Skip to main content
Log in

Archaeal community dynamics and detection of ammonia-oxidizing archaea during composting of cattle manure using culture-independent DNA analysis

  • Environmental Biotechnology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

The composting process is carried out under aerobic conditions involving bacteria, archaea, and fungi. Little is known about the diversity of archaeal community in compost, although they may play an important role in methane production and ammonia oxidation. In the present study, archaeal community dynamics during cattle manure composting were analyzed using a clone library of the archaeal 16S rRNA gene. The results indicated that methane-producing archaea (methanogen) and ammonia-oxidizing archaea (AOA) may be the dominant microbes throughout the composting. The community consisted primarily of Methanocorpusculum-like and Methanosarcina-like sequences until day 2, while the number of Candidatus Nitrososphaera-like sequences increased from day 6 to day 30. Methanosarcina thermophila-like sequences were dominant from day 2, suggesting that M. thermophila-like species can adapt to increasing temperature or nutrient loss. A denaturant gradient gel electrophoresis analysis of the archaeal amoA genes revealed that the dominant amoA gene sequence with 99% homology to that of Candidatus Nitrososphaera gargensis was identical to those obtained from a different composting facility. These data suggested that AOA may play a role in ammonia oxidation in several composting practices. Our results provide fundamental information regarding archaeal community dynamics that will help in understanding the collective microbial community in compost.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Adair KL, Schwartz E (2008) Evidence that ammonia-oxidizing archaea are more abundant than ammonia-oxidizing bacteria in semiarid soils of northern Arizona, USA. Microb Ecol 56:420–426

    Article  CAS  PubMed  Google Scholar 

  • Ashelford KE, Chuzhanova NA, Fry JC, Jones AJ, Weightman AJ (2005) At least 1 in 20 16S rRNA sequence records currently held in public repositories is estimated to contain substantial anomalies. Appl Environ Microbiol 71:7724–7736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beck-Friis B, Pell M, Sonesson U, Jönsson H, Kirchmann H (2000) Formation and emission of N2O and CH4 from compost heaps of organic household waste. Environ Monit Assess 62:317–331

    Article  CAS  Google Scholar 

  • Beman JM, Francis CA (2006) Diversity of ammonia-oxidizing archaea and bacteria in the sediments of a hypernutrified subtropical estuary: Bahía del Tóbari, Mexico. Appl Environ Microbiol 72:7767–7777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bernal MP, Alburquerque JA, Moral R (2009) Composting of animal manures and chemical criteria for compost maturity assessment. A review. Bioresour Technol 100:5444–5453

    Article  CAS  PubMed  Google Scholar 

  • Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P (2008) Mesophilic crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat Rev Microbiol 6:245–252

    Article  CAS  PubMed  Google Scholar 

  • Cahyani VR, Matsuya K, Asakawa S, Kimura M (2004) Succession and phylogenetic profile of methanogenic archaeal communities during the composting process of rice straw estimated by PCR-DGGE. Soil Sci Plant Nutr 50:555–563

    Article  CAS  Google Scholar 

  • Chin KJ, Lukow T, Conrad R (1999) Effect of temperature on structure and function of the methanogenic archaeal community in an anoxic rice field soil. Appl Environ Microbiol 65:2341–2349

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coolen MJ, Abbas B, van Bleijswijk J, Hopmans EC, Kuypers MM, Wakeham SG, Sinninghe Damsté JS (2007) Putative ammonia-oxidizing Crenarchaeota in suboxic waters of the Black Sea: a basin-wide ecological study using 16S ribosomal and functional genes and membrane lipids. Environ Microbiol 9:1001–1016

    Article  CAS  PubMed  Google Scholar 

  • de la Torre JR, Walker CB, Ingalls AE, Könneke M, Stahl DA (2008) Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. Environ Microbiol 10:810–818

    Article  CAS  PubMed  Google Scholar 

  • Dees PM, Ghiorse WC (2001) Microbial diversity in hot synthetic compost as revealed by PCR-amplified rRNA sequences from cultivated isolates and extracted DNA. FEMS Microbiol Ecol 35:207–216

