Predominance of thaumarchaeal ammonia oxidizer abundance and transcriptional activity in an acidic fen

Environmental Microbiology

Volumn 14, Issue 11, 2012, Pages 3013-3025

  Herrmann, Martina ^a   Hädrich, Anke ^a   Küsel, Kirsten ^a  

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIA; RNA 16S; WATER;

ARCHAEAL GENE; ARCHAEON; ARTICLE; BACTERIAL GENE; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIUM; BIODIVERSITY; CHEMISTRY; GENE DOSAGE; GENE EXPRESSION REGULATION; GENETICS; GERMANY; METABOLISM; MICROBIOLOGY; NITRIFICATION; OXIDATION REDUCTION REACTION; PH; PHYSIOLOGY;

AMMONIA; ARCHAEA; BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; BIODIVERSITY; GENE DOSAGE; GENE EXPRESSION REGULATION, ARCHAEAL; GENE EXPRESSION REGULATION, BACTERIAL; GENES, ARCHAEAL; GENES, BACTERIAL; GERMANY; HYDROGEN-ION CONCENTRATION; NITRIFICATION; OXIDATION-REDUCTION; RNA, RIBOSOMAL, 16S; SOIL MICROBIOLOGY; WATER;

ARCHAEA; BACTERIA (MICROORGANISMS); NITROSOSPIRA;

EID: 84867995377     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2012.02882.x     Document Type: Article

References (67)

