Production of N2O by ammonia oxidizing bacteria at subfreezing temperatures as a model for assessing the N2O anomalies in the vostok ice core

Geomicrobiology Journal

Volumn 24, Issue 5, 2007, Pages 451-459

  Miteva, Vanya ^a   Sowers, Todd ^a   Brenchley, Jean ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

N2O anomalies; Nitrosomonas cryotolerans, N2O production; Stable isotopes; Subfreezing temperatures; Vostok ice cores

Indexed keywords

BACTERIUM; ICE CORE; LAST GLACIAL; METABOLISM; MICROBIOLOGY; NITRATE; STABLE ISOTOPE;

BACTERIA (MICROORGANISMS); NITROSOMONADALES; NITROSOMONAS; NITROSOMONAS CRYOTOLERANS;

EID: 34548048815     PISSN: 01490451     EISSN: 15210529     Source Type: Journal    
DOI: 10.1080/01490450701437693     Document Type: Article

References (53)

1. Abyzov, S. S., Barkov, N. I., Bobin, N. E., Koudryashov, B. B., Lipenkov, V. Y., Mitskevich, I. N., Pashkevich, V. M. and Poglazova, M. N. (1998) The ice sheet of central Antarctica as an object of study of past ecological events on the earth. Izv Akad Nauk USSR Ser Biol, 5, pp. 610-616.
2. Bakermans, C., Tsapin, A. I., Souza-Egipsy, V., Gilichinsky, D. A. and Nealson, K. H. (2003) Reproduction and metabolism at -10°C of bacteria isolated from Siberian permafrost. Environ Microbiol, 5:4, pp. 321-326.
3. Bano, N. and Hollibaugh, J. T. (2000) Diversity and distribution of DNA sequences with affinity to ammonia-oxidizing bacteria of the beta subdivision of the class Proteobacteria in the Arctic ocean. Appl Environ Microbiol, 66, pp. 1960-1969.
4. 2O of the West Pacific and East Indian Oceans during the El Nino southern oscillation event of 1987. J Geophys Res, 94, pp. 14865-14877.
5. Casciotti, K. L., Sigman, D. M. and Ward, B. B. (2003) Linking diversity and stable isotope fractionation in ammonia-oxidizing bacteria. Geomicrobiol J, 20, pp. 335-353.
6. Christner, B. C. (2002) Incorporation of DNA and protein precursors into macromolecules by bacteria at -15°C. Appl Environ Microbiol, 68, pp. 6435-6643.
7. Christner, B. C., Mosley-Thompson, E., Thompson, L. G. and Reeve, J. N. (2001) Isolation of bacteria and 16S rDNAs from Lake Vostok accretion ice. Environ Microbiol, 3, pp. 570-577.
8. Colliver, B. B. and Stephenson, T. (2000) Production of nitrogen oxide and dinitrogen oxide by autotrophic nitrifiers. Biotechnol Adv, 18, pp. 219-232.
9. Geets, J., Boon, N. and Verstraete, W. (2006) Strategies of aerobic ammonia-oxidizing bacteria for coping with nutrient and oxygen fluctuations. FEMS Microbiol Ecol, 58, pp. 1-13.
10. Gieseke, A., Tarre, S., Green, M. and de Beer, D. (2006) Nitrification in a biofilm at low pH values: Role of in situ microenvironments and acid tolerance. Appl Environ Microbiol, 72:6, pp. 4283-4292.
11. Ginestet, P., Audic, J. M., Urbain, V. and Block, J. C. (1998) Estimation of nitrifying bacterial activities by measuring oxygen uptake in the presence of the metabolic inhibitors allylthiourea and azide. Appl Environ Microbiol, 64:6, pp. 2266-2268.
12. 2O from lakeshore soils in an Antarctic dry valley. Soil Biol Biochem, 38, pp. 3120-3129.
13. Hollibaugh, J. T., Bano, N. and Ducklow, H. W. (2002) Widespread distribution in polar oceans of a 16S rRNA gene sequence with affinity to Nitrosospira-like ammonia-oxidizing bacteria. Appl Environ Microbiol, 68, pp. 1478-1484.
14. Johnstone, B. H. and Jones, R. D. (1988) Recovery of a marine chemolitotrophic amonium-oxidizing bacterium during energy-source deprivation. Can J Microbiol, 34, pp. 1347-1350.
15. Jones, R. D. and Morita, R. Y. (1985) Low temperature growth and whole-cell kinetics of a marine ammonium oxidizer. Marine Ecol-Progress Ser, 21:3, pp. 239-243.
