Influence of temperature on the composition and activity of denitrifying soil communities

FEMS Microbiology Ecology

Volumn 73, Issue 1, 2010, Pages 134-148

  Braker, Gesche ^a   Schwarz, Julia ^a   Conrad, Ralf ^a  

^a MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

Author keywords

Abundance; Activity; Community composition; Denitrifiers; Temperature

Indexed keywords

BACTERIAL DNA; NITRATE; NITRITE REDUCTASE;

ABUNDANCE; AGRICULTURAL SOIL; COMMUNITY COMPOSITION; DENITRIFICATION; DIVERSITY INDEX; ENZYME ACTIVITY; LABORATORY METHOD; MICROBIAL ACTIVITY; PHYLOGENETICS; POLYMORPHISM; SOIL ECOSYSTEM; SOIL MICROORGANISM; SUBSTRATE; TEMPERATURE EFFECT;

ARTICLE; BACTERIAL GENE; BACTERIUM; DNA SEQUENCE; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; MOLECULAR CLONING; PHYLOGENY; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; SOIL; TEMPERATURE;

BACTERIA; CLONING, MOLECULAR; DNA, BACTERIAL; GENES, BACTERIAL; NITRATES; NITRITE REDUCTASES; PHYLOGENY; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; SEQUENCE ANALYSIS, DNA; SOIL; SOIL MICROBIOLOGY; TEMPERATURE;

EID: 77953176281     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/j.1574-6941.2010.00884.x     Document Type: Article

References (70)

