Identifying response groups of soil nitrifiers and denitrifiers to grazing and associated soil environmental drivers in Tibetan alpine meadows

Soil Biology and Biochemistry

Volumn 77, Issue , 2014, Pages 89-99

  Xie, Zhen ^a   Le Roux, Xavier ^b   Wang, Chuanpei ^a   Gu, Zhenkuan ^a   An, Miao ^a   Nan, Huaiyan ^a   Chen, Binze ^a   Li, Fan ^a   Liu, Yongjun ^a   Du, Guozhen ^a   Feng, Huyuan ^a   Ma, Xiaojun ^a  

^a LANZHOU UNIVERSITY   (China)

^b UNIVERSITÉ LYON 1   (France)

Author keywords

Abundance; AmoA; AOA; AOB; Community structure; NirK; NirS; Soil nitrogen cycling

Indexed keywords

AMMONIA; MICROORGANISMS; NITRIFICATION; SOIL MOISTURE;

ABUNDANCE; AMOA; AOA; AOB; COMMUNITY STRUCTURES; NIRK; NIRS; SOIL NITROGEN;

DENITRIFICATION;

ABUNDANCE; ALPINE ENVIRONMENT; COMMUNITY STRUCTURE; MEADOW; MICROBIAL ACTIVITY; NITRATE; SOIL MICROORGANISM; SOIL NITROGEN; SOIL ORGANIC MATTER;

CHINA; XIZANG;

EID: 84903892766     PISSN: 00380717     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.soilbio.2014.06.024     Document Type: Article

References (94)

