Methane formation in aerobic environments - CSIRO Publishing

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F. Keppler et al., Environ. Chem. 2009, 6, 459–465. doi:10.1071/EN09137

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 RöckmannF and Jörg-Peter SchnitzlerG A Max-Planck-Institute

for Chemistry, D-55128 Mainz, Germany. 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: [email protected] B Institute

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.

Introduction Methane (CH4 ) plays a central role as a radiatively and chemically active gas in our atmosphere.[1] According to established knowledge, it is produced primarily by methanogens under anaerobic conditions in wetlands, rice fields, landfills and the gastrointestinal tracts of ruminants and termites, and by non-microbial emissions from fossil fuel use and biomass burning. The global atmospheric CH4 loss is dominated by the reaction with hydroxyl radicals in the troposphere. This loss term can be constrained by measurements of methyl chloroform, an anthropogenic tracer with similar chemistry to that of CH4 and well known emissions.[2] Accounting also for minor CH4 loss processes such as stratospheric destruction and microbial consumption in soils, the total sink strength is 500–600 Tg year−1 .[3] As atmospheric CH4 levels have been rather constant in the last decade until 2007, this must be balanced by a total global source of the same magnitude. Partitioning the source between categories that make up the 500–600 Tg year−1 is, however, a major challenge. Bottom-up estimates are prone to large errors from © CSIRO 2009

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up-scaling. Top-down inverse modelling studies[4] use extended measurement series at the surface, the CH4 isotopic composition, and the newly available satellite observations to constrain the relative source strengths[5] and investigate recent changes in the CH4 budget. The space-borne measurements (Fig. 1) are particularly valuable in the tropics, where surface measurements do not constrain inversion calculations well and they have resulted in upward estimates of tropical CH4 emissions, although the recent correction of a retrieval bias has moderated this revision to ∼200 Tg year−1 tropical emissions.[6] A newly identified source that might contribute a fraction of the tropical emissions could be the direct release by vegetation, as suggested by Keppler et al.[7] who reported from laboratory experiments that living plants, plant litter and the structural plant component pectin emit CH4 to the atmosphere under aerobic conditions. This unexpected new source and its global strength have been intensely debated and remain controversial.[8–14] The original extrapolation of emissions from living plants of 62– 236 Tg CH4 year−1[7] is likely an overestimate and several studies (Table 1) suggested much lower but still potentially 1448-2517/09/060459

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Global total column average of methane as measured from SCIAMACHY onboard ENVISAT from 2003 through 2005.

important CH4 fluxes from vegetation.[8,14–18] While flux measurements using towers above plant canopies usually reveal a net soil sink,[19] the direct detection and measurement of smaller CH4 emissions from canopy foliage is problematic[20] and vegetation emissions have only been quantified directly in the field by using static flux chambers.[21,22] Uncertainties in the partitioning of the currently understood global CH4 budget could accommodate a non-microbial source of up to 10% of the total, notably in the tropics, for which source attribution based on inverse modelling is ambiguous and cannot be resolved without process-based studies. By adopting this 10% as an upper limit, the global CH4 release by vegetation should range between levels that are insignificant to a maximum of 50–60 Tg year−1 . These values are similar to the range of alternative extrapolations for possible vegetation emissions (Table 1). Although the contribution of vegetation to the global budget remains equivocal, the processes leading to CH4 formation in aerobic environments are receiving increased attention by various scientific disciplines. Combining recent observations in plant, animal and marine biology, it is now apparent that several reaction pathways exist by which CH4 is generated under aerobic conditions, suggesting that non-methanogenic biological formation may be ubiquitous in terrestrial and marine ecosystems.

