Archaeal dominated ammonia-oxidizing communities in Icelandic grassland soils are moderately affected by long-term N fertilization and geothermal heating

Frontiers in Microbiology

Volumn 3, Issue OCT, 2012, Pages

  Daebeler, Anne ^a,b   Abell, Guy C J ^c   Bodelier, Paul L E ^a   Bodrossy, Levente ^c   Frampton, Dion M F ^c   Hefting, Mariet M ^b   Laanbroek, Hendrikus J ^a,b  

^a NETHERLANDS INSTITUTE OF ECOLOGY NIOO KNAW   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

^c CSIRO   (Australia)

Author keywords

Ammonia oxidizing archaea; Ammonia oxidizing bacteria; AmoA; Fertilization; Grassland soil; Niche formation; Temperature

Indexed keywords

EID: 84875830795     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2012.00352     Document Type: Article

References (58)

1. Adair, K., and Schwartz, E. (2011). "Stable isotope probing with 18Owater to investigate growth and mortality of ammonia oxidizing bacteria and archaea in soil," in Methods Enzymol, ed G. K. Martin (Burlington MA: Academic Press), 155-169
2. Alves, R. J. E. (2011). AmmoniaOxidizing Archaea from High Artic Soils. M.Sc. thesis, University of Lisbon, Repository. http://hdl.handle.net/10451/4027
3. Avrahami, S., Jia, Z., Neufeld, J. D., Murrell, J. C., Conrad, R., and Kusel, K. (2011). Active autotrophic ammonia-oxidizing bacteria in biofilm enrichments from simulated creek ecosystems at two ammonium concentrations respond to temperature manipulation. Appl.Environ.Microbiol.77, 7329-7338
4. Banerjee, S., and Siciliano, S. D. (2012). Factors driving potential ammonia oxidation in Canadian arctic ecosystems: does spatial scale matter? Appl. Environ. Microbiol. 78, 346-353
5. Bonheyo,G.,Frias-Lopez,J.,and Fouke, B. (2005). "A test for airborne dispersal of thermophilic bacteria from hot springs," in Geothermal Biology and Geochemistry in Yellowstone National Park. Proceedings of the Thermal Biology Institute Workshop, eds W. P. Inskeep and T. R. Mcdermott (Montana State University Publications), 327-340. http://www.geology.illinois.edu/people/fouke/Sites/Fouke_2006_MSU_ Aerosol.pdf
6. Boyle-Yarwood, S. A., Bottomley, P. J., and Myrold, D. D. (2008). Community composition of ammonia-oxidizing bacteria and archaea in soils under stands of red alderandDouglasfirinOregon. Environ. Microbiol. 10, 2956-2965
7. Chen, X., Zhang, L.-M., Shen, J.-P., Wei, W.-X., and He, J.-Z. (2011). Abundance and community structure of ammonia-oxidizing archaea and bacteria in an acid paddy soil. Biol. Fert. Soils 47, 323-331
8. Di, H. J., Cameron, K. C., Shen, J. P., Winefield, C. S., O'Callaghan, M., Bowatte, S., et al. (2009). Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nat. Geosci. 2, 621-624
9. Di, H. J., Cameron, K. C., Shen, J.-P., Winefield, C. S., O'Callaghan, M., Bowatte, S., et al. (2010). Ammoniaoxidizing bacteria and archaea grow under contrasting soil nitrogen conditions. FEMS Microbiol. Ecol. 72, 386-394
10. Ellis, D. G., Bizzoco, R. W., and Kelley, S. T. (2008). Halophilic Archaea determined from geothermal steam vent aerosols. Environ. Microbiol. 10, 1582-1590
11. Enwall, K., Nyberg, K., Bertilsson, S., Cederlund, H., Stenström, J., and Hallin, S. (2007). Long-term impact of fertilization on activity and composition of bacterial communities and metabolic guilds in agricultural soil. Soil Biol. Biochem. 39, 106-115
12. Erguder, T. H., Nico, B., Lieven, W., Massimo, M., and Willy, V. (2009). Environmental factors shaping the ecological niches of ammoniaoxidizing archaea. FEMS Microbiol. Rev. 33, 855-869
13. Fan,F.L.,Yang,Q.B.,Li,Z.J., Wei,D.,Cui,X.,andLiang,Y.C. (2011). Impacts of organic and inorganic fertilizers on nitrification in a cold climate soil are linked to the bacterial ammonia oxidizer community. Microb. Ecol. 62, 982-990
14. Fierer, N., Carney, K., Horner-Devine, M., and Megonigal, J. (2009) The biogeography of ammoniaoxidizing bacterial communities in soil. Microb. Ecol. 58, 435-445
15. 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. U.S.A. 102, 14683-14688
16. Gubry-Rangin, C., Hai, B., Quince, C., Engel,M.,Thomson,B.C.,James, P., et al. (2011). Niche specialization of terrestrial archaeal ammonia oxidizers. Proc. Natl. Acad. Sci. U.S.A. 108, 21206-21211
