Biology and Fertility of Soils

, Volume 51, Issue 4, pp 511–516 | Cite as

Manure-associated stimulation of soil-borne methanogenic activity in agricultural soils

  • Adrian Ho
  • Alaa El-Hawwary
  • Sang Yoon Kim
  • Marion Meima-Franke
  • Paul Bodelier
Short Communication


The growing human population and scarcity of arable land necessitate agriculture intensification to meet the global food demand. Intensification of agricultural land entails manure input into agrosystems which have been associated to increased methane emission. We investigated the immediate short-term response of methane production and the methanogens after manure amendments in agricultural soils and determined the relevance of the manure-derived methanogenic population in its contribution to soil methane production. We followed methane production in a series of unamended and manure-amended batch incubations: (i) manure and soil, (ii) sterilized manure and soil, and (iii) manure and sterilized soil. Moreover, we determined the methanogenic abundance using a quantitative PCR targeting the mcrA gene. Results show that the soil-borne methanogenic community was significantly stimulated by manure amendment, resulting in increased methane production and mcrA gene abundance; manure-derived methanogenic activity contributed only marginally to overall methane production. Accordingly, our results highlighted the importance of the resident methanogenic community and physiochemical properties of a residue when considering methane mitigation strategies in agricultural soils.


Methane production Methanogens Manure-amendment mcrA Agricultural management 

Supplementary material

374_2015_995_Fig3_ESM.jpg (688 kb)
Figure S1

Methane production in un-amended and amended wetland agricultural soil with (A) 10 %, (B) 20 %, and (C) 40 %w/w manure (mean ± s.d; n = 4). (JPEG 687 kb)

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High resolution image (EPS 1194 kb)
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Figure S2

Methane production in un-amended and amended oxic soil with (A) 10 %, (B) 20 %, and (C) 40 %w/w manure (mean ± s.d; n = 4). Note the different scales on the y-axis. (JPEG 869 kb)

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High resolution image (EPS 1377 kb)
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Figure S3

Methane production in soils and gamma-irradiated (sterilized) soils for wetland (A) and oxic (B) agricultural soils, and (C) methane production in incubations containing only (sterilized) manure (mean ± s.d; n = 4). Note the different scales on the x- and y-axis. (JPEG 821 kb)

374_2015_995_MOESM3_ESM.eps (1.3 mb)
High resolution image (EPS 1370 kb)
374_2015_995_Fig6_ESM.jpg (908 kb)
Figure S4

Methane production after prolonged incubation (16 d) in sterilized wetland (A) and oxic (B) agricultural soils amended with 10 %w/w manure (mean ± s.d; n = 2) in comparison to other treatments (mean ± s.d; n = 4). Note the different scales on the y-axis. (JPEG 908 kb)

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High resolution image (EPS 1402 kb)
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Figure S5

Correlation of mcrA gene abundance and methane production rate at a significant level (p < 0.005; linear regression). Data was integrated from the un-amended and 10 %w/w manure-amended incubations for both soils. (JPEG 854 kb)

374_2015_995_MOESM5_ESM.eps (1.2 mb)
High resolution image (EPS 1198 kb)


