Responses of the terrestrial ammonia-oxidizing archaeon Ca. Nitrososphaera viennensis and the ammonia-oxidizing bacterium Nitrosospira multiformis to nitrification inhibitors

FEMS Microbiology Letters

Volumn 344, Issue 2, 2013, Pages 121-129

  Shen, Tianlin ^a,b,c   Stieglmeier, Michaela ^b   Dai, Jiulan ^a   Urich, Tim ^b   Schleper, Christa ^b  

^a SHANDONG UNIVERSITY   (China)

^b UNIVERSITY OF VIENNA   (Austria)

^c National Engineering Laboratory for Efficient Utilization of Soil and Fertilizer Resources   (China)

Author keywords

Ammonia oxidation; Archaea; Nitrite; PTIO; Soil

Indexed keywords

2 (4 CARBOXYPHENYL) 4,4,5,5 TETRAMETHYLIMIDAZOLINE 1 OXYL 3 OXIDE; AGRICULTURAL CHEMICAL; ALLYLTHIOUREA; AMMONIA; DICYANODIAMIDE; GUTIMINE; NITRAPYRIN; NITRIFICATION INHIBITOR; SULFATHIAZOLE; THIOUREA DERIVATIVE; UNCLASSIFIED DRUG;

AMMONIA OXIDATION; AMMONIA OXIDIZING ARCHAEON; ARTICLE; BACTERIAL METABOLISM; BACTERIUM CULTURE; CONCENTRATION (PARAMETERS); CONCENTRATION RESPONSE; CONTROLLED STUDY; INHIBITION KINETICS; MEDIAN EFFECTIVE CONCENTRATION; NITRIFICATION; NITROSOSPHAERA VIENNENSIS; NITROSOSPIRA; NITROSOSPIRA MULTIFORMIS; NONHUMAN; OXIDATION; PRIORITY JOURNAL; SOIL MICROFLORA; SPECIES COMPARISON;

AMMONIA; ARCHAEA; BENZOATES; FERTILIZERS; GUANIDINES; IMIDAZOLES; NITRIFICATION; NITROSOMONADACEAE; OXIDATION-REDUCTION; PICOLINES; SULFATHIAZOLES; THIOUREA;

ARCHAEA; BACTERIA (MICROORGANISMS); NITROSOSPIRA MULTIFORMIS;

EID: 84879503831     PISSN: 03781097     EISSN: 15746968     Source Type: Journal    
DOI: 10.1111/1574-6968.12164     Document Type: Article

References (72)

