Crenarchaeota and their role in the nitrogen cycle in a subsurface radioactive thermal spring in the Austrian Central Alps

Applied and Environmental Microbiology

Volumn 74, Issue 19, 2008, Pages 5934-5942

  Weidler, Gerhard W ^a   Gerbl, Friedrich W ^a   Stan Lotter, Helga ^a  

^a UNIVERSITY OF SALZBURG   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIA; AMMONIUM COMPOUNDS; BACTERIOLOGY; BIOFILMS; BIOFILTERS; COLLOIDS; DENITRIFICATION; ELECTROPHORESIS; FLUORESCENCE MICROSCOPY; GELATION; GEOTHERMAL SPRINGS; MICROSCOPIC EXAMINATION; NITRIFICATION; OFFSHORE OIL WELL PRODUCTION; OXIDATION; RADIOACTIVE MATERIALS; RADIOACTIVITY; SOILS; SPRINGS (COMPONENTS);

16S RRNA GENES; AMMONIA OXIDATIONS; ARCHAEA; ARCHAEAL; ARCHAEAL CELLS; AUSTRIA; BACTERIAL; CENTRAL ALPS; CRENARCHAEOTA; DENATURING GRADIENT GEL ELECTROPHORESIS ANALYSES; FILTERED WATERS; FISH ANALYSES; FLUORESCENCE IN SITU HYBRIDIZATIONS; FRESHWATER; GENE SEQUENCES; MICROCOSM EXPERIMENTS; NITROGEN CYCLES; NOVEL CLUSTERS; PROKARYOTIC COMMUNITIES; SEMIQUANTITATIVE; SPRING INS;

GENES;

4',6 DIAMIDINO 2 PHENYLINDOLE; AMMONIA; BACTERIAL PROTEIN; FRESH WATER; NITRITE; PROTEIN AMOA; RNA 16S; UNCLASSIFIED DRUG; ARCHAEAL DNA; ARCHAEAL PROTEIN; NITROGEN; QUATERNARY AMMONIUM DERIVATIVE;

AMMONIUM; BIOFILM; DATABASE; ELECTROKINESIS; GEL; GENETIC ANALYSIS; MICROCOSM; NITRITE; NITROGEN CYCLE; OXIDATION; PROKARYOTE; RNA; THERMAL SPRING;

ARTICLE; AUSTRIA; BIOFILM; CONTROLLED STUDY; CRENARCHAEOTA; DENATURING GRADIENT GEL ELECTROPHORESIS; FLUORESCENCE IN SITU HYBRIDIZATION; GENE LIBRARY; GENE SEQUENCE; MICROCOSM; NITRIFICATION; NITROGEN CYCLE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION; RADIOACTIVITY; STAINING; THERMAL SPRING; UNINDEXED SEQUENCE; BIODIVERSITY; CHEMISTRY; CLUSTER ANALYSIS; DNA DENATURATION; DNA SEQUENCE; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; PHYLOGENY; POLYACRYLAMIDE GEL ELECTROPHORESIS; SEQUENCE HOMOLOGY;

ALPS; AUSTRIA; CENTRAL ALPS; CENTRAL EUROPE; EURASIA; EUROPE;

ARCHAEA; BACTERIA (MICROORGANISMS); CRENARCHAEOTA; PROKARYOTA;

ARCHAEAL PROTEINS; AUSTRIA; BIODIVERSITY; CLUSTER ANALYSIS; CRENARCHAEOTA; DNA, ARCHAEAL; ELECTROPHORESIS, POLYACRYLAMIDE GEL; HOT SPRINGS; IN SITU HYBRIDIZATION, FLUORESCENCE; MOLECULAR SEQUENCE DATA; NITRITES; NITROGEN; NUCLEIC ACID DENATURATION; PHYLOGENY; QUATERNARY AMMONIUM COMPOUNDS; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 54449092101     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.02602-07     Document Type: Article

References (54)

