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Temporal changes in abundance and composition of ammonia-oxidizing bacterial and archaeal communities in a drained peat soil in relation to N2O emissions

  • SOILS, SEC 5 • SOIL AND LANDSCAPE ECOLOGY • RESEARCH ARTICLE
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Abstract

Purpose

Boreal peat soils comprise about 3% of the terrestrial environments, and when drained, they become sources of the greenhouse gas nitrous oxide (N2O). Ammonia oxidation can result in N2O emissions, either directly or by fuelling denitrification, but we know little about the ecology of ammonia-oxidizing bacteria (AOB) and archaea (AOA) in peat soils. Our aim was to determine temporal alterations in abundance and composition of these communities in a drained and forested peat soil in relation to N2O emissions and ammonia oxidation activity.

Materials and methods

The peat was sampled at three different depths in the upper 0.5 m over a period of 9 months covering two summer and two winter samplings. Community composition and abundance were determined by T-RFLP and quantitative real-time PCR of the bacterial and archaeal amoA genes. Potential ammonia oxidation rates were measured using the chlorate inhibition technique, and in situ N2O emission was determined using chambers.

Results and discussion

The soil parameters displayed little spatial and temporal heterogeneity, which probably explained why there were no depth-related effects on the abundance, composition, or activity of the ammonia oxidizers. In contrast to most terrestrial environments, the AOB dominated numerically over the AOA. Both groups changed in community composition between sampling occasions, although the AOB showed more significant seasonal signatures than the AOA. Temporal changes in abundance were only observed for the AOB, with a decrease in numbers from May to March. Such differences were not reflected by the activity or N2O emissions.

Conclusions

The high ammonium concentrations in the peat soil likely favored the AOB over the AOA, and we hypothesize that they were more active than the AOA and therefore responded to climatic and environmental changes. However, other processes rather than ammonia oxidation were likely responsible for N2O emissions at the site.

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References

  • Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46

    Google Scholar 

  • Bardgett RD, Lovell RD, Hobbs PJ, Jarvis SC (1999) Seasonal changes in soil microbial communities along a fertility gradient of temperate grasslands. Soil Biol Biochem 31:1021–1030

    Article  CAS  Google Scholar 

  • Belser LW, Mays EL (1980) Specific inhibition of nitrite oxidation by chlorate and its use in assessing nitrification in soils and sediments. Appl Environ Microbiol 39:505–510

    CAS  Google Scholar 

  • Berg P, Rosswall T (1985) Ammonium oxidizer numbers, potential and actual oxidation rates in two Swedish arable soils. Biol Fertil Soils 1:131–140

    Article  CAS  Google Scholar 

  • Berg P, Rosswall T (1987) Seasonal variations in abundance and activity of nitrifiers in four arable cropping systems. Microb Ecol 13:75–87

    Article  Google Scholar 

  • Bohrerova Z, Stralkova R, Podesvova J, Bohrer G, Pokorny E (2004) The relationship between redox potential and nitrification under different sequences of crop rotations. Soil Till Res 77:25–33

    Article  Google Scholar 

  • Boyle-Yarwood SA, Bottomley PJ, Myrold DD (2008) Community composition of ammonia-oxidizing bacteria and archaea in soils under stands of red alder and Douglas fir in Oregon. Environ Microbiol 10:2956–2965

    Article  CAS  Google Scholar 

  • Bremner JM, Breitenbeck GA, Blackmer AM (1981) Effect of anhydrous ammonia fertilization on emission of nitrous oxide from soils. J Environ Qual 10:77–80

    Article  CAS  Google Scholar 

  • Caffrey JM, Bano N, Kalanetra K, Hollibaugh JT (2007) Ammonia oxidation and ammonia-oxidizing bacteria and archaea from estuaries with differing histories of hypoxia. ISME J 1:660–662

    Article  Google Scholar 

  • Di HJ, Cameron KC, Shen JP, Winefield CS, O’Callaghan M, Bowatte S, He JZ (2009) Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nature Geosci 2:621–624

