Methanotrophy in Acidic Soils, Including Northern Peatlands

  • Tobin J. Verbeke
  • Svetlana N. Dedysh
  • Peter F. DunfieldEmail author
Reference work entry
Part of the Handbook of Hydrocarbon and Lipid Microbiology book series (HHLM)


Methane oxidizing microorganisms are present and active in diverse acidic environments including peatlands, geothermal areas, and forest soils. Methanotrophic communities in acidic environments have been examined using cultivation-based physiological analyses as well as cultivation-independent molecular approaches, including omic-technologies. Most investigations have focused on moderately acidophilic, aerobic methanotrophs belonging to the phylum Proteobacteria that are capable of growth as low as pH 4. However, some Verrucomicrobia are capable of oxidizing methane aerobically at pH 1. Alphaproteobacteria methanotrophs generally dominate the methanotrophic communities in acidic oligotrophic bogs, while Gammaproteobacteria methanotrophs are more predominant in minerotrophic fens. The Verrucomicrobia methanotrophs appear to be limited to geothermal or sulfidic environments. Recent evidence has suggested that anaerobic methane oxidation may also be important in acidic peatland environments. The known diversity and metabolic potential of aerobic and anaerobic methanotrophs that are active under acidic conditions has advanced in recent years. This chapter will summarize cultivation, molecular ecology, taxonomy, and physiology studies of acidophilic methanotrophs.



anaerobic oxidation of methane


fluorescence in situ hybridization


phospholipid fatty acid


particulate methane monooxygenase


stable isotope probing


soluble methane monooxygenase


  1. Anvar SY, Frank J, Pol A, Schmitz A, Kraaijeveld K, den Dunnen JT, Op den Camp HJM (2014) The genomic landscape of the verrucomicrobial methanotroph Methylacidiphilum fumariolicum SolV. BMC Genomics 15:914. Scholar
  2. Beal E, House C, Orphan VJ (2009) Manganese- and iron-dependent marine methane oxidation. Science 325:184–187. Scholar
  3. Belova SE, Baani M, Suzina NE, Bodelier PL, Liesack W, Dedysh SN (2011) Acetate utilization as a survival strategy of peat-inhabiting Methylocystis spp. Environ Microbiol Rep 3:36–46. Scholar
  4. Belova SE, Kulichevskaya IS, Bodelier PL, Dedysh SN (2013) Methylocystis bryophila sp. nov., a facultatively methanotrophic bacterium from acidic Sphagnum peat, and emended description of the genus Methylocystis (ex Whittenbury et al. 1970) Bowman et al. 1993. Int J Syst Evol Microbiol 63:1096–1104. Scholar
  5. Berestovskaya YY, Vasilieva L, Chestnykh O, Zavarzin GA (2002) Methanotrophs of the psychrophilic microbial community of the Russian Arctic tundra. Mikrobiologiia 71:460–466Google Scholar
  6. Blazewicz SJ, Petersen DG, Waldrop MP, Firestone MK (2012) Anaerobic oxidation of methane in tropical and boreal soils: ecological significance in terrestrial methane cycling. J Geophys Res Biogeosci 117:G02033. Scholar
  7. Bouckaert R, Heled J, Kuhnert D, Vaughan T, Wu C, Xie D, Suchard MA, Rambaut A, Drummond A (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol 10:e1003537. Scholar
  8. Bragina A, Berg C, Muller H, Moser D, Berg G (2013) Insights into functional bacterial diversity and its effects on Alpine bog ecosystem functioning. Sci Rep 3:1955.
