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Environmental problems - Chemical approaches
RESEARCH ARTICLE

Methane formation in aerobic environments

Frank Keppler A H , Mihály Boros B , Christian Frankenberg C , Jos Lelieveld A , Andrew McLeod D , Anna Maria Pirttilä E , Thomas Röckmann F and Jörg-Peter Schnitzler G
+ Author Affiliations
- Author Affiliations

A Max-Planck-Institute for Chemistry, D-55128 Mainz, Germany.

B Institute of Surgical Research, University of Szeged, H-6722 Szeged, Hungary.

C Netherlands Institute for Space Research (SRON), Sorbonnelaan 2, NL-3584 CA Utrecht, the Netherlands.

D School of GeoSciences, University of Edinburgh, Crew Building, The King’s Buildings, West Mains Road, Edinburgh, EH9 3JN, United Kingdom.

E Department of Biology, University of Oulu, PO Box 3000, FIN-90014 Oulu, Finland.

F Institute for Marine and Atmospheric Research Utrecht, Utrecht University, NL-3584 CC Utrecht, the Netherlands.

G Institute for Meteorology and Climate Research (IMK-IFU), Karlsruhe Institute of Technology, D-82467 Garmisch-Partenkirchen, Germany.

H Corresponding author. Email: frank.keppler@mpic.de

Environmental Chemistry 6(6) 459-465 https://doi.org/10.1071/EN09137
Submitted: 3 November 2009  Accepted: 17 November 2009   Published: 18 December 2009

Environmental context. Methane is an important greenhouse gas and its atmospheric concentration has drastically increased since pre-industrial times. Until recently biological methane formation has been associated exclusively with anoxic environments and microbial activity. In this article we discuss several alternative formation pathways of methane in aerobic environments and suggest that non-microbial methane formation may be ubiquitous in terrestrial and marine ecosystems.

Abstract. Methane (CH4), the second principal anthropogenic greenhouse gas after CO2, is the most abundant reduced organic compound in the atmosphere and plays a central role in atmospheric chemistry. Therefore a comprehensive understanding of its sources and sinks and the parameters that control emissions is prerequisite to simulate past, present and future atmospheric conditions. Until recently biological CH4 formation has been associated exclusively with anoxic environments and methanogenic activity. However, there is growing and convincing evidence of alternative pathways in the aerobic biosphere including terrestrial plants, soils, marine algae and animals. Identifying and describing these sources is essential to complete our understanding of the biogeochemical cycles that control CH4 in the atmospheric environment and its influence as a greenhouse gas.


Acknowledgements

We thank N. Brüggemann, E. Damm, M. Ghyczy, A. Jugold, C. Kammann, D. Messenger, A. Sessitsch, J. Stefels, I. Vigano, Z. Wang and A. Wishkerman for presenting their work at the ‘First workshop on aerobic methane formation in the environment including plants and animals’ held on 26 and 27 February 2009 at the MPI for Chemistry in Mainz. We are grateful to J. Hamilton and K. Smith for reviewing the manuscript. We thank EON Ruhrgas for financial support of the workshop. F. Keppler is supported by the European Science Foundation (European Young Investigator Award) and the German Science Foundation (KE 884/2–1).


References


[1]   Forster P., Ramaswamy V., Artaxo P., Berntsen T., Betts R., Fahey D. W., Haywood J., Lean J., et al., Changes in atmospheric constituents and in radiative forcing, in Climate Change 2007: The Physical Science Basis Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (Eds S. Solomon, M. Manning, Z. Chen, M. Marquis, K. B. Averyt, M. Tignor, H. L. Miller) 2007 (Cambridge University Press: Cambridge, UK).

