Responses of ammonia-oxidizing bacterial and archaeal populations to organic nitrogen amendments in low-nutrient groundwater

Applied and Environmental Microbiology

Volumn 76, Issue 8, 2010, Pages 2517-2523

  Reed, David W ^a   Smith, Jason M ^b   Francis, Christopher A ^b   Fujita, Yoshiko ^a  

^a IDAHO NATIONAL LABORATORY   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIA OXIDIZERS; AMMONIA OXIDIZING BACTERIA; ARCHAEA; ARCHAEAL; ARCHAEAL POPULATION; COPY NUMBER; FIELD SCALE; GROUNDWATER CONDITIONS; IN-SITU GROWTH; MONOOXYGENASES; NITRATE LEVELS; NITROSOMONAS; OPERATIONAL TAXONOMIC UNITS; ORGANIC NITROGEN; PCR ANALYSIS; PHYLOTYPES; SNAKE RIVER PLAINS; UREA HYDROLYSIS;

AQUIFERS; BACTERIOLOGY; BIOREMEDIATION; GENES; GROUNDWATER RESOURCES; HYDROLYSIS; METABOLISM; UREA;

AMMONIA;

AMMONIA; ARCHAEAL PROTEIN; BACTERIAL PROTEIN; MOLASSES; NITRATE; UREA;

ALLUVIAL PLAIN; BIOREMEDIATION; GENE; GROUNDWATER; HYDROLYSIS; NITRIFICATION; NUTRIENT LIMITATION; POLYMERASE CHAIN REACTION; PROKARYOTE; UREA;

ARCHAEBACTERIUM; ARTICLE; BACTERIUM; CLASSIFICATION; CLUSTER ANALYSIS; DNA SEQUENCE; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION REACTION; PHYLOGENY; UNITED STATES;

AMMONIA; ARCHAEA; ARCHAEAL PROTEINS; BACTERIA; BACTERIAL PROTEINS; CLUSTER ANALYSIS; IDAHO; MOLASSES; MOLECULAR SEQUENCE DATA; NITRATES; OXIDATION-REDUCTION; PHYLOGENY; SEQUENCE ANALYSIS, DNA; SOIL MICROBIOLOGY; UREA; WATER MICROBIOLOGY;

SNAKE RIVER; UNITED STATES;

ARCHAEA; BACTERIA (MICROORGANISMS); NITROSOMONADALES; NITROSOMONAS;

EID: 77950571122     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02436-09     Document Type: Article

References (45)