  1. Achtnich C, Bak F, Conrad R (1995) Competition for electron donors among nitrate reducers, ferric iron reducers, sulfate reducers, and methanogens in anoxic paddy soil. Biol Fertil Soils 19:65–72CrossRefGoogle Scholar
  2. Angel R, Claus P, Conrad R (2012) Methanogenic archaea are globally ubiquitous in aerated soils and become active under wet anoxic conditions. ISME J 6:847–862CrossRefPubMedCentralPubMedGoogle Scholar
  3. Conrad R (2009) The global methane cycle: recent advances in understanding the microbial processes involved. Environ Microbiol Rep 1:285–292CrossRefPubMedGoogle Scholar
  4. Gattinger A, Hofle MG, Schloter M, Embacher A, Bohme F, Munch JC, Labrenz M (2007) Traditional cattle manure application determines abundance, diversity, and activity of methanogenic Archaea in arable European soil. Environ Microbiol 9:612–624CrossRefPubMedGoogle Scholar
  5. Ho A, Lüke C, Frenzel P (2011) Recovery of methanotrophs from disturbance: population dynamics, evenness and functioning. ISME J 5:750–758CrossRefPubMedCentralPubMedGoogle Scholar
  6. Ho A, Lüke C, Reim A, Frenzel P (2013) Selective stimulation in a natural community of methane oxidizing bacteria: effects of copper on pmoA transcription and activity. Soil Biol Biochem 65:211–216CrossRefGoogle Scholar
  7. Kim SY, Pramanik P, Bodelier PLE, Kim PJ (2014a) Cattle manure enhances methanogens diversity and methane emissions compared to swine manure under rice paddy. PLoS ONE 9:e113593. doi:10.1371/journal.pone.0113593 CrossRefPubMedCentralPubMedGoogle Scholar
  8. Kim SY, Pramanik P, Gutierrez J, Hwang HY, Kim PJ (2014b) Comparison of methane emission characteristics in air-dried and composted cattle manure amended paddy soil during rice cultivation. Agric Ecosyst Environ 197:60–67CrossRefGoogle Scholar
  9. Kittelmann S, Seedorf H, Walters WA, Clemente JC, Knight R, Gordon JI, Janssen PH (2013) Simultaneous amplicon sequencing to explore co-occurrence patterns of bacterial, archaeal and eukaryotic microorganisms in rumen microbial communities. PLoS ONE 8:e47879. doi:10.1371/journal.pone.0047879 CrossRefPubMedCentralPubMedGoogle Scholar
  10. Lueders T, Chin K-J, Conrad R, Friedrich M (2001) Molecular analyses of methyl-coenzyme M reductase α-subunit (mcrA) genes in rice field soil and enrichment cultures reveal the methanogenic phenotype of a novel archaeal lineage. Environ Microbiol 3:194–204CrossRefPubMedGoogle Scholar
  11. Luton PE, Wayne JM, Sharp RJ, Riley PW (2002) The mcrA gene as an alternative to the 16S rRNA in the phylogenetic analysis of methanogen population in landfill. Microbiology 148:3521–3530PubMedGoogle Scholar
  12. Ma K, Conrad R, Lu Y (2012) Responses of methanogens mcrA genes and their transcripts to an alternate dry/wet cycle of paddy field soil. Appl Environ Microbiol 78:445–454CrossRefPubMedCentralPubMedGoogle Scholar
  13. Nisbet EG, Dlugokencky EJ, Bousquet P (2014) Methane on the rise—again. Science 343:493–495CrossRefPubMedGoogle Scholar
  14. Peters V, Conrad R (1995) Methanogenic and other strictly anaerobic bacteria in desert soil and other oxic soils. Appl Environ Microbiol 61:1673–1676PubMedCentralPubMedGoogle Scholar
  15. Poulsen M, Schwab C, Jensen BB, Engberg RM, Spang A, Canibe N, Højberg O, Milinovich G, Fragner L, Schleper C, Weckwerth W, Lund P, Schramm A, Urich T (2013) Methylotrophic methanogenic Thermoplasmata implicated in reduced methane emissions from bovine rumen. Nat Commun 4:1428. doi:10.1038/ncomms2432 CrossRefPubMedGoogle Scholar
  16. Radl V, Gattinger A, Chronakova A, Nemcova A, Cuhel J, Simek M, Munch JC, Schloter M, Elhottova D (2007) Effects of cattle husbandry on abundance and activity of methanogenic archaea in upland soils. ISME J 1:443–452CrossRefPubMedGoogle Scholar
  17. Rastogi G, Ranade DR, Yeole TY, Gupta AK, Patole MS, Shouche YS (2008) Molecular analyses of methanogen diversity associated with cattle dung. World J Microbiol Biotechnol 24:2973–2979CrossRefGoogle Scholar
  18. Skinner C, Gattinger A, Muller A, Mäder P, FlieBbach A, Stolze M, Ruser R, Niggli U (2014) Greenhouse gas fluxes from agricultural soils under organic and non-organic management—a global meta-analysis. Sci Total Environ 468:553–563CrossRefPubMedGoogle Scholar
  19. Sommer SG, Sherlock RR, Khan RZ (1996) Nitrous oxide and methane emissions from pig slurry amended soils. Soil Biol Biochem 28:1541–1544CrossRefGoogle Scholar
  20. Steinberg LM, Regan JM (2008) Phylogenetic comparison of the methanogenic communities from an acidic, oligotrophic fen and an anaerobic digester treating municipal wastewater sludge. Appl Environ Microbiol 74:6663–6671CrossRefPubMedCentralPubMedGoogle Scholar
  21. Thangarajan R, Bolan NS, Tian G, Naidu R, Kunhikrishnan A (2013) Role of organic amendment application on greenhouse gas emission from soil. Sci Total Environ 465:72–96CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Adrian Ho
    • 1
  • Alaa El-Hawwary
    • 1
  • Sang Yoon Kim
    • 1
  • Marion Meima-Franke
    • 1
  • Paul Bodelier
    • 1
  1. 1.Department of Microbial EcologyNetherlands Institute of Ecology (NIOO-KNAW)WageningenThe Netherlands

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