Evidence for different contributions of archaea and bacteria to the ammonia-oxidizing potential of diverse oregon soils

Applied and Environmental Microbiology

Volumn 76, Issue 23, 2010, Pages 7691-7698

  Taylor, Anne E ^a   Zeglin, Lydia H ^a   Dooley, Sandra ^b   Myrold, David D ^a   Bottomley, Peter J ^a  

^a OREGON STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIA OXIDIZING BACTERIA; ARCHAEA; AZOXYSTROBIN; BACTERIAL PROTEIN; EUKARYOTIC PROTEIN SYNTHESIS; FOREST SOILS; KANAMYCINS; MONOOXYGENASES; OXIDIZING POTENTIALS; PASTURE SOILS; SOIL SLURRY;

ACETYLENE; AGRICULTURE; AMMONIA; BACTERIOLOGY; DENITRIFICATION; LIGHTING; MICROORGANISMS; NITRIFICATION; OXIDATION; THIOUREAS; UREA;

SOILS;

AMMONIA;

ACETYLENE; AMMONIA; ANTIBIOTICS; BACTERIUM; DOMINANCE; ENZYME ACTIVITY; FUNGUS; INHIBITOR; NITRIFICATION; PASTURE; POLLUTANT REMOVAL; PROKARYOTE; SLURRY; SOIL MICROORGANISM;

ARCHAEBACTERIUM; ARTICLE; BACTERIUM; METABOLISM; MICROBIOLOGY; NITRIFICATION; OXIDATION REDUCTION REACTION; UNITED STATES;

AMMONIA; ARCHAEA; BACTERIA; NITRIFICATION; OREGON; OXIDATION-REDUCTION; SOIL MICROBIOLOGY;

OREGON; UNITED STATES;

BACTERIA (MICROORGANISMS); EUKARYOTA; FUNGI;

EID: 78650313827     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01324-10     Document Type: Article

References (60)