  9. Caldwell S, Laidler J, Brewer E, Eberly J, Sandborgh S, Colwell F (2008) Anaerobic oxidation of methane: mechanisms, bioenergetics, and the ecology of associated microorganisms. Environ Sci Technol 42:6791–6799. Scholar
  10. Carere CR, Hards K, Houghton KM, Power JF, McDonald B, Collet C, Gapes DJ, Sparling R, Boyd ES, Cook GM, Greening C, Stott MB (2017) Mixotrophy drives niche expansion of verrucomicrobial methanotrophs. ISME J 11:2599–2610. Scholar
  11. Castaldi S, Tedesco D (2005) Methane production and consumption in an active volcanic environment of Southern Italy. Chemosphere 58:131–139. Scholar
  12. Chen Y, Dumont MG, McNamara NP, Chamberlain PM, Bodrossy L, Stralis-Pavese N, Murrell JC (2008a) Diversity of the active methanotrophic community in acidic peatlands as assessed by mRNA and SIP–PLFA analyses. Environ Microbiol 10:446–459. Scholar
  13. Chen Y, Dumont MG, Neufeld JD, Bodrossy L, Stralis-Pavese N, McNamara NP, Ostle N, Briones MJ, Murrell JC (2008b) Revealing the uncultivated majority: combining DNA stable-isotope probing, multiple displacement amplification and metagenomic analyses of uncultivated Methylocystis in acidic peatlands. Environ Microbiol 10:2609–2622. Scholar
  14. Christiansen JR, Romero AJB, Jørgensen NOG, Glaring MA, Jørgensen CJ, Berg LK, Elberling B (2014) Methane fluxes and the functional groups of methanotrophs and methanogens in a young Arctic landscape on Disko Island, West Greenland. Biogeochemistry 122:15–33. Scholar
  15. Ciais P, Sabine C, Bala G, Bopp L, Brovkin V, Canadell J, Chhabra A, DeFries R, Galloway J, Heimann M, Jones C, Le Quere C, Myneni R, Piao S, Thornton P (2013) Carbon and other biogeochemical cycles. In: Heinze C, Tans P, Vesala T (eds) Climate change 2013: the physical science basis. Intergovernmental panel on climate change. Cambridge University Press, Cambridge, pp 465–570Google Scholar
  16. Danilova OV, Kulichevskaya IS, Rozova ON, Detkova EN, Bodelier PL, Trotsenko YA, Dedysh SN (2013) Methylomonas paludis sp. nov., the first acid-tolerant member of the genus Methylomonas, from an acidic wetland. Int J Syst Evol Microbiol 63:2282–2289. Scholar
  17. Danilova OV, Belova SE, Gagarinova IV, Dedysh SN (2016a) Microbial community composition and methanotroph diversity of a subarctic wetland in Russia. Mikrobiologiia 85:583–591. Scholar
  18. Danilova OV, Suzina NE, Van De Kamp J, Svenning MM, Bodrossy L, Dedysh SN (2016b) A new cell morphotype among methane oxidizers: a spiral-shaped obligately microaerophilic methanotroph from northern low-oxygen environments. ISME J 10:2734–2743. Scholar
  19. Dean JF, Middelburg JJ, Röckmann T, Aerts R, Blauw LG, Egger M, Jetten MSM, de Jong AEE, Meisel OH, Rasigraf O, Slomp CP, in’t Zandt MH, Dolman AJ (2018) Methane feedbacks to the global climate system in a warmer world. Rev Geophys. Scholar
  20. Dedysh SN (2009) Exploring methanotroph diversity in acidic northern wetlands: molecular and cultivation-based studies. Microbiology 78:655–669. Scholar
  21. Dedysh SN, Dunfield PF (2018) Facultative methane oxidizers. In: TJ (ed) Microbial Communities Utilizing Hydrocarbons and Lipids: Members, Metagenomics and Ecophysiology, Handbook of Hydrocarbon and Lipid Microbiology, Springer Nature, Switzerland. Scholar
