Biology and Fertility of Soils

, Volume 54, Issue 4, pp 533–547 | Cite as

Dung application increases CH4 production potential and alters the composition and abundance of methanogen community in restored peatland soils from Europe

  • Juliane Hahn
  • Heli Juottonen
  • Hannu Fritze
  • Eeva-Stiina Tuittila
Original Paper

Abstract

Peatland restoration via rewetting aims to recover biological communities and biogeochemical processes typical to pristine peatlands. While rewetting promotes recovery of C accumulation favorable for climate mitigation, it also promotes methane (CH4) emissions. The potential for exceptionally high emissions after rewetting has been measured for Central European peatland sites previously grazed by cattle. We addressed the hypothesis that these exceptionally high CH4 emissions result from the previous land use. We analyzed the effects of cattle dung application to peat soils in a short- (2 weeks), a medium- (1 year) and a long-term (grazing) approach. We measured the CH4 production potentials, determined the numbers of methanogens by mcrA qPCR, and analyzed the methanogen community by mcrA T-RFLP-cloning-sequencing. Dung application significantly increased the CH4 production potential in the short- and the medium-term approach and non-significantly at the cattle-grazed site. The number of methanogens correlated with the CH4 production in the short- and the long-term approach. At all three time horizons, we found a shift in methanogen community due to dung application and a transfer of rumen methanogen sequences (Methanobrevibacter spp.) to the peatland soil that seemed related to increased CH4 production potential. Our findings indicate that cattle grazing of drained peatlands changes their methanogenic microbial community, may introduce rumen-associated methanogens and leads to increased CH4 production. Consequently, rewetting of previously cattle-grazed peatlands has the potential to lead to increased CH4 emissions. Careful consideration of land use history is crucial for successful climate mitigation with peatland rewetting.

Keywords

Climate mitigation Rewetting Methane Cattle grazing Methanogen Land use 

Notes

Acknowledgements

Our thanks go to Aino Korrensalo, Salli Uljas, Maria Gutierrez Janne Sormunen, and Javier Andrés Jimenez who kindly helped in carrying and spreading dung to experimental sites and in sampling in Finland, Wilfried Bock for guidance and Steffen Kaufmane for sampling the sites in Germany. Furthermore, we thank Risto Linnainmaa for dung for the field experiment, Tero Tuomivirta for discussions regarding qPCR, and Sirpa Tiikkainen for guidance in cloning and sequencing.

Supplementary material

374_2018_1279_MOESM1_ESM.pdf (492 kb)
ESM 1 (PDF 491 kb)

