Simazine application inhibits nitrification and changes the ammonia-oxidizing bacterial communities in a fertilized agricultural soil

FEMS Microbiology Ecology

Volumn 78, Issue 3, 2011, Pages 511-519

  Hernández, Marcela ^a,b   Jia, Zhongjun ^a,c   Conrad, Ralf ^a   Seeger, Michael ^b  

^a MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^b DEPARTAMENTO DE FÍSICA   (Chile)

^c INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

Author keywords

Ammonia oxidizing Archaea; Ammonia oxidizing Bacteria; Herbicide; Nitrification; Nitrosospira; Simazine

Indexed keywords

AMMONIA; AMMONIA MONOOXYGENASE; ARCHAEAL DNA; BACTERIAL DNA; FERTILIZER; HERBICIDE; OXIDOREDUCTASE; SIMAZINE;

ACETYLENE; AGRICULTURAL SOIL; AMMONIA; BACTERIUM; ELECTROKINESIS; FERTILIZER APPLICATION; INHIBITION; INHIBITOR; MICROBIAL COMMUNITY; MICROBIAL ECOLOGY; MICROCOSM; NITRIFICATION; NITROGEN CYCLE; OXIDATION; PESTICIDE APPLICATION; POLYMERASE CHAIN REACTION; SIMAZINE;

AGRICULTURE; ARCHAEBACTERIUM; ARTICLE; BACTERIUM; DENATURING GRADIENT GEL ELECTROPHORESIS; DNA FINGERPRINTING; DNA SEQUENCE; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; METHODOLOGY; MICROBIOLOGY; NITRIFICATION; NITROGEN CYCLE; OXIDATION REDUCTION REACTION; PHYLOGENY; SOIL;

AGRICULTURE; AMMONIA; ARCHAEA; BACTERIA; DENATURING GRADIENT GEL ELECTROPHORESIS; DNA FINGERPRINTING; DNA, ARCHAEAL; DNA, BACTERIAL; FERTILIZERS; HERBICIDES; NITRIFICATION; NITROGEN CYCLE; OXIDATION-REDUCTION; OXIDOREDUCTASES; PHYLOGENY; SEQUENCE ANALYSIS, DNA; SIMAZINE; SOIL; SOIL MICROBIOLOGY;

BACTERIA (MICROORGANISMS); NITROSOMONADALES; NITROSOSPIRA;

EID: 81155148822     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/j.1574-6941.2011.01180.x     Document Type: Article

References (46)