  22. Dedysh SN, Liesack W, Khmelenina VN, Suzina NE, Trotsenko YA, Semrau JD, Bares AM, Panikov NS, Tiedje JM (2000) Methylocella palustris gen. nov., sp. nov., a new methane-oxidizing acidophilic bacterium from peat bogs, representing a novel subtype of serine-pathway methanotrophs. Int J Syst Evol Microbiol 50:955–969. Scholar
  23. Dedysh SN, Derakshani M, Liesack W (2001) Detection and enumeration of methanotrophs in acidic sphagnum peat by 16S rRNA fluorescence in situ hybridization, including the use of newly developed oligonucleotide probes for Methylocella palustris. Appl Environ Microbiol 67:4850–4857. Scholar
  24. Dedysh SN, Khmelenina VN, Suzina NE, Trotsenko YA, Semrau JD, Liesack W, Tiedje JM (2002) Methylocapsa acidiphila gen. nov., sp. nov., a novel methane-oxidizing and dinitrogen-fixing acidophilic bacterium from Sphagnum bog. Int J Syst Evol Microbiol 52:251–261. Scholar
  25. Dedysh SN, Dunfield PF, Derakshani M, Stubner S, Heyer J, Liesack W (2003) Differential detection of type II methanotrophic bacteria in acidic peatlands using newly developed 16S rRNA-targeted fluorescent oligonucleotide probes. FEMS Microbiol Ecol 43:299–308. Scholar
  26. Dedysh SN, Berestovskaya YY, Vasylieva LV, Belova SE, Khmelenina VN, Suzina NE, Trotsenko YA, Liesack W, Zavarzin GA (2004) Methylocella tundrae sp. nov., a novel methanotrophic bacterium from acidic tundra peatlands. Int J Syst Evol Microbiol 54:151–156. Scholar
  27. Dedysh SN, Knief C, Dunfield PF (2005) Methylocella species are facultatively methanotrophic. J Bacteriol 187:4665–4670. Scholar
  28. Dedysh SN, Belova SE, Bodelier PL, Smirnova KV, Khmelenina VN, Chidthaisong A, Trotsenko YA, Liesack W, Dunfield PF (2007) Methylocystis heyeri sp. nov., a novel type II methanotrophic bacterium possessing ‘signature’ fatty acids of type I methanotrophs. Int J Syst Evol Microbiol 57:472–479. Scholar
  29. Dedysh SN, Didriksen A, Danilova OV, Belova SE, Liebner S, Svenning MM (2015) Methylocapsa palsarum sp. nov., a methanotroph isolated from a sub-Arctic discontinuous permafrost ecosystem. Int J Syst Evol Microbiol 65:3618–3624. Scholar
  30. Dumont MG (2014) Primers: functional marker genes for methylotrophs and methanotrophs. In: McGenity TJ, Timmis KN, Nogales B (eds) Hydrocarbon and lipid microbiology protocols. Springer, Berlin, pp 57–77. Scholar
  31. Dunfield PF, Dedysh SN (2014) Methylocella: a gourmand among methanotrophs. Trends Microbiol 22:368–369. Scholar
  32. Dunfield PF, Khmelenina VN, Suzina NE, Trotsenko YA, Dedysh SN (2003) Methylocella silvestris sp. nov., a novel methanotroph isolated from an acidic forest cambisol. Int J Syst Evol Microbiol 53:1231–1239. Scholar
  33. Dunfield PF, Yuryev A, Senin P, Smirnova AV, Stott MB, Hou S, Ly B, Saw JH, Zhou Z, Ren Y (2007) Methane oxidation by an extremely acidophilic bacterium of the phylum Verrucomicrobia. Nature 450:879–882. Scholar
  34. Dunfield PF, Belova SE, Vorob’ev AV, Cornish SL, Dedysh SN (2010) Methylocapsa aurea sp. nov., a facultative methanotroph possessing a particulate methane monooxygenase, and emended description of the genus Methylocapsa. Int J Syst Evol Microbiol 60:2659–2664. Scholar