References

  1. Aapala K, Sallantaus T, Haapalehto T (2008) Ecological restoration of drained peatlands. In: Korhonen R, Korpela L, Sarkkola S (eds) Finland-Fenland. Finnish Peatland Society & Maahenki, Helsinki, pp 243–249Google Scholar
  2. Abascal F, Zardoya R, Posada D (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21:2104–2105CrossRefPubMedGoogle Scholar
  3. Aguilar OA, Maghirang R, Trabue SL, Erickson LE (2014) Experimental research on the effects of water application on greenhouse gas emissions from beef cattle feedlots. Int J Energy Environ Eng 5:1–12CrossRefGoogle Scholar
  4. Augustin J, Chojnicki B (2008) Austausch von klimarelevanten Spurengasen, Klimawirkung und Kohlenstoffdynamik in den ersten Jahren nach der Wiedervernässung von degradiertem Niedermoorgrünland. In: Gelbrecht J, Zak D, Augustin J (eds) Phosphor- und Kohlenstoff- Dynamik und Vegetationsentwicklung in wiedervernässten Mooren des Peenetals in Mecklenburg-Vorpommern – Status, Steuergrößen und Handlungsmöglichkeiten, 26th edn. Institut für Gewässerökologie und Binnenfischerei, Berlin, pp 50–67Google Scholar
  5. Basiliko N, Blodau C, Roehm C, Bengtson P, Moore TR (2007) Regulation of decomposition and methane dynamics across natural, commercially mined, and restored northern peatlands. Ecosystems 10:1148–1165CrossRefGoogle Scholar
  6. Bessetti J (2007) An introduction to PCR inhibitors. Profiles DNA 10:9–10Google Scholar
  7. Blume H-P, Stahr K, Leinweber P (2011) Bodenkundliches Praktikum: Eine Einführung in pedologisches Arbeiten für Ökologen, insbesondere Land- und Forstwirte, und für Geowissenschaftler. Kapitel 5 Laboruntersuchungen, 3rd edn. Spektrum Akademischer Verlag, HeidelbergGoogle Scholar
  8. Buttler A, Grosvernier P, Matthey Y (1998) A new sampler for extracting undisturbed surface peat cores for growth pot experiments. New Phytol 140:355–360CrossRefGoogle Scholar
  9. Cadillo-Quiroz H, Brauer S, Yashiro E, Sun C, Yavitt JB, Zinder S (2006) Vertical profiles of methanogenesis and methanogens in two contrasting acidic peatlands in central New York State, USA. Environ Microbiol 8:1428–1440CrossRefPubMedGoogle Scholar
  10. Carberry CA, Kenny DA, Kelly AK, Waters SM (2014a) Quantitative analysis of ruminal methanogenic microbial populations in beef cattle divergent in phenotypic residual feed intake (RFI) offered contrasting diets. J Anim Sci Biotechnol 5:41CrossRefPubMedPubMedCentralGoogle Scholar
  11. Carberry CA, Waters SM, Kenny DA, Creevey CJ (2014b) Rumen methanogenic genotypes differ in abundance according to host residual feed intake phenotype and diet type. Appl Environ Microbiol 80:586–594CrossRefPubMedPubMedCentralGoogle Scholar
  12. Danielsson R, Dicksved J, Sun L, Gonda H, Müller B, Schnürer A, Bertilsson J (2017) Methane production in dairy cows correlates with rumen methanogenic and bacterial community structure. Front Microbiol 8:284CrossRefGoogle Scholar
  13. Dierßen K, Dierßen B (2008) Moore. 16 Tabellen. Ulmer. StuttgartGoogle Scholar
  14. Drösler M, Adelmann W, Augustin J, Bergmann L, Beyer C, Chojnicki B, Förster C, Freibauer A, Giebels M, Görlitz S, Höper H, Kantelhardt J, Liebersbach H, Hahn-Schöfl M, Minke M, Petschow U, Pfadenhauer J, Schaller L, Schägner P, Sommer M, Thuille A, Werhan M (2013) Klimaschutz durch Moorschutz. Schlussbericht des Vorhabens “Klimaschutz - Moornutzungsstrategien” 2006–2010. FreisingGoogle Scholar
  15. Elhottova D, Koubová A, Šimek M, Cajthaml T, Jirout J, Esperschuetz J, Schloter M, Gattinger A (2012) Changes in soil microbial communities as affected by intensive cattle husbandry. Appl Soil Ecol 58:56–65CrossRefGoogle Scholar
  16. Ferry JG (ed) (2012) Methanogenesis: ecology, physiology, biochemistry & genetics. Springer, DordrechtGoogle Scholar
  17. Flessa H, Beese F (2000) Laboratory estimates of trace gas emissions following surface application and injection of cattle slurry. J Environ Qual 29:262CrossRefGoogle Scholar
