Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 48, 2012, Pages 19709-19714

  Sanford, Robert A ^a   Wagner, Darlene D ^b   Wu, Qingzhong ^a,c   Chee Sanford, Joanne C ^d   Thomas, Sara H ^c   Cruz García, Claribel ^c   Rodríguez, Gina ^c,e   Massol Deyá, Arturo ^e   Krishnani, Kishore K ^f   Ritalahti, Kirsti M ^g,h   Nissen, Silke ^g,h   Konstantinidis, Konstantinos T ^b,c   Löffler, Frank E ^g,h,i  

^a ILLINOIS STATE GEOLOGICAL SURVEY   (United States)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^c Georgia Institute of Technology   (United States)

^d US Department of Agriculture Agricultural Research Service   (United States)

^e UNIVERSITY OF PUERTO RICO   (Puerto Rico)

^f ICAR NATIONAL INSTITUTE OF ABIOTIC STRESS MANAGEMENT   (India)

^g UNIVERSITY OF TENNESSEE   (United States)

^h OAK RIDGE NATIONAL LABORATORY   (United States)

ⁱ University of Tennessee   (United States)

Author keywords

Climate change; Nitrogen cycle

Indexed keywords

AMMONIA; NITROUS OXIDE REDUCTASE;

ANAEROMYXOBACTER DEHALOGENAN; ARTICLE; CONTROLLED STUDY; DENITRIFICATION; GENETIC VARIABILITY; GENOME; GREENHOUSE GAS; MICROBIAL ACTIVITY; NITROUS OXIDE EMISSION; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; POPULATION ABUNDANCE; PRIORITY JOURNAL; SOIL MICROFLORA;

BACTERIA; BASE SEQUENCE; DNA PRIMERS; GENETIC VARIATION; MOLECULAR SEQUENCE DATA; NITRIFICATION; OXIDOREDUCTASES; PHYLOGENY; POLYMERASE CHAIN REACTION; SOIL MICROBIOLOGY;

ANAEROMYXOBACTER DEHALOGENANS; BACTERIA (MICROORGANISMS);

EID: 84870354056     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1211238109     Document Type: Article

References (58)