Keppler et al.[7] suggested that the methyl moiety of the esterified carboxyl groups (methoxyl groups) of pectin was involved in CH4 formation. Extending this idea, Vigano et al.,[25] McLeod et al.[27] and Bruhn et al.[31] showed that release of CH4 from structural components (e.g. pectin and lignin) as well as fresh and dried leaf tissue depends on UV irradiation. The fact that UV irradiation was excluded by Dueck et al.,[10] Beerling et al.[9] and Kirschbaum and Walcroft[11] might explain the absence of CH4 emissions in their studies. Notably, Vigano et al.[25] demonstrated CH4 emissions from the same 13 C-labelled material used by Dueck et al.[10] when treated with UV-irradiation. On the other hand, the high emission rates originally reported inside glass vials by Keppler et al.[7] did not involve above-ambient UV levels, and these observations are still not understood. Furthermore, the removal of methoxyl groups[27,31] stopped CH4 production from UV-irradiated pectin. These observations agree with those of Keppler et al.[32] who employed isotopicallylabelled pectin to demonstrate that methoxyl groups in plant pectin are indeed precursors of CH4. These studies provide unambiguous evidence that CH4 can be formed from methoxyl groups of pectin under the influence of UV irradiation (including natural sunlight[27] ). Isotope studies using natural abundance and labelled material[25,32] indicate that at least one additional CH4 source must exist. Therefore, other plant biomolecules containing methoxyl groups, e.g. fatty acids or S-adenosylmethionine (SAM),[33] should also be investigated as possible precursors of CH4 formation. Brüggemann et al.[30] demonstrated small aerobic CH4 emissions from poplar shoot cultures even at ambient temperature and low light conditions, and notably in the absence of UVirradiation. In contrast, Nisbet et al.[13] suggested that soilderived CH4 from the transpiration stream is the source of reported foliar CH4 emission. However, this cannot explain the evidence of several stable isotope-labelling studies.[25,30,32] In further studies, Wang et al.[23] reported net emissions of CH4

Vegetation-derived methane Intensive work on the mechanisms and strength of CH4 emissions from plant matter has been initiated. Whilst some studies[9–13] did not observe any CH4 emissions from plant leaves, several others[22–31] clearly identified aerobic CH4 release from foliage. But how can these opposing results be rationalised? Insights that may help reconcile the discrepancies come from studies that consider potential plant precursors and mechanistic details of CH4 release from plant material. 460

Megonigal and Guenther[12]

from shrubs of Mongolian Steppe and Cao et al.[22] from grassland of the Qinghai–Tibet Plateau, although it is not clear if emissions observed by the latter study truly originate from vegetation.[34]

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Stress-related mechanisms? An important role of UV-generated reactive oxygen species (ROS) was postulated by Messenger et al.[28,29] who used ROSscavengers and ROS-generators to reveal that hydoxyl radicals (• OH) and singlet oxygen (but not hydrogen peroxide or superoxide radicals) are involved in CH4 release from pectin. The requirement of specific ROS to generate CH4 from plant material might be a key to understand the functional mechanisms of aerobic CH4 emission and could explain the divergent results of published CH4 emission data from plants. All environmental stresses, both biotic and abiotic, as well as cellular signalling processes involve ROS formation.[35–37] In future research, it will be essential to consider the plant’s oxidative status, the nature and subcellular location of processes involving ROS production (i.e. mitochondria or chloroplast, see below) and other possible reaction mechanisms to understand the full environmental significance of processes that may lead to aerobic CH4 formation. In line with this hypothesis, McLeod et al.[27] demonstrated CH4 (and also ethane and ethene) release in tobacco using a bacterial pathogen and chemical generators of ROS. Qaderi and Reid[38] reported that temperature and water stress increased a subsequent CH4 emission using six plant species, whereas Wang et al.[24] showed that physical injury (by cutting) also elicits aerobic CH4 emissions. Infestation or injury is generally accompanied by an emission surge of volatile organic compounds (VOC), i.e. methanol, acetaldehyde, and the greenleaf volatile (Z)-3-hexenyl acetate and other aliphatic esters of (Z)-3-hexen-1-ol resulting from transient oxidative stress.[39,40] The emission of CH4 is possibly a hitherto overlooked integral part of this defence reaction of plants (Fig. 2).

Global VOC (volatile organic compounds) emissions model assuming VOCs and CH4 have similar biochemical origin. Range dependent on land cover and weather data.

Ferretti et al.[18] 0–213 Mass balance, ice core isotope ratios using: Pre-industrial, ‘best estimate’ 0–46 Tg year−1 , ‘maximum estimate’ 9–103 Tg year−1 ; Modern source, ‘best estimate’ 0–176 Tg year−1 , ‘maximum estimate’ 0–213 Tg year−1 .

Butenhoff and Khalil[17] 20–69 Leaf emission rates of Keppler et al.[7] scaled using model of cloud cover and canopy shading. Scaled using LAI, 36 Tg year−1 ; scaled using foliage biomass, 20 Tg year−1 , maximum expected 69 Tg year−1 .

Houweling et al.[8]

Parsons et al.[14] 53

85–125 to maximum present day Atmospheric transport model, isotope ratios, mass balance. Pre-industrial plausible value upper limit 125 Tg year−