1. Abbasi MK & Adams WA (1998) Loss of nitrogen in compacted grassland soil by simultaneous nitrification and denitrification. Plant Soil 200: 265-277.
2. Akaike T & Maeda H (1996) Quantitation of nitric oxide using 2-phenyl-4, 4, 5, 5-tetramethylimidazoline-1-oxyl 3-oxide (PTIO). Methods Enzymol 268: 211-221.
3. Amano F & Noda T (1995) Improved detection of nitric oxide radical (NO.) production in an activated macrophage culture with a radical scavenger, carboxy PTIO and Griess reagent. FEBS Lett 368: 425-428.
4. Amberger A (1989) Research on dicyandiamide as a nitrification inhibitor and future outlook. Commun Soil Sci Plant Anal 20: 1933-1955.
5. Andersen JS, Holst H, Spliid H, Andersen H, Baun A & Nyholm N (1998) Continuous ecotoxicological data evaluated relative to a control response. J Agric Biol Environ Stat 3: 405-420.
6. 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.
7. Bartossek R, Spang A, Weidler G, Lanzen A & Schleper C (2012) Metagenomic analysis of ammonia-oxidizing archaea affiliated with the soil group. Front Microbiol 3: 208-222.
8. +, and CO oxidation by methanotrophs and nitrifiers. Microbiol Rev 53: 68-84.
9. Belser LW & Schmidt EL (1981) Inhibitory effect of nitrapyrin on three genera of ammonia-oxidizing nitrifiers. Appl Environ Microbiol 41: 819-821.
10. Brown GM (1962) The biosynthesis of folic acid II. Inhibition by sulfonamides. J Biol Chem 237: 536-540.
11. Bruns MA, Stephen JR, Kowalchuk GA, Prosser JI & Paul EA (1999) Comparative diversity of ammonia oxidizer 16S rRNA gene sequences in native, tilled, and successional soils. Appl Environ Microbiol 65: 2994-3000.
12. Burkhardt M, Stamm C, Waul C, Singer H & Muller S (2005) Surface runoff and transport of sulfonamide antibiotics and tracers on manured grassland. J Environ Qual 34: 1363-1371.
13. 2O mitigation tool in the IPCC inventory methodology for agricultural soils. Nutr Cycl Agroecosyst 78: 1-14.
14. Daebeler A, Abell GC, Bodelier PL, Bodrossy L, Frampton DM, Hefting MM & Laanbroek HJ (2012) Archaeal dominated ammonia-oxidizing communities in Icelandic grassland soils are moderately affected by long-term N fertilization and geothermal heating. Front Microbiol 3: 352-366.
15. Dai Y, Di HJ, Cameron KC & He JZ (2012) Effects of nitrogen application rate and a nitrification inhibitor dicyandiamide on ammonia oxidizers and N(2)O emissions in a grazed pasture soil. Sci Total Environ (Epub ahead of print).
16. Dang H, Zhang X, Sun J, Li T, Zhang Z & Yang G (2008) Diversity and spatial distribution of sediment ammonia-oxidizing Crenarchaeota in response to estuarine and environmental gradients in the Changjiang Estuary and East China Sea. Microbiology 154: 2084-2095.
17. de la Torre JR, Walker CB, Ingalls AE, Konneke M & Stahl DA (2008) Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. Environ Microbiol 10: 810-818.
18. Delong EF & Yayanos AA (1986) Biochemical function and ecological significance of novel bacterial lipids in deep-sea procaryotes. Appl Environ Microbiol 51: 730-737.
19. Di HJ & Cameron KC (2005) Reducing environmental impacts of agriculture by using a fine particle suspension nitrification inhibitor to decrease nitrate leaching from grazed pastures. Agric Ecosyst Environ 109: 202-212.
20. Ehhalt D, Prather M, Dentener F et al. (2001) Atmospheric chemistry and greenhouse gases. Climate Change 2001: The Scientific Basis. Contribution of Working Group I to the Third Assessment Report of the Intergovernmental Panel on Climate Change (Houghton JT, Ding Y & Griggs DJ et al., eds). Cambridge University Press, Cambridge.
21. Ellis A, Lu H, Li CG & Rand MJ (2001) Effects of agents that inactivate free radical NO (NO*) on nitroxyl anion-mediated relaxations, and on the detection of NO* released from the nitroxyl anion donor Angeli's salt. Br J Pharmacol 134: 521-528.
22. Francis CA, Roberts KJ, Beman JM, Santoro AE & Oakley BB (2005) Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. P Natl Acad Sci USA 102: 14683-14688.