1. Adamczyk, J., M. Hesselsoe, N. Iversen, M. Horn, A. Lehner, P. H. Nielsen, M. Schloter, P. Roslev, and M. Wagner. 2003. The isotope array, a new tool that employs substrate-mediated labeling of rRNA for determination of microbial community structure and function. Appl. Environ. Microbiol. 69: 6875-6887.
2. Andersson, A. F., M. Lundgren, S. Eriksson, M. Rosenlund, R. Bernander, and P. Nilsson. 2006. Global analysis of mRNA stability in the archaeon Sulfolobus. Genome Biol. 7:R99.
3. Avrahami, S., and B. J. A. Bohannan. 2007. Response of Nitrosospira sp. strain AF-like ammonia oxidizers to changes in temperature, soil moisture content, and fertilizer concentration. Appl. Environ. Microbiol. 73:1166-1173.
4. Avrahami, S., W. Liesack, and R. Conrad. 2003. Effects of temperature and fertilizer on activity and community structure of soil ammonia oxidizers. Environ. Microbiol. 5:691-705.
5. +, and CO oxidation by methanotrophs and nitrifiers. Microbiol. Rev. 53:68-84.
6. Bell, S. D., and S. P. Jackson. 1998. Transcription and translation in Archaea: A mosaic of eukaryal and bacterial features. Trends Microbiol. 6:222-228.
7. Beman, J. M., B. N. Popp, and C. A. Francis. 2008. Molecular and biogeochemical evidence for ammonia oxidation by marine Crenarchaeota in the Gulf of California. ISME J. 2:429-441.
8. Berg, P., L. Klemedtsson, and T. Rosswall. 1982. Inhibitory effect of low partial pressures of acetylene on nitrification. Soil Biol. Biochem. 14:301-303.
9. Bini, E., V. Dikshit, K. Dirksen, M. Drozda, and P. Blum. 2002. Stability of mRNA in the hyperthermophilic archaeon Sulfolobus solfataricus. RNA 8:1129-1136.
10. Bock, E., and H.-P. Koops. 1992. The genus Nitrobacter and related genera, p. 2302-2309. In A. Balows, M. Trüper, M. Dworkin, W. Harder, and K.-H. Schleifer (ed.), The prokaryotes, 2nd ed., vol. 3. Springer- Verlag, New York, NY.
11. Bollmann, A., and R. Conrad. 1997. Recovery of nitrification and production of NO and N2O after exposure of soil to acetylene. Biol. Fertil. Soils 25:41-46.
12. Bollmann, A., I. Schmidt, A. M. Saunders, and M. H. Nicolaisen. 2005. Influence of starvation on potential ammonia-oxidizing activity and amoA mRNA levels of Nitrosospira briensis. Appl. Environ. Microbiol. 71:1276-1282.
13. Cherif-Zahar, B., A. Durand, I. Schmidt, N. Hamdaoui, I. Matic, M. Merrick, and G. Matassi. 2007. Evolution and functional characterization of the RH50 gene from the ammonia-oxidizing bacterium Nitrosomonas europaea. J. Bacteriol. 189:9090-9100.
14. Csaki, R., L. Bodrossy, J. Klem, J. C. Murrell, and K. L. Kovacs. 2003. Genes involved in the copper-dependent regulation of soluble methane monooxygenase of Methylococcus capsulatus (Bath): Cloning, sequencing and mutational analysis. Microbiol. Rev. 149:1785-1795.
15. de la Torre, J. R., C. B. Walker, A. E. Ingalls, M. Konneke, and D. A. Stahl. 2008. Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. Environ. Microbiol. 10:810-818.
16. Dennis, P. P. 1997. Ancient ciphers: Translation in Archaea. Cell 89:1007-1010.
17. Di, H. J., K. C. Cameron, J. P. Shen, C. S. Winefield, M. O'Callaghan, S. Bowatte, and J. Z. He. 2009. Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nat. Geosci. 2:621-624.
18. Ensign, S. A. 1996. Aliphatic and chlorinated alkenes and epoxides as inducers of alkene monooxygenase and epoxidase activities in Xanthobacter strain Py2. Appl. Environ. Microbiol. 62:61-66.
19. Francis, C. A., K. J. Roberts, J. M. Beman, A. E. Santoro, and B. B. Oakley. 2005. Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc. Natl. Acad. Sci. U. S. A. 102:14683-14688.
20. Ginestet, P., J. M. Audic, V. Urbain, and J. C. Block. 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.