  35. Erikstad H, Birkeland NK (2015) Draft genome sequence of “Candidatus Methylacidiphilum kamchatkense” strain Kam1, a thermoacidophilic methanotrophic Verrucomicrobium. Genome Announc 3:e00065. Scholar
  36. Esson KC, Lin X, Kumaresan D, Chanton JP, Murrell JC, Kostka JE (2016) Alpha- and gammaproteobacterial methanotrophs codominate the active methane-oxidizing communities in an acidic boreal peat bog. Appl Environ Microbiol 82:2363–2371. Scholar
  37. Etiope G, Klusman R (2002) Geologic emissions of methane to the atmosphere. Chemosphere 49:777–789. Scholar
  38. Ettwig KF, Zhu B, Speth D, Keltjens JT, Jetten MSM, Kartal B (2016) Archaea catalyze iron-dependent anaerobic oxidation of methane. Proc Natl Acad Sci U S A 113:12792–12796. Scholar
  39. Giggenbach W (1995) Variations in the chemical and isotopic composition of fluids discharged from the Taupo Volcanic Zone, New Zealand. J Volcanol Geotherm Res 68:89–116. Scholar
  40. Gorham E (1991) Northern peatlands: role in the carbon cycle and probable response to climactic warming. Ecol Appl 1:183–195. Scholar
  41. Graef C, Hestnes AG, Svenning MM, Frenzel P (2011) The active methanotrophic community in a wetland from the high Arctic. Environ Microbiol Rep 3:466–472. Scholar
  42. Grodnitskaya ID, Trusova MY, Syrtsov SN, Koroban NV (2018) Structure of microbial communities of peat soils in two bogs in Siberian tundra and forest zones. Microbiology 87:89–102. Scholar
  43. Gupta V, Smemo KA, Yavitt JB, Basiliko N (2012) Active methanotrophs in two contrasting North American peatland ecosystems revealed using DNA-SIP. Microb Ecol 63:438–445. Scholar
  44. Gupta V, Smemo KA, Yavitt JB, Fowle D, Branfireun B, Basiliko N (2013) Stable isotopes reveal widespread anaerobic methane oxidation across latitude and peatland type. Environ Sci Technol 47:8273–8279. Scholar
  45. Hamilton R, Kits K, Ramonovskaya V, Rozova O, Yurimoto H, Iguchi H, Khmelenina V, Sakai Y, Dunfield PF, Klotz M, Knief C, Op den Camp HJM, Jetten MSM, Bringel F, Vuilleumier S, Svenning M, Shapiro N, Woyke T, Trotsenko YA, Stein L, Kaluzhnaya M (2015) Draft genomes of gammaproteobacterial methanotrophs isolated from terrestrial ecosystems. Genome Announc 3:e00515.
  46. Han D, Dedysh SN, Liesack W (2018) Unusual genomic traits suggest Methylocystis bryophila S285 to be well adapted for life in peatlands. Genome Biol Evol 10:623–628. Scholar
  47. Hanson RS, Hanson TE (1996) Methanotrophic bacteria. Microbiol Rev 60:439–471PubMedPubMedCentralGoogle Scholar
  48. Haroon MF, Hu S, Shi Y, Imelfort M, Keller J, Hugenholtz P, Yuan Z, Tyson GW (2013) Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage. Nature 500:567–570. Scholar
  49. Ho A, Kerckhof FM, Luke C, Reim A, Krause S, Boon N, Bodelier PL (2013) Conceptualizing functional traits and ecological characteristics of methane-oxidizing bacteria as life strategies. Environ Microbiol Rep 5:335–345. Scholar
  50. Holmes AJ, Roslev R, McDonald IR, Iversen N, Henriksen K, Murrell JC (1999) Characterization of methanotrophic bacterial populations in soils showing atmospheric methane uptake. Appl Environ Microbiol 65:3312–3318PubMedPubMedCentralGoogle Scholar
