Skip to main content
Log in

Ammonia-oxidizing communities in agricultural soil incubated with organic waste residues

  • Original Paper
  • Published:
Biology and Fertility of Soils Aims and scope Submit manuscript

Abstract

The impact of organic compounds present in different kinds of organic fertilizers, i.e., anaerobically digested household waste, composted organic household waste, swine manure, and cow manure, on microbial communities in arable soil was investigated using microcosms. Soil was amended with dried residues or organic extracts of the residues and incubated for 12 weeks at 25°C. The microbial community composition was investigated by phospholipid fatty acid (PLFA) analysis, and the community of ammonia-oxidizing bacteria (AOB) was assessed by denaturing gradient gel electrophoresis (DGGE) of 16S rDNA fragments, followed by sequencing. All dried residues increased the AOB activity, determined as potential ammonia oxidation, whereas the organic extracts from the thermophilically digested waste and the swine manure caused a decreased potential activity. However, no differences in the DGGE banding patterns were detected, and the same AOB sequences were present in all samples treated with the residue extracts. Moreover, the PLFA composition showed that none of the residue additions affected the overall microbial community structure in the soil. We conclude that the AOB community composition was not affected by the organic compounds in the fertilizers, although the activity in some cases was.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Avrahami S, Conrad R, Braker G (2002) Effect of soil ammonium concentration on N2O release and on the community structure of ammonia oxidisers and denitrifiers. Appl Environ Microbiol 68:5685–5692

    PubMed  CAS  Google Scholar 

  • Avrahami S, Liesack W, Conrad R (2003) Effects of temperature and fertilizer on activity and community structure of soil ammonia oxidizers. Environ Microbiol 5:691–705

    Article  PubMed  CAS  Google Scholar 

  • Balkwill DL, Leach FR, Wilson JT, McNabb JF, White DC (1988) Equivalence of microbial biomass measures based on membrane lipid and cell wall components, adenosine thriphospate, and direct counts in subsurface aquifer sediments. Microb Ecol 16:73–84

    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

    PubMed  CAS  Google Scholar 

  • Bruns MA, Stephen JR, Kowalchuk GA, Prosser JI, Paul EA (1999) Comparative diversity of ammonia oxidizer 16S rRNA gene sequences in native, tilled, and successional soils. Appl Environ Microbiol 65:2994–3000

    PubMed  CAS  Google Scholar 

  • Bååth E, Frostegård Å, Fritze H (1992) Soil bacterial biomass, activity, phospholipid fatty acid pattern, and pH tolerance in an area polluted with alkaline dust deposition. Appl Environ Microbiol 58:4026–4031

    PubMed  Google Scholar 

  • Bååth E, Díaz-Raviña M, Frostegård Å, Campbell CD (1998) Effect of metal-rich sludge amendments on the soil microbial community. Appl Environ Microbiol 64:238–245

    PubMed  Google Scholar 

  • Ceccherini MT, Castaldini M, Piovanelli C, Hastings RC, McArthy AJ, Bazzicalupo M, Miclaus N (1997) Effects of swine manure fertilization on autotrophic ammonia oxidising bacteria in soil. Appl Soil Ecol 7:149–157

    Article  Google Scholar 

  • Chang Y-J, Anwar Hussain AKM, Stephen JR, Mullens MD, White DC, Peacock A (2001) Impact of herbicides on the abundance and structure of indigenous β-subgroup ammonia-oxidizer communities in soil microcosms. Environ Toxicol Chem 20:2462–2468

    Article  PubMed  CAS  Google Scholar 

  • Debosz K, Petersen SO, Kure LK, Ambus P (2002) Evaluating effects of sewage sludge and household compost on soil physical and microbial properties. Appl Soil Ecol 19:237–248

    Article  Google Scholar 

  • Düring R-A, Gäth S (2002) Utilization of municipal organic wastes in agriculture: where do we stand, where do we go? J Plant Nutr Soil Sci 165:544–556

    Article  Google Scholar 

  • Eklind Y, Beck-Friis B, Bengtsson S, Ejlertsson J, Kirchmann H, Mathisen B, Nordkvist E, Sonesson U, Svensson BH, Torstensson L (1997) Chemical characterisation of source-separated organic household wastes. Swed J Agric Res 27:167–178

    CAS  Google Scholar 

  • Engwall M, Schnürer A (2002) Fate of Ah-receptor agonists in organic household waste during anaerobic degradation–estimation of levels using EROD induction in organ cultures of chick embryo livers. Sci Total Environ 27:105–108

    Article  Google Scholar 

  • Frostegård Å, Tunlid A, Bååth E (1993) Phospholipid fatty acid composition, biomass, and activity of microbial communities from two soil types experimentally exposed to different heavy metals. Appl Environ Microbiol 59:3605–3617

    PubMed  Google Scholar 

  • Frostegård Å, Petersen SO, Bååth E, Nielsen TH (1997) Dynamics of a microbial community associated with manure hot spots as revealed by phospholipid fatty acid analyses. Appl Environ Microbiol 63:2224–2231