1. 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.
2. Beman, J. M., K. J. Roberts, L. Wegley, F. Rohwer, and C. A. Francis. 2007. Distribution and diversity of archaeal ammonia monooxygenase genes associated with corals. Appl. Environ. Microbiol. 73:5642-5647.
3. Cleveland, C. C., and D. Liptzin. 2007. C:N:F stoichiometry in soil: is there a "Redfield ratio" for the microbial biomass? Biogeochemistry 85:235-252.
4. Colwell, F. S., and R. M. Lehman. 1997. Carbon source utilization profiles for microbial communities from hydrologically distinct zones in a basalt aquifer. Microb. Ecol. 33:240-251.
5. de la Torre, J. R., C. B. Walker, A. E. Ingalls, M. Könneke, and D. A. Stahl. 2008. Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. Environ. Microbiol. 10:810-818.
6. 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.
7. Erwin, D. P., I. K. Erickson, M. E. Delwiche, F. S. Colwell, J. L. Strap, and R. L. Crawford. 2005. Diversity of oxygenase genes from methane- and ammonia-oxidizing bacteria in the Eastern Snake River Plain aquifer. Appl. Environ. Microbiol. 71:2016-2025.
8. Francis, C. A., J. M. Beman, and M. M. M. Kuypers. 2007. New processes and players in the nitrogen cycle: the microbial ecology of anaerobic and archaeal ammonia oxidation. ISME J. 1:19-27.
9. Francis, C. A., K. J. Roberts, J. M. Beman, A. E. Santero, 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.
10. Freeman, S., D. Reed, and Y. Fujita. 2006. Testing the specificity of primers to environmental ammonia monooxygenase (amoA) genes in groundwater treated with urea to promote calcite precipitation. U.S. DOE J. Undergrad. Res. 6:114-118.
11. Fujita, Y., F. G. Ferris, D. L. Lawson, and F. S. Colwell. 2000. Calcium carbonate precipitation by ureolytic subsurface bacteria. Geomicrobiol. J. 17:305-318.
12. Fujita, Y., G. D. Redden, J. C. Ingram, M. M. Cortez, F. G. Ferris, and R. W. Smith. 2004. Strontium incorporation into calcite generated by bacterial ureolysis. Geochim. Cosmochim. Acta 68:3261-3270.
13. Fujita, Y., J. L. Taylor, T. L. T. Gresham, M. E. Delwiche, F. S. Colwell, T. L. McLing, L. M. Petzke, and R. W. Smith. 2008. Stimulation of microbial urea hydrolysis in groundwater to enhance calcite precipitation. Environ. Sci. Technol. 42:3025-3032.
14. Hazen, T. C. 1997. Bioremediation, p. 247-266. In P. S. Amy and D. L. Haldeman (ed.), The microbiology of the terrestrial deep subsurface. CRC Press LLC, Boca Raton, FL.
15. Head, I. M., W. D. Hiorns, T. M. Embley, A. J. McCarthy, and J. R. Saunders. 1993. The phylogeny of autotrophic ammonia-oxidizing bacteria as determined by analysis of 16S ribosomal-RNA gene-sequences. J. Gen. Microbiol. 139:1147-1153.
16. Herrmann, M., A. M. Saunders, and A. Schramm. 2008. Archaea dominate the ammonia-oxidizing community in the rhizosphere of the freshwater macrophyte Littorella uniflora. Appl. Environ. Microbiol. 74:3279-3283.
17. Ivanova, I. A., J. R. Stephen, Y. J. Chang, J. Bruggemann, P. E. Long, J. P. McKinley, G. A. Kowalchuk, D. C. White, and S. J. Macnaughton. 2000. A survey of 16S rRNA and amoA genes related to autotrophic ammoniaoxidizing bacteria of the beta-subdivision of the class proteobacteria in contaminated groundwater. Can. J. Microbiol. 46:1012-1020.
18. Könneke, 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. (Pubitemid 41613550)
19. Koper, T. E., A. F. El-Sheikh, J. M. Norton, and M. G. Klotz. 2004. Ureaseencoding genes in ammonia-oxidizing bacteria. Appl. Environ. Microbiol. 70:2342-2348.
20. Kowalchuk, G. A., and J. R. Stephen. 2001. Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annu. Rev. Microbiol. 55:485-529.
21. Lam, P., M. M. Jensen, G. Lavik, D. F. McGinnis, B. Muller, C. J. Schubert, R. Amann, B. Thamdrup, and M. M. M. Kuypers. 2007. Linking crenarchaeal and bacterial nitrification to anammox in the Black Sea. Proc. Natl. Acad. Sci. U. S. A. 104:7104-7109.
22. Lehman, R. M., S. P. O'Connell, A. Banta, J. K. Fredrickson, A. L. Reysenbach, T. L. Kieft, and F. S. Colwell. 2004. Microbiological comparison of core and groundwater samples collected from a fractured basalt aquifer with that of dialysis chambers incubated in situ. Geomicrobiol. J. 21:169-182.