1. 2O emissions. J Soils Sediments 11: 1399-1407.
2. de Boer, W., and Kowalchuk, G.A. (2001) Nitrification in acid soils: microorganisms and mechanisms. Soil Biol Biochem 33: 853-866.
3. Daims, H., Brühl, A., Amann, R., Schleifer, K.-H., and Wagner, M. (1999) The domain-specific probe EUB338 is insufficient for the detection of all bacteria: development and evalulation of a more comprehensive probe set. Syst Appl Microbiol 22: 434-444.
4. Delong, E.F. (1992) Archaea in coastal marine environments. Proc Natl Acad Sci USA 89: 5685-5689.
5. Dowrick, D.J., Hughes, S., Freeman, C., Lock, M.A., Reynolds, B., and Hudson, J.A. (1999) Nitrous oxide emissions from a gully mire in mid-Wales, UK, under simulated summer drought. Biogeochemistry 44: 151-162.
6. Erguder, T.H., Boon, N., Wittebolle, L., Marzorati, M., and Verstraete, W. (2009) Environmental factors shaping the ecological niches of ammonia-oxidizing archaea. FEMS Microbiol Rev 33: 855-869.
7. Foken, T. (2003) Lufthygienisch-Bioklimatische Kennzeichnung des oberen Egertales. Bayreuther Forum Oekol 100: 1-118.
8. Francis, C.A., Roberts, K.J., Beman, J.M., Santoro, A.E., and Oakley, B.B. (2005) Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc Natl Acad Sci USA 102: 14683-14688.
9. Gaynard, T.J., and Armstrong, W. (1987) Some aspects of internal plant aeration in amphibious habitats. In Plant Life in Aquatic and Amphibious Habitats. Crawford, R.M.M. (ed.). Oxford, UK: Blackwell Scientific Publications, pp. 303-320.
10. Glatzel, S., Forbrich, I., Krüger, C., Lemke, S., and Gerold, G. (2008) Small scale controls of greenhouse gas release under elevated N deposition rates in a restoring peat bog in NW Germany. Biogeosciences 5: 925-935.
11. 2O and NO fluxes and soil concentrations. Global Change Biol 16: 220-233.
12. Grasshoff, K., Ehrhardt, M., and Kremling, K. (1983) Methods of Seawater Analysis, 2nd edn. Weinheim, Germany: Verlag Chemie.
13. Gubry-Rangin, C., Nicol, G.W., and Prosser, J.I. (2010) Archaea rather than bacteria control nitrification in two agricultural acidic soils. FEMS Microbiol Ecol 74: 566-574.
14. Gubry-Rangin, C., Hai, B., Quince, C., Engel, M., Thomson, B.C., James, P., etal. (2011) Niche specialization of terrestrial archaeal ammonia oxidizers. Proc Natl Acad Sci USA 108: 21206-21211.
15. Hamberger, A., Horn, M.A., Dumont, M.G., Murrell, J.C., and Drake, H.L. (2008) Anaerobic consumers of monosaccharides in a moderately acidic fen. Appl Environ Microbiol 74: 3112-3120.
16. Hansel, C.M., Fendorf, S., Jardine, P.M., and Francis, C.A. (2008) Changes in bacterial and archaeal community structure and functional diversity along a geochemically variable soil profile. Appl Environ Microbiol 74: 1620-1633.
17. Hayden, M.J., and Ross, D.S. (2005) Denitrification as a nitrogen removal mechanism in a Vermont Peatland. J Environ Qual 34: 2052-2061.
18. Hefting, M., Clément, J.C., Dowrick, D., Cosandey, A.C., Bernal, S., Cimpian, C., etal. (2004) Water table elevation controls on soil nitrogen cycling in riparian wetlands along a European climatic gradient. Biogeochemistry 67: 113-134.
19. Herrmann, M., Saunders, A.M., and Schramm, A. (2008) Archaea dominate the ammonia-oxidizing community in the rhizosphere of the freshwater macrophyte Littorella uniflora. Appl Environ Microbiol 74: 3279-3283.
20. Herrmann, M., Saunders, A.M., and Schramm, A. (2009) Effect of lake trophic status and rooted macrophytes on diversity and abundance of ammonia-oxidizing prokaryotes in freshwater sediments. Appl Environ Microbiol 75: 3127-3136.
21. Herrmann, M., Scheibe, A., Avrahami, S., and Küsel, K. (2011) Ammonium availability affects the ratio of ammonia-oxidizing bacteria to ammonia-oxidizing archaea in simulated creek ecosystems. Appl Environ Microbiol 77: 1896-1899.
22. Höfferle, S., Nicol, G.W., Pal, L., Hacin, J., Prosser, J.I., and Mandic-Mulec, I. (2010) Ammonium supply rate influences archaeal and bacterial ammonia oxidizers in a wetland soil vertical profile. FEMS Microbiol Ecol 74: 302-315.
23. Klappenbach, J.A., Saxman, P.R., Cole, J.R., and Schmidt, T.M. (2001) rrnDB: the ribosomal RNA operon copy number database. Nucleic Acids Res 29: 181-184.