23. Freney JR (1997) Strategies to reduce gaseous emissions of nitrogen from irrigated agriculture. Nutr Cycl Agroecosyst 48: 155-160.
24. Galloway JN, Townsend AR, Erisman JW et al. (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320: 889-892.
25. Giles J (2005) Fallout of fertilizers set too low, studies warn. Nature 434: 262.
26. Ginestet P, Audic JM, Urbain VV & Block JC (1998) Estimation of nitrifying bacterial activities by measuring oxygen uptake in the presence of the metabolic inhibitors allylthiourea and azide. Appl Environ Microbiol 64: 2266-2268.
27. Glass ADM (2003) Nitrogen use efficiency of crop plants: physiological constraints upon nitrogen absorption. Crit Rev Plant Sci 22: 453-470.
28. Gruber N & Galloway JN (2008) An Earth-system perspective of the global nitrogen cycle. Nature 451: 293-296.
29. Hallam SJ, Konstantinidis KT, Putnam N et al. (2006) Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum. P Natl Acad Sci USA 103: 18296-18301.
30. 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. P Natl Acad Sci USA 105: 2134-2139.
31. He JZ, Shen JP, Zhang LM, Zhu YG, Zheng YM, Xu MG & Di H (2007) 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 9: 2364-2374.
32. Hooper AB & Terry KR (1973) Specific inhibitors of ammonia oxidation in Nitrosomonas. J Bacteriol 115: 480-485.
33. Hyman MR, Kim CY & Arp DJ (1990) Inhibition of ammonia monooxygenase in Nitrosomonas europaea by carbon disulfide. J Bacteriol 172: 4775-4782.
34. Jia Z & Conrad R (2009) Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil. Environ Microbiol 11: 1658-1671.
35. Jung MY, Park SJ, Min D et al. (2011) Enrichment and characterization of an autotrophic ammonia-oxidizing archaeon of mesophilic crenarchaeal group I.1a from an agricultural soil. Appl Environ Microbiol 77: 8635-8647.
36. Kim BK, Jung MY, Yu DS, Park SJ, Oh TK, Rhee SK & Kim JF (2011) Genome sequence of an ammonia-oxidizing soil archaeon, "Candidatus Nitrosoarchaeum koreensis" MY1. J Bacteriol 193: 5539-5540.
37. Kim JG, Jung MY, Park SJ et al. (2012) Cultivation of a highly enriched ammonia-oxidizing archaeon of thaumarchaeotal group I.1b from an agricultural soil. Environ Microbiol 14: 1528-1543.
38. Lehtovirta-Morley LE, Stoecker K, Vilcinskas A, Prosser JI & Nicol GW (2011) Cultivation of an obligate acidophilic ammonia oxidizer from a nitrifying acid soil. P Natl Acad Sci USA 108: 15892-15897.
39. Leininger S, Urich T, Schloter M et al. (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442: 806-809.
40. McCarty GW (1999) Modes of action of nitrification inhibitors. Biol Fert Soils 29: 1-9.
41. Moir JL, Cameron KC & Di HJ (2007) Effects of the nitrification inhibitor dicyandiamide on soil mineral N, pasture yield, nutrient uptake and pasture quality in a grazed pasture system. Soil Use Manage 23: 111-120.
42. Mosier AC, Lund MB & Francis CA (2012a) Ecophysiology of an ammonia-oxidizing archaeon adapted to low-salinity habitats. Microb Ecol 64: 955-963.
43. Mosier AC, Allen EE, Kim M, Ferriera S & Francis CA (2012b) Genome sequence of "Candidatus Nitrosoarchaeum limnia" BG20, a low-salinity ammonia-oxidizing archaeon from the San Francisco Bay Estuary. J Bacteriol 194: 2119-2120.
44. Mosier AC, Allen EE, Kim M, Ferriera S & Francis CA (2012c) Genome sequence of "Candidatus Nitrosopumilus salaria" BD31, an ammonia-oxidizing archaeon from the San Francisco Bay Estuary. J Bacteriol 194: 2121-2122.
45. Nicol GW & Schleper C (2006) Ammonia-oxidising Crenarchaeota: important players in the nitrogen cycle? Trends Microbiol 14: 207-212.
46. 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.
47. Pitcher A, Rychlik N, Hopmans EC et al. (2010) Crenarchaeol dominates the membrane lipids of Candidatus Nitrososphaera gargensis, a thermophilic Group I. 1b Archaeon. ISME J 4: 542-552.
48. Powell SJ & Prosser JI (1986) Inhibition of ammonium oxidation by nitrapyrin in soil and liquid culture. Appl Environ Microbiol 52: 782-787.
49. 2 fixation by archaea and bacteria in an agricultural soil. P Natl Acad Sci USA 108: 4170-4175.