1. Amann, R. I. 1995. In situ identification of micro-organisms by whole cell hybridization with rRNA-targeted nucleic acid probes, section 3.3.6., p. 1-15. In A. D. L. Akkermans, J. D. van Elsas, and F. J. de Bruijn (ed.), Molecular microbial ecology manual. Kluwer Academic Publishers, Dordrecht, The Netherlands.
2. Amann, R. I., B. J. Binder, R. J. Olson, S. W. Chisholm, R. Devereux, and D. A. Stahl. 1990. Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl. Environ. Microbiol. 56:1919-1925.
3. Beman, M. J., and C. A. Francis. 2006. Diversity of ammonia-oxidizing Archaea and Bacteria in the sediments of a hypernutrified subtropical estuary: Bahía del Tóbari, Mexico. Appl. Environ. Microbiol. 72:7767-7777.
4. Bock, E., and M. Wagner. 2006. Oxidation of inorganic nitrogen compounds as an energy source, p. 457-495. In M. Dworkin, S. Falkow, E. Rosenberg, K.-H. Schleifer, and E. Stackebrandt (ed.), The prokaryotes, 3rd ed., vol. 2. Springer Science and Business Media, LLC, Berlin, Germany.
5. Buol, S. W., R. J. Southard, R. C. Graham, and P. A. McDaniel. 2003. Soil genesis and classification, 5th ed. Iowa State Press, Ames.
6. Burggraf, S., T. Mayer, R. Amann, S. Schadhauser, C. R. Woese, and K. O. Stetter. 1994. Identifying members of the domain Archaea with rRNA-targeted oligonucleotide probes. Appl. Environ. Microbiol. 60:3112-3119.
7. 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.
8. Cudrigh, S. F. 2002. Die Wasserwegigkeit des Gasteiner Thermalwassers. Diploma thesis. University of Salzburg, Salzburg, Austria.
9. Daniels, L., N. Belay, and B. S. Rajagopal. 1986. Assimilatory reduction of sulfate and sulfite by methanogenic bacteria. Appl. Environ. Microbiol. 51: 703-709.
10. 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.
11. DeLong, E. F. 1992. Archaea in coastal marine environments. Proc. Natl. Acad. Sci. USA 89:5685-5689.
12. Engel, A. S., M. L. Porter, L. A. Stern, S. Quinlan, and P. C. Bennett. 2004. Bacterial diversity and ecosystem function of filamentous microbial mats from aphotic (cave) sulfidic springs dominated by chemolithoautotrophic "Epsilonproteobacteria." FEMS Microbiol. Ecol. 51:31-53.
13. 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.
14. 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. USA 102:14683-14688.
15. Hallam, S. J., K. T. Konstantinidis, N. Putnam, C. Schleper, Y.-I. Watanabe, J. Sugahara, C. Preston, J. de la Torre, P. M. Richardson, and E. F. DeLong. 2006. Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum. Proc. Natl. Acad. Sci. USA 103:18296-18301.
16. 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.
17. 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. USA 105:2134- 2139.
18. Hirayama, H., K. Takai, F. Inagaki, Y. Yamato, M. Suzuki, K. H. Nealson, and K. Horikoshi. 2005. Bacterial community shift along a subsurface geothermal water stream in a Japanese gold mine. Extremophiles 9:169-184.
19. Holmes, A. J., A. Costello, M. E. Lidstrom, and J. C. Murrell. 1995. Evidence that participate methane monooxygenase and ammonia monooxygenase may be evolutionarily related. FEMS Microbiol. Lett. 132:203-208.
20. Holmes, A. J., N. A. Tujula, M. Holley, A. Contos, J. M. James, P. Rogers, and M. R. Gillings. 2001. Phylogenetic structure of unusual aquatic microbial formations in Nullarbor caves, Australia. Environ. Microbiol. 3:256-264.
21. Hutchens, E., S. Radajewski, M. G. Dumont, I. R. McDonald, and J. C. Murrell. 2004. Analysis of methanotrophic bacteria in Movile cave by stable isotope probing. Environ. Microbiol. 6:111-120.
22. Jurgens, G., F.-O. Glockner, R. Amann, A. Saano, L. Montonen, M. Likolammi, and U. Munster. 2000. Identification of novel archaea in bacterioplankton of a boreal forest lake by phylogenetic analysis and fluorescent in situ hybridization. FEMS Microbiol. Ecol. 34:45-56.
23. Kemnitz, D., S. Kolb, and R. Conrad. 2007. High abundance of Crenarchaeota in a temperate acidic forest soil. FEMS Microbiol. Ecol. 60:442-448.
24. Kimura, H., M. Sugihara, H. Yamamoto, B. K. C. Patel, K. Kato, and S. Hanada. 2005. Microbial community in a geothermal aquifer associated with the subsurface of the Great Artesian Basin, Australia. Extremophiles 9:407-414.
25. 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.
26. Kowalchuk, G. A., J. R. Stephen, W. De Boer, J. I. Prosser, M. T. Embley, and J. W. Woldendorp. 1997. Analysis of ammonia-oxidizing bacteria of the - subdivision of the class Proteobacteria in coastal sand dunes by denaturing gradient gel electrophoresis and sequencing of PCR-amplified 16S ribosomal DNA fragments. Appl. Environ. Microbiol. 63:1489-1497.