17. Hallin, S., Jones, C. M., Schloter, M., and Philippot, L. (2009). Relationship between N-cycling communities and ecosystem functioning in a 50-year-old fertilization experiment. ISME J. 3, 597-605
18. He, J.-Z., Ju-Pei, S., Li-Mei, Z., Yong-Guan, Z., Yuan-Ming, Z., Ming-Gang, X., et al. (2007). Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices. Environ. Microbiol. 9, 2364-2374
19. Holmes, A. J., Costello, A., Lidstrom, M. E., and Murrell, J. C. (1995). Evidence that participate methane monooxygenase and ammonia monooxygenase may be evolutionarily related. FEMS Microbiol. Lett. 132, 203-208
20. Hornek, R., Pommerening-Röser, A., Koops, H.-P., Farnleitner, A. H., Kreuzinger, N., Kirschner, A., et al. (2006). Primers containing universal bases reduce multiple amoA gene specific DGGE band patterns when analysing the diversity of beta-ammonia oxidizers in the environment. J. Microbiol. Methods 66, 147-155
21. Horz, H.-P., Barbrook, A., Field, C. B., and Bohannan, B. J. M. (2004). Ammonia-oxidizing bacteria respond to multifactorial global change. Proc. Natl. Acad. Sci. U.S.A. 101, 15136-15141
22. Ijichi, M., and Hamasaki, K. (2011). Community structure of ammoniaoxidizing marine archaea differs by depth of collection and temperature of cultivation. J. Oceanogr. 67, 739-745
23. Jung, J., Yeom, J., Kim, J., Han, J., Lim, H. S., Park, H., et al. (2011). Change in gene abundance in the nitrogen biogeochemical cycle with temperature and nitrogen addition in Antarctic soils. Res. Microbiol. 162, 1018-1026
24. Kelly, J. J., Policht, K., Grancharova, T., and Hundal, L. S. (2011). Distinct responses in ammonia-oxidizing archaea and bacteria after addition of biosolids to an agricultural soil. Appl.Environ.Microbiol.77, 6551-6558
25. Kowalchuk,G.A.,Stephen,J.R.,De Boer,W.,Prosser,J.I.,Embley,T. M., and Woldendorp, J. W. (1997). Analysis of ammonia-oxidizing bacteria of the beta 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
26. Lamb, E. G., Han, S., Lanoil, B. D., Henry, G. H. R., Brummell, M. E., Banerjee, S., et al. (2011). A high Arctic soil ecosystem resists longterm environmental manipulations. Global Change Biol. 17, 3187-3194.
27. Leininger, S., Urich, T., Schloter, M., Schwark,L.,Qi,J.,Nicol,G.W., et al. (2006). Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442, 806-809
28. Levicnik-Hofferle,S.,Nicol,G.W., Ausec, L., Mandic-Mulec, I., and Prosser, J. I. (2012). Stimulation of thaumarchaeal ammonia oxidation by ammonia derived from organic nitrogen but not added inorganic nitrogen. FEMS Microbiol. Ecol. 80, 114-123
29. Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Yadhukumar, et al. (2004). ARB: a software environment for sequence data. Nucl. Acids Res. 32, 1363-1371
30. Lueders, T., Manefield, M., and Friedrich, M. W. (2004). Enhanced sensitivity of DNAand rRNAbased stable isotope probing by fractionation and quantitative analysis of isopycnic centrifugation gradients. Environ. Microbiol. 6, 73-78
31. McCaig,A.E.,Embley,T.M.,and Prosser, J. I. (1994). Molecular analysis of enrichment cultures of marine ammonia oxidisers. FEMS Microbiol. Lett. 120, 363-367
32. Minchin, P. R. (1987). An evaluation of the relative robustness of the techniques for ecological ordination. Vegetatio 69, 89-107
33. Nemergut,D.R.,Townsend,A.R., Sattin, S. R., Freeman, K. R., Fierer, N., Neff, J. C., et al. (2008). The effects of chronic nitrogen fertilization on alpine tundra soil microbial communities: implications for carbon and nitrogen cycling. Environ. Microbiol. 10, 3093-3105
34. Nicol,G.W.,Sven,L.,Christa,S.,and James, I. P. (2008). The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environ. Microbiol. 10, 2966-2978
35. Okano, Y., Hristova, K. R., Leutenegger, C. M., Jackson, L. E., Denison, R. F., Gebreyesus, B., et al. (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
36. Oksanen, J., Blanchet, G., Kindt, R., Legendre, P., O'Hara, R. G., Simpson, G. L., et al. (2010). Vegan: community ecology package. R package version 1. 17-11. Available online at: http://CRAN.R-project.org/package=vegan. [Accessed 2011]