21. Gvakharia, B. O., P. J. Bottomley, D. J. Arp, and L. A. Sayavedra-Soto. 2009. Construction of recombinant Nitrosomonas europaea expressing green fluorescent protein in response to co-oxidation of chloroform. Appl. Microbiol. Biotechnol. 82:1179-1185.
22. Hageman, R. H., and D. P. Hucklesby. 1971. Nitrate reductase in higher plants. Methods Enzymol. 23:491-503.
23. Halsey, K. H., L. A. Sayavedra-Soto, P. J. Bottomley, and D. J. Arp. 2006. Site-directed amino acid substitutions in the hydroxylase at subunit of butane monooxygenase from Pseudomonas butanovora: Implications for substrates knocking at the gate. J. Bacteriol. 188:4962-4969.
24. Hamamura, N., C. M. Yeager, and D. J. Arp. 2001. Two distinct monooxygenases for alkane oxidation in Nocardioides sp. strain CF8. Appl. Environ. Microbiol. 67:4992-4998.
25. Hatzenpichler, R., E. V. Lebedeva, E. Spieck, K. Stoecker, A. Richter, H. Daims, and M. Wagner. 2008. A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proc. Natl. Acad. Sci. U. S. A. 105: 2134-2139.
26. Hofman, T., and H. Lees. 1953. The biochemistry of the nitrifying organisms. IV. The respiration and intermediary metabolism of Nitrosomonas. Biochem. J. 54:579-583.
27. Hooper, A. B., and K. R. Terry. 1973. Specific inhibitors of ammonia oxidation in Nitrosomonas. J. Bacteriol. 115:480-485.
28. 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. 267:1524-1545.
29. Hyman, M. R., and D. J. Arp. 1988. Acetylene inhibition of metalloenzymes. Anal. Biochem. 173:207-220.
30. Hyman, M. R., and P. M. Wood. 1985. Suicidal inactivation and labeling of ammonia monooxygenase by acetylene. Biochem. J. 227:719-725.
31. Jager, A., R. Samorski, F. Pfeifer, and G. Klug. 2002. Individual gvp transcript segments in Haloferax mediterranei exhibit varying half-lives, which are differentially affected by salt concentration and growth phase. Nucleic Acids Res. 30:5436-5443.
32. Jia, Z. J., and R. Conrad. 2009. Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil. Environ. Microbiol. 11:1658-1671.
33. Jiang, Q. Q., and L. R. Bakken. 1999. Comparison of Nitrosospira strains isolated from terrestrial environments. FEMS Microbiol. Ecol. 30:171-186.
34. Kester, R. A., W. De Boer, and H. J. Laanbroek. 1996. Short exposure to acetylene to distinguish between nitrifier and denitrifier nitrous oxide production in soil and sediment. FEMS Microbiol. Ecol. 20:111-120.
35. Konneke, M., A. E. Bernhard, J. R. de la Torre, C. B. Walker, J. B. Waterbury, and D. A. Stahl. 2005. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543-546.
36. Leininger, S., T. Urich, M. Schloter, L. Schwark, J. Qi, G. W. Nicol, J. I. Prosser, S. C. Schuster, and C. Schleper. 2006. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806-809.
37. Madigan, M. T., J. M. Martinko, and T. D. Brock. 2006. Brock biology of microorganisms, 11th ed. Pearson Prentice Hall, Upper Saddle River, NJ.
38. Mahendrappa, M. K., R. L. Smith, and A. T. Christiansen. 1966. Nitrifying organisms affected by climatic region in western United States. Soil Sci. Soc. Am. Proc. 30:60-62.
39. Martens-Habbena, W., P. M. Berube, H. Urakawa, J. R. de la Torre, and D. A. Stahl. 2009. Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature 461:976-979.
40. Mincer, T. J., M. J. Church, L. T. Taylor, C. Preston, D. M. Kar, and E. F. DeLong. 2007. Quantitative distribution of presumptive archaeal and bacterial nitrifiers in Monterey Bay and the North Pacific Subtropical Gyre. Environ. Microbiol. 9:1162-1175.
41. Mosier, A. C., and C. A. Francis. 2008. Relative abundance and diversity of ammonia-oxidizing archaea and bacteria in the San Francisco Bay estuary. Environ. Microbiol. 10:3002-3016.
42. Myers, R. J. K. 1975. Temperature effects on ammonification and nitrification in a tropical soil. Soil Biol. Biochem. 7:83-86.
