Rapid and dissimilar response of ammonia oxidizing archaea and bacteria to nitrogen and water amendment in two temperate forest soils

Microbiological Research

Volumn 167, Issue 2, 2012, Pages 103-109

  Szukics, Ute ^a   Hackl, Evelyn ^a   Zechmeister Boltenstern, Sophie ^b   Sessitsch, Angela ^a  

^a AIT AUSTRIAN INSTITUTE OF TECHNOLOGY   (Austria)

^b UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

Author keywords

AmoA; AOA; AOB; Forest soil; Nitrification; Nitrogen amendment; Soil moisture

Indexed keywords

AMMONIA OXIDATION; AMMONIA OXIDIZING BACTERIA; AMOA; AOA; AOB; ARCHAEA; ARCHAEAL; BIOCHEMICAL PROCESS; COMMUNITY COMPOSITION; ENVIRONMENTAL FACTORS; FOREST SOILS; MICROBIAL COMMUNITIES; NITRIFICATION RATES; PHYLOGENETIC GROUPS; QUANTITATIVE PCR; SOIL MICRO-ORGANISMS; SOIL NITROGEN; TEMPERATE FORESTS; WATER-FILLED PORE SPACE;

AMMONIA; BACTERIA; DENITRIFICATION; NITRIFICATION; NITROGEN; OXIDATION; POLYMERASE CHAIN REACTION; SOIL MOISTURE;

FORESTRY;

AMMONIA; AMMONIA MONOOXYGENASE; ARCHAEAL DNA; BACTERIAL DNA; NITRATE; NITROGEN; OXIDOREDUCTASE; WATER;

ABUNDANCE; AMMONIA; BACTERIUM; BIOCHEMICAL COMPOSITION; COMMUNITY COMPOSITION; FOREST SOIL; MICROBIAL COMMUNITY; NITRIFICATION; NITROGEN CYCLE; PHYLOGENETICS; PRISTINE ENVIRONMENT; PROKARYOTE; SOIL MICROORGANISM; SOIL MOISTURE; SOIL NITROGEN; TEMPERATE FOREST;

ARCHAEBACTERIUM; ARTICLE; BACTERIUM; BIOTA; DNA FINGERPRINTING; GENETICS; METABOLISM; MICROBIOLOGY; NITRIFICATION; OXIDATION REDUCTION REACTION; REAL TIME POLYMERASE CHAIN REACTION; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; TREE;

AMMONIA; ARCHAEA; BACTERIA; BIOTA; DNA FINGERPRINTING; DNA, ARCHAEAL; DNA, BACTERIAL; NITRATES; NITRIFICATION; NITROGEN; OXIDATION-REDUCTION; OXIDOREDUCTASES; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; REAL-TIME POLYMERASE CHAIN REACTION; SOIL MICROBIOLOGY; TREES; WATER;

AMMONIA; BACTERIA; FORESTS; MICROORGANISMS; NITRIFICATION; NITROGEN; OXIDATION; SOIL; WATER;

AUSTRIA;

ARCHAEA; BACTERIA (MICROORGANISMS); NITROSOMONADALES;

EID: 84855507357     PISSN: 09445013     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.micres.2011.04.002     Document Type: Article

References (47)