1. Amann RI, Ludwig W Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59 : 143 169.
2. 2O emission rates in a California meadow soil are influenced by fertilizer level, soil moisture and the community structure of ammonia-oxidizing bacteria. Global Change Biol 15 : 643 655.
3. Avrahami S Conrad R (2003) Patterns of community change among ammonia oxidizers in meadow soils upon long-term incubation at different temperatures. Appl Environ Microb 69 : 6152 6164.
4. Avrahami S, Liesack W Conrad R (2003) Effects of temperature and fertilizer on activity and community structure of soil ammonia oxidizers. Environ Microbiol 5 : 691 705.
5. Azam F, Muller C, Weiske A, Benckiser G Ottow JCG (2002) Nitrification and denitrification as sources of atmospheric nitrous oxide - role of oxidizable carbon and applied nitrogen. Biol Fert Soils 35 : 54 61.
6. Bailey LD (1976) Effects of temperature and root on denitrification in a soil. Can J Soil Sci 56 : 79 87.
7. Barnard R, Leadley PW Hungate BA (2005) Global change, nitrification, and denitrification: a review. Global Biogeochem Cy 19 : doi
8. Boyle SA, Rich JJ, Bottomley PJ, Cromack K Myrold DD (2006) Reciprocal transfer effects on denitrifying community composition and activity at forest and meadow sites in the Cascade Mountains of Oregon. Soil Biol Biochem 38 : 870 878.
9. Braker G Tiedje JM (2003) Nitric oxide reductase (norB) genes from pure cultures and environmental samples. Appl Environ Microb 69 : 3476 3483.
10. Braker G, Fesefeldt A Witzel KP (1998) Development of PCR primer systems for amplification of nitrite reductase genes (nirK and nirS) to detect denitrifying bacteria in environmental samples. Appl Environ Microb 64 : 3769 3775.
11. Bremer C, Braker G, Matthies D, Reuter A, Engels C Conrad R (2007) Impact of plant functional group, plant species, and sampling time on the composition of nirK-type denitrifier communities in soil. Appl Environ Microb 73 : 6876 6884.
12. Bremer C, Braker G, Matthies D, Beierkuhnlein C Conrad R (2009) 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 70 : 377 387.
13. Briones AM Jr. Reichardt W (1999) Estimating microbial population counts by 'most probable number' using Microsoft Excel. J Microbiol Meth 35 : 157 161.
14. Calderon FJ, Jackson LE, Scow KM Rolston DE (2001) Short-term dynamics of nitrogen, microbial activity, and phospholipid fatty acids after tillage. Soil Sci Soc Am J 65 : 118 126.
15. Cavigelli MA Robertson GP (2000) The functional significance of denitrifier community composition in a terrestrial ecosystem. Ecology 81 : 1402 1414.
16. Cavigelli MA Robertson GP (2001) Role of denitrifier diversity in rates of nitrous oxide consumption in a terrestrial ecosystem. Soil Biol Biochem 33 : 297 310.
17. 2O in two soils. Biol Fert Soils 28 : 19 26.
18. Cheneby D, Philippot L, Hartmann A, Henault C Germon JC (2000) 16S rDNA analysis for characterization of denitrifying bacteria isolated from three agricultural soils. FEMS Microbiol Ecol 34 : 121 128.
19. Colbourn P (1993) Limits to denitrification in two pasture soils in a temperate maritime climate. Agr Ecosyst Environ 43 : 49 68.
20. Cookson WR, Osman M, Marschner P, Abaye DA, Clark I, Murphy DV, Stockdale EA Watson CA (2007) Controls on soil nitrogen cycling and microbial community composition across land use and incubation temperature. Soil Biol Biochem 39 : 744 756.
21. Dandie CE, Burton DL, Zebarth BJ, Henderson SL, Trevors JT Goyer C (2008) Changes in bacterial denitrifier community abundance over time in an agricultural field and their relationship with denitrification activity. Appl Environ Microb 74 : 5997 6005.
22. De Klein CAM Van Logtestijn RSP (1996) Denitrification in grassland soils in the Netherlands in relation to irrigation, N-application rate, soil water content and soil temperature. Soil Biol Biochem 28 : 231 237.
23. Dendooven L, Splatt P Anderson JM (1996) Denitrification in permanent pasture soil as affected by different forms of C substrate. Soil Biol Biochem 28 : 141 149. (Pubitemid 2619837)
24. Dunbar J, Ticknor LO Kuske CR (2001) Phylogenetic specificity and reproducibility and new method for analysis of terminal restriction fragment profiles of 16S rRNA genes from bacterial communities. Appl Environ Microb 67 : 190 197.
25. 2O emissions from land use. Plant Soil 309 : 147 167.
26. Flanagan DA, Gregory LG, Carter JP, Karakas-Sen A, Richardson DJ Spiro S (1999) Detection of genes for periplasmic nitrate reductase in nitrate respiring bacteria and in community DNA. FEMS Microbiol Lett 177 : 263 270.
27. Gamble TN, Betlach MR Tiedje JM (1977) Numerically dominant denitrifying bacteria from world soils. Appl Environ Microb 33 : 926 939.
28. Gödde M Conrad R (1998) Simultaneous measurement of nitric oxide production and consumption in soil using a simple static incubation system, and the effect of soil water content on the contribution of nitrification. Soil Biol Biochem 30 : 433 442.
29. Gödde M Conrad R (1999) Immediate and adaptational temperature effects on nitric oxide production and nitrous oxide release from nitrification and denitrification in two soils. Biol Fert Soils 30 : 33 40.
30. Gregory LG, Karakas-Sen A, Richardson DJ Spiro S (2000) Detection of genes for membrane-bound nitrate reductase in nitrate-respiring bacteria and in community DNA. FEMS Microbiol Lett 183 : 275 279.
31. Groffman PM, Altabet MA, Bohlke JK, Butterbach-Bahl K, David MB, Firestone MK, Giblin AE, Kana TM, Nielsen LP Voytek MA (2006) Methods for measuring denitrification: diverse approaches to a difficult problem. Ecol Appl 16 : 2091 2122.
32. 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 J 3 : 597 605.
33. Henckel T, Friedrich M Conrad R (1999) Molecular analyses of the methane-oxidizing microbial community in rice field soil by targeting the genes of the 16S rRNA, particulate methane monooxygenase, and methanol dehydrogenase. Appl Environ Microb 65 : 1980 1990.
34. Heylen K, Gevers D, Vanparys B, Wittebolle L, Geets J, Boon N De Vos P (2006) The incidence of nirS and nirK and their genetic heterogeneity in cultivated denitrifiers. Environ Microbiol 8 : 2012 2021.