37. Park, B.-J., Park, S.-J., Yoon, D.N., Schouten, S., Sinninghe Damste, J. S., and Rhee, S.-K. (2010). Cultivation of autotrophic ammonia-oxidizing archaea from marine sediments in coculture with sulfur-oxidizing bacteria. Appl.Environ.Microbiol.76, 7575-7587
38. Pester, M., Rattei, T., Flechl, S., Gröngröft, A., Richter, A., Overmann, J. R.-H., et al. (2011). 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
39. Petersen, D. G., Blazewicz, S. J., Firestone, M., Herman, D. J., Turetsky, M., and Waldrop, M. (2012). Abundance of microbial genes associated with nitrogen cycling as indices of biogeochemical process rates across a vegetation gradient in Alaska. Environ. Microbiol. 14, 993-1008
40. R Development Core Team. (2011). R: A Language and Environment for Statistical Computing. 2.13.1 ed. Vienna, Australia: R Foundation for Statistical Computing
41. 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
42. 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
43. Schleper, C., and Nicol, G. W. (2010). "Ammonia-oxidizing archaea - physiology, ecology, evolution," in Advances in Microbial Physiology. 1 Edn. ed R. K. Poole. (London: Elsevier Ltd.) 1-41
44. Schloss, P. D., Westcott, S. L., Ryabin, T., Hall, J. R., Hartmann, M., Hollister, E. B., et al. (2009). Introducing mothur: opensource, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537-7541
45. Shen, J.-P., Li-Mei, Z., Yong-Guan, Z., Jia-Bao, Z., and Ji-Zheng, H. (2008). Abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea communities of an alkaline sandy loam. Environ. Microbiol. 10, 1601-1611
46. Shen,X.Y.,Zhang,L.M.,Shen,J. P.,Li,L.H.,Yuan,C.L.,and He, J. Z. (2011). Nitrogen loading levels affect abundance and composition of soil ammonia oxidizing prokaryotes in semiarid temperate grassland. J. Soils Sed. 11, 1243-1252
47. Szukics, U., Hackl, E., Zechmeister Boltenstern, S., and Sessitsch, A. (2012). Rapid and dissimilar response of ammonia oxidizing archaea and bacteria to nitrogen and water amendment in two temperate forest soils. Microbiol. Res. 167, 103-109
48. Tourna, M., Freitag, T. E., Nicol, G. W., and Prosser, J. I. (2008). Growth, activity and temperature responses of ammonia-oxidizing archaea and bacteria in soil microcosms. Environ. Microbiol. 10, 1357-1364
49. Treusch, A. H., Leininger, S., Kletzin, A.,Schuster,S.C.,Klenk,H.-P.,and Schleper, C. (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. Verhamme, D. T., Prosser, J. I., and Nicol, G. W. (2011). Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. ISME J. 5, 1067-1071
51. Walker, C. B., de La Torre, J. R., Klotz, M. G., Urakawa, H., Pinel, N., Arp, D. J., et al. (2010). Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea Proc. Natl. Acad. Sci. U.S.A. 107, 8818-8823
52. Weedon, J. T., Kowalchuk, G. A., Aerts, R., Van Hal, J., Van Logtestijn, R. K. S. P., Tas, N., et al. (2012). Summer warming accelerates sub-arctic peatland nitrogen cycling without changing enzyme pools or microbial community structure. Global Change Biol. 18, 138-150
53. Wertz,S.,Leigh,A.K.K.,andGrayston, S. J. (2012). Effects of long-term fertilization of forest soils on potential nitrification and on the abundance and community structure of ammonia oxidizers and nitrite oxidizers. FEMS Microbiol. Ecol. 79, 142-154
54. Wessen, E., Soderstrom, M., Stenberg, M., Bru, D., Hellman, M., Welsh, A., et al. (2011). Spatial distribution of ammonia-oxidizing bacteria and archaea across a 44-hectare farm related to ecosystem functioning. ISME J. 5, 1213-1225
55. Yao, H., Gao, Y., Nicol, G. W., Campbell, C. D., Prosser, J. I., Zhang, L., et al. (2011). Links between ammonia oxidizer community structure, abundance, and nitrification potential in acidic soils. Appl.Environ.Microbiol.77, 4618-4625
56. Yergeau, E., Hogues, H., Whyte, L. G., and Greer, C. W. (2010). The functional potential of high Arctic permafrost revealed by metagenomic sequencing, qPCR and microarray analyses. ISME J. 4, 1206-1214
57. Zhang, L.-M., Hu, H.-W., Shen, J.-P., and He, J.-Z. (2012). Ammoniaoxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils. ISME J. 6, 1032-1045
58. Zhang, L.-M., Wang, M., Prosser, J. I., Zheng, Y.-M., and He, J.-Z. (2009). Altitude ammonia-oxidizing bacteria and archaea in soils of Mount Everest. FEMS Microbiol. Ecol. 70, 52-61