  18. Freibauer A (2008) The methane fraction of the carbon balance in restored temperate peatlands. Geophys Res Abstr 10:1607–7962Google Scholar
  19. Freitag TE, Prosser JI (2009) Correlation of methane production and functional gene transcriptional activity in a peat soil. Appl Environ Microbiol 75:6679–6687CrossRefPubMedPubMedCentralGoogle Scholar
  20. 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
  21. Gorham E (1991) Northern peatlands: role in the carbon cycle and probable responses to climatic warming. Ecol Appl 1:182–195CrossRefPubMedGoogle Scholar
  22. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321CrossRefPubMedGoogle Scholar
  23. Hahn J, Köhler S, Glatzel S, Jurasinski G (2015) Methane exchange in a coastal fen in the first year after flooding—a systems shift. PLoS One 10:e0140657CrossRefPubMedPubMedCentralGoogle Scholar
  24. Hamza MA, Anderson WK (2005) Soil compaction in cropping systems. Soil Tillage Res 82:121–145CrossRefGoogle Scholar
  25. Hargreaves SK, Roberto AA, Hofmockel KS (2013) Reaction- and sample-specific inhibition affect standardization of qPCR assays of soil bacterial communities. Soil Biol Biochem 59:89–97CrossRefGoogle Scholar
  26. Harms G, Layton AC, Dionisi HM, Gregory IR, Garrett VM, Hawkins SA, Robinson KG, Sayler GS (2003) Real-time PCR quantification of nitrifying bacteria in a municipal wastewater treatment plant. Environ Sci Technol 37:343–351CrossRefPubMedGoogle Scholar
  27. Haynes RJ, Williams PH (1993) Nutrient cycling and soil fertility in the grazed pasture ecosystem. In: Sparks DL (ed) Advances in agronomy. Academic Press, San Diego, CA, pp 119–199Google Scholar
  28. Hendriks DMD, van Huissteden J, Dolman AJ, van der Molen MK (2007) The full greenhouse gas balance of an abandoned peat meadow. Biogeosciences 4:411–424CrossRefGoogle Scholar
  29. Ho A, El-Hawwary A, Kim SY, Meima-Franke M, Bodelier P (2015) Manure-associated stimulation of soil-borne methanogenic activity in agricultural soils. Biol Fertil Soils 51:511–516CrossRefGoogle Scholar
  30. Jaatinen K, Fritze H, Laine J, Laiho R (2007) Effects of short- and long-term water-level drawdown on the populations and activity of aerobic decomposers in a boreal peatland. Glob Chang Biol 13:491–510CrossRefGoogle Scholar
  31. Jaatinen K, Laiho R, Vuorenmaa A, del Castillo U, Minkkinen K, Pennanen T, Penttilä T, Fritze H (2008) Responses of aerobic microbial communities and soil respiration to water-level drawdown in a northern boreal fen. Environ Microbiol 10:339–353CrossRefPubMedGoogle Scholar
  32. Janssen PH, Kirs M (2008) Structure of the archaeal community of the rumen. Appl Environ Microbiol 74:3619–3625CrossRefPubMedPubMedCentralGoogle Scholar
  33. Jauhiainen J, Limin S, Silvennoinen H, Vasander H (2008) Carbon dioxide and methane fluxes in drained tropical peat before and after hydrological restoration. Ecology 89:3503–3514CrossRefPubMedGoogle Scholar
  34. Joosten H, Tanneberger F (2017) Peatland use in Europe. In: Joosten H, Tanneberger F, Moen A (eds) Mires and peatlands of Europe: status, distribution and conservation. Schweizerbart Science Publishers, Stuttgart, pp 155–176Google Scholar
  35. Juottonen H, Hynninen A, Nieminen M, Tuomivirta T, Tuittila E-S, Nousiainen H, Kell DK, Yrjälä K, Tervahauta A, Fritze H (2012) Methane-cycling microbial communities and methane emission in natural and restored peatlands. Appl Environ Microbiol 78:6386–6389CrossRefPubMedPubMedCentralGoogle Scholar
  36. Juottonen H, Kotiaho M, Robinson D, Merila P, Fritze H, Tuittila E-S (2015) Microform-related community patterns of methane-cycling microbes in boreal sphagnum bogs are site specific. FEMS Microbiol Ecol 91:fiv094CrossRefPubMedGoogle Scholar
  37. Juottonen H, Tuittila E-S, Juutinen S, Fritze H, Yrjälä K (2008) Seasonality of rDNA- and rRNA-derived archaeal communities and methanogenic potential in a boreal mire. ISME J 2:1157–1168CrossRefPubMedGoogle Scholar