16. Jones, R. D., Morita, R. Y., Koops, H. P. and Watson, S. W. (1988) A new marine ammonium-oxidizing bacterium, Nitrosomonas cryotolerans sp. nov. Can J Microbiol, 34, pp. 1122-1128.
17. Junge, K., Eicken, H. and Deming, J. W. (2003) Motility of Colwellia psychrerythraea strain 34H at subzero temperatures. Appl Environ Microbiol, 69, pp. 4282-4284.
18. Junge, K., Eicken, H. and Deming, J. W. (2004) Bacterial activity at -2 to -20°C in Arctic wintertime sea ice. Appl Environ Microbiol, 70, pp. 550-557.
19. Junge, K., Eicken, H., Swanson, B. D. and Deming, J. W. (2006) Bacterial incorporation of leucine into protein down to -20°C with evidence for potential activity in sub-eutectic saline ice formations. Cryobiology, 52, pp. 417-429.
20. Karl, D. M., Bird, D. F., Björkman, K., Houlihan, T., Shackelford, R. and Tupas, L. (1999) Microorganisms in the accreted ice of Lake Vostok, Antarctica. Science, 286, pp. 2144-2147.
21. 2 concentration. Soil Biol Biochem, 36, pp. 687-699.
22. Konneke, M., Bernhard, A. E., de la Torre, J. R., Walker, C. B., Waterbury, J. B. and Stahl, D. A. (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature, 437:7058, pp. 543-546.
23. Koponen, H. T., Flöjt, L. and Martikainen, P. J. (2004) Nitrous oxide emissions from agricultural soils at low temperatures: A laboratory microcosm study. Soil Biol Biochem, 36, pp. 757-766.
24. Mader, H. M., Pettit, M. E., Wadham, J. L., Wolff, E. W. and Parkes, R. J. (2006) Subsurface ice as a microbial habitat. Geology, 34, pp. 169-172.
25. Miteva, V. I. and Brenchley, J. E. (2005) Detection and isolation of ultrasmall microorganisms from a 120,000 year old Greenland glacier ice core. Appl Environ Microbiol, 71, pp. 7806-7818.
26. Miteva, V. I., Sheridan, P. P. and Brenchley, J. E. (2004) Phylogenetic and physiological diversity of microorganisms isolated from a deep Greenland ice core. Appl Environ Microbiol, 70, pp. 202-221.
27. 2O emissions and product ratios of nitrification and denitrification as affected by freezing and thawing. Soil Biol Biochem, 38, pp. 3411-3420.
28. Panikov, N. S., Flanagan, P. W., Oechel, W. C., Mastepanov, M. A. and Christensen, T. R. (2006) Microbial activity in soils frozen to below -39°C. Soil Biol Biochem, 38, pp. 785-794.
29. Panikov, N. S. and Sizova, M. V. (2007) Growth kinetics of microorganisms isolated from Alaskan soil and permafrost in solid media frozen down to -35°C. FEMS Microbiol Ecol, 59, pp. 500-512.
30. Petit, J. R., Jouzel, J., Raynaud, D., Barkov, N. I., Barnola, J. M., Basile, I., Bender, M., Chappellaz, J., Davis, M., Delaygue, G., Delmotte, M., Kotlyakov, V. M., Legrand, M., Lipenkov, V. Y., Lorius, C., Pepin, L., Ritz, C., Saltzman, E. and Stievenard, M. (1999) Climate and atmospheric history of the past 420,000 years from the Vostok ice core, Antarctica. Nature, 399, pp. 429-436.
31. Price, P. B. (2000) A habitat for psychrophiles in deep Antarctic ice. Proc Natl Acad Sci, 97, pp. 1247-1251.
32. Price, B. P. and Sowers, T. (2004) Temperature dependence of metabolic rates for microbial growth, maintenance, and survival. Proc Natl Acad Sci, 101, pp. 4631-4636.
33. Shaw, L. J., Nicol, G. W., Smith, Z., Fear, J., Prosser, J. I. and Baggs, E. M. (2006) Nitrosospira spp. can produce nitrous oxide via a nitrifier denitrification pathway. Environ Microbiol, 8, pp. 214-222.
34. Siegenthaler, U., Stocker, T., Monnin, E., Luthi, D., Schwander, J., Stauffer, B., Raynaud, D., Barnola, J-M, Fischer, H., Masson-Delmotte, V. and Jouzel, J. (2005) Stable carbon cycle-climate relationship during the late Pleistocene. Science, 310, pp. 1313-1317.