    PubMed  Google Scholar 

  • Girvan MS, Bullimore J, Pretty JN, Osborn M, Ball AS (2003) Soil type is the primary determinant of the composition of the total and active bacterial communities in arable soils. Appl Environ Microbiol 69:1800–1809

    Article  PubMed  CAS  Google Scholar 

  • Goring CAI, Laskowski DA (1982) The effects of pesticides on nitrogen transformations in agricultural soils. In: Stevenson J (ed) Nitrogen in agricultural soils. Agronomy monograph 22, pp 689–720

  • Grossi G, Lichtig J, Krauss P (1998) PCDD/F, PCB and PAH content of Brazilian compost. Chemosphere 37:2153–2160

    Article  PubMed  CAS  Google Scholar 

  • Hastings RC, Ceccherini MT, Miclaus N, Saunders JR, Bazzicalupo M, McArthy AJ (1997) Direct molecular biological analyses of ammonia oxidising bacteria populations in cultivated soil plots treated with swine manure. FEMS Microbiol Ecol 23:45–54

    Article  CAS  Google Scholar 

  • Hiorns WD, Hastings RC, Head IM, McArthy AJ, Saunders JR, Pickup RW, Hall GH (1995) Amplification of 16S ribosomal RNA genes of autotrophic ammonia-oxidising bacteria. Microbiology 141:2793–2800

    Article  PubMed  Google Scholar 

  • Hobbs PJ, Misselbrook TH, Pain BF (1998) Emission rates of odorous compounds from pig slurries. J Sci Food Agric 77:341–348

    Article  CAS  Google Scholar 

  • Ibekwe AM, Kennedy AC (1998) Phospholipid fatty acid profiles and carbon utilization patterns for analysis of microbial community structure under field and greenhouse conditions. FEMS Microbiol Ecol 26:151–163

    Article  CAS  Google Scholar 

  • Ibekwe AM, Kennedy AC, Frohne PS, Papiernik SK, Yang CH, Crowley DE (2002) Microbial diversity along a transect of agronomic zones. FEMS Microbiol Ecol 39:183–191

    Article  CAS  PubMed  Google Scholar 

  • Jensen MT, Cox RP, Jensen BB (1995) 3-Methylindole (skatole) and indole production by mixed populations of pig fecal bacteria. Appl Environ Microbiol 61:3180–3184

    PubMed  CAS  Google Scholar 

  • Kowalchuk GA, Stephen JR, De Boer W, Prosser JI, Embley TM, Woldendorp JW (1997) Analysis of ammonia-oxidising bacteria of the β-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

    PubMed  CAS  Google Scholar 

  • Levén L, Schnürer A (2005) Effects of temperature on biological degradation of phenols, benzoates and phthalates under methanogenic conditions. Int Biodeterior Biodegrad 55:153–160

    Article  CAS  Google Scholar 

  • Marinari S, Masciandaro G, Ceccanti B, Grego S (2000) Influence of organic and mineral fertilisers on soil biological and physical properties. Bioresour Technol 72:9–17

    Article  CAS  Google Scholar 

  • Mendum TA, Sockett RE, Hirsch PR (1999) Use of molecular and isotopic techniques to monitor the response of autotrophic ammonia-oxidizing populations of the β-subdivisions of the class proteobacteria in arable soils to nitrogen fertilizer. Appl Environ Microbiol 65:4155–4162

    PubMed  CAS  Google Scholar 

  • Nicolaisen MH, Ramsing NB (2002) Denaturing gradient gel electrophoresis (DGGE) approaches to study the diversity of ammonia-oxidizing bacteria. J Microbiol Methods 50:189–203

    Article  PubMed  CAS  Google Scholar 

  • Nilsson M-L, Kylin H, Sundin P (2000) Major extractable organic compounds in the biologically degradable fraction of fresh, composted and anaerobically digested household waste. Acta Agric Scand, B Soil Plant Sci 50:57–65

    CAS  Google Scholar 

  • Nyberg K, Sundh I, Johansson M, Schnürer A (2004) Presence of potential ammonia oxidation (PAO) inhibiting substances in anaerobic digestion residues. Appl Soil Ecol 26:107–112

    Article  Google Scholar 

  • Oved T, Shaviv A, Goldrath T, Mandelbaum RT, Minz D (2001) Influence of effluent irrigation on community composition and function of ammonia-oxidizing bacteria in soil. Appl Environ Microbiol 67:3426–3433

    Article  PubMed  CAS  Google Scholar 

  • Pankhurst C (1997) Biodiversity of soil organisms as an indicator of soil health. In: Pankhurst C, Doube B, Gupta V (eds) Biological indicators of soil health. CAB International, Wallingford, UK

    Google Scholar 

  • Peacock AD, Mullen MD, Ringelberg DB, Tyler DD, Hedrick DB, Gale PM, White DC (2001) Soil microbial community responses to dairy manure or ammonium nitrate applications. Soil Biol Biochem 33:1011–1019