1. Altesor A., Oesterheld M., Leoni E., Lezama F., Rodríguez C. Effect of grazing on community structure and productivity of a Uruguayan grassland. Plant Ecol. 2005, 179:83-91.
2. Augustine D., Frank D. Effects of migratory grazers on spatial heterogeneity of soil nitrogen properties in a grassland ecosystem. Ecology 2001, 82:3149-3162.
3. Avrahami S., Conrad R. Patterns of community change among ammonia oxidizers in meadow soils upon long-term incubation at different temperatures. Appl. Environ. Microbiol. 2003, 69:6152-6164.
4. 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.
5. Banerjee S., Siciliano S.D. Spatially tripartite interactions of denitrifiers in arctic ecosystems: activities, functional groups and soil resources. Environ. Microbiol. 2012, 14:2601-2613.
6. Bardgett R.D., Wardle D.A. Herbivore-mediated linkages between aboveground and belowground communities. Ecology 2003, 84:2258-2268.
7. Bender M., Wood C. Total phosphorous in soil. Methods of Phosphorus Analysis for Soils, Sediments, Residuals, and Waters, Southern Cooperative Series Bulletin No. 396. Washington, D.C. 2000, 45-49. G.M. Pierzynski (Ed.).
8. Braker G., Fesefeldt 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. Appl. Environ. Microbiol. 1998, 64:3769-3775.
9. Braker G., Dorsch P., Bakken L.R. Genetic characterization of denitrifier communities with contrasting intrinsic functional traits. FEMS Microbiol. Ecol. 2012, 79:542-554.
10. Bremer C., Braker G., Matthies D., Beierkuhnlein C., Conrad R. Plant presence and species combination, but not diversity, influence denitrifier activity and the composition of nirK-type denitrifier communities in grassland soil. FEMS Microbiol. Ecol. 2009, 70:377-387.
11. Bremer C., Braker G., Matthies D., Reuter A., Engels C., Conrad R. Impact of plant functional group, plant species, and sampling time on the composition of nirK-type denitrifier communities in soil. Appl. Environ. Microbiol. 2007, 73:6876-6884.
12. Chen H., Wang M., Wu N., Wang Y., Zhu D., Gao Y., Peng C. Nitrous oxide fluxes from the littoral zone of a lake on the Qinghai-Tibetan Plateau. Environ. Monit. Assess. 2011, 182:545-553.
13. 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. Appl. Environ. Microbiol. 2007, 73:485-491.
14. Dandie C.E., Wertz S., Leclair C.L., Goyer C., Burton D.L., Patten C.L., Zebarth B.J., Trevors J.T. Abundance, diversity and functional gene expression of denitrifier communities in adjacent riparian and agricultural zones. FEMS Microbiol. Ecol. 2011, 77:69-82.
15. De Deyn G.B., Cornelissen J.H., Bardgett R.D. Plant functional traits and soil carbon sequestration in contrasting biomes. Ecol. Lett. 2008, 11:516-531.
16. Di H.J., Cameron K.C., Shen J.P., Wineeld C.S., O'Callaghan M., Bowatte S., He J.Z. Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nat. Geosci. 2009, 2:621-624.
17. 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 Microbiol. Ecol. 2010, 72:386-394.
18. Enwall K., Throback I.N., Stenberg M., Soderstrom M., Hallin S. Soil resources influence spatial patterns of denitrifying communities at scales Compatible with land management. Appl. Environ. Microbiol. 2010, 76:2243-2250.
19. 2 in the ocean. Nature 1997, 387:272-275.
20. Ford H., Rousk J., Garbutt A., Jones L., Jones D.L. Grazing effects on microbial community composition, growth and nutrient cycling in salt marsh and sand dune grasslands. Biology Fertility Soils 2012, 49:89-98.
21. 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. Proc. Natl. Acad. Sci. USA 2005, 102:14683-14688.
22. French E., Kozlowski J.A., Mukherjee M., Bullerjahn G., Bollmann A. Ecophysiological characterization of ammonia-oxidizing archaea and bacteria from freshwater. Appl. Environ. Microbiol. 2012, 78:5773-5780.
23. Gao Y.H., Luo P., Wu N., Chen H., Wang G.X. Impacts of grazing intensity on nitrogen pools and nitrogen cycle in an alpine meadow on the eastern Tibetan Plateau. Appl. Ecol. Environ. Res. 2008, 6:69-79.
24. 2 pulse labeling. Glob. Change Biol. 2012, 18:528-538.