    Article  CAS  Google Scholar 

  • Di HJ, Cameron KC, Sherlock RR, Shen JP, He JZ, Winefield CS (2010a) Nitrous oxide emissions from grazed grassland as affected by a nitrification inhibitor, dicyandiamide, and relationships with ammonia-oxidizing bacteria and archaea. J Soils Sediments 10:943–954

    Article  CAS  Google Scholar 

  • Di HJ, Cameron KC, Shen JP, Winefield CS, O’Callaghan M, Bowatte S, He JZ (2010b) Ammonia-oxidizing bacteria and archaea grow under contrasting soil nitrogen conditions. FEMS Microbiol Ecol 72:386–394

    Article  CAS  Google Scholar 

  • Erguder TH, Boon N, Wittebolle L, Marzorati M, Verstraete W (2009) Environmental factors shaping the ecological niches of ammonia-oxidizing archaea. FEMS Microbiol Rev 33:855–869

    Article  CAS  Google Scholar 

  • Gorham E (1991) Northern peatlands: role in the carbon cycle and probable responses to climatic warming. Ecol Appl 1:182–195

    Article  Google Scholar 

  • Hallin S, Jones CM, Schloter M, Philippot L (2009) Relationship between N-cycling communities and ecosystem functioning in a 50-year-old fertilization experiment. ISME J 3:597–605

    Article  CAS  Google Scholar 

  • He JZ, Shen JP, Zhang LM, Zhu YG, Zheng YM, Xu MG, Di H (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

    Article  CAS  Google Scholar 

  • Hermansson A, Bäckman JSK, Svensson BH, Lindgren P-E (2004) Quantification of ammonia-oxidizing bacteria in limed and non-limed acidic coniferous forest soil using real-time PCR. Soil Biol Biochem 36:1935–1941

    Article  CAS  Google Scholar 

  • Hochberg Y (1988) A sharper Bonferroni procedure for multiple tests of significance. Biomet 75:800–802

    Article  Google Scholar 

  • Höfferle S, Nicil G, Pal L, Hacin J, Prosser JI, Mandic-Mulec I (2010) Ammonium supply rate influences archaeal and bacterial ammonia oxidisers in a wetland soil vertical profile. FEMS Microbiol Ecol 74:302–315

    Article  Google Scholar 

  • Jia Z, Conrad R (2009) Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil. Environ Microbiol 11:1658–1671

    Article  CAS  Google Scholar 

  • Kasimir-Klemedtsson Å, Klemedtsson L, Berglund K, Martikainen P, Silvola J, Oenema O (1997) Greenhouse gas emissions from farmed organic soils: a review. Soil Use Manage 13:245–250

    Article  Google Scholar 

  • Killham K (1987) A new perfusion system for the measurement and characterization of potential rates of soil nitrification. Plant Soil 97:267–272

    Article  CAS  Google Scholar 

  • Koops H-P, Purkhold U, Pommerening-Röser A, Timmermann G, Wagner M (2006) The lithoautotrophic ammonia-oxidizing bacteria. The Prokaryotes 5:778–811

    Article  Google Scholar 

  • Kowalchuk GA, Stephen JR (2001) Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annu Rev Microbiol 55:485–529

    Article  CAS  Google Scholar 

  • Laverman AM, Zoomer HR, van Verseveld HW, Verhoef HA (2000) Temporal and spatial variation of nitrogen transformations in a coniferous forest soil. Soil Biol Biochem 32:1661–1670

    Article  CAS  Google Scholar 

  • Laverman A, Speksnijder A, Braster M, Kowalchuk G, Verhoef H, van Verseveld H (2001) Spatiotemporal stability of an ammonia-oxidizing community in a nitrogen-saturated forest soil. Microb Ecol 42:35–45

    CAS  Google Scholar 

  • Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC, Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806–809

    Article  CAS  Google Scholar 

  • Lipson DA, Schmidt SK (2004) Seasonal changes in an alpine soil bacterial community in the Colorado Rocky Mountains. Appl Environ Microbiol 70:2867–2879

    Article  CAS  Google Scholar 

  • Maljanen M, Hytönen J, Martikainen PJ (2001) Fluxes of N2O, CH4 and CO2 on afforested boreal agricultural soils. Plant Soil 231:113–121