    Article  CAS  Google Scholar 

  • Pell M, Stenberg B, Torstensson L (1998) Potential denitrification and nitrification tests for evaluation of pesticide effect in soil. Ambio 27:24–28

    Google Scholar 

  • Petersen SO, Henriksen K, Mortensen GK, Krogh PH, Brandt KK, Sørensen J, Madsen T, Petersen J, Grøn C (2003) Recycling of sewage sludge and household compost to arable land: fate and effects of organic contaminants, and impact on soil fertility. Soil Tillage Res 72:139–152

    Article  Google Scholar 

  • Phillips CJ, Harris D, Dollhopf SL, Gross KL, Prosser JI, Eldor AP (2000) Effects of agronomic treatments on structure and function of ammonia-oxidizing communities. Appl Environ Microbiol 66:5410–5418

    Article  PubMed  CAS  Google Scholar 

  • Pinkart HC, Ringelberg DB, Piceno YM, MacNaughton SJ, White DC (2002) Biochemical approaches to biomass measurements and community structure analysis. In: Hurst CJ (ed) Manual of environmental microbiology. ASM Press, Herndon, VA, USA

    Google Scholar 

  • Purkhold U, Pommerening-Röser A, Juretschko S, Schmid MC, Koops H-P, Wagner M (2000) Phylogeny of all recognised species of ammonia oxidizers based on comparative 16S rRNA and amoA sequence analysis: implications for molecular diversity surveys. Appl Environ Microbiol 66:5368–5382

    Article  PubMed  CAS  Google Scholar 

  • Purkhold U, Wagner M, Timmerman G, Pommerening-Röser A, Koops H-P (2003) 16S rRNA and amoA-based phylogeny of 12 novel betaproteobacterial ammonia-oxidizing isolates: extension of the dataset and proposal of a new lineage within the nitrosomonads. Int J Syst Evol Microbiol 53:1485–1494

    Article  PubMed  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Skordilis A (1994) Characteristics of the household waste in Greece. Fresenius Environ Bull 3:457–461

    CAS  Google Scholar 

  • Smårs S, Beck-Friis B, Jönsson H, Kirchmann H (2001) An advanced experimental composting reactor for systematic simulation studies. J Agric Eng Res 78:415–422

    Article  Google Scholar 

  • Steger K, Jarvis Å, Smårs S, Sundh I (2003) Comparison of signature lipid methods to determine microbial community structure in compost. J Microbiol Methods 55:371–382

    Article  PubMed  CAS  Google Scholar 

  • Stenberg B, Johansson M, Pell M, Sjödahl-Svensson K, Stenström J, Torstensson L (1998) Microbial biomass and activities in soil as affected by frozen and cold storage. Soil Biol Biochem 30:393–402

    Article  CAS  Google Scholar 

  • Stephen JR, Chang Y-J, Macnaughton SJ, Kowalchuk GA, Leung K, Flemming CA, White DC (1999) Effect of toxic metals on indigenous soil β-subgroup proteobacterium ammonia oxidizer community structure and protection against toxicity by inoculated metal-resistant bacteria. Appl Environ Microbiol 65:95–101

    PubMed  CAS  Google Scholar 

  • Tiveljung A, Backstrom J, Forsum U, Monstein HJ (1995) Broad-range PCR amplification and DNA sequence analysis reveals variable motifs in 16S rRNA genes of Mobiluncus species. APMIS 103:755–793

    Article  PubMed  CAS  Google Scholar 

  • Torstensson L (1993) Guidelines. Soil biological variables in environmental hazard assessment. Swedish Environmental Protection Agency Report no 4262

  • Torstensson L (1997) Microbial assays in soils. In: Tarradellas J (ed) Soil ecotoxicology. CRC Press, Boca Raton

    Google Scholar 

  • Tu CM (1994) Effects of herbicides and fumigants on microbial activities in soil. Bull Environ Contam Toxicol 53:12–17

    Article  PubMed  CAS  Google Scholar 

  • Ulén B (1997) Leaching of plant nutrients and heavy metals during the composting of household wastes and chemical characterization of the final product. Acta Agric Scand 47:142–148

    Google Scholar 

  • Van de Peer Y, De Wachter R (1994) TREECON for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. Comput Appl Biosci 10:569–570

    PubMed  Google Scholar 

  • Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

Financial support for this work was provided by the Swedish University of Agricultural Sciences within the strategic research programme “Organic Waste—Resource or Risk in Sustainable Agriculture” (1999–2003), and The Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (Formas; 22.9/2001–2124).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Karin Nyberg.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nyberg, K., Schnürer, A., Sundh, I. et al. Ammonia-oxidizing communities in agricultural soil incubated with organic waste residues. Biol Fertil Soils 42, 315–323 (2006). https://doi.org/10.1007/s00374-005-0029-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00374-005-0029-6

Keywords

Navigation