50. Purkhold U, Pommerening-Roser A, Juretschko S, Schmid MC, Koops HP & Wagner M (2000) Phylogeny of all recognized species of ammonia oxidizers based on comparative 16S rRNA and amoA sequence analysis: implications for molecular diversity surveys. Appl Environ Microbiol 66: 5368-5382.
51. Purkhold U, Wagner M, Timmermann G, Pommerening-Roser A & Koops HP (2003) 16S rRNA and amoA-based phylogeny of 12 novel betaproteobacterial ammonia-oxidizing isolates: extension of the dataset and proposal of a new lineage within the nitrosomonads. Int J Syst Evol Microbiol 53: 1485-1494.
52. 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.
53. Schleper C & Nicol GW (2010) Ammonia-oxidising archaea-physiology, ecology and evolution. Adv Microb Physiol 57: 1-41.
54. Schouten S, Hopmans EC, Baas M et al. (2008) Intact Membrane Lipids of "Candidatus Nitrosopumilus maritimus", a cultivated representative of the cosmopolitan mesophilic group I Crenarchaeota. Appl Environ Microbiol 74: 2433-2440.
55. Shen JP, Zhang LM, Zhu YG, Zhang JB & He JZ (2008) Abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea communities of an alkaline sandy loam. Environ Microbiol 10: 1601-1611.
56. Singh SN & Verma A (2007) The potential of nitrification inhibitors to manage the pollution effect of nitrogen fertilizers in agricultural and other soils: a review. Environ Pract 9: 266-279.
57. Sinninghe Damste JS, Rijpstra WI, Hopmans EC et al. (2012) Intact polar and core glycerol dibiphytanyl glycerol tetraether lipids of group I.1a and I.1b thaumarchaeota in soil. Appl Environ Microbiol 78: 6866-6874.
58. Spang A, Poehlein A, Offre P et al. (2012) The genome of the ammonia-oxidizing Candidatus Nitrososphaera gargensis: insights into metabolic versatility and environmental adaptations. Environ Microbiol 14: 3122-3145.
59. Stahl DA & de la Torre JR (2012) Physiology and diversity of ammonia-oxidizing archaea. Annu Rev Microbiol 66: 83-101.
60. Subbarao GV, Nakahara K, Hurtado MP et al. (2009) Evidence for biological nitrification inhibition in Brachiaria pastures. P Natl Acad Sci USA 106: 17302-17307.
61. Tourna M, Stieglmeier M, Spang A et al. (2011) Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. P Natl Acad Sci USA 108: 8420-8425.
62. Trenkel ME (1997) Improving Fertilizer Use Efficiency: Controlled-release and Stabilized Fertilizers in Agriculture. International Fertilizer Industry Association, Paris.
63. 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.
64. Vajrala N, Martens-Habbena W, Sayavedra-Soto LA, Schauer A, Bottomley PJ, Stahl DA & Arp DJ (2013) Hydroxylamine as an intermediate in ammonia oxidation by globally abundant marine archaea. P Natl Acad Sci USA 110: 1006-1011.
65. Walker CB, de la Torre JR, Klotz MG et al. (2010) Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. P Natl Acad Sci USA 107: 8818-8823.
66. Ward BB & O'Mullan GD (2002) Worldwide distribution of Nitrosococcus oceani, a marine ammonia-oxidizing gamma-proteobacterium, detected by PCR and sequencing of 16S rRNA and amoA genes. Appl Environ Microbiol 68: 4153-4157.
67. Wuchter C, Abbas B, Coolen MJL et al. (2006) Archaeal nitrification in the ocean. P Natl Acad Sci USA 103: 12317-12322.
68. Xia W, Zhang C, Zeng X et al. (2011) Autotrophic growth of nitrifying community in an agricultural soil. ISME J 5: 1226-1236.
69. Yan J, Haaijer SC, Op den Camp HJ et al. (2012) Mimicking the oxygen minimum zones: stimulating interaction of aerobic archaeal and anaerobic bacterial ammonia oxidizers in a laboratory-scale model system. Environ Microbiol 14: 3146-3158.
70. Yao H, Gao Y, Nicol GW et al. (2011) Links between ammonia oxidizer community structure, abundance, and nitrification potential in acidic soils. Appl Environ Microbiol 77: 4618-4625.
71. Zacherl B & Amberger A (1990) Effect of the nitrification inhibitors dicyandiamide, nitrapyrin and thiourea on Nitrosomonas europaea. Nutr Cycl Agroecosyst 22: 37-44.
72. Zhang LM, Hu HW, Shen JP & He JZ (2012) Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils. ISME J 6: 1032-1045.