1. Alvey S & Crowley DE (1995) Influence of organic amendments on biodegradation of atrazine as a nitrogen source. J Environ Qual 24: 1156-1162.
2. 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.
3. +-N. Biol Fertil Soils 40: 427-431.
4. Barra Caracciolo AB, Grenni P, Ciccoli R, Di Landa G & Cremisini C (2005) Simazine biodegradation in soil: analysis of bacterial community structure by in situ hybridization. Pest Manag Sci 61: 863-869.
5. Berg P, Klemedtsson L & Rosswall T (1982) Inhibitory effect of low partial pressures of acetylene on nitrification. Soil Biol Biochem 14: 301-303.
6. Chen X-P, Zhu YG, Xia Y, Shen JP & He JZ (2008) Ammonia-oxidizing archaea: important players in paddy rhizosphere soil? Environ Microbiol 10: 1978-1987.
7. De Boer W & Kowalchuk GA (2001) Nitrification in acid soils: micro-organisms and mechanisms. Soil Biol Biochem 33: 853-866.
8. de la Torre JR, Walker CB, Ingalls AE, Könneke M & Stahl DA (2008) Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. Environ Microbiol 10: 810-818.
9. Devers M, Azhari NE, Kolic NU & Martin-Laurent F (2007) Detection and organization of atrazine-degrading genetic potential of seventeen bacterial isolates belonging to divergent taxa indicate a recent common origin of their catabolic functions. FEMS Microbiol Lett 273: 78-86.
10. Di HJ, Cameron KC, Shen JP, Winefield CS, O'Callaghan M, Bowatte S & He JZ (2009) Nitrification driven by Bacteria and not Archaea in nitrogen-rich grassland soils. Nat Geosci 2: 621-624.
11. Dinamarca MA, Cereceda-Balic F, Fadic X & Seeger M (2007) Analysis of s-triazine degrading microbial communities in soils using most-probable-number enumeration and tetrazolium-salt detection. Int Microbiol 10: 209-215.
12. Gaur AC & Misra KC (1977) Studies on the effects of herbicides on soil nitrification. Plant Soil 46: 5-15.
13. Govantes F, García-González V, Porrúa O, Platero AI, Jiménez-Fernandez A & Santero E (2010) Regulation of the atrazine-degradative genes in Pseudomonas sp. strain ADP. FEMS Microbiol Lett 310: 1-8.
14. Gruber N & Galloway JN (2008) An Earth-system perspective of the global nitrogen cycle. Nature 451: 293-296.
15. Hart SC, Stark JM, Davidson EA & Firestone MK (1994) Nitrogen mineralization, immobilization, and nitrification. Methods of Soil Analysis, Part 2, Microbiological and Biochemical Properties. Book series no. 5 (Weaver RW, Angle S, Bottomley P, Bezdiecek D, Smith S, Tabatabai A & Wollum A, eds), pp. 985-1018. Soil Science Society of America, Madison, WI.
16. Hatzenpichler R, Lebedeva EV, Spieck E, Stoecker K, Richter A, Daims H & Wagner M (2008) A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proc Natl Acad Sci USA 105: 2134-2139.
17. Hernández M, Morgante V, Ávila M, Villalobos P, Miralles P, González M & Seeger M (2008a) Novel s-triazine-degrading bacteria isolated from agricultural soils of central Chile for herbicide bioremediation. Electron J Biotechnol 11: 1-7. doi: 10.2225/vol11-issue5-fulltext-4.
18. Hernández M, Villalobos P, Morgante V, González M, Reiff C, Moore E & Seeger M (2008b) Isolation and characterization of a novel simazine-degrading bacterium from agricultural soil of central Chile, Pseudomonas sp. MHP41. FEMS Microbiol Lett 286: 184-190.
19. 2-labeling studies of the de novo synthesis of polypeptides by Nitrosomonas europaea during recovery from acetylene and light inactivation of ammonia monooxygenase. J Biol Chem 267: 1534-1545.
20. Jia Z & Conrad R (2009) Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil. Environ Microbiol 7: 1658-1671.
21. Könneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB & Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437: 543-546.
22. Kowalchuk GA & Stephen JR (2001) Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annu Rev Microbiol 55: 485-529.
23. Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC & Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442: 806-809.
24. Li X, Zhang H, Wu M, Su Z & Zhang C (2008) Impact of acetochlor on ammonia-oxidizing bacteria in microcosm soils. J Environ Sci 20: 1126-1131.
25. Ludwig W, Strunk O, Westram R, et al. (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363-1371.
26. Martínez B, Tomkins J, Wackett LP, Wing R & Sadowsky MJ (2001) Complete nucleotide sequence and organization of the atrazine catabolic plasmid pADP-1 from Pseudomonas sp. strain ADP. J Bacteriol 183: 5684-5697.
27. Martens-Habbena W, Berube PM, Urakawa H, de la Torre JR & Stahl DA (2009) Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature 461: 976-979.
28. McCarty GW & Bremner JM (1989) Inhibition of nitrification in soil by heterocyclic nitrogen compounds. Biol Fertil Soils 8: 204-211.
29. McCarty GW (1999) Modes of action of nitrification inhibitors. Biol Fertil Soils 29: 1-9.
30. Morgante V, López-López A, Flores C, González M, González B, Vásquez M, Rosselló-Mora R & Seeger M (2010) Bioaugmentation with Pseudomonas sp. strain MHP41 promotes simazine attenuation and bacterial community changes in agricultural soils. FEMS Microbiol Ecol 71: 114-126. Erratum in FEMS Microbiol Ecol (2010) 72: 152.
31. Morgante V, Flores C, Fadic X, González M, Hernández M, Cereceda-Balic F & Seeger M (2011) Influence of microorganisms and leaching on simazine attenuation in agricultural soils. J Environ Management, in press. doi: 10.1016/j.jenvman.2011.06.045.
32. Nicol GW, Leininger S, Schleper C & Prosser JI (2008) The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing Archaea and Bacteria. Environ Microbiol 10: 2966-2978.
33. Norton JM, Klotz MG & Stein LY et at. (2008) Complete genome sequence of Nitrosospira multiformis, an ammonia-oxidizing bacterium from the soil environment. Appl Environ Microbiol 74: 3559-3572.
34. Offre P, Prosser JI & Nicol GW (2009) Growth of ammonia-oxidizing Archaea in soil microcosms is inhibited by acetylene. FEMS Microbiol Ecol 70: 99-108.
35. Park BJ, Park SJ, Yoon DN, Schouten S, Sinninghe Damste JS & Rhee SK (2010) Cultivation of autotrophic ammonia-oxidizing archaea from marine sediments in coculture with sulfur-oxidizing bacteria. Appl Environ Microbiol 76: 7575-7587.
36. 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. Appl Environ Microbiol 63: 4704-4712.
37. Schauss K, Focks A, Leininger S, et al. (2009) Dynamics and functional relevance of ammonia-oxidizing Archaea in two agricultural soils. Environ Microbiol 11: 446-456.
38. Seeger M, Hernández M, Méndez V, Ponce B, Córdova M & González M (2010a) Bacterial degradation and bioremediation of chlorinated herbicides and biphenyls. J Soil Sci Plant Nutr 10: 320-332.
39. Seeger M, Morgante V & Hernández M (2010b) Bacterial degradation of herbicides in soils. Bacterial Populations: Basic and Applied Aspects of Their Structure and Evolution, Vol. 1 (Lodeiro A, ed.), pp. 97-115. Transworld Research Network, Kerala, India.
40. Stewart FJ, Ulloa O & DeLong EF (2011) Microbial metatranscriptomics in a permanent marine oxygen minimum zone. Environ Microbiol doi: 10.1111/j.1462-2920.2010.02400.
41. Tourna M, Freitag TE, Nicol GW & Prosser JI (2008) Growth, activity and temperature responses of ammonia-oxidizing Archaea and Bacteria in soil microcosms. Environ Microbiol 10: 1357-1364.
42. Tourna M, Stieglmeier M, Spang A, et al. (2011) Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proc Natl Acad Sci USA 108: 8420-8425.
43. Treusch AH, Leininger S, Kletzin A, Schuster SC, Klenk HP & Schleper C (2005) Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling. Environ Microbiol 7: 1985-1995.
44. Verhamme DT, Prosser JI & Nicol GW (2011) Ammonia concentration determines differential growth of ammonia-oxidising Archaea and Bacteria in soil microcosms. ISME J 5: 1067-1071.
45. Wackett LP, Sadowsky MJ, Martínez B & Shapir N (2002) Biodegradation of atrazine and related s-triazine compounds: from enzymes to field studies. Appl Microbiol Biotechnol 58: 39-45.
46. Wessén E, Söderström M, Stenberg M, Bru D, Hellman M, Welsh A, Thomsen F, Klemedtson L, Philippot L & Hallin S (2011) Spatial distribution of ammonia-oxidizing bacteria and archaea across a 44-hectare farm related to ecosystem functioning. ISME J 5: 1213-1225.