1. Galloway JN, et al. (2004) Nitrogen cycles: Past, present, and future. Biogeochemistry 70(2):153-226.
2. Finlayson-Pitts BJ, Pitts JN (2000) Chemistry of the Upper and Lower Atmosphere (Academic, San Diego).
3. Lashof DA, Ahuja DR (1990) Relative contributions of greenhouse gas emissions to global warming. Nature 344(5):529-531.
4. Forster PV, et al., eds (2007) Changes in Atmospheric Constituents and in Radiative Forcing (Cambridge Univ Press, Cambridge, UK).
5. Cicerone RJ (1987) Changes in stratospheric ozone. Science 237(4810):35-42.
6. Crutzen PJ (1970) Influence of nitrogen oxides on atmospheric ozone content. Q J R Meteorol Soc 96(408):320-325.
7. 2O): The dominant ozone-depleting substance emitted in the 21st century. Science 326(5949):123-125.
8. Wang B, Dukarevich M, Sun EI, Yen MR, Jr., Saier MH, Jr. (2009) Membrane porters of ATP-binding cassette transport systems are polyphyletic. J Membr Biol 231(1):1-10.
9. Machida T, Nakazawa T, Fujii Y, Aoki A, Watanabe O (1995) Increase in the atmospheric nitrous oxide concentration during the last 250 years. Geophys Res Lett 22(21):2921-2924.
10. Bouwman AF, Van der Hoek KM, Olivier JGJ (1995) Uncertainties in the global source distribution of nitrous oxide. J Geophys Res 100(D2):2785-2800.
11. Bremner JM, Blackmer AM (1979) Effects of acetylene and soil water content on emission of nitrous oxide from soil. Nature 280(5271):380-381.
12. 2O emissions from a nitrogen-enriched river. Environ Sci Technol 33(1):21-25.
13. 2O budget. Nature 335(6185):57-59.
14. 2O and NO from fertilized fields: Summary of available measurement data. Global Biogeochem Cycles 16(4):1058-1071.
15. Mahne I, Tiedje JM (1995) Criteria and methodology for identifying respiratory denitrifiers. Appl Environ Microbiol 61(3):1110-1115.
16. Megonigal JP, Hines ME, Visscher PT (2004) Anaerobic metabolism: Linkages to trace gases and aerobic processes. Biogeochemistry, ed Schlesinger WH (Elsevier-Pergamon, Oxford, UK), pp 317-474.
17. Poth M (1986) Dinitrogen production from nitrite by a Nitrosomonas isolate. Appl Environ Microbiol 52(4):957-959.
18. Stremińska MA, Felgate H, Rowley G, Richardson DJ, Baggs EM (2012) Nitrous oxide production in soil isolates of nitrate-ammonifying bacteria. Environ Microbiol Rep 4(1):66-71.
19. Takaya N (2002) Dissimilatory nitrate reduction metabolisms and their control in fungi. J Biosci Bioeng 94(6):506-510.
20. Wrage N, Velthof GL, van Beusichem ML, Oenema O (2001) Role of nitrifier denitrification in the production of nitrous oxide. Soil Biol Biochem 33(12):1723-1732.
21. Zumft WG (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61(4):533-616.
22. 2+. Appl Environ Microbiol 71(9):5267-5274.
23. Cooper DC, Picardal FW, Schimmelmann A, Coby AJ (2003) Chemical and biological interactions during nitrate and goethite reduction by Shewanella putrefaciens 200. Appl Environ Microbiol 69(6):3517-3525.
24. Rakshit S, Matocha CJ, Coyne MS (2008) Nitrite reduction by siderite. Soil Sci Soc Am J 72(4):1070-1077.
25. Henderson SL, et al. (2010) Changes in denitrifier abundance, denitrification gene mRNA levels, nitrous oxide emissions, and denitrification in anoxic soil microcosms amended with glucose and plant residues. Appl Environ Microbiol 76(7):2155-2164.
26. Smith P, et al. (2007) Policy and technological constraints to implementation of greenhouse gas mitigation options in agriculture. Agric Ecosyst Environ 118(1-4):6-28.
27. Morales SE, Cosart T, Holben WE (2010) Bacterial gene abundances as indicators of greenhouse gas emission in soils. ISME J 4(6):799-808.
28. Wallenstein MD, Myrold DD, Firestone M, Voytek M (2006) Environmental controls on denitrifying communities and denitrification rates: Insights from molecular methods. Ecol Appl 16(6):2143-2152.
29. Zumft WG, Körner H (2007) Nitrous oxide reductases. Biology of the nitrogen cycle, eds Bothe H, Ferguson SJ, Newton WE (Elsevier, Amsterdam), pp 67-81.
30. 2O) to dinitrogen by Bacteria and Archaea. Adv Microb Physiol 52(4):107-227.
31. Tiedje JM, ed (1988) Ecology of Denitrification and Dissimiatory Nitrate Reduction to Ammonium (Wiley, New York).
32. Payne WJ, Grant MA, Shapleigh J, Hoffman P (1982) Nitrogen oxide reduction in Wolinella succinogenes and Campylobacter species. J Bacteriol 152(2):915-918.