  38. Komulainen V-M, Nykänen H, Martikainen PJ, Laine J (1998) Short-term effect of restoration on vegetation change and methane emissions from peatlands drained for forestry in southern Finland. Can J For Res 28:402–411CrossRefGoogle Scholar
  39. Komulainen V-M, Tuittila E-S, Vasander H, Laine J (1999) Restoration of drained peatlands in southern Finland. Initial effects on vegetation change and CO2 balance. J Appl Ecol 36:634–648CrossRefGoogle Scholar
  40. Lafleur PM, Roulet NT, Bubier JL, Frolking S, Moore TR (2003) Interannual variability in the peatland-atmosphere carbon dioxide exchange at an ombrotrophic bog. Glob Biogeochem Cycles 17:1–13CrossRefGoogle Scholar
  41. Laiho R, Penttilä T, Fritze H (2017) Reindeer droppings may increase methane production potential in subarctic wetlands. Soil Biol Biochem 113:260–262CrossRefGoogle Scholar
  42. Laine J, Vasander H, Laiho R (1995) Long-term effects of water level drawdown on the vegetation of drained pine mires in southern Finland. J Appl Ecol 32:785–802CrossRefGoogle Scholar
  43. Liu C, Guo T, Chen Y, Meng Q, Zhu C, Huang H (2018) Physicochemical characteristics of stored cattle manure affect methane emissions by inducing divergence of methanogens that have different interactions with bacteria. Agric Ecosyst Environ 253:38–47CrossRefGoogle Scholar
  44. Lovell RD, Jarvis SC (1996) Effect of cattle dung on soil microbial biomass C and N in a permanent pasture soil. Soil Biol Biochem 28:291–299CrossRefGoogle Scholar
  45. Luton PE, Wayne JM, Sharp RJ, Riley PW (2002) The mcrA gene as an alternative to 16S rRNA in the phylogenetic analysis of methanogen populations in landfill. Microbiology 148:3521–3530CrossRefPubMedGoogle Scholar
  46. Mäkiranta P, Laiho R, Fritze H, Hytönen J, Laine J, Minkkinen K (2009) Indirect regulation of heterotrophic peat soil respiration by water level via microbial community structure and temperature sensitivity. Soil Biol Biochem 41:695–703CrossRefGoogle Scholar
  47. Maljanen M, Virkajärvi P, Martikainen PJ (2012) Dairy cow excreta patches change the boreal grass swards from sink to source of methane. Agric Food Sci 21:91–99Google Scholar
  48. Marinier M (2004) The role of cotton-grass (Eriophorum vaginatum) in the exchange of CO2 and CH4 at two restored peatlands, eastern Canada. Écoscience 11:141–149CrossRefGoogle Scholar
  49. Morris R, Schauer-Gimenez A, Bhattad U, Kearney C, Struble CA, Zitomer DH, Maki JS (2014) Methyl coenzyme M reductase (mcrA) gene abundance correlates with activity measurements of methanogenic H(2)/CO(2)-enriched anaerobic biomass. Microb Biotechnol 7:77–84CrossRefPubMedGoogle Scholar
  50. Morris R, Tale VP, Mathai PP, Zitomer DH, Maki JS (2016) mcrA gene abundance correlates with hydrogenotrophic methane production rates in full-scale anaerobic waste treatment systems. Lett Appl Microbiol 62:111–118CrossRefPubMedGoogle Scholar
  51. Moss AR, Jouany J-P, Newbold J (2000) Methane production by ruminants, its contribution to global warming. Ann Zootech 49:231–253CrossRefGoogle Scholar
  52. Myhre G, Shindell D, Bréon FM, Collins W, Fuglestvedt J, Huang J, Koch D, Lamarque JF, Lee D, Mendoza B, Nakajima T, Robock A, Stephens G, Takemura T, Zhang H (2013) Anthropogenic and Natural Radiative Forcing. In: Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USAGoogle Scholar
  53. Nellemann C, Corcoran E (2010) Dead planet, living planet. Biodiversity and ecosystem restoration for sustainable development : a rapid response assessment. Birkeland Trykkeri, NorwayGoogle Scholar
  54. Nilsson M, Sagerfors J, Buffam I, Laudon H, Eriksson T, Grelle A, Klemedtsson L, Weslien PER, Lindroth A (2008) Contemporary carbon accumulation in a boreal oligotrophic minerogenic mire—a significant sink after accounting for all C-fluxes. Glob Chang Biol 14:2317–2332CrossRefGoogle Scholar