23. 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.
24. Ludwig, W., O. Strunk, R. Westram, L. Richter, H. Meier, Yadhukumar, A. Buchner, T. Lai, S. Steppi, G. Jobb, W. Förster, I. Brettske, S. Gerber, A. W. Ginhart, O. Gross, S. Grumann, S. Hermann, R. Jost, A. König, T. Liss, R. Lüßmann, M. May, B. Nonhoff, B. Reichel, R. Strehlow, A. Stamatakis, N. Stuckmann, A. Vilbig, M. Lenke, T. Ludwig, A. Bode, and K.-H. Schleifer. 2004. ARB: a software environment for sequence data. Nucleic Acids Res. 32:1363-1371.
25. 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.
26. 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.
27. 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.
28. Newby, D. T., D. W. Reed, L. M. Petzke, A. L. Igoe, M. E. Delwiche, F. F. Roberto, J. P. McKinley, M. J. Whiticar, and F. S. Colwell. 2004. Diversity of methanotroph communities in a basalt aquifer. FEMS Microbiol. Ecol. 48:333-344.
29. O'Connell, S. P., R. M. Lehman, O. Snoeyenbos-West, V. D. Winston, D. E. Cummings, M. E. Watwood, and F. S. Colwell. 2003. Detection of euryarchaeota and crenarchaeota in an oxic basalt aquifer. FEMS Microbiol. Ecol. 44:165-173.
30. Okano, Y., K. R. Hristova, C. M. Leutenegger, L. E. Jackson, R. F. Denison, B. Gebreyesus, D. Lebauer, and K. M. Scow. 2004. Application of real-time PCR to study effects of ammonium on population size of ammonia-oxidizing bacteria in soil. Appl. Environ. Microbiol. 70:1008-1016.
31. Prosser, J. L, and G. W. Nicol. 2008. Relative contributions of archaea and bacteria to aerobic ammonia oxidation in the environment. Environ. Microbiol. 10:2931-2941.
32. Purkhold, U., A. Pommerening-Roser, S. Juretschko, M. C. Schmid, H. P. Koops, and M. Wagner. 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.
33. Rope, A. M., D. W. Reed, and Y. Fujita. Development of an improved standard for quantification of the amoA gene in environmental samples. U.S. DOE J. Undergrad. Res., in press.
34. 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.
35. Santoro, A. E., C. A. Francis, N. R. de Sieyes, and A. B. Boehm. 2008. Shifts in the relative abundance of ammonia-oxidizing bacteria and archaea across physicochemical gradients in a subterranean estuary. Environ. Microbiol. 10:1068-1079.
36. Schloss, P. D., and J. Handelsman. 2005. Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl. Environ. Microbiol. 71:1501-1506.
37. 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.
38. Stephen, J. R., Y. J. Chang, S. J. Macnaughton, G. A. Kowalchuk, K. T. Leung, C. A. Flemming, and D. C. White. 1999. Effect of toxic metals on indigenous soil β-subgroup proteobacterium ammonia oxidizer community structure and protection against toxicity by inoculated metal-resistant bacteria. Appl. Environ. Microbiol. 65:95-101.
39. Taylor, J. L. 2003. Stimulation of microbial urea hydrolysis in groundwater for remediation of metal contaminants. M.S. thesis. Idaho State University, Pocatello, ID.
40. 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.
41. van der Wielen, P. W. J. J., S. Voost, and D. van der Kooij. 2009. Ammoniaoxidizing bacteria and archaea in groundwater treatment and drinking water distribution systems. Appl. Environ. Microbiol. 75:4687-4695.
42. Warren, L. A., P. A. Maurice, N. Parmar, and F. G. Ferris. 2001. Microbially mediated calcium carbonate precipitation: implications for interpreting calcite precipitation and for solid-phase capture of inorganic contaminants. Geomicrobiol. J. 18:93-115.
43. Wells, G. F., H. D. Park, C. H. Yeung, B. Eggleston, C. A. Francis, and C. S. Criddle. 2009. Ammonia-oxidizing communities in a highly aerated full-scale activated sludge bioreactor: betaproteobacterial dynamics and low relative abundance of Crenarchaea. Environ. Microbiol. 11:2310-2328.
44. Wuchter, C., B. Abbas, M. J. L. Coolen, L. Herfort, J. van Bleyswijk, P. Timmers, M. Strous, E. Teira, G. J. Herndl, J. J. Middelburg, S. Scheuten, and J. S. S. Damste. 2006. Archaeal nitrification in the ocean. Proc. Natl. Acad. Sci. U. S. A. 103:12317-12322.
45. Zhang, L. M., M. Wang, J. I. Prosser, Y. M. Zheng, and J. Z. He. 2009. Altitude ammonia-oxidizing bacteria and archaea in soils of Mount Everest. FEMS Microbiol. Ecol. 70:52-61.