1. Adair K.L., Schwartz E. Evidence that ammonia-oxidizing archaea are more abundant than ammonia-oxidizing bacteria in semiarid soils of Northern Arizona. Microb Ecol 2008, 56:420-426.
2. Avrahami S., Liesack W., Conrad R. Effects of temperature and fertilizer on activity and community structure of soil ammonia oxidizers. Environ Microb 2003, 5:691-705.
3. Belser L.W., Mays E.L. Specific inhibition of nitrite oxidation by chlorate and its use in assessing nitrification in soils and sediments. Appl Environ Microb 1980, 39:505-510.
4. Boyle-Yarwood S.A., Bottomley P.J., Myrold D.D. Community composition of ammonia-oxidizing bacteria and archaea in soils under stands of red alder and Douglas fir in Oregon. Environ Microb 2008, 10:2956-2965.
5. Buckley D.H., Schmidt T.M. The structure of microbial communities in soil and the lasting impact of cultivation. Microb Ecol 2001, 42:11-21.
6. Cavagnaro T.R., Jackson L.E., Hristova K., Scow K.M. Short-term population dynamics of ammonia oxidizing bacteria in an agricultural soil. Appl Soil Ecol 2008, 40:13-18.
7. Ceccherini M.T., Ascher J., Agnelli A., Certini G., Pietramellara G., Piovanelli C., et al. Tree bark and soil ammonia oxidizers: a molecular study on a historical forest of central Italy. Fresenius Environ Bull 2008, 17:882-889.
8. Clarke K.R. Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 1993, 18:117-143.
9. Enwall K., Nyberg K., Bertilsson S., Cederlund H., Stentröm J., Hallin S. Long-term impact of fertilization on activity and composition of bacterial communities and metabolic guilds in agricultural soil. Soil Biol Biochem 2007, 39:106-115.
10. Erguder T.H., Boon N., Wittebolle L., Marzolati M., Verstraete W. Environmental factors shaping the ecological niches of ammonia-oxidizing archaea. FEMS Microb Rev 2009, 33:855-869.
11. Francis C.A., Roberts K.J., Beman J.M., Santoro A.E., Oakley B.B. Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. PNAS 2005, 102:14683-14688.
12. Francis C.A., Beman J.M., Kuypers M.M. New processes and players in the nitrogen cycle: the microbial ecology of anaerobic and archaeal ammonia oxidation. ISME J 2007, 1:19-27.
13. Hackl E., Bachmann G., Zechmeister-Boltenstern S. Microbial nitrogen turnover in soils under different types of natural forest. Forest Ecol Manage 2004, 188:101-112.
14. Hallam S.J., Mincer T.J., Schleper C., Preston C.M., Roberts K.J., Richardson P.M., et al. Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine Crenarchaeota. PLOS Biol 2006, 4:520-536.
15. Hartmann M., Enkerli J., Widmer F. Residual polymerase activity-induced bias in terminal restriction fragment length polymorphism analysis. Environ Microbiol 2007, 9:555-559.
16. Hayden H.L., Drake J., Imhof M., Oxeley A.P.A., Norng S., Mele P.M. The abundance of nitrogen cycle genes amoA and nifH depends on land-uses and soil types in South-Eastern Australia. Soil Biol Biochem 2010, 42:1774-1783.
17. He J., Shen J., Zhang L., Zhu Y., Zheng Y., Xu M., et al. 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 2007, 9:2364-2374.
18. Herndl G.J., Reinthaler T., Teira E., van Aken H., Veth C., Pernthaler A., et al. Contribution of archaea to total prokaryotic production in the deep Atlantic ocean. Appl Environ Microbiol 2005, 71:2303-2309.
19. Jia Z., Conrad R. Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil. Environ Microbiol 2009, 11:1658-1671.
20. Junier P., Junier T., Witzel K.P. TRiFLe, a program for in silico terminal restriction fragment length polymorphism analysis with user-defined sequence sets. Appl Environ Microbiol 2008, 74:6452-6456.
21. Junier P., Molina V., Dorador C., Hadas O., Kim O.S., Junier T., et al. Phylogenetic and functional marker genes to study ammonia-oxidizing microorganisms (AOM) in the environment. Appl Microbiol Biotechnol 2010, 85:425-440.
22. Kenkel N.C., Orloci L. Applying metric and nonmetric multidimensional scaling to some ecological studies: some new results. Ecology 1986, 67:919-928.
23. Kitzler B., Zechmeister-Boltenstern S., Holtermann C., Skiba U., Butterbach-Bahl K. Nitrogen oxides emission from two beech forests subjected to different nitrogen loads. Biogeoscience 2006, 3:293-310.