  51. Hou S, Makarova KS, Saw JH, Senin P, Ly BV, Zhou Z, Ren Y, Wang J, Galperin MY, Omelchenko MV, Wolf YI, Yutin N, Koonin EV, Stott MB, Mountain BW, Crowe MA, Smirnova AV, Dunfield PF, Feng L, Wang L, Alam M (2008) Complete genome sequence of the extremely acidophilic methanotroph isolate V4, Methylacidiphilum infernorum, a representative of the bacterial phylum Verrucomicrobia. Biol Direct 3:26. Scholar
  52. Hribljan JA, Suárez E, Heckman KA, Lilleskov EA, Chimner RA (2016) Peatland carbon stocks and accumulation rates in the Ecuadorian páramo. Wetl Ecol Manag 24:113–127. Scholar
  53. Hu BL, Shen LD, Lian X, Zhu Q, Liu S, Huang Q, He ZF, Geng S, Cheng DQ, Lou LP, Xu XY, Zheng P, He YF (2014) Evidence for nitrite-dependent anaerobic methane oxidation as a previously overlooked microbial methane sink in wetlands. Proc Natl Acad Sci U S A 111:4495–4500. Scholar
  54. Iguchi H, Yurimoto H, Sakai Y (2010) Methylovulum miyakonense gen. nov., sp. nov., a type I methanotroph isolated from forest soil. Int J Syst Evol Microbiol 61:810–815. Scholar
  55. Islam T, Jensen S, Reigstad LJ, Larsen O, Birkeland NK (2008) Methane oxidation at 55οC and pH 2 by a thermoacidophilic bacterium belonging to the Verrucomicrobia phylum. Proc Natl Acad Sci U S A 105:300–304. Scholar
  56. Islam T, Torsvik V, Larsen O, Bodrossy L, Ovreas L, Birkeland NK (2016) Acid-tolerant moderately thermophilic methanotrophs of the class Gammaproteobacteria isolated from tropical topsoil with methane seeps. Front Microbiol 7:851. Scholar
  57. Jaatinen K, Tuittila ES, Laine J, Yrjälä K, Fritze H (2005) Methane-oxidizng bacteria in a Finnish raised mire complex: effects of site fertility and drainage. Microb Ecol 50:429–439. Scholar
  58. Khadem AF, van Teeseling MC, van Niftrik L, Jetten MSM, Op den Camp HJM, Pol A (2012) Genomic and physiological analysis of carbon storage in the verrucomicrobial methanotroph “Ca. Methylacidiphilum fumariolicum” SolV. Front Microbiol 3:345.
  59. Kip N, van Winden JM, Pan Y, Bodrossy L, Reichart GJ, Smolders AJP, Jetten MSM, Sinninghe Damsté JS, Op den Camp HJM (2010) Global prevalence of methane oxiation by symbiotic bacteria in peat-moss ecosystems. Nat Geosci 3:617–621. Scholar
  60. Kip N, Dutilh BE, Pan Y, Bodrossy L, Neveling K, Kwint MP, Jetten MSM, Op den Camp HJM (2011a) Ultra-deep pyrosequencing of pmoA amplicons confirms the prevalence of Methylomonas and Methylocystis in Sphagnum mosses from a Dutch peat bog. Environ Microbiol Rep 3:667–673. Scholar
  61. Kip N, Ouyang W, van Winden J, Raghoebarsing A, van Niftrik L, Pol A, Pan Y, Bodrossy L, van Donselaar EG, Reichart GJ, Jetten MSM, Damsté JS, Op den Camp HJM (2011b) Detection, isolation, and characterization of acidophilic methanotrophs from Sphagnum mosses. Appl Environ Microbiol 77:5643–5654. Scholar
  62. Knief C (2015) Diversity and habitat preferences of cultivated and uncultivated aerobic methanotrophic bacteria evaluated based on pmoA as molecular marker. Front Microbiol 6:1346. Scholar
  63. Knief C, Dunfield PF (2005) Response and adaptation of different methanotrophic bacteria to low methane mixing ratios. Environ Microbiol 7:1307–1317. Scholar
  64. Knief C, Vanitchung S, Harvey NW, Conrad R, Dunfield PF, Chidthaisong A (2005) Diversity of methanotrophic bacteria in tropical upland soils under different land uses. Appl Environ Microbiol 71:3826–3831. Scholar