    Article  CAS  Google Scholar 

  • Martens-Habbena W, Berube PM, Urakawa H, de la Torre JR, Stahl DA (2009) Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature 461:976–U234

    Article  CAS  Google Scholar 

  • Martikainen PJ (1985) Nitrous oxide emission associated with autotrophic ammonium oxidation in acid coniferous forest soil. Appl Environ Microbiol 50:1519–1525

    CAS  Google Scholar 

  • Martikainen PJ, de Boer W (1993) Nitrous oxide production and nitrification in acidic soil from a Dutch coniferous forest. Soil Biol Biochem 25:343–347

    Article  CAS  Google Scholar 

  • Mertens J, Broos K, Wakelin SA, Kowalchuk GA, Springael D, Smolders E (2009) Bacteria, not archaea, restore nitrification in a zinc-contaminated soil. ISME J 3:916–923

    Article  CAS  Google Scholar 

  • Mørkved PT, Dörsch P, Bakken LR (2007) The N2O product ratio of nitrification and its dependence on long-term changes in soil pH. Soil Biol Biochem 39:2048–2057

    Article  Google Scholar 

  • Nicol GW, Leininger S, Schleper C, Prosser JI (2008) The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environ Microbiol 10:2966–2978

    Article  CAS  Google Scholar 

  • Nykanen H, Alm J, Lang K, Silvola J, Martikainen PJ (1995) Emissions of CH4, N2O and CO2 from a virgin fen and a fen drained for grassland in Finland. J Biogeography 22:351–357

    Article  Google Scholar 

  • Offre PR, Prosser JI, Nicol GW (2009) Growth of ammonia-oxidizing archaea in soil microcosms is inhibited by acetylene. FEMS Microbiol Ecol 70:99–108

    Article  CAS  Google Scholar 

  • Oksanen J, Kindt R, Legendre P, O’Hara B, Simpson GL, Solymos P, Stevens MHH, Wagner H (2009) Vegan: community ecology package. R package version 1.16-12. http://vegan.r-forge.r-project.org/. Accessed Feb 2009

  • Rasche F, Knapp D, Kaiser C, Koranda M, Kitzler B, Zechmeister-Boltenstern S, Richer A, Sessitsch A (2010) Seasonality and resource availability control bacterial and archaeal communities in soils of a temperate beech forest. ISME J 5:389–402

    Article  Google Scholar 

  • Ravishankara AR, Daniel JS, Portmann RW (2009) Nitrous oxide (N2O): the dominant ozone-depleting substance emitted in the 21st century. Science 326:123–125

    Article  CAS  Google Scholar 

  • Reay DS, Nedwell DB, McNamara N, Ineson P (2005) Effect of tree species on methane and ammonium oxidation capacity in forest soils. Soil Biol Biochem 37:719–730

    Article  CAS  Google Scholar 

  • Regina K, Nykänen H, Silvola J, Martikainen P (1996) Fluxes of nitrous oxide from boreal peatlands as affected by peatland type, water table level and nitrification capacity. Biogeochem 35:401–418

    Article  CAS  Google Scholar 

  • Regina K, Syväsalo E, Hannukkala A, Esala M (2004) Fluxes of N2O from farmed peat soils in Finland. Europ J Soil Sci 55:591–599

    Article  CAS  Google Scholar 

  • Rotthauwe JH, Witzel KP, 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

    CAS  Google Scholar 

  • Sahan E, Muyzer G (2008) Diversity and spatio-temporal distribution of ammonia-oxidizing Archaea and Bacteria in sediments of the Westerschelde estuary. FEMS Microbiol Ecol 64:175–186

    Article  CAS  Google Scholar 

  • Santoro AE, Francis CA, de Sieyes NR, Boehm AB (2008) Shifts in the relative abundance of ammonia-oxidizing bacteria and archaea across physicochemical gradients in a subterranean estuary. Environ Microbiol 10:1068–1079

    Article  CAS  Google Scholar 

  • Schleper C, Nicol GW (2010) Ammonia-oxidising archaea—physiology, ecology and evolution. In: Pool RK (ed) Advances in microbial physiology, vol 57. Academic, Oxford, pp 1–41