43. Nicol, G. W., S. Leininger, C. Schleper, and J. I. Prosser. 2008. The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environ. Microbiol. 10:2966-2978.
44. Norton, J. M., J. J. Alzerreca, Y. Suwa, and M. G. Klotz. 2002. Diversity of ammonia monooxygenase operon in autotrophic ammonia-oxidizing bacteria. Arch. Microbiol. 177:139-149.
45. Nyerges, G., and L. Y. Stein. 2009. Ammonia cometabolism and product inhibition vary considerably among species of methanotrophic bacteria. FEMS Microbiol. Lett. 297:131-136.
46. Offre, P., J. I. Prosser, and G. W. Nicol. 2009. Growth of ammonia-oxidizing archaea in soil microcosms is inhibited by acetylene. FEMS Microbiol. Ecol. 70:99-108.
47. Ratajczak, A., W. Geissdorfer, and W. Hillen. 1998. Expression of alkane hydroxylase from Acinetobacter sp. strain ADP1 is induced by a broad range of n-alkanes and requires the transcriptional activator AlkR. J. Bacteriol. 180:5822-5827.
48. Rotthauwe, J. H., K. P. Witzel, and W. Liesack. 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.
49. Sayavedra-Soto, L. A., C. M. Byrd, and D. J. Arp. 2001. Induction of butane consumption in Pseudomonas butanovora. Arch. Microbiol. 176:114-120.
50. Schauss, K., A. Focks, S. Leininger, A. Kotzerke, H. Heuer, S. Thiele-Bruhn, S. Sharma, B. M. Wilke, M. Matthies, K. Smalla, J. C. Munch, W. Amelung, M. Kaupenjohann, M. Schloter, and C. Schleper. 2009. Dynamics and functional relevance of ammonia-oxidizing archaea in two agricultural soils. Environ. Microbiol. 11:446-456.
51. Schmidt, E. L., and L. W. Belser. 1994. Autotrophic nitrifying bacteria, p. 159-177. In R. W. Weaver, S. Angle, P. J. Bottomley, D. Bezdicek, S. Smith, A. Tabatabai, and A. Wollum (ed.), Methods of soil analysis, part 2. Microbiological and biochemical properties. Soil Science Society of America, Inc., Madison, WI.
52. Spear, J. R., H. A. Barton, C. E. Robertson, C. A. Francis, and N. R. Pace. 2007. Microbial community biofabrics in a geothermal mine adit. Appl. Environ. Microbiol. 73:6172-6180.
53. Stark, J. M., and M. K. Firestone. 1996. Kinetic characteristics of ammonium- oxidizer communities in a California oak and woodland-annual grassland. Soil Biol. Biochem. 28:1307-1317.
54. Tourna, M., T. E. Freitag, G. W. Nicol, and J. I. Prosser. 2008. Growth, activity and temperature responses of ammonia-oxidizing archaea and bacteria in soil microcosms. Environ. Microbiol. 10:1357-1364.
55. Treusch, A. H., S. Leininger, A. Kletzin, S. C. Schuster, H. P. Klenk, and C. Schleper. 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.
56. Wei, X., L. A. Sayavedra-Soto, and D. J. Arp. 2007. Characterization of the ferrioxamine uptake system of Nitrosomonas europaea. Microbiology 153: 3963-3972.
57. Weidler, G. W., M. Dornmayr-Pfaffenhuemer, F. W. Gerbl, W. Heinen, and H. Stan-Lotter. 2007. Communities of Archaea and Bacteria in a subsurface radioactive thermal spring in the Austrian Central Alps, and evidence of ammonia-oxidizing Crenarchaeota. Appl. Environ. Microbiol. 73:259-270.
58. Wuchter, C., B. Abbas, M. J. Coolen, L. Herfort, J. van Bleijswijk, P. Timmers, M. Strous, E. Teira, G. J. Herndl, J. J. Middelburg, S. Schouten, and J. S. S. Damste. 2006. Archaeal nitrification in the ocean. Proc. Natl. Acad. Sci. U. S. A. 103:12317-12322.
59. Yeager, C. M., P. J. Bottomley, D. J. Arp, and M. R. Hyman. 1999. Inactivation of toluene 2-monooxygenase in Burkholderia cepacia G4 by alkynes. Appl. Environ. Microbiol. 65:632-639.
60. Zhang, C. L., Q. Ye, Z. Y. Huang, W. J. Li, J. Q. Chen, Z. Q. Song, W. D. Zhao, C. Bagwell, W. P. Inskeep, C. Ross, L. Gao, J. Wiegel, C. S. Romanek, E. L. Shock, and B. P. Hedlund. 2008. Global occurrence of archaeal amoA genes in terrestrial hot springs. Appl. Environ. Microbiol. 74:6417-6426.