  65. Knief C, Kolb S, Bodelier PL, Lipski A, Dunfield PF (2006) The active methanotrophic community in hydromorphic soils changes in response to changing methane concentration. Environ Microbiol 8:321–333. Scholar
  66. Kravchenko I, Kizilova A, Menko E, Sirin A (2015) Methane cycling microbial communities in natural and drained sites of Taldom Peatland, Moscow region, Russia. Ann Res Rev Biol 6:121–132. Scholar
  67. Krumholz LR, Hollenback JL, Roskes SJ, Ringelberg DB (1995) Methanogensis and methanotroph within a Sphagnum peatland. FEMS Microbiol Ecol 18:215–224. Scholar
  68. Luesken FA, Wu ML, Op den Camp HJM, Keltjens JT, Stunnenberg H, Francoijs KJ, Strous M, Jetten MSM (2012) Effect of oxygen on the anaerobic methanotroph ‘Candidatus Methylomirabilis oxyfera’: kinetic and transcriptional analysis. Environ Microbiol 14(4):1024–1034. Scholar
  69. Martineau C, Whyte LG, Greer CW (2010) Stable isotope probing analysis of the diversity and activity of methanotrophic bacteria in soils from the Canadian high Arctic. Appl Environ Microbiol 76:5773–5784. Scholar
  70. McDonald IR, Uchiyama H, Kambe S, Yagi K, Murrell JC (1997) The soluble methane monooxygenase gene cluster of the trichloroethylene-degrading methanotroph Methylocystis sp. strain M. Appl Environ Microbiol 63(5):1898–1904PubMedPubMedCentralGoogle Scholar
  71. Mohammadi S, Pol A, van Alen TA, Jetten MSM, Op den Camp HJM (2017) Methylacidiphilum fumariolicum SolV, a thermoacidophilic ‘Knallgas’ methanotroph with both an oxygen-sensitive and -insensitive hydrogenase. ISME J 11:945–958. Scholar
  72. Morris SA, Radajewski S, Willison TW, Murrell JC (2002) Identification of the functionally active methanotroph population in a peat soil microcosm by stable-isotope probing. Appl Environ Microbiol 68:1446–1453. Scholar
  73. Omelchenko MV, Vasilieva LV, Zavarzin GA, Saveleva ND, Lysenko AM, Mityushina LL, Khmelenina VN, Trotsenko YA (1996) A novel psychrophilic methanotroph of the genus Methylobacter. Mikrobiologiya 65:384–389Google Scholar
  74. Pagaling E, Yang K, Yan T (2014) Pyrosequencing reveals correlations between extremely acidophilic bacterial communities with hydrogen sulphide concentrations, pH and inert polymer coatings at concrete sewer crown surfaces. J Appl Microbiol 117:50–64. Scholar
  75. Page SE, Rieley JO, Banks CJ (2011) Global and regional importance of the tropical peatland carbon pool. Glob Chang Biol 17:798–818. Scholar
  76. Pol A, Heijmans K, Harhangi HR, Tedesco D, Jetten MSM, Op den Camp HJM (2007) Methanotrophy below pH 1 by a new Verrucomicrobia species. Nature 450:874–878. Scholar
  77. Pratscher J, Vollmers J, Wiegand S, Dumont MG, Kaster AK (2018) Unravelling the identity, metabolic potential and global biogeography of the atmospheric methane-oxidizing upland soil cluster α. Environ Microbiol. Scholar
  78. Putkinen A, Larmola T, Tuomivirta T, Siljanen HM, Bodrossy L, Tuittila ES, Fritze H (2012) Water dispersal of methanotrophic bacteria maintains functional methane oxidation in Sphagnum mosses. Front Microbiol 3:15. Scholar
  79. Putkinen A, Larmola T, Tuomivirta T, Siljanen HM, Bodrossy L, Tuittila ES, Fritze H (2014) Peatland succession induces a shift in the community composition of Sphagnum-associated active methanotrophs. FEMS Microbiol Ecol 88:596–611. Scholar