27. 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. USA 104:7104-7109.
28. Larsen, N., G. J. Olsen, B. L. Maidak, M. J. McCaughey, R. Overbeek, T. J. Macke, T. L. Marsh, and C. R. Woese. 1993. The ribosomal data base project. Nucleic Acids Res. 21:3021-3023.
29. 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.
30. Macalady, J. L., D. S. Jones, and E. H. Lyon. 2007. Extremely acidic, pendulous cave wall biofilms from the Frasassi cave system, Italy. Environ. Microbiol. 9:1402-1414.
31. Macalady, J. L., E. H. Lyon, B. Koffman, L. K. Albertson, K. Meyer, S. Galdenzi, and S. Mariani. 2006. Dominant microbial populations in limestone-corroding stream biofilms, Frasassi cave system, Italy. Appl. Environ. Microbiol. 72:5596-5609.
32. Massana, R., A. E. Murray, C. M. Preston, and E. F. DeLong. 1997. Vertical distribution and phylogenetic characterization of marine planktonic archaea in the Santa Barbara channel. Appl. Environ. Microbiol. 63:50-56.
33. Meisinger, D. B., J. Zimmermann, W. Ludwig, K.-H. Schleifer, G. Wanner, M. Schmid, P. C. Bennett, A. S. Engel, and N. M. Lee. 2007. In situ detection of novel Acidobacteria in microbial mats from a chemolithoautotrophically based cave ecosystem (Lower Kane Cave, WY, USA). Environ. Microbiol. 9:1523-1534.
34. Muyzer, G., E. C. de Waal, and A. G. Uitterlinden. 1993. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 59:695-700.
35. Nicol, G. W., L. A. Glover, and J. I. Prosser. 2003. The impact of grassland management on archaeal community structure in upland pasture rhizosphere soil. Environ. Microbiol. 5:152-162.
36. Northup, D. E., S. M. Barns, L. E. Yu, M. N. Spilde, R. T. Schelble, K. E. Dano, L. J. Crossey, C. A. Connolly, P. J. Bosten, D. O. Natvig, and C. N. Dahm. 2003. Diverse microbial communities inhabiting ferromanganese deposits in Lechuguilla and Spider caves. Environ. Microbiol. 5:1071-1086.
37. Northup, D. E., and K. H. Lavoie. 2001. Geomicrobiology of caves: a review. Geomicrobiol. J. 18:199-222.
38. Ollier, C., and C. Pain. 2000. The origin of mountains. Routledge, London, United Kingdom.
39. Øvreås, L., L. Forney, F. L. Daae, and V. Torsvik. 1997. Distribution of bacterioplankton in meromictic Lake Saelenvannet, as determined by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA. Appl. Environ. Microbiol. 63:3367-3373.
40. 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.
41. Reigstad, L. J., A. Richter, H. Daims, T. Urich, L. Schwark, and C. Schleper. 2008. Nitrification in terrestrial hot springs of Iceland and Kamchatka. FEMS Microbiol. Ecol. 64:167-174.
42. 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.
43. Schaefer, D. M., C. L. Davis, and M. P. Bryant. 1980. Ammonia saturation constants for predominant species of rumen bacteria. J. Dairy Sci. 63:1248-1263.
44. Simon, H. M., C. E. Jahn, L. T. Bergerud, M. K. Sliwinski, P. J. Weimer, D. K. Willis, and R. M. Goodman. 2005. Cultivation of mesophilic soil crenarchaeotes in enrichment cultures from plant roots. Appl. Environ. Microbiol. 71:4751-4760.
45. 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.
46. Stahl, D. A., and R. I. Amann. 1991. Development and application of nucleic acid probes in bacterial systematics, p. 205-248. In E. Stackebrandt and M. Goodfellow (ed.), Sequencing and hybridization techniques in bacterial systematics. John Wiley & Sons, Chichester, England.
47. Takai, K., D. P. Moser, M. DeFlaun, T. C. Onstott, and J. K. Fredrickson. 2001. Archaeal diversity in waters from deep South African gold mines. Appl. Environ. Microbiol. 67:5750-5760.
48. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:4876-4882.
49. 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.
50. 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.
51. Whitman, W. B., D. C. Coleman, and W. J. Wiebe. 1998. Prokaryotes: the unseen majority. Proc. Natl. Acad. Sci. USA 95:6578-6583.
52. Wuchter, C., B. Abbas, M. J. L. Coolen, L. Herfort, J. van Bleijswijk, P. Timmers, M. Strous, E. Teira, G. J. Herndl, J. J. Middelburg, S. Schouten, and J. S. Sinninghe Damste. 2006. Archaeal nitrification in the ocean. Proc. Natl. Acad. Sci. USA 103:12317-12322.
53. Xu, Y., and N. Glansdorff. 2007. Lessons from extremophiles: early evolution and border conditions of life, p. 409-421. In C. Gerday and N. Glansdorff (ed.), Physiology and biochemistry of extremophiles. ASM Press, Washington, DC.
54. Zhou, J., Y. Gu, C. Zou, and M. Mo. 2007. Phylogenetic diversity of bacteria in an earth-cave in Guizhou province, southwest of China. J. Microbiol. 45:105-112.