35. 2O record spanning the penultimate deglaciation from the Vostok ice core. J Geophys Res, 106, pp. 31,903-931,914.
36. Sowers, T., Alley, R. B. and Jubenville, J. (2003) Elemental and isotopic records of atmospheric nitrous oxide covering the last 106,000 years from the GISP II and Taylor Dome ice cores. Science, 301, pp. 945-948.
37. Sowers, T. and Jubenville, J. (2000) A modified extraction technique for liberating occluded gases from ice cores. J Geophys Res, 105, pp. 29,155-129,164.
38. Spahni, R., Chappellaz, J., Stocker, T., Loulergue, L., Hausammann, G., Kawamura, K., Fluckiger, J., Schwander, J., Raynaud, D., Masson-Delmotte, V. and Jouzel, J. (2005) Atmospheric methane and nitrous oxide of the late Pleistocene from Antarctic ice cores. Science, 310, pp. 317-1321.
39. Stehr, G. S., Zörner, S., Bottcher, B. and Koops, H. P. (1995) Exopolymers: An ecological characteristic of a floc-attached, ammonia-oxidizing bacterium. Microbiol Ecol, 30:2, pp. 115-126.
40. Stein, L. Y. and Yung, U. L. (2003) Production, isotopic composition, and atmospheric fate of biologically produced nitrous oxide. Annu Rev Earth Planet Sci, 31, pp. 329-356.
41. Sutka, R. L., Ostrom, N. E., Ostrom, P. H., Breznak, J. A., Gandhi, H. and Pitt, A. J. (2006) Distinguishing nitrous oxide production from nitrification and denitrification on the basis of isotopomer abundances. Appl Environ Microbiol, 72, pp. 638-644.
42. 2O. Intern J Mass Spectrom Ion Processes, 142, pp. 163-175.
43. Teepe, R., Brumme, R. and Beese, F. (2000) Nitrous oxide emissions from frozen soils under agricultural, fallow and forest land. Soil Biol Biochem, 32, pp. 1807-1810.
44. Teepe, R., Brumme, R. and Beese, F. (2001) Nitrous oxide emissions from soil during freezing and thawing periods. Soil Biol Biochem, 33, pp. 1269-1275.
45. Vorobyova, E., Soina, V., Gorlenko, M., Minkovskaya, N., Zalinova, N., Mamukelashvili, A., Gilichinsky, D. A., Rivkina, E. and Vishnivetskaya, T. (1997) The deep cold biosphere: Facts and hypothesis. FEMS Microbiol Rev, 20, pp. 277-290.
46. Voytek, M. A., Priscu, J. C. and Ward, B. B. (1999) The distribution and relative abundance of ammonia-oxidizing bacteria in lakes of the McMurdo Valley, Antarctica. Hydrobiologia, 401, pp. 113-130.
47. Wagner, D., Spieck, E., Bock, E. and Pfeiffer, E. M. (2002) Microbial life in terrestrial permafrost: Methanogenesis and nitrification in Gelisols as potentials for exobiological processes. Astrobiology. The quest for the conditions of life, pp. 143-159. Springer, Berlin
48. Ward, B. B. and Priscu, J. C. (1997) Detection and characterization of denitrifying bacteria from a permanently ice-covered Antarctic lake. Hydrobiologia, 347, pp. 57-68.
49. Watson, S. W. (1965) Characteristics of a marine nitrifying bacterium Nitrosocistis oceanus sp. nov. Limnol Oceanogr, 10, pp. 3278-3289.
50. Wilhelm, R., Abeliovich, A. and Nejidat, A. (1998) Effect of long-term ammonia starvation on the oxidation of ammonia and hydroxylamine by Nitrosomonas europaea. J. Biochem., 124, pp. 811-815.
51. Wrage, N., Velthof, G. L., van Beusichem, M. L. and Oenema, O. (2001) Role of nitrifier denitrification in the production of nitrous oxide. Soil Biol Biochem, 33, pp. 1723-1732.
52. Xiang, S. R., DL.Z, T., Yao, A., Xu, B. Q., Wu, G. J., Wang, Y. Q., Xu, B. Q. and Wang, X. R. (2004) Bacterial diversity in Malan ice core from the Tibetan plateau. Folia Microbiol, 49, pp. 269-276.
53. Xiang, S., Yao, T., An, L. Z., Xu, B. Q., Wu, G. J., Wang, Y. Q. and Chen, X. R. (2005) 16S rRNA sequences and difference in bacteria isolated from the Muztag Ata Glacier at increasing depths. Appl Environ Microbiol, 71, pp. 4619-4627.