25. Hallin S., Jones C.M., Schloter M., Philippot L. Relationship between N-cycling communities and ecosystem functioning in a 50-year-old fertilization experiment. ISME J. 2009, 3:597-605.
26. Han G., Hao X., Zhao M., Wang M., Ellert B.H., Willms W., Wang M. Effect of grazing intensity on carbon and nitrogen in soil and vegetation in a meadow steppe in Inner Mongolia. Agric. Ecosyst. Environ. 2008, 125:21-32.
27. 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. Environ. Microbiol. 2007, 9:2364-2374.
28. Heijden M.G.A.V.D., Bardgett R.D., Straalen N.M.V. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol. Lett. 2008, 11:296-310.
29. 2O fluxes in an alpine meadow ecosystem on the Tibetan plateau. Soil. Biol. Biochem. 2010, 42:944-952.
30. Johnston A., Dormaar J.F., Smoliak S. Long-term grazing effects on fescue. J.Range Manag. 1971, 24:185-188.
31. 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.
32. Ka J.-O., Urbance J., Ye R.W., Ahn T.-Y., Tiedje J.M. Diversity of oxygen and N-oxide regulation of nitrite reductases in denitrifying bacteria. FEMS Microbiol. Lett. 1997, 156:55-60.
33. Kandeler E., Deiglmayr 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. Appl. Environ. Microbiol. 2006, 72:5957-5962.
34. Khalil M.I., Richards K.G. Denitrification enzyme activity and potential of subsoils under grazed grasslands assayed by membrane inlet mass spectrometer. Soil. Biol. Biochem. 2011, 43:1787-1797.
35. Krause S., Le Roux X., Niklaus P.A., Bodegom P.M.V., Lennon J.T., Bertilsson S., Grossart H.-P., Philippot L., Bodelier P.L. Trait-based approaches for understanding microbial biodiversity and ecosystem functioning. Front. Microbiol. 2014, 5:251.
36. Lage M.D., Reed H.E., Weihe C., Crain C.M., Martiny J.B. Nitrogen and phosphorus enrichment alter the composition of ammonia-oxidizing bacteria in salt marsh sediments. ISME J. 2010, 4:933-944.
37. Lavorel S., Garnier E. Predicting changes in community composition and ecosystem functioning from plant traits: revisiting the Holy Grail. Funct. Ecol. 2002, 16:545-556.
38. Le Roux X., Bardy M., Loiseau P., Louault F. Stimulation of soil nitrification and denitrification by grazing in grasslands: do changes in plant species composition matter?. Oecologia 2003, 137:417-425.
39. Le Roux X., Poly F., Currey P., Commeaux C., Hai B., Nicol G.W., Prosser J.I., Schloter M., Attard E., Klumpp K. Effects of aboveground grazing on coupling among nitrifier activity, abundance and community structure. ISME J. 2008, 2:221-232.
40. Le Roux X., Schmid B., Poly F., Barnard R.L., Niklaus P.A., Guillaumaud N., Habekost M., Oelmann Y., Philippot L., Salles J.F., Schloter M., Steinbeiss S., Weigelt A. Soil environmental conditions and microbial build-up mediate the effect of plant diversity on soil nitrifying and denitrifying enzyme activities in temperate grasslands. PLoS One 2013, 8:e61069.
41. 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.
42. Leriche H., Le Roux X., Desnoyers F., Benest D., Simioni G., Abbadie L. Grass response to clipping in an African savanna: testing the grazing optimisation hypothesis. Ecol. Appl. 2003, 13:1346-1354.
43. Levičnik-Höfferle Š., Nicol G.W., Ausec L., Mandić-Mulec I., Prosser J.I. Stimulation of thaumarchaeal ammonia oxidation by ammonia derived from organic nitrogen but not added inorganic nitrogen. FEMS Microbiol. Ecol. 2012, 80:114-123.
44. 2O in an alpine meadow affected by yak excreta on the Qinghai-Tibetan plateau during summer grazing periods. Soil. Biol. Biochem. 2009, 41:718-725.
45. Lindsay E.A., Colloff M.J., Gibb N.L., Wakelin S.A. The abundance of microbial functional genes in grassy woodlands is influenced more by soil nutrient enrichment than by recent weed invasion or livestock exclusion. Appl. Environ. Microbiol. 2010, 76:5547-5555.
46. Liu N., Zhang Y., Chang S., Kan H., Lin L. Impact of grazing on soil carbon and microbial biomass in typical steppe and desert steppe of Inner Mongolia. PLoS ONE 2012, 7:e36434.
47. Liu T., Nan Z., Hou F. Grazing intensity effects on soil nitrogen mineralization in semi-arid grassland on the Loess Plateau of northern China. Nutrient Cycl. Agroecosyst. 2011, 91:67-75.
