Abundance of ammonia-oxidizing archaea and bacteria along an estuarine salinity gradient in relation to potential nitrification rates

Applied and Environmental Microbiology

Volumn 76, Issue 4, 2010, Pages 1285-1289

  Bernhard, Anne E ^a   Landry, Zachary C ^a,d   Blevins, Alison ^b   De La Torre, José R ^b,e   Giblin, Anne E ^c   Stahl, David A ^b  

^a The Holleran Center for Community Action and Public Policy   (United States)

^b University of Washington   (United States)

^c ECOSYSTEMS CENTER   (United States)

^d OREGON STATE UNIVERSITY   (United States)

^e SAN FRANCISCO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALTERNATIVE ENERGY SOURCE; AMMONIA OXIDIZING BACTERIA; ARCHAEA; POTENTIAL NITRIFICATION; SALINITY GRADIENTS;

AMMONIA; BACTERIOLOGY; DENITRIFICATION; NITRIFICATION; OXIDATION;

SALINITY MEASUREMENT;

AMMONIA; FRESH WATER; NITROGEN; SEA WATER;

ABUNDANCE; BACTERIUM; ESTUARINE ECOSYSTEM; EUKARYOTE; NITRIFICATION; SALINITY;

ARCHAEAL GENE; ARCHAEBACTERIUM; ARTICLE; BACTERIAL GENE; BACTERIUM; BETAPROTEOBACTERIA; CLASSIFICATION; ECOSYSTEM; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION REACTION; PHYLOGENY; SALINITY; SEDIMENT;

AMMONIA; ARCHAEA; BACTERIA; BETAPROTEOBACTERIA; ECOSYSTEM; FRESH WATER; GENES, ARCHAEAL; GENES, BACTERIAL; GEOLOGIC SEDIMENTS; MOLECULAR SEQUENCE DATA; NITROGEN; OXIDATION-REDUCTION; PHYLOGENY; SALINITY; SEAWATER; WATER MICROBIOLOGY;

EID: 76649087327     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02018-09     Document Type: Article

References (36)