[2]   J. Lelieveld , P. J. Crutzen , F. J. Dentener , Changing concentration, lifetime and climate forcing of atmospheric methane. Tellus B 1998 , 50,  128.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[3]   Denman K. L., Brasseur G., Chidthaisong A., Ciais P., Cox P. M., Dickinson R. E., Hauglustaine D., Heinze C., et al., Couplings between changes in the climate system and biogeochemistry, in Climate Change 2007: The Physical Science Basis Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (Eds S. Solomon, M. Manning, Z. Chen, M. Marquis, K. B. Averyt, M. Tignor, H. L. Miller) 2007 (Cambridge University Press: Cambridge, UK).

[4]   S. Houweling , T. Kaminski , F. Dentener , J. Lelieveld , M. Heimann , Inverse modeling of methane sources and sinks using the adjoint of a global transport model. J. Geophys. Res. – Atmos. 1999 , 104,  26137.
        | Crossref | GoogleScholarGoogle Scholar | CAS |  open url image1

[5]   P. Bergamaschi , C. Frankenberg , J. F. Meirink , M. Krol , F. Dentener , T. Wagner , U. Platt , J. O. Kaplan , et al. Satellite chartography of atmospheric methane from SCIAMACHYon board ENVISAT: 2. Evaluation based on inverse model simulations. J. Geophys. Res. – Atmos. 2007 , 112,  D02304.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[6]   C. Frankenberg , P. Bergamaschi , A. Butz , S. Houweling , J. F. Meirink , J. Notholt , A. K. Petersen , H. Schrijver , T. Warneke , I. Aben , Tropical methane emissions: A revised view from SCIAMACHY onboard ENVISAT. Geophys. Res. Lett. 2008 , 35,  L15811.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[7]   F. Keppler , J. T. G. Hamilton , M. Brass , T. Rockmann , Methane emissions from terrestrial plants under aerobic conditions. Nature 2006 , 439,  187.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[8]   S. Houweling , T. Rockmann , I. Aben , F. Keppler , M. Krol , J. F. Meirink , E. J. Dlugokencky , C. Frankenberg , Atmospheric constraints on global emissions of methane from plants. Geophys. Res. Lett. 2006 , 33,  L15821.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[9]   D. J. Beerling , T. Gardiner , G. Leggett , A. McLeod , W. P. Quick , Missing methane emissions from leaves of terrestrial plants. Glob. Change Biol. 2008 , 14,  1821.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[10]   T. A. Dueck , R. de Visser , H. Poorter , S. Persijn , A. Gorissen , W. de Visser , A. Schapendonk , J. Verhagen , et al. No evidence for substantial aerobic methane emission by terrestrial plants: a 13C-labelling approach. New Phytol. 2007 , 175,  29.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[11]   M. U. F. Kirschbaum , A. Walcroft , No detectable aerobic methane efflux from plant material, nor from adsorption/desorption processes. Biogeosciences 2008 , 5,  1551.
        |  CAS |  open url image1

[12]   J. P. Megonigal , A. B. Guenther , Methane emissions from upland forest soils and vegetation. Tree Physiol. 2008 , 28,  491.
        |  CAS | PubMed |  open url image1

[13]   R. E. R. Nisbet , R. Fisher , R. H. Nimmo , D. S. Bendall , P. M. Crill , A. V. Gallego-Sala , E. R. C. Hornibrook , E. López-Juez , et al. Emission of methane from plants. Proc. R. Soc. B – Biol. Sci. 2009 , 276,  1347.
        | Crossref | GoogleScholarGoogle Scholar | CAS |  open url image1

[14]   A. J. Parsons , P. C. D. Newton , H. Clark , F. M. Kelliher , Scaling methane emissions from vegetation. Trends Ecol. Evol. 2006 , 21,  423.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[15]   Kirschbaum M. U. F., Niinemets Ü., Bruhn D., Winters A. J., How important is aerobic methane release by plants? in Functional Plant Science and Biotechnology 2007, pp. 138–145 (Global Science Books: UK).