    Article  CAS  PubMed  Google Scholar 

  • DeLong EF (1992) Archaea in coastal marine environments. Proc Natl Acad Sci USA 89:5685–5689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB (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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fukumoto Y, Osada T, Hanajima D, Haga K (2003) Patterns and quantities of NH3, N2O and CH4 emissions during swine manure composting without forced aeration-effect of compost pile scale. Bioresour Technol 89:109–114

    Article  CAS  PubMed  Google Scholar 

  • Gattinger A, Höfle MG, Schloter M, Embacher A, Böhme F, Munch JC, Labrenz M (2007) Traditional cattle manure application determines abundance, diversity and activity of methanogenic Archaea in arable European soil. Environ Microbiol 9:612–624

    Article  CAS  PubMed  Google Scholar 

  • Großkopf R, Janssen PH, Liesack W (1998) Diversity and structure of the methanogenic community in anoxic rice paddy soil microcosms as examined by cultivation and direct 16S rRNA gene sequence retrieval. Appl Environ Microbiol 64:960–969

    Article  PubMed  PubMed Central  Google Scholar 

  • Haga K (1999) Development of composting technology in animal waste treatment —review. Asian–Aus J Ani Sci 12:604–606

    Article  Google Scholar 

  • Hall JE (1999) Nutrient recycling: the European experience. Asian–Aus. J Anim Sci 12:667–674

    Google Scholar 

  • Hao X, Chang C, Larney F, Travis G (2001) Greenhouse gas emissions during cattle feedlot manure composting. J Environ Qual 30:376–386

    Article  CAS  PubMed  Google Scholar 

  • Hao X, Chang C, Larney FJ (2004) Carbon, nitrogen balances and greenhouse gas emission during cattle feedlot manure composting. J Environ Qual 33:37–44

    Article  CAS  PubMed  Google Scholar 

  • Hatzenpichler R, Lebedeva E, Spieck E, Stoecker K, Richter A, Daims H, Wagner M (2008) A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proc Natl Acad Sci U S A 105:2134–2139

    Article  PubMed  PubMed Central  Google Scholar 

  • He Y, Inamori Y, Mizuochi M, Kong H, Iwami N, Sun T (2000) Measurements of N2O and CH4 from the aerated composting of food waste. Sci Total Environ 254:65–74

    Article  CAS  PubMed  Google Scholar 

  • Hellmann B, Zelles L, Palojarvi A, Bai Q (1997) Emission of climate-relevant trace gases and succession of microbial communities during open-windrow composting. Appl Environ Microbiol 63:1011–1018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Insam H, de Bertoldi M (2007) Microbiology of the composting process. In: Diaz LF, de Bertoldi M, Bidlingmaier W, Stentiford E (eds) Compost science and technology. Elsevier Ltd., Oxford, UK, pp 26–48

    Google Scholar 

  • Ishii K, Fukui M, Takii S (2000) Microbial succession during a composting process as evaluated by denaturing gradient gel electrophoresis analysis. J Appl Microbiol 89:768–777

    Article  CAS  PubMed  Google Scholar 

  • Jäckel U, Thummes K, Kämpfer P (2005) Thermophilic methane production and oxidation in compost. FEMS Microbiol Ecol 52:175–184

    Article  CAS  PubMed  Google Scholar 

  • Jiang H, Huang Q, Dong H, Wang P, Wang F, Li W, Zhang C (2010) RNA-based investigation of ammonia-oxidizing archaea in hot springs of Yunnan Province, China. Appl Environ Microbiol

  • Karakashev D, Batstone D, Angelidaki I (2005) Influence of environmental conditions on methanogenic compositions in anaerobic biogas reactors. Appl Environ Microbiol 71:331–338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klamer M, Bååth E (1998) Microbial community dynamics during composting of straw material studied using phospholipid fatty acid analysis. FEMS Microbiol Ecol 27:9–20

    Article  CAS  Google Scholar 

  • Könneke M, Bernhard A, de la Torre J, Walker C, Waterbury J, Stahl D (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543–546

    Article  CAS  PubMed  Google Scholar 

  • Kreader C (1996) Relief of amplification inhibition in PCR with bovine serum albumin or T4 gene 32 protein. Appl Environ Microbiol 62:1102–1106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuroda K, Hanajima D, Fukumoto Y, Suzuki K, Kawamoto S, Shima J, Haga K (2004) Isolation of thermophilic ammonium-tolerant bacterium and its application to reduce ammonia emission during composting of animal wastes. Biosci Biotechnol Biochem 68:286–292