  80. Raghoebarsing AA, Smolders AJP, Schmid MC, Rijpstra WIC, Wolters-Arts M, Derksen J, Jetten MSM, Schouten S, Sinninghe Damsté JS, Lamers LPM, Roelofs JGM, Op den Camp HJM, Strous M (2005) Methanotrophic symbionts provide carbon for photosynthesis in peat bogs. Nature 436:1153–1156. Scholar
  81. Richter-Menge J, Mathis J (2017) The Arctic: overview. In: Blunden J, Arndt D (eds) State of the climate in 2016, vol 98. American Meteorological Society, Boston, p S129. Scholar
  82. Ricke P, Kube M, Nakagawa S, Erkel C, Reinhardt R, Liesack W (2005) First genome data from uncultured upland soil cluster alpha methanotrophs provide further evidence for a close phylogenetic relationship to Methylocapsa acidiphila B2 and for high-affinity methanotrophy involving particulate methane monooxygenase. Appl Environ Microbiol 71:7472–7482. Scholar
  83. Segers R (1998) Methane production and methane consumption: a review of processes underlying wetland methane fluxes. Biogeochemistry 41:23–51CrossRefGoogle Scholar
  84. Sharp CE, Op den Camp HJM, Tamas I, Dunfield PF (2013) Unusual members of the PVC superphylum: the methanotrophic Verrucomicrobia genus “Methylacidiphilum”. In: Fuerst J (ed) Planctomycetes: cell structure, origins and biology. Springer, Berlin, pp 211–227CrossRefGoogle Scholar
  85. Sharp CE, Smirnova AV, Graham JM, Stott MB, Khadka R, Moore TR, Grasby SE, Strack M, Dunfield PF (2014) Distribution and diversity of Verrucomicrobia methanotrophs in geothermal and acidic environments. Environ Microbiol 16:1867–1878. Scholar
  86. 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 7:539. Scholar
  87. Siljanen HM, Saari A, Krause S, Lensu A, Abell GC, Bodrossy L, Bodelier PL, Martikainen PJ (2011) Hydrology is reflected in the functioning and community composition of methanotrophs in the littoral wetland of a boreal lake. FEMS Microbiol Ecol 75:430–445. Scholar
  88. Smemo KA, Yavitt JB (2007) Evidence for anaerobic CH4 oxidation in freshwater peatlands. Geomicrobiol J 24:583–597. Scholar
  89. Smemo KA, Yavitt JB (2011) Anaerobic oxidation of methane: an underappreciated aspect of methane cycling in peatland ecosystems? Biogeosciences 8:779–793. Scholar
  90. Smith L, MacDonald G, Velichko A, Beilman D, Borisova O, Frey K, Kremenetski K, Sheng Y (2004) Siberian peatlands a net carbon sink and global methane source since the early Holocene. Science 303:353–355. Scholar
  91. Sundh I, Borga P, Nilsson M, Svensson BH (1995) Estimation of cell numbers of methanotrophic bacteria in boreal peatlands based on analysis of specific phospholipid fatty acids. FEMS Microbiol Ecol 18:103–112. Scholar
  92. Svenning MM, Hestnes AG, Wartiainen I, Stein L, Klotz MG, Kaluzhnaya M, Spang A, Bringel F, Vuilleumier S, Lajus A, Medigue C, Bruce D, Cheng J, Goodwin L, Ivanova N, Han J, Han C, Hauser LJ, Held B, Land M, Lapidus A, Lucas S, Nolan M, Pitluck S, Woyke T (2011) Genome sequence of the Arctic methanotroph Methylobacter tundripaludum SV96. J Bacteriol 193(22):6418–6419. Scholar
  93. Tavormina PL, Orphan VJ, Kalyuzhnaya MG, Jetten MSM, Klotz MG (2011) A novel family of functional operons encoding methane/ammonia monooxygenase-related proteins in gammaproteobacterial methanotrophs. Environ Microbiol Rep 3:91–100. Scholar
