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 GA 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).
[1]
[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 |
[3]
[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 |
[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 |
[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 |
[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 |
[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 |
[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 |
[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 |
[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 |
[12]
J. P. Megonigal ,
A. B. Guenther ,
Methane emissions from upland forest soils and vegetation.
Tree Physiol. 2008
, 28, 491.
|
CAS |
PubMed |
[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 |
[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 |
[15]
[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 |
[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 |
[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 |
[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.
[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 |
[21]
E. Sanhueza ,
L. Donoso ,
Methane emission from tropical savanna Trachypogon sp. grasses.
Atmos. Chem. Phys. 2006
, 6, 5315.
|
CAS |
[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 |
[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 |
[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 |
[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 |
[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 |
[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 |
[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 |
[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 |
[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 |
[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 |
[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 |
[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 |
[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 |
[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 |
[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 |
[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 |
[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 |
[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 |
[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 |
[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 |
[42]
[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 |
[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 |
[45]
R. S. Hanson ,
T. E. Hanson ,
Methanotrophic bacteria.
Microbiol. Rev. 1996
, 60, 439.
|
CAS |
PubMed |
[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 |
[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 |
[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 |
[49]
S. N. Dedysh ,
C. Knief ,
P. F. Dunfield ,
Methylocella species are facultatively methanotrophic.
J. Bacteriol. 2005
, 187, 4665.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[50]
M. Boros ,
A. Wolfard ,
M. Ghyczy ,
In vivo evidence of reductive stress-induced methane production.
Shock 1999
, 12, 199.
[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 |
[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 |
[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 |
[54]
K. K. Niyogi ,
Safety valves for photosynthesis.
Curr. Opin. Plant Biol. 2000
, 3, 455.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[55]
[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 |
[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 |
[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 |
[59]
R. M. Moore ,
A photochemical source of methyl chloride in saline waters.
Environ. Sci. Technol. 2008
, 42, 1933.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[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 |
[61]
A. Kock ,
S. Gebhardt ,
H. W. Bange ,
Methane emissions from the upwelling area off Mauritania (NW Africa).
Biogeosciences 2008
, 5, 1119.
|
CAS |