    Article  CAS  PubMed  Google Scholar 

  • Larney F, Hao X (2007) A review of composting as a management alternative for beef cattle feedlot manure in southern Alberta, Canada. Bioresour Technol 98:3221–3227

    Article  CAS  PubMed  Google Scholar 

  • Le Treut H, Somerville R, Cubasch U, Ding Y, Mauritzen C, Mokssit A, Peterson T, Prather M (2007) Historical Overview of Climate Change. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA, pp 95–127

    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  PubMed  Google Scholar 

  • Mackie R, Stroot P, Varel V (1998) Biochemical identification and biological origin of key odor components in livestock waste. J Anim Sci 76:1331–1342

    Article  CAS  PubMed  Google Scholar 

  • McCaig A, Glover L, Prosser J (1999) Molecular analysis of bacterial community structure and diversity in unimproved and improved upland grass pastures. Appl Environ Microbiol 65:1721–1730

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller DN, Varel VH (2001) In vitro study of the biochemical origin and production limits of odorous compounds in cattle feedlots. J Anim Sci 79:2949–2956

    Article  CAS  PubMed  Google Scholar 

  • Miller DN, Bryant JE, Madsen EL, Ghiorse WC (1999) Evaluation and optimization of DNA extraction and purification procedures for soil and sediment samples. Appl Environ Microbiol 65:4715–4724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Osada T, Fukumoto Y (2001) Development of a new dynamic chamber system for measuring harmful gas emissions from composting livestock waste. Water Sci Technol 44:79–86

    Article  CAS  PubMed  Google Scholar 

  • Park HD, Wells GF, Bae H, Criddle CS, Francis CA (2006) Occurrence of ammonia-oxidizing archaea in wastewater treatment plant bioreactors. Appl Environ Microbiol 72:5643–5647

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peters S, Koschinsky S, Schwieger F, Tebbe CC (2000) Succession of microbial communities during hot composting as detected by PCR–single-strand-conformation polymorphism-based genetic profiles of small-subunit rRNA genes. Appl Environ Microbiol 66:930–936

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reigstad L, Richter A, Daims H, Urich T, Schwark L, Schleper C (2008) Nitrification in terrestrial hot springs of Iceland and Kamchatka. FEMS Microbiol Ecol 64:167–174

    Article  CAS  PubMed  Google Scholar 

  • Reuter T, Xu W, Alexander T, Stanford K, Xu Y, McAllister T (2009) Purification of polymerase chain reaction (PCR)-amplifiable DNA from compost piles containing bovine mortalities. Bioresour Technol 100:3343–3349

    Article  CAS  PubMed  Google Scholar 

  • Ryckeboer J, Mergaert J, Vaes K, Klammer S, De Clercq D, Coosemans J, Insam H, Swings J (2003) A survey of bacteria and fungi occurring during composting and self-heating processes. Ann Microbiol 53:349–410

    Google Scholar 

  • Sasaki H, Nonaka J, Otawa K, Kitazume O, Asano R, Sasaki T, Nakai Y (2009) Analysis of the bacterial community in the livestock manure-based composting process. Asian–Aus J Ani Sci 22:113–118

    Article  Google Scholar 

  • Schloss P, Hay A, Wilson D, Gossett J, Walker L (2005) Quantifying bacterial population dynamics in compost using 16S rRNA gene probes. Appl Microbiol Biotechnol 66:457–463

    Article  CAS  PubMed  Google Scholar 

  • Schloss P, Westcott S, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singleton DR, Furlong MA, Rathbun SL, Whitman MB (2001) Quantitative comparisons of 16S rRNA gene sequence libraries from environmental samples. Appl Environ Microbiol 67:4374–4376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Snell-Castro R, Godon J, Delgenès J, Dabert P (2005) Characterisation of the microbial diversity in a pig manure storage pit using small subunit rDNA sequence analysis. FEMS Microbiol Ecol 52:229–242