  55. Oleszczuk R, Regina K, Szajdak L, Höper H, Maryganova V (2008) Impacts of agricultural untilization of peat soils on the greenhouse gas balance. In: Strack M (Ed) Peatlands and climate change, Jyväskylä pp 70–97Google Scholar
  56. Parish F, Sirin A, Charman D, Joosten H, Minayeva T, Silvius M, Stringer L (eds) (2008) Assessment on peatlands, biodiversity and climate change. Main report. Global Environment Centre, Kuala LumpurGoogle Scholar
  57. Peltoniemi K, Laiho R, Juottonen H, Bodrossy L, Kell DK, Minkkinen K, Mäkiranta P, Mehtätalo L, Penttilä T, Siljanen HMP, Tuittila E-S, Tuomivirta T, Fritze H (2016) Responses of methanogenic and methanotrophic communities to warming in varying moisture regimes of two boreal fens. Soil Biol Biochem 97:144–156CrossRefGoogle Scholar
  58. Pfadenhauer J, Grootjans A (1999) Wetland restoration in Central Europe: aims and methods. Appl Veg Sci 2:95–106CrossRefGoogle Scholar
  59. Prem EM, Reitschuler C, Illmer P (2014) Livestock grazing on alpine soils causes changes in abiotic and biotic soil properties and thus in abundance and activity of microorganisms engaged in the methane cycle. Eur J Soil Biol 62:22–29CrossRefGoogle Scholar
  60. Putkinen A, Tuittila E-S, Siljanen HMP, Bodrossy L, Fritze H (2018) Recovery of methane turnover and associated microbial communities in restored cutover peatlands is strongly linked with increasing Sphagnum abundance. Soil Biol Biochem 116:110–119CrossRefGoogle Scholar
  61. R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  62. Radl V, Gattinger A, Chronakova A, Nemcova A, Cuhel J, Šimek 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
  63. Scheffer F, Schachtschabel P, Blume H-P (2002) Lehrbuch der Bodenkunde. Spektrum, Akad. Verl. HeidelbergGoogle Scholar
  64. Schloss PD, Westcott SL, 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 75:7537–7541CrossRefPubMedPubMedCentralGoogle Scholar
  65. Shin EC, Choi BR, Lim WJ, Hong SY, An CL, Cho KM, Kim YK, An JM, Kang JM, Lee SS, Kim H, Yun HD (2004) Phylogenetic analysis of archaea in three fractions of cow rumen based on the 16S rDNA sequence. Anaerobe 10:313–319CrossRefPubMedGoogle Scholar
  66. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Soding J, Thompson JD, Higgins DG (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539CrossRefPubMedPubMedCentralGoogle Scholar
  67. Sirohi SK, Pandey N, Singh B, Puniya AK (2010) Rumen methanogens: a review. Indian J Microbiol 50:253–262CrossRefPubMedPubMedCentralGoogle Scholar
  68. Smith P, Bustamante M, Ahammad H, Clark H, Dong H, Elsiddig EA, Haberl H, Harper R, House J, Jafari M, Masera O, Mbow C, Ravindranath NH, Rice CW, Robeldo Abad C, Romanovskaya A, Sperling F, Tubiello F (2014) Agriculture, forestry and other land use (AFOLU). In: Edenhofer O, Pichs-Madruga R, Sokona Y, Farahanj E, Kadner S, Seyboth K, Adler A, Baum I, Brunner S, Eickemeier P, Kriemann B, Savolainen J, Schlömer S, von Stechow C, Zwickel T, Minx JC (eds) Climate change 2014: mitigation of climate change. Contribution of working group III to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, pp 811–922Google Scholar
  69. Söllinger A, Schwab C, Weinmaier T, Loy A, Tveit AT, Schleper C, Urich T (2016) Phylogenetic and genomic analysis of Methanomassiliicoccales in wetlands and animal intestinal tracts reveals clade-specific habitat preferences. FEMS Microbiol Ecol 92:fiv149CrossRefPubMedGoogle Scholar
  70. 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 74:6663–6671CrossRefPubMedPubMedCentralGoogle Scholar
  71. TerBraak CJF, Smilauer P (2012) Canoco reference manual and user’s guide: software for ordination, version 5.0. Microcomputer Power, IthacaGoogle Scholar
  72. Toes A-CM, Daleke MH, Kuenen JG, Muyzer G (2008) Expression of copA and cusA in Shewanella during copper stress. Microbiology 154:2709–2718CrossRefPubMedGoogle Scholar
