, Liesack W, (1997) The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Applied Environmental Microbiology 63: 4704-4712.
67. Michotey V, Méjean V, Bonin P, (2000) Comparison of methods for quantification of cytochrome cd1-denitrifying bacteria in environmental marine samples. Applied Environmental Microbiology 66: 1564-1571.
68. Throbäck IN, Enwall K, Jarvis A, Hallin S, (2004) Reassessing PCR primers targeting nirS, nirK and nosZ genes for community surveys of denitifying bacteria with DGGE. FEMS Microbiology Ecology 49: 401-417.