48. 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. Biol. Biochem. 2010, 42:1944-1951.
49. Medina-Roldan E., Paz-Ferreiro J., Bardgett R.D. Grazing-induced effects on soil properties modify plant competitive interactions in semi-natural mountain grasslands. Oecologia 2012, 170:159-169.
50. Mehlich A. Mehlich 3 soil test extractant: a modification of Mehlich 2 extractant. Commun. Soil. Sci. Plant. Anal. 1984, 15:1409-1416.
51. Milchunas D.G., Lauenroth W.K. Quantitative effects of grazing on vegetation and soils over a global range of environments. Ecol. Monogr. 1993, 63:327-366.
52. 2O-metabolizing palsa peat. Appl. Environ. Microbiol. 2012, 78:5584-5596.
53. 2O emission patterns from acidic peat soils in arctic tundra. ISME J. 2012, 6:1058-1077.
54. Patra A.K., Abbadie L., Clays-Josserand A., Degrange V., Grayston S.J., Loiseau P., Louault F., Mahmood S., Nazaret S., Philippot L., Poly F., Prosser J.I., Richaume A., Roux X.L. Effects of grazing on microbial functional groups involved in soil N dynamics. Ecol. Monogr. 2005, 75:65-80.
55. Patra A.K., Abbadie L., Clays-Josserand A., Degrange V., Grayston S.J., Guillaumaud N., Loiseau P., Louault F., Mahmood S., Nazaret S., Philippot L., Poly F., Prosser J.I., Le Roux X. 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. Environ. Microbiol. 2006, 8:1005-1016.
56. Pei S., Fu H., Wan C. Changes in soil properties and vegetation following exclosure and grazing in degraded Alxa desert steppe of Inner Mongolia, China. Agric. Ecosyst. Environ. 2008, 124:33-39.
57. Philippot L., Cuhel J., Saby N.P., Cheneby D., Chronakova A., Bru D., Arrouays D., Martin-Laurent F., Simek M. Mapping field-scale spatial patterns of size and activity of the denitrifier community. Environ. Microbiol. 2009, 11:1518-1526.
58. Prosser J.I. Autotrophic nitrification in bacteria. Adv. Microb. Physiol. 1989, 30:125-181.
59. Prosser J.I., Nicol G.W. Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation. Trends Microbiol. 2012, 20:523-531.
60. Reeder J.D., Schuman G.E., Morgan J.A., Lecain D.R. Response of organic and inorganic carbon and nitrogen to long-term grazing of the shortgrass steppe. Environ. Manage. 2004, 33:485-495.
61. Robson T., Lavorel S., Clement J., Le Roux X. Neglect of mowing and manuring leads to slower nitrogen cycling in subalpine grasslands. Soil. Biol. Biochem. 2007, 39:930-941.
62. 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. Appl. Environ. Microbiol. 1997, 63:4704-4712.
63. Rui Y., Wang S., Xu Z., Wang Y., Chen C., Zhou X., Kang X., Lu S., Hu Y., Lin Q., Luo C. Warming and grazing affect soil labile carbon and nitrogen pools differently in an alpine meadow of the Qinghai-Tibet Plateau in China. J.Soils Sediments 2011, 11:903-914.
64. Schloss P.D., Handelsman J. Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl. Environ. Microbiol. 2005, 71:1501-1506.
65. Schuman G.E., Reeder J.D., Manley J.T., Hart R.H., Manley W.A. Impact of grazing management on the carbon and nitrogen balance of a mixed-grass rangeland. Ecol. Appl. 1999, 9:65-77.
66. Shan Y., Chen D., Guan X., Zheng S., Chen H., Wang M., Bai Y. Seasonally dependent impacts of grazing on soil nitrogen mineralization and linkages to ecosystem functioning in Inner Mongolia grassland. Soil. Biol. Biochem. 2011, 43:1943-1954.
67. Steffens M., Kölbl A., Totsche K.U., Kögel-Knabner I. Grazing effects on soil chemical and physical properties in a semiarid steppe of Inner Mongolia (P.R. China). Geoderma 2008, 143:63-72.
68. Stopnisek N., Gubry-Rangin C., Hofferle S., Nicol G.W., Mandic-Mulec I., Prosser J.I. Thaumarchaeal ammonia oxidation in an acidic forest peat soil is not influenced by ammonium amendment. Appl. Environ. Microbiol. 2010, 76:7626-7634.
69. Su M., Kleineidam K., Schloter M. Influence of different litter quality on the abundance of genes involved in nitrification and denitrification after freezing and thawing of an arable soil. Biol. Fertil. Soils 2010, 46:537-541.
70. Su Y.Z., Zhao H.L., Zhang T.H., Zhao X.Y. Soil properties following cultivation and non-grazing of a semi-arid sandy grassland in northern China. Soil. Tillage Res. 2004, 75:27-36.