33. Simon J, Einsle O, Kroneck PMH, Zumft WG (2004) The unprecedented nos gene cluster of Wolinella succinogenes encodes a novel respiratory electron transfer pathway to cytochrome c nitrous oxide reductase. FEBS Lett 569(1-3):7-12.
34. Petrie L, North NN, Dollhopf SL, Balkwill DL, Kostka JE (2003) Enumeration and characterization of iron(III)-reducing microbial communities from acidic subsurface sediments contaminated with uranium(VI). Appl Environ Microbiol 69(12):7467-7479.
35. Sanford RA, Cole JR, Tiedje JM (2002) Characterization and description of Anaeromyxobacter dehalogenans gen. nov., sp. nov., an aryl-halorespiring facultative anaerobic myxobacterium. Appl Environ Microbiol 68(2):893-900.
36. Thomas SH, Padilla-Crespo E, Jardine PM, Sanford RA, Löffler FE (2009) Diversity and distribution of Anaeromyxobacter strains in a uranium-contaminated subsurface environment with a nonuniform groundwater flow. Appl Environ Microbiol 75(11):3679-3687.
37. Philippot L (2002) Denitrifying genes in bacterial and Archaeal genomes. Biochim Biophys Acta 1577(3):355-376.
38. Velasco L, Mesa S, Xu CA, Delgado MJ, Bedmar EJ (2004) Molecular characterization of nosRZDFYLX genes coding for denitrifying nitrous oxide reductase of Bradyrhizobium japonicum. Antonie van Leeuwenhoek 85(3):229-235.
39. Kern M, Simon J (2009) Electron transport chains and bioenergetics of respiratory nitrogen metabolism in Wolinella succinogenes and other Epsilonproteobacteria. Biochim Biophys Acta 1787(6):646-656.
40. Liu X, et al. (2008) The nos gene cluster from gram-positive bacterium Geobacillus thermodenitrificans NG80-2 and functional characterization of the recombinant NosZ. FEMS Microbiol Lett 289(1):46-52.
41. Richardson D, Felgate H, Watmough N, Thomson A, Baggs E (2009) Mitigating release of the potent greenhouse gas N2O from the nitrogen cycle - could enzymic regulation hold the key? Trends Biotechnol 27(7):388-397.
42. 2 by soil microorganisms. Soil Biol Biochem 10(3):187-191.
43. Berks BC, Palmer T, Sargent F (2005) Protein targeting by the bacterial twin-arginine translocation (Tat) pathway. Curr Opin Microbiol 8(2):174-181.
44. den Blaauwen T, Driessen AJM (1996) Sec-dependent preprotein translocation in bacteria. Arch Microbiol 165(1):1-8.
45. A, Cu-S enzyme nitrous oxide reductase. J Mol Microbiol Biotechnol 10(2-4):154-166.
46. Cuypers H, Viebrock-Sambale A, Zumft WG (1992) NosR, a membrane-bound regulatory component necessary for expression of nitrous oxide reductase in denitrifying Pseudomonas stutzeri. J Bacteriol 174(16):5332-5339.
47. Honisch U, Zumft WG (2003) Operon structure and regulation of the nos gene region of Pseudomonas stutzeri, encoding an ABC-type ATPase for maturation of nitrous oxide reductase. J Bacteriol 185(6):1895-1902.
48. Geets J, et al. (2007) Real-time PCR assay for the simultaneous quantification of nitrifying and denitrifying bacteria in activated sludge. Appl Microbiol Biotechnol 75(1):211-221.
49. 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. Appl Environ Microbiol 72(8):5181-5189.
50. 2 O-producing Bacillus isolates harboring the nosZ gene. FEMS Microbiol Ecol 76(3):541-552.
51. Kloos K, Mergel A, Rosch C, Bothe H (2001) Denitrification within the genus Azospirillum and other associative bacteria. Aust J Plant Physiol 28(9):991-998.
52. Scala DJ, Kerkhof LJ (1998) Nitrous oxide reductase (nosZ) gene-specific PCR primers for detection of denitrifiers and three nosZ genes from marine sediments. FEMS Microbiol Lett 162(1):61-68.
53. Throbäck IN, Enwall K, Jarvis Å, Hallin S (2004) Reassessing PCR primers targeting nirS, nirK and nosZ genes for community surveys of denitrifying bacteria with DGGE. FEMS Microbiol Ecol 49(3):401-417.
54. 2O emissions from land use. Plant Soil 309(1-2):147-167.
55. Canfield DE, Glazer AN, Falkowski PG (2010) The evolution and future of Earth's nitrogen cycle. Science 330(6001):192-196.
56. 2O, and NO). Microbiol Rev 60(4):609-640.
57. 2 emissions and denitrifier community size and activity. Appl Environ Microbiol 76(6):1870-1878.
58. 2O flux to incremental fertilizer addition in a continuous maize (Zea mays L.) cropping system. Glob Change Biol 11(2):1712-1719.