[16]   M. U. F. Kirschbaum , D. Bruhn , D. M. Etheridge , J. R. Evans , G. D. Farquhar , R. M. Gifford , K. I. Paul , A. J. Winters , A comment on the quantitative significance of aerobic methane release by plants. Funct. Plant Biol. 2006 , 33,  521.
        | Crossref | GoogleScholarGoogle Scholar | CAS |  open url image1

[17]   C. L. Butenhoff , M. A. K. Khalil , Global methane emissions from terrestrial plants. Environ. Sci. Technol. 2007 , 41,  4032.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[18]   D. F. Ferretti , J. B. Miller , J. W. C. White , K. R. Lassey , D. C. Lowe , D. M. Etheridge , Stable isotopes provide revised global limits of aerobic methane emissions from plants. Atmos. Chem. Phys. 2007 , 7,  237.
        |  CAS |  open url image1

[19]   C. J. P. Smeets , R. Holzinger , I. Vigano , A. H. Goldstein , T. Röckmann , Eddy covariance methane measurements at a Ponderosa pine plantation in California. Atmos. Chem. Phys. Discuss. 2009 , 9,  5201.
         open url image1

[20]   D. R. Bowling , J. B. Miller , M. E. Rhodes , S. P. Burns , R. K. Monson , D. Baer , Soil, plant, and transport influences on methane in a subalpine forest under high ultraviolet irradiance. Biogeosciences 2009 , 6,  1311.
        |  CAS |  open url image1

[21]   E. Sanhueza , L. Donoso , Methane emission from tropical savanna Trachypogon sp. grasses. Atmos. Chem. Phys. 2006 , 6,  5315.
        |  CAS |  open url image1

[22]   G. M. Cao , X. L. Xu , R. J. Long , Q. L. Wang , C. T. Wang , Y. G. Du , X. Q. Zhao , Methane emissions by alpine plant communities in the Qinghai–Tibet Plateau. Biol. Lett. 2008 , 4,  681.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[23]   Z. P. Wang , X. G. Han , G. G. Wang , Y. Song , J. Gulledge , Aerobic methane emission from plants in the Inner Mongolia Steppe. Environ. Sci. Technol. 2008 , 42,  62.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[24]   Z. P. Wang , J. Gulledge , J. Q. Zheng , W. Liu , L. H. Li , X. G. Han , Physical injury stimulates aerobic methane emissions from terrestrial plants. Biogeosciences 2009 , 6,  615.
        |  CAS |  open url image1

[25]   I. Vigano , H. van Weelden , R. Holzinger , F. Keppler , A. McLeod , T. Röckmann , Effect of UV radiation and temperature on the emission of methane from plant biomass and structural components. Biogeosciences 2008 , 5,  937.
        |  CAS |  open url image1

[26]   I. Vigano , T. Röckmann , R. Holzinger , A. van Dijk , F. Keppler , M. Greule , W. A. Brand , H. Geilmann , H. van Weelden , The stable isotope signature of methane emitted from plant material under UV irradiation. Atmos. Environ. 2009 , 43,  5637.
        | Crossref | GoogleScholarGoogle Scholar | CAS |  open url image1

[27]   A. R. McLeod , S. C. Fry , G. J. Loake , D. J. Messenger , D. S. Reay , K. A. Smith , B.-W. Yun , Ultraviolet radiation drives methane emissions from terrestrial plant pectins. New Phytol. 2008 , 180,  124.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[28]   D. J. Messenger , A. R. McLeod , S. C. Fry , The role of ultraviolet radiation, photosensitizers, reactive oxygen species and ester groups in mechanisms of methane formation from pectin. Plant Cell Environ. 2009 , 32,  1.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[29]   D. J. Messenger , A. R. McLeod , S. C. Fry , Reactive oxygen species in aerobic methane formation from vegetation. Plant Signal. Behav. 2009 , 4,  1.
        | PubMed |  open url image1