35. Heylen K, Vanparys B, Gevers D, Wittebolle L, Boon N De Vos P (2007) Nitric oxide reductase (norB) gene sequence analysis reveals discrepancies with nitrite reductase (nir) gene phylogeny in cultivated denitrifiers. Environ Microbiol 9 : 1072 1077.
36. Høj L, Olsen RA Torsvik VL (2008) Effects of temperature on the diversity and community structure of known methanogenic groups and other archaea in high Arctic peat. ISME J 2 : 37 48.
37. Horz HP, Rich V, Avrahami S Bohannan BJM (2005) Methane-oxidizing bacteria in a California upland grassland soil: diversity and response to simulated global change. Appl Environ Microb 71 : 2642 2652.
38. Hume NP, Fleming MS Horne AJ (2002) Plant carbohydrate limitation on nitrate reduction in wetland microcosms. Water Res 36 : 577 584.
39. Jacobson SN Alexander M (1980) Nitrate loss from soil in relation to temperature, carbon source and denitrifier populations. Soil Biol Biochem 12 : 501 505.
40. Kandeler E, Brune T, Enowashu E, Dorr N, Guggenberger G, Lamersdorf N Philippot L (2009) Response of total and nitrate-dissimilating bacteria to reduced N deposition in a spruce forest soil profile. FEMS Microbiol Ecol 67 : 444 454.
41. 2 production by Alcaligenes faecalis p. J Appl Microbiol 101 : 655 667.
42. King D Nedwell DB (1984) Changes in the nitrate-reducing community of an anaerobic saltmarsh sediment in response to seasonal selection by temperature. J Gen Microbiol 130 : 2935 2941.
43. Kloos K, Mergel A, Rosch C Bothe H (2001) Denitrification within the genus Azospirillum and other associative bacteria. Aust J Plant Physiol 28 : 991 998.
44. Maag M Vinther FP (1996) Nitrous oxide emission by nitrification and denitrification in different soil types and at different soil moisture contents and temperatures. Appl Soil Ecol 4 : 5 14.
45. Mahne I Tiedje JM (1995) Criteria and methodology for identifying respiratory denitrifiers. Appl Environ Microb 61 : 1110 1115.
46. Malhi SS, McGill WB Nyborg M (1990) Nitrate losses in soils - effect of temperature, moisture and substrate concentration. Soil Biol Biochem 22 : 733 737.
47. Mancino CF, Torello WA Wehner DJ (1988) Denitrification losses from Kentucky bluegrass sod. Agron J 80 : 148 153.
48. 2O emissions and denitrifier community abundance in soil. Soil Biol Biochem 40 : 2553 2562.
49. 2O-Emissionen und Denitrifikationsabgaben von Böden einer Jungmoränenlandschaft in Schleswig-Holstein. PhD Thesis, Christian-Albrechts-Universität, Kiel, Germany.
50. Mohanty SR, Bodelier PLE Conrad R (2007) Effect of temperature on composition of the methanotrophic community in rice field and forest soil. FEMS Microbiol Ecol 62 : 24 31.
51. Nömmik H (1956) Investigations on denitrification in soil. Acta Agr Scand 6 : 195 228.
52. Paul EA Clark FE (eds) (1989) Soil Microbiology and Biochemistry. Academic Press
53. Petri R Imhoff JF (2000) The relationship of nitrate reducing bacteria on the basis of narH gene sequences and comparison of narH and 16S rDNA based phylogeny. Syst Appl Microbiol 23 : 47 57.
54. Pettersson M Baath E (2003) Temperature-dependent changes in the soil bacterial community in limed and unlimed soil. FEMS Microbiol Ecol 45 : 13 21.
55. 2O). Biogeosciences 3 : 651 661.
56. Rich JJ Myrold DD (2004) Community composition and activities of denitrifying bacteria from adjacent agricultural soil, riparian soil, and creek sediment in Oregon, USA. Soil Biol Biochem 36 : 1431 1441.
57. Rich JJ, Heichen RS, Bottomley PJ, Cromack K Myrold DD (2003) Community composition and functioning of denitrifying bacteria from adjacent meadow and forest soils. Appl Environ Microb 69 : 5974 5982.
58. Ricke P, Kolb S Braker G (2005) Application of a newly developed ARB software-integrated tool for in silico terminal restriction fragment length polymorphism analysis reveals the dominance of a novel pmoA cluster in a forest soil. Appl Environ Microb 71 : 1671 1673.
59. Rustad LE, Campbell JL, Marion GM, Norby RJ, Mitchell MJ, Hartley AE, Cornelissen JHC Gurevitch J (2001) A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126 : 543 562.
60. Saad OALO Conrad R (1993a) Adaptation to temperature of nitric oxide-producing nitrate-reducing bacterial populations in soil. Syst Appl Microbiol 16 : 120 125.
61. Saad OALO Conrad R (1993b) Temperature-dependence of nitrification, denitrification, and turnover of nitric oxide in different soils. Biol Fert Soils 15 : 21 27.
62. Schimel J (1995) Ecosystem consequences of microbial diversity and community structure. Ecological Studies, Vol. 113 (Chapin F Körner F, eds), pp. 239 254. Springer Verlag
63. Schimel JP Gulledge J (1998) Microbial community structure and global trace gases. Global Change Biol 4 : 745 758.
64. Walker JKM, Egger KN Henry GHR (2008) Long-term experimental warming alters nitrogen-cycling communities but site factors remain the primary drivers of community structure in high arctic tundra soils. ISME J 2 : 982 995.
65. Wallenstein MD, Myrold DD, Firestone M Voytek M (2006) Environmental controls on denitrifying communities and denitrification rates: insights from molecular methods. Ecol Appl 16 : 2143 2152.
66. Wertz S, Dandie CE, Goyer C, Trevors JT Patten CL (2009) Diversity of nirK denitrifying genes and transcripts in an agricultural soil. Appl Environ Microb 75 : 7365 7377.
67. Wolsing M Priemé A (2004) Observation of high seasonal variation in community structure of denitrifying bacteria in arable soil receiving artificial fertilizer and cattle manure by determining T-RFLP of nir gene fragments. FEMS Microbiol Ecol 48 : 261 271.
68. Yoshinari T Knowles R (1976) Acetylene inhibition of nitrous-oxide reduction by denitrifying bacteria. Biochem Bioph Res Co 69 : 705 710.
69. Zogg GP, Zak DR, Ringelberg DB, MacDonald NW, Pregitzer KS White DC (1997) Compositional and functional shifts in microbial communities due to soil warming. Soil Sci Soc Am J 61 : 475 481.
70. Zumft WG (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol R 61 : 533 616.