    Article  CAS  PubMed  Google Scholar 

  • Spang A, Hatzenpichler R, Brochier-Armanet C, Rattei T, Tischler P, Spieck E, Streit W, Stahl DA, Wagner M, Schleper C (2010) Distinct gene set in two different lineages of ammonia-oxidizing archaea supports the phylum Thaumarchaeota. Trends Microbiol 18:331–340

    Article  CAS  PubMed  Google Scholar 

  • Sprenger W, van Belzen M, Rosenberg J, Hackstein J, Keltjens J (2000) Methanomicrococcus blatticola gen. nov., sp. nov., a methanol- and methylamine-reducing methanogen from the hindgut of the cockroach Periplaneta americana. Int J Syst Evol Microbiol 50(Pt 6):1989–1999

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596

    Article  CAS  PubMed  Google Scholar 

  • Tang J, Kanamori T, Inoue Y, Yasuta T, Yoshida S, Katayama A (2004) Changes in the microbial community structure during thermophilic composting of manure as detected by the quinone profile method. Process Biochem 39:1999–2006

    Article  CAS  Google Scholar 

  • Thummes K, Schäfer J, Kämpfer P, Jäckel U (2007) Thermophilic methanogenic Archaea in compost material: occurrence, persistence and possible mechanisms for their distribution to other environments. Syst Appl Microbiol 30:634–643

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Treusch A, Leininger S, Kletzin A, Schuster S, Klenk H, 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

    Article  CAS  PubMed  Google Scholar 

  • Venter J, Remington K, Heidelberg J, Halpern A, Rusch D, Eisen J, Wu D, Paulsen I, Nelson K, Nelson W, Fouts D, Levy S, Knap A, Lomas M, Nealson K, White O, Peterson J, Hoffman J, Parsons R, Baden-Tillson H, Pfannkoch C, Rogers Y, Smith H (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66–74

    Article  PubMed  Google Scholar 

  • Whitehead TR, Cotta MA (1999) Phylogenetic diversity of methanogenic archaea in swine waste storage pits. FEMS Microbiol Lett 179:223–226

    Article  CAS  PubMed  Google Scholar 

  • Whitman WB, Bowen TL, Boone DR (2006) The methanogenic bacteria. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds) The prokaryotes, 3rd edn. Springer, New York, pp 165–207

    Chapter  Google Scholar 

  • Yamada T, Suzuki A, Ueda H, Ueda Y, Miyauchi K, Endo G (2008) Successions of bacterial community in composting cow dung wastes with or without hyperthermophilic pre-treatment. Appl Microbiol Biotechnol 81:771–781

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto N, Otawa K, Nakai Y (2009) Bacterial communities developing during composting processes in animal manure treatment facilities. Asian-Aus J Ani Sci 22:900–905

    Article  CAS  Google Scholar 

  • Yamamoto N, Otawa K, Nakai Y (2010) Diversity and abundance of ammonia-oxidizing bacteria and ammonia-oxidizing archaea during cattle manure composting. Microb Ecol 60:807–815

  • Zinder S, Sowers K, Ferry J (1985) Notes: Methanosarcina thermophila sp. nov., a thermophilic, acetotrophic, methane-producing bacterium. Int J Syst Bacteriol 35:522–523

    Article  Google Scholar 

Download references

Acknowledgements

This work was partially supported by the Foundation of the Ministry of Education, Culture, Sports, Science, and Technology, Japan, as a “Project of Integrated Compost Science” and by a grant from the Livestock Technology Association, Japan. We would like to thank M. Tannai for making and managing compost.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yutaka Nakai.

Electronic supplementary material

Fig. S1

Phylogenetic tree of the archaeal 16S rRNA gene sequences obtained from composting materials. Boot-strap values (>60%) are indicated at the branch points. All sequences obtained from the present study are indicated in bold letters. The scale bar represents 5% sequence divergence. Accession numbers are indicated in parentheses. (TIFF 9039 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yamamoto, N., Asano, R., Yoshii, H. et al. Archaeal community dynamics and detection of ammonia-oxidizing archaea during composting of cattle manure using culture-independent DNA analysis. Appl Microbiol Biotechnol 90, 1501–1510 (2011). https://doi.org/10.1007/s00253-011-3153-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-011-3153-2

Keywords

Navigation