[30]   N. Brüggemann , R. Meier , D. Steigner , I. Zimmer , S. Louis , J. P. Schnitzler , Nonmicrobial aerobic methane emission from poplar shoot cultures under low-light conditions. New Phytol. 2009 , 182,  912.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[31]   D. Bruhn , T. N. Mikkelsen , J. Obro , W. G. T. Willats , P. Ambus , Effects of temperature, ultraviolet radiation and pectin methyl esterase on aerobic methane release from plant material. Plant Biol. 2009 , 11,  43.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[32]   F. Keppler , J. T. G. Hamilton , W. C. McRoberts , I. Vigano , M. Brass , T. Rockmann , Methoxyl groups of plant pectin as a precursor of atmospheric methane: evidence from deuterium labelling studies. New Phytol. 2008 , 178,  808.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[33]   M. Ghyczy , C. Torday , J. Kaszaki , A. Szabo , M. Czobel , M. Boros , Hypoxia-induced generation of methane in mitochondria and eukaryotic cells – an alternative approach to methanogenesis. Cell. Physiol. Biochem. 2008 , 21,  251.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[34]   S. P. Wang , X. X. Yang , X. W. Lin , Y. G. Hu , C. Y. Luo , G. P. Xu , Z. Zhang , A. Su , X. Chang , Z. Chao , J. Duan , Methane emission by plant communities in an alpine meadow on the Qinghai–Tibetan Plateau: a new experimental study of alpine meadows and oat pasture. Biol. Lett. 2009 , 5,  535.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[35]   K. Apel , H. Hirt , Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 2004 , 55,  373.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[36]   I. M. Møller , P. E. Jensen , A. Hansson , Oxidative modifications to cellular components in plants. Annu. Rev. Plant Biol. 2007 , 58,  459.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[37]   P. Schopfer , A. Liszkay , M. Bechtold , G. Frahry , A. Wagner , Evidence that hydroxyl radicals mediate auxin-induced extension growth. Planta 2002 , 214,  821.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[38]   M. M. Qaderi , D. M. Reid , Methane emissions from six crop species exposed to three components of global climate change: temperature, ultraviolet-B radiation and water stress. Physiol. Plant. 2009 , 137,  139.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[39]   B. Davison , A. Brunner , C. Ammann , C. Spirig , M. Jocher , A. Neftel Cut-induced , VOC emissions from agricultural grasslands. Plant Biol. 2008 , 10,  76.
        |  CAS | | Crossref |  open url image1

[40]   E. Körner , C. C. von Dahl , G. Bonaventure , I. T. Baldwin , Pectin methylesterase NaPME1 contributes to the emission of methanol during insect herbivory and to the elicitation of defence responses in Nicotiana attenuata. J. Exp. Bot. 2009 , 60,  2631.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[41]   N. V. Doronina , E. G. Ivanova , N. E. Suzina , Y. A. Trotsenko , Methanotrophs and methylobacteria are found in woody plant tissues within the winter period. Microbiology 2004 , 73,  702.
        | Crossref | GoogleScholarGoogle Scholar | CAS |  open url image1

[42]   Pirttilä A. M., Hohtola A., Ivanova E. G., Fedorov D. N. F., Doronina N. V., Trotsenko Y. A., Identification and localization of methylotrophic plant-associated bacteria, in Prospects and Applications for Plant Associated Microbes A Laboratory Manual, Part A: Bacteria (Eds S. Sorvari, A. M. Pirttilä) 2008, pp. 218–224 (Karhukopio OY: Turku, Finland).

[43]   L. F. W. Roesch , F. A. O. Camargo , F. M. Bento , E. W. Triplett , Biodiversity of diazotrophic bacteria within the soil, root and stem of field-grown maize. Plant Soil 2008 , 302,  91.
        | Crossref | GoogleScholarGoogle Scholar | CAS |  open url image1

[44]   D. Seghers , L. Wittebolle , E. M. Top , W. Verstraete , S. D. Siciliano , Impact of agricultural practices on the Zea mays L. endophytic community. Appl. Environ. Microbiol. 2004 , 70,  1475.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[45]   R. S. Hanson , T. E. Hanson , Methanotrophic bacteria. Microbiol. Rev. 1996 , 60,  439.
        |  CAS | PubMed |  open url image1