  73. Tuittila E-S, Komulainen V-M, Vasander H, Laine J (1999) Restored cut-away peatland as a sink for atmospheric CO 2. Oecologia 120:563–574CrossRefPubMedGoogle Scholar
  74. Tuittila E-S, Komulainen V-M, Vasander H, Nykänen H, Martikainen PJ, Laine J (2000) Methane dynamics of a restored cut-away peatland. Glob Chang Biol 6:569–581CrossRefGoogle Scholar
  75. Turetsky MR, Kotowska A, Bubier JL, Dise NB, Crill P, Hornibrook ERC, Minkkinen K, Moore TR, Myers-Smith IH, Nykänen H, Olefeldt D, Rinne J, Saarnio S, Shurpali N, Tuittila E-S, Waddington JM, White JR, Wickland KP, Wilmking M (2014) A synthesis of methane emissions from 71 northern, temperate, and subtropical wetlands. Glob Chang Biol 20:2183–2197CrossRefPubMedGoogle Scholar
  76. Turunen J, Tomppo E, Tolonen K, Reinikainen A (2002) Estimating carbon accumulation rates of undrained mires in Finland—application to boreal and subarctic regions. The Holocene 12:69–80CrossRefGoogle Scholar
  77. Taylor CD, McBride BC, Wolfe RS, Bryant MP (1974) Coenzyme M, essential for growth of a rumen strain of Methanobacterium ruminantium. J Bacteriol 120:974-975Google Scholar
  78. Urbanová Z, Picek T, Bárta J (2011) Effect of peat re-wetting on carbon and nutrient fluxes, greenhouse gas production and diversity of methanogenic archaeal community. Ecol Eng 37:1017–1026CrossRefGoogle Scholar
  79. Vasander H, Tuittila E-S, Lode E, Lundin L, Ilomets M, Sallantaus T, Heikkilä R, Pitkänen M-L, Laine J (2003) Status and restoration of peatlands in northern Europe. Wetl Ecol Manag 11:51–63CrossRefGoogle Scholar
  80. Waddington JM, Day SM (2007) Methane emissions from a peatland following restoration. J Geophys Res 112:2156–2202CrossRefGoogle Scholar
  81. Waddington JM, Strack M, Greenwood MJ (2010) Toward restoring the net carbon sink function of degraded peatlands—short-term response in CO2 exchange to ecosystem-scale restoration. J Geophys Res 115:1–13CrossRefGoogle Scholar
  82. Watanabe T, Kimura M, Asakawa S (2007) Dynamics of methanogenic archaeal communities based on rRNA analysis and their relation to methanogenic activity in Japanese paddy field soils. Soil Biol Biochem 39:2877–2887CrossRefGoogle Scholar
  83. Wilson D, Couwenberg J, Evans CD, Murdiyarso D, Page SE, Renou-Wilson F, Rieley JO, Sirin A, Strack M, Tuittila E-S (2016) Greenhouse gas emission factors associated with rewetting of organic soils. Mires Peat 17:1–28Google Scholar
  84. Wilson D, Tuittila E-S, Alm J, Laine J, Farrell EP, Byrne KA (2007) Carbon dioxide dynamics of a restored maritime peatland. Écoscience 14:71–80CrossRefGoogle Scholar
  85. Wright A-DG, Auckland CH, Lynn DH (2007) Molecular diversity of methanogens in feedlot cattle from Ontario and Prince Edward Island, Canada. Appl Environ Microbiol 73:4206–4210CrossRefPubMedPubMedCentralGoogle Scholar
  86. Yang Y, Li X, Liu J, Zhou Z, Zhang T, Wang X (2017) Bacterial diversity as affected by application of manure in red soils of subtropical China. Biol Fertil Soils 53:639–649CrossRefGoogle Scholar
  87. Yavitt JB, Williams CJ, Wieder RK (2005) Soil chemistry versus environmental controls on production of CH4 and CO2 in northern peatlands. Eur J Soil Sci 56:169–178CrossRefGoogle Scholar
  88. Yrjälä K, Tuomivirta T, Juottonen H, Putkinen A, Lappi K, Tuittila E-S, Penttilä T, Minkkinen K, Laine J, Peltoniemi K, Fritze H (2011) CH4 production and oxidation processes in a boreal fen ecosystem after long-term water table drawdown. Glob Chang Biol 17:1311–1320CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.School of Forest SciencesUniversity of Eastern FinlandJoensuuFinland
  2. 2.Faculty of Agricultural and Environmental SciencesUniversity of RostockRostockGermany
  3. 3.Natural Resources Institute Finland (Luke)HelsinkiFinland
  4. 4.Department of Biological and Environmental ScienceUniversity of JyväskyläJyväskyläFinland

Personalised recommendations