  94. Tourova T, Omelchenko MV, Fegeding K, Vasilieva L (1999) The phylogenetic position of Methylobacter psychrophilus sp. nov. Mikrobiologiia 68:493–495Google Scholar
  95. Trotsenko YA, Khmelenina VN (2005) Aerobic methanotrophic bacteria of cold ecosystems. FEMS Microbiol Ecol 53:15–26. Scholar
  96. Tveit A, Schwacke R, Svenning MM, Urich T (2013) Organic carbon transformations in high-Arctic peat soils: key functions and microorganisms. ISME J 7:299–311. Scholar
  97. Tveit AT, Ulrich T, Svenning MM (2014) Metatranscriptomic analysis of Arctic peat soil microbiota. Appl Environ Microbiol 80:5761–5772. Scholar
  98. Tveit AT, Urich T, Frenzel P, Svenning MM (2015) Metabolic and trophic interactions modulate methane production by Arctic peat microbiota in response to warming. Proc Natl Acad Sci U S A 112:E2507–E2516. Scholar
  99. Vaksmaa A, van Alen TA, Ettwig KF, Lupotto E, Vale G, Jetten MSM, Luke C (2017) Stratification of diversity and activity of methanogenic and methanotrophic microorganisms in a nitrogen-fertilized Italian paddy soil. Front Microbiol 8:2127.
  100. van Teesling MC, Pol A, Harhangi HR, van der Zwart S, Jetten MS, Op den Camp HJM, van Niftrik L (2014) Expanding the verrucomicrobial methanotrophic world: description of three novel species of Methylacidimicrobium gen. nov. Appl Environ Microbiol 80:6782–6781. Scholar
  101. Vorobev AV, Baani M, Doronina NV, Brady AL, Liesack W, Dunfield PF, Dedysh SN (2011) Methyloferula stellata gen. nov., sp. nov., an acidophilic, obligately methanotrophic bacterium that possesses only a soluble methane monooxygenase. Int J Syst Evol Microbiol 61:2456–2463. Scholar
  102. Wartiainen I, Hestnes AG, McDonald IR, Svenning MM (2006) Methylobacter tundripaludum sp. nov., a methane-oxidizing bacterium from Arctic wetland soil on the Svalbard islands, Norway (78° N). Int J Syst Evol Microbiol 56:109–113. Scholar
  103. Welte CU, Rasigraf O, Vaksmaa A, Versantvoort W, Arshad A, Op den Camp HJM, Jetten MSM, Luke C, Reimann J (2016) Nitrate- and nitrite-dependent anaerobic oxidation of methane. Environ Microbiol Rep 8:941–955. Scholar
  104. Yu L, Huang Y, Zhang W, Li T, Sun W (2017) Methane uptake in global forest and grassland soils from 1981 to 2010. Sci Total Environ 607–608:1163–1172. Scholar
  105. Yule CM, Lim YY, Lim TY (2016) Degradation of tropical Malaysian peatlands decreases levels of phenolics in soil and in leaves of Macaranga pruinosa. Front Earth Sci 4:45. Scholar
  106. Zhu B, van Dijk G, Fritz C, Smolders AJM, Pol A, Jetten MSM, Ettwig KF (2012) Anaerobic oxidization of methane in a minerotrophic peatland: enrichment of nitrite-dependent methane-oxidizing bacteria. Appl Environ Microbiol 78(24):8657–8665. Scholar

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Authors and Affiliations

  • Tobin J. Verbeke
    • 1
  • Svetlana N. Dedysh
    • 2
  • Peter F. Dunfield
    • 1
    Email author
  1. 1.Department of Biological SciencesUniversity of CalgaryCalgaryCanada
  2. 2.S. N. Winogradsky Institute of Microbiology, Research Center of Biotechnology, Russian Academy of SciencesMoscowRussia

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