[46]   B. Gilbert , B. Assmus , A. Hartmann , P. Frenzel , In situ localization of two methanotrophic strains in the rhizosphere of rice plants. FEMS Microbiol. Ecol. 1998 , 25,  117.
        | Crossref | GoogleScholarGoogle Scholar | CAS |  open url image1

[47]   G. M. King , In situ analyses of methane oxidation associated with the roots and rhizomes of a bur reed, Sparganium eurycarpum, in a Maine wetland. Appl. Environ. Microbiol. 1996 , 62,  4548.
        |  CAS | PubMed |  open url image1

[48]   A. A. Raghoebarsing , A. J. P. Smolders , M. C. Schmid , W. I. C. Rijpstra , M. Wolters-Arts , J. Derksen , M. S. M. Jetten , S. Schouten , et al. Methanotrophic symbionts provide carbon for photosynthesis in peat bogs. Nature 2005 , 436,  1153.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[49]   S. N. Dedysh , C. Knief , P. F. Dunfield , Methylocella species are facultatively methanotrophic. J. Bacteriol. 2005 , 187,  4665.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[50]   M. Boros , A. Wolfard , M. Ghyczy , In vivo evidence of reductive stress-induced methane production. Shock 1999 , 12,  199.
         open url image1

[51]   M. Ghyczy , C. Torday , J. Kaszaki , A. Szabo , M. Czobel , M. Boros , Oral phosphatidylcholine pretreatment decreases ischemia-reperfusion-induced methane generation and the response in the small intestine. Shock 2008 , 30,  596.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[52]   M. Ghyczy , C. Torday , M. Boros , Simultaneous generation of methane, carbon dioxide, and carbon monoxide from choline and ascorbic acid – a defensive mechanism against reductive stress? FASEB J. 2003 , 17,  1124.
        |  CAS | PubMed |  open url image1

[53]   M. Ghyczy , M. Boros , Electrophilic methyl groups present in the diet ameliorate pathological states induced by reductive and oxidative stress: a hypothesis. Br. J. Nutr. 2001 , 85,  409.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[54]   K. K. Niyogi , Safety valves for photosynthesis. Curr. Opin. Plant Biol. 2000 , 3,  455.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[55]   Kiene R. P., Production and consumption of methane in aquatic systems, in Microbial Production and Consumption of Greenhouse Gases: Methane, Nitrogen Oxides, and Halomethanes (Eds J. E. Rogers, W. B. Whitman) 1991, pp. 111–146 (American Society Microbiology: Washington, DC).

[56]   D. M. Karl , B. D. Tilbrook , Production and transport of methane in oceanic particulate organic-matter. Nature 1994 , 368,  732.
        | Crossref | GoogleScholarGoogle Scholar | CAS |  open url image1

[57]   E. Damm , R. P. Kiene , J. Schwarz , E. Falck , G. Dieckmann , Methane cycling in Arctic shelf water and its relationship with phytoplankton biomass and DMSP. Mar. Chem. 2008 , 109,  45.
        | Crossref | GoogleScholarGoogle Scholar | CAS |  open url image1

[58]   H. W. Bange , G. Uher , Photochemical production of methane in natural waters: implications for its present and past oceanic source. Chemosphere 2005 , 58,  177.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[59]   R. M. Moore , A photochemical source of methyl chloride in saline waters. Environ. Sci. Technol. 2008 , 42,  1933.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[60]   D. M. Karl , L. Beversdorf , K. M. Bjorkman , M. J. Church , A. Martinez , E. F. DeLong , Aerobic production of methane in the sea. Nat. Geosci. 2008 , 1,  473.
        | Crossref | GoogleScholarGoogle Scholar | CAS |  open url image1

[61]   A. Kock , S. Gebhardt , H. W. Bange , Methane emissions from the upwelling area off Mauritania (NW Africa). Biogeosciences 2008 , 5,  1119.
        |  CAS |  open url image1