24. Könneke M., Bernhard A.E., de la Torre J.R., Walker C.B., Waterbury J.B., Stahl D.A. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 2005, 437:543-546.
25. Leininger S., Urich T., Schloter M., Schwark L., Qi J., Nicol G.W., et al. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 2006, 17:806-809.
26. Ludwig W., Strunk O., Westram R., Richter L., Meier H., Yadhukumar, et al. ARB: a software environment for sequence data. Nucleic Acid Res 2004, 32:1363-1371.
27. Mendum T.A., Sockett R.E., Hirsch P.R. Use of molecular and isotopic techniques to monitor the response of autotrophic ammonia-oxidizing populations of the β subdivision of the class proteobacteria in arable soils to nitrogen fertilizer. Appl Environ Microbiol 1999, 65:4155-4162.
28. Mendum T.A., Hirsch P.R. Changes in the population structure of β-group autotrophic ammonia oxidising bacteria in arable soils in response to agricultural practice. Soil Biol Biochem 2002, 34:1479-1485.
29. Minchin P.R. An evaluation of the relative robustness of techniques for ecological ordination. Plant Ecol 1987, 69:89-107.
30. Nicol G.W., Schleper C., Ammonia-oxidising Crenarchaeota: important players in the nitrogen cycle? Trends Microbiol 2006, 14:207-212.
31. Nicol G.W., Campbell C.D., Chapman S.J., Prosser J.I. Afforestation of moorland leads to changes in crenarchaeal community structure. FEMS Microbiol Ecol 2007, 60:51-59.
32. Nicol G.W., Leininger S., Schleper C., Prosser J.I. The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia-oxidizing archaea and bacteria. Environ Microbiol 2008, 10:2966-2978.
33. Okano Y., Hristova K.R., Leutenegger C.M., Jackson L.E., Denison R.F., Gebreyesus B., et al. Application of real-time PCR to study effects of ammonium on population size of ammonia-oxidizing bacteria in soil. Appl Environ Microbiol 2004, 70:1008-1016.
34. Ouverney C.C., Fuhrman J.A. Marine planktonic archaea take up amino acids. Appl Environ Microbiol 2000, 66:4829-4833.
35. Park S.J., Park B.J., Rhee S.K. Comparative analysis of archaeal 16A rRNA and amoA genes to estimate the abundance and diversity of ammonia-oxidizing archaea in marine sediments. Extremophiles 2008, 12:605-615.
36. Prosser J.I., Nicol G.W. Relative contributions of archaea and bacteria to aerobic ammonia oxidation in the environment. Environ Microbiol 2008, 10:2931-2941.
37. Rotthauwe J.H., Witzel K.P., Liesack W. The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl Environ Microbiol 1997, 62:4704-4712.
38. Santoro A.E., Francis C.A., de Sieyes N.R., Boehm A.B. Shifts in the relative abundance of ammonia-oxidizing bacteria and archaea across physicochemical gradients in a subterranean estuary. Environ Microbiol 2008, 10:1068-1079.
39. Schauss K., Focks A., Leininger S., Kotzerke A., Heuer H., Thiele-Bruhn S., et al. Dynamics and functional relevance of ammonia-oxidizing archaea in two agricultural soils. Environ Microbiol 2009, 11:446-456.
40. Schinner F., öhlinger R., Kandeler E., Margesin R. Methods in soil biology 1996, Springer Verlag, Berlin.
41. Shen J.P., Zhang L.M., Zhu Y.J.Z., He J.Z. Abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea communities of an alkaline sandy loam. Environ Microbiol 2008, 10:1601-1611.
42. Shen J.P., He J.Z., Zhang L.M. Effect of ammonium on abundance and community structure of soil ammonia oxidizer in different Chinese soils 2008, vol. 12. International Society for Microbial Ecology - ISME, Cairns.
43. 2O emissions and nirK abundance. Biol Fert Soils 2009, 45:855-863.
44. Szukics U., Abell G.C.J., Hödl V., Mitter B., Sessitsch A., Hackl E., et al. Nitrifiers and denitrifiers respond rapidly to changed moisture and increasing temperature in a pristine forest soil. FEMS Microbiol Ecol 2010, 72:395-406.
45. Treusch A.H., Leininger S., Kletzin A., Schuster S.C., Klenk H.P., Schleper C. Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling. Environ Microbiol 2005, 7:1985-1995.
46. Wuchter C., Abbas B., Coolen M.J.L., Herfort L., van Bleijswijk J., Timmers P., et al. Archaeal nitrification in the ocean. Proc Natl Acad Sci USA 2006, 103:12317-12322.
47. Ying J., Zhang L., He J. Putative ammonia-oxidizing bacteria and archaea in an acidic red soil with different land utilization patterns. Environ Microbiol Rep 2010, 2:304-312.