71. Su Y.Z., Li Y.L., Cui J.Y., Zhao W.Z. Influences of continuous grazing and livestock exclusion on soil properties in a degraded sandy grassland, Inner Mongolia, northern China. Catena 2005, 59:267-278.
72. Sun D.S., Wesche K., Chen D.D., Zhang S.H., Wu G.L., Du G.Z., Comerford N.B. Grazing depresses soil carbon storage through changing plant biomass and composition in a Tibetan alpine meadow. Plant Soil. Environ. 2011, 57:271-278.
73. Sundareshwar P.V., Morris J.T., Koepfler E.K., Fornwalt B. Phosphorus limitation of coastal ecosystem processes. Science 2003, 299:563-565.
74. Szukics U., Abell G.C., 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 Microbiol. Ecol. 2010, 72:395-406.
75. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biology Evol. 2011, 28:2731-2739.
76. Team R.C. R: a Language and Environment for Statistical Computing 2012, R Foundation for Statistical Computing, Vienna, Austria, Open access available at:. http://cran.r-project.org.
77. Throback I.N., Enwall K., Jarvis A., Hallin S. Reassessing PCR primers targeting nirS, nirK and nosZ genes for community surveys of denitrifying bacteria with DGGE. FEMS Microbiol. Ecol. 2004, 49:401-417.
78. Tiedje J.M. Ecology of denitrification and dissimilatory nitrate reduction to ammonium. Biology Anaerob. Microorg. 1988, 717:179-244.
79. Tourna M., Freitag T.E., Prosser J.I. Stable isotope probing analysis of interactions between ammonia oxidizers. Appl. Environ. Microbiol. 2010, 76:2468-2477.
80. Verhamme D.T., Prosser J.I., Nicol G.W. Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. ISME J. 2011, 5:1067-1071.
81. Vitousek P.M., Howarth R.W. Nitrogen limitation on land and in the sea how can it occur. Biogeochemistry 1991, 13:87-115.
82. 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. Environ. Microbiol. 2005, 7:676-684.
83. Wertz S., Leigh A.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 Microbiol. Ecol. 2012, 79:142-154.
84. Wu G.L., Liu Z.H., Zhang L., Chen J.M., Hu T.M. Long-term fencing improved soil properties and soil organic carbon storage in an alpine swamp meadow of western China. Plant Soil. 2010, 332:331-337.
85. 2O production in a semi-arid grassland ecosystem. Biogeochemistry 2008, 88:103-115.
86. Yan T., Fields Matthew W., Wu L., Zu Y., Tiedje J.M., Zhou J. Molecular diversity and characterization of nitrite reductase gene fragments (nirK and nirS) from nitrate- and uranium-contaminated groundwater. Environ. Microbiol. 2003, 5:13-24.
87. Yang Y., Wu L., Lin Q., Yuan M., Xu D., Yu H., Hu Y., Duan J., Li X., He Z., Xue K., van Nostrand J., Wang S., Zhou J. Responses of the functional structure of soil microbial community to livestock grazing in the Tibetan alpine grassland. Glob. Change Biol. 2013, 19:637-648.
88. Yao H., Bowman D., Shi W. Seasonal variations of soil microbial biomass and activity in warm- and cool-season turfgrass systems. Soil. Biol. Biochem. 2011, 43:1536-1543.
89. Yoshida M., Ishii S., Otsuka S., Senoo K. Temporal shifts in diversity and quantity of nirS and nirK in a rice paddy field soil. Soil. Biol. Biochem. 2009, 41:2044-2051.
90. Yuan Q., Liu P., Lu Y. Differential responses of nirK- and nirS-carrying bacteria to denitrifying conditions in the anoxic rice field soil. Environ. Microbiol. Reports 2012, 4:113-122.
91. Zhang Y., Wang G., Wang Y. Changes in alpine wetland ecosystems of the Qinghai-Tibetan plateau from 1967 to 2004. Environ. Monit. Assess. 2011, 180:189-199.
92. Zhao Y., Peth S., Hallett P., Wang X., Giese M., Gao Y., Horn R. Factors controlling the spatial patterns of soil moisture in a grazed semi-arid steppe investigated by multivariate geostatistics. Ecohydrology 2011, 4:36-48.
93. Zheng Y., Yang W., Sun X., Wang S.P., Rui Y.C., Luo C.Y., Guo L.D. Methanotrophic community structure and activity under warming and grazing of alpine meadow on the Tibetan Plateau. Appl. Microbiol. Biotechnol. 2012, 93:2193-2203.
94. Zumft W.G. Cell biology and molecular basis of denitrification. Microbiol. Mol. Biology Rev. 1997, 61:533.