24. Könneke, 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: 543-546.
25. Kravchenko, I.K. (2002) Methane oxidation in boreal peat soils treated with various nitrogen compounds. Plant Soil 242: 157-162.
26. Küsel, K., Blöthe, M., Schulz, D., Reiche, M., and Drake, H.L. (2008) Microbial reduction of iron and porewater biogeochemistry in acidic peatlands. Biogeosciences 5: 1537-1549.
27. Laanbroek, H.J. (2010) Methane emission from natural wetlands: interplay between emergent macrophytes and soil microbial processes. A mini-review. Ann Bot 105: 141-153.
28. Laverman, A.M., Speksnijder, A.G.C., Braster, M., Kowalchuk, G.A., Verhoef, H.A., and van Verseveld, H.W. (2001) Spatiotemporal stability of an ammonia-oxidizing community in a nitrogen-saturated forest soil. Microb Ecol 42: 35-45.
29. Lee, Z.M., Bussema, C., 3rd, and Schmidt, T.M. (2009) rrnDB: documenting the number of rRNA and tRNA genes in bacteria and archaea. Nucleic Acids Res 37: 489-493.
30. Lehtovirta-Morley, L.E., Stoecker, K., Vilcinskas, A., Prosser, J.I., and Nicol, G.W. (2011) Cultivation of an obligate acidophilic ammonia oxidizer from a nitrifying acid soil. Proc Natl Acad Sci USA 108: 15892-15897.
31. Leininger, S., Urich, T., Schloter, M., Schwark, L., Qi, J., Nicol, G.W., etal. (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442: 806-809.
32. Loy, A., Lehner, A., Lee, N., Adamczyk, J., Meier, H., Ernst, J., etal. (2002) Oligonucleotide microarray for 16S rRNA gene-based detection of all recognized lineages of sulfate-reducing prokaryotes in the environment. Appl Environ Microbiol 68: 5064-5081.
33. Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Kumar, Y., etal. (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363-1371.
34. Manabe, S., and Wetherald, R.T. (1986) Reduction in summer soil wetness induced by an increase in atmospheric carbon dioxide. Science 232: 626-628.
35. Martens-Habbena, W., Berube, P.M., Urakawa, H., de la Torre, J.R., and Stahl, D.A. (2009) Ammonia oxidation kinetics determine niche separation of nitrifying archaea and bacteria. Nature 461: 976-981.
36. Martikainen, P.J., Nykänen, H., Crill, P., and Silvola, J. (1993) Effect of a lowered water table on nitrous oxide fluxes from northern peatlands. Nature 366: 51-53.
37. Mertens, J., Broos, K., Wakelin, S.A., Kowalchuk, G.A., Springael, D., and Smolders, E. (2009) Bacteria, not archaea, restore nitrification in a zinc-contaminated soil. ISME J 3: 916-923.
38. 2 emissions and uptake in a fen in Germany. Ecol Appl 21: 391-401.
39. Muyzer, G., Brinkhoff, T., Nübel, U., Santegoeds, C., Schafer, H., and Wawer, C. (1997) Denaturing gradient gel electrophoresis (DGGE) in microbial ecology. In Molecular Microbial Ecology Manual. Akkermans, A.D.L., van Elsas, J.D., de Bruijn, F.J. (eds). Dordrecht, the Netherlands: Kluwer Academic Publishers, pp. 1-27.
40. Nicol, G.W., Leininger, S., Schleper, C., and Prosser, J.I. (2008) The influence of soil pH on the diversity, abundance, and transcriptional activity of ammonia oxidizing archaea and bacteria. Environ Microbiol 10: 2966-2978.
41. Nicolaisen, M.H., and Ramsing, N.B. (2002) Denaturing gradient gel electrophoresis (DGGE) approaches to study the diversity of ammonia-oxidizing bacteria. J Microbiol Methods 50: 189-203.
42. Olde Venterink, H., Davidsson, T.E., Kiehl, K., and Leonardson, L. (2002) Impact of drying and re-wetting on N, P and K dynamics in a wetland soil. Plant Soil 243: 119-130.
43. Onodera, Y., Nakagawa, T., Takahashi, R., and Tokuyama, T. (2010) Seasonal change in vertical distribution of ammonia-oxidizing archaea and bacteria and their nitrification in temperate forest soil. Microbes Environ 25: 28-35.
44. 2O fluxes of an acidic fen. Appl Environ Microbiol 76: 1125-1134.
45. Pester, M., Schleper, C., and Wagner, M. (2011) The Thaumarchaeota: an emerging view of their phylogeny and ecophysiology. Curr Opin Microbiol 14: 300-306.
46. Pester, M., Rattei, T., Flechi, S., Gröngröft, A., Richter, A., Overmann, J., etal. (2012) amoA-based consensus phylogeny of ammonia-oxidizing archaea and deep sequencing of amoA genes from soils of four different geographic regions. Environ Microbiol 14: 525-539.