1. Agogue, H., M. Brink, J. Dinasquet, and G. J. Herndl. 2008. Major gradients in putatively nitrifying and non-nitrifying Archaea in the deep North Atlantic. Nature 456:788-792.
2. Balls, P. W., N. Brockie, J. Dobson, and W. Johnston. 1996. Dissolved oxygen and nitrification in the upper Forth Estuary during summer (1982-92): patterns and trends. Estuar. Coast. Shelf Sci. 42:117-134.
3. +, and CO oxidation by methanotrophs and nitriflers. Microbiol. Rev. 53:68-84.
4. Beman, J. M., and C. A. Francis. 2006. Diversity of ammonia-oxidizing archaea and bacteria in the sediments of a hypernutrifled subtropical estuary: Bahía del Tóbari, Mexico. Appl. Environ. Microbiol. 72:7767-7777.
5. 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.
6. 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.
7. Bernhard, A. E., T. Donn, A. E. Giblin, and D. A. Stahl. 2005. Loss of diversity of ammonia-oxidizing bacteria correlates with increasing salinity in an estuary system. Environ. Microbiol. 7:1289-1297.
8. Bernhard, A. E., J. Tucker, A. E. Giblin, and D. A. Stahl. 2007. Functionally distinct communities of ammonia-oxidizing bacteria along an estuarine salinity gradient. Environ. Microbiol. 9:1439-1447.
9. Caffrey, J. M., N. Bano, K. Kalanetra, and J. T. Hollibaugh. 2007. Ammonia oxidation and ammonia-oxidizing bacteria and archaea from estuaries with differing histories of hypoxia. ISME J. 1:660-662.
10. Coolen, M. J. L., B. Abbas, J. Van Bleijswijk, E. C. Hopmans, M. M. M. Kuypers, S. G. Wakeham, and J. S. Sinninghe Damste. 2007. Putative ammonia-oxidizing Crenarchaeota in suboxic waters of the Black Sea: a basinwide ecological study using 16S ribosomal and functional genes and membrane lipids. Environ. Microbiol. 9:1001-1016.
11. 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.
12. Dunning, A. M., P. Talmud, and S. E. Humphries. 1988. Errors in the polymerase chain reaction. Nucleic Acids Res. 16:10393.
13. 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. Nat. Acad. Sci. U. S. A. 102:14683-14688.
14. Hallam, S. J., T. J. Mincer, C. Schleper, C. M. Preston, K. Roberts, P. M. Richardson, and E. F. DeLong. 2006. Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine Crenarchaeota. PLoS Biol. 4:e95.
15. 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. Nat. Acad. Sci. U. S. A. 105: 2134-2139.
16. Hopkinson, C. S. J., A. E. Giblin, J. Tucker, and R. H. Garritt. 1999. Benthic metabolism and nutrient cycling along an estuarine salinity gradient. Estuaries 22:863-881.
17. Ingalls, A. E., S. R. Shah, R. L. Hansman, L. I. Aluwihare, G. M. Santos, E. R. M. Druffel, and A. Pearson. 2006. Quantifying archaeal community autotrophy in the mesopelagic ocean using natural radiocarbon. Proc. Nat. Acad. Sci. U. S. A. 103:6442-6447.
18. Iriarte, A., I. de Madariaga, F. Diez-Garagarza, M. Revilla, and E. Orive. 1996. Primary plankton production, respiration and nitrification in a shallow temperate estuary during summer. J. Exp. Mar. Biol. Ecol. 208:127-151.
19. Jia, Z., and R. Conrad. 2009. Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil. Environ. Microbiol. 11: 1658-1671.
20. Koenneke, M., A. E. Bernhard, J. R. de la Torre, C. B. Walker, J. B. Waterbury, and D. A. Stahl. 2005. Isolation of an autotrophic ammoniaoxidizing marine archaeon. Nature 437:543-546.
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. Nat. Acad. Sci. U. S. A. 104:7104-7109.
22. 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. (Pubitemid 44258909)
23. 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. (Pubitemid 38854737)
24. 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 461:976-981.
25. Mincer, T. J., M. J. Church, L. T. Taylor, C. Preston, D. M. Karl, and E. F. DeLong. 2007. Quantitative distribution of presumptive archaeal and bacterial nitriflers in Monterey Bay and the North Pacific Subtropical Gyre. Environ. Microbiol. 9:1162-1175.
26. Moin, N. S., K. A. Nelson, A. Bush, and A. E. Bernhard. 2009. Distribution and diversity of archaeal and bacterial ammonia-oxidizers in salt marsh sediment. Appl. Environ. Microbiol. 75:7461-7468.
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. Nelson, K. A., N. S. Moin, and A. E. Bernhard. 2009. Archaeal diversity and the prevalence of Crenarchaeota in salt marsh sediments. Appl. Environ. Microbiol. 75:4211-4215.
29. Ouverney, C. C., and J. A. Fuhrman. 2000. Marine planktonic Archaea take up amino acids. Appl. Environ. Microbiol. 66:4829-4833.
30. Park, H.-D., G. F. Wells, H. Bae, C. S. Criddle, and C. A. Francis. 2006. Occurrence of ammonia-oxidizing archaea in wastewater treatment plant bioreactors. Appl. Environ. Microbiol. 72:5643-5647.
31. Santoro, A. E., C. A. Francis, N. R. De Sieves, 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.
32. Somville, M. 1984. Use of nitrifying activity measurements for describing the effect of salinity on nitrification in the Scheldt Estuary. Appl. Environ. Microbiol. 47:424-426.
33. Strous, M., J. A. Fuerst, E. H. M. Kramer, S. Logemann, G. Muyzer, K. T. van de Pas-Schoonen, R. Webb, J. G. Kuenen, and M. S. M. Jetten. 1999. Missing lithotroph identified as new planctomycete. Nature 400:446-449. (Pubitemid 29361796)
34. Treusch, A. H., S. Leininger, A. Kietzin, 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.
35. Weidler, G. W., M. Dornmayr-Pfaffenhuemer, F. 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.
36. Wuchter, C., B. Abbas, M. J. L. Coolen, L. Herfort, J. Van Bleijswijk, P. Timmers, M. Strous, E. Teira, G. J. Herndl, J. J. Middleburg, S. Schouten, and J. S. Sinninghe Damste. 2006. Archaeal nitrification in the ocean. Proc. Nat. Acad. Sci. U. S. A. 103:12317-12322.