    Google Scholar 

  • Schuster M, Conrad R (1992) Metabolism of nitric oxide and nitrous oxide during nitrification and denitrification in soil at different incubation conditions. FEMS Microbiol Lett 101:133–143

    Article  CAS  Google Scholar 

  • Shen JP, Zhang LM, Zhu YG, Zhang JB, He JZ (2008) Abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea communities of an alkaline sandy loam. Environ Microbiol 10:1601–1611

    Article  CAS  Google Scholar 

  • Smit E, Leeflang P, Gommans S, van den Broek J, van Mil S, Wernars K (2001) Diversity and seasonal fluctuations of the dominant members of the bacterial soil community in a wheat field as determined by cultivation and molecular methods. Appl Environ Microbiol 67:2284–2291

    Article  CAS  Google Scholar 

  • Stralis-Pavese N, Sessitsch A, Weilharter A, Reichenauer T, Riesing J, Csontos J, Murrell CJ, Bodrossy L (2004) Optimization of diagnostic microarray for application in analysing landfill methanotroph communities under different plant covers. Environ Microbiol 6:347–363

    Article  CAS  Google Scholar 

  • Swensen B, Bakken LR (1998) Nitrification potential and urease activity in a mineral subsoil. Soil Biol Biochem 30:1333–1341

    Article  CAS  Google Scholar 

  • Torstensson L (ed) (1993) Guidelines—soil biological variables in environmental hazard assessment. Swedish Environmental Protection Agency report no. 4262. Swedish EPA, Stockholm

    Google Scholar 

  • Tourna M, Freitag TE, Nicol GW, Prosser JI (2008) Growth, activity and temperature responses of ammonia-oxidizing archaea and bacteria in soil microcosms. Environ Microbiol 10:1357–1364

    Article  CAS  Google Scholar 

  • Tourna M, Stieglmeier M, Spang A, Könneke M, Schintlmeister A, Urich T, Engel M, Schloter M, Wagner M, Richter A, Schleper C (2011) Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proc Natl Acad Sci USA 108:8420–8425

    Article  CAS  Google Scholar 

  • Wells GF, Park HD, Yeung CH, Eggleston B, Francis CA, Criddle CS (2009) Ammonia-oxidizing communities in a highly aerated full-scale activated sludge bioreactor: betaproteobacterial dynamics and low relative abundance of Crenarchaea. Environ Microbiol 11:2310–2328

    Article  CAS  Google Scholar 

  • Weslien P, Klemedtsson ÅK, Börjesson G, Klemedtson L (2009) Strong pH influence on N2O and CH4 fluxes from forested organic soils. EurJ Soil Sci 60:311–320

    Article  CAS  Google Scholar 

  • Wessén E, Nyberg K, Jansson JK, Hallin S (2010) Responses of bacterial and archaeal ammonia oxidizers to soil organic and fertilizer amendments under long-term management. Appl Soil Ecol 45:193–200

    Article  Google Scholar 

  • Wessén E, Söderström M, Stenberg B, Hellman M, Thomsen F, Klemedtson L, Philippot L, Hallin S (2011) Spatial distribution of ammonia oxidizing bacteria and archaea across a 44-hectare farm related to ecosystem functioning. ISME J 5(7):1213–1225

    Article  Google Scholar 

  • Zhang LM, Offre PR, He JZ, Verhamme DT, Nicol GW, Prosser JI (2010) Autotrophic ammonia oxidation by soil thaumarchaea. Proc Natl Acad Sci USA 107:17240–17245

    Article  CAS  Google Scholar 

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Acknowledgments

We thank C. Jones for statistical help. The Swedish University of Agricultural Sciences, The Swedish Research Council Formas financing the Uppsala Microbiomics Center, and the METHECO project (European Science Foundation) provided funding.

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Correspondence to Sara Hallin.

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Responsible editor: Ji-Zheng He

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Andert, J., Wessén, E., Börjesson, G. et al. Temporal changes in abundance and composition of ammonia-oxidizing bacterial and archaeal communities in a drained peat soil in relation to N2O emissions. J Soils Sediments 11, 1399–1407 (2011). https://doi.org/10.1007/s11368-011-0413-9

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