47. Pommerening-Röser, A., and Koops, H.-P. (2005) Environmental pH as an important factor for the distribution of urease positive ammonia-oxidizing bacteria. Microbiol Res 160: 27-35.
48. Regina, K., Nykanen, H., Silvola, J., and Martikainen, P.J. (1996) Fluxes of nitrous oxide from boreal peatlands as affected by peatland type, water table level and nitrification capacity. Biogeochemistry 35: 401-418.
49. Reiche, M., Torburg, G., and Küsel, K. (2008) Competition of Fe(III) reduction and methanogenesis in an acidic fen. FEMS Microbiol Ecol 65: 88-101.
50. Reiche, M., Hädrich, A., Lischeid, G., and Küsel, K. (2009) Impact of manipulated drought and heavy rainfall events on peat mineralization processes and source-sink functions of an acidic fen. J Geophys Res 114: G02021.
51. Reigstad, L.J., Richter, A., Daims, H., Urich, T., Schwark, L., and Schleper, C. (2008) Nitrification in terrestrial hot springs of Iceland and Kamchatka. FEMS Microbiol Ecol 64: 167-174.
52. Rooney-Varga, J.N., Giewat, M.W., Duddleston, K.N., Chanton, J.P., and Hines, M.E. (2007) Links between archaeal community structure, vegetation type and methanogenic pathway in Alaskan peatlands. FEMS Microbiol Ecol 60: 240-251.
53. Rotthauwe, J.-H., Witzel, K.-P., and Liesack, W. (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.
54. Roulet, N., Moore, T., Bubier, J., and Lafleur, P. (1992) Northern fens - Methane flux and climatic change. Tellus 44B: 100-105.
55. Schloss, P.D., Westcott, S.L., Ryabin, T., Hall, J.R., Hartmann, M., Hollister, E.B., etal. (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75: 7537-7541.
56. Singleton, D.R., Furlong, M.A., Rathbun, S.L., and Whitman, W.B. (2001) Quantitative comparisons of 16S rRNA gene sequence libraries from environmental samples. Appl Environ Microbiol 67: 4374-4376.
57. Stephen, J.R., Kowalchuk, G.A., Bruns, M.-A.V., McCaig, A.E., Phillips, C.J., Embley, T.M., and Prosser, J.I. (1998) Analysis of beta-subgroup proteobacterial ammonia-oxidizer populations in soil by denaturing gradient gel electrophoresis analysis and hierarchical phylogenetic probing. Appl Environ Microbiol 64: 2958-2965.
58. Stopnisek, N., Gubry-Rangin, C., Höfferle, S., Nicol, G.W., Mandic-Mulec, I., and Prosser, J.I. (2010) Thaumarchaeal ammonia oxidation in an acidic forest peat soil is not influenced by ammonium amendment. Appl Environ Microbiol 76: 7626-7634.
59. Takai, K., and Horikoshi, K. (2000) Rapid detection and quantification of members of the archaeal community by quantitative PCR using fluorogenic probes. Appl Environ Microbiol 66: 5066-5072.
60. Taylor, K., Rowland, A.P., and Jones, H.E. (2001) Molinia caerulea (L.) Moench. J Ecol 89: 126-144.
61. Velghe, N., and Claeys, A. (1985) Rapid spectrophotometric determination of nitrate in mineral waters with resorcinol. Analyst 110: 313-314.
62. Weijers, J.W.H., Schouten, S., van der Linden, M., van Geel, B., and Sinninghe Damsté, J.S. (2004) Water table related variations in the abundance of intact archaeal membrane lipids in a Swedish peat bog. FEMS Microbiol Lett 239: 51-56.
63. Widdel, F., and Bak, F. (1991) Gram-negative mesophilic sulfate-reducing bacteria. In The Prokaryotes, 2nd edn, Vol. 4. Balows, A., Trüper, H.G., Dworkin, M., Harder, W., and Schleifer, K.-H. (eds). New York, NY, USA: Springer, pp. 3352-3378.
64. Williams, R.I., and Wheatley, R.E. (1988) Nitrogen mineralization and water-table height in oligotrophic deep peat. Biol Fertil Soils 6: 141-147.
65. Xu, M., Schnorr, J., Keibler, B., and Simon, H.M. (2012) Comparative analysis of 16S rRNA and amoA genes from archaea selected with organic and inorganic amendments in enrichment culture. Appl Environ Microbiol 78: 2137-2146.
66. Yao, H., Gao, Y., Nicol, G.W., Campbell, C.D., Prosser, J.I., Zhang, L., etal. (2011) Links between ammonia oxidizer community structure, abundance, and nitrification potential in acidic soils. Appl Environ Microbiol 77: 4618-4625.
67. Zhang, L.-M., Hu, H.-W., Shen, J.-P., and He, J.-Z. (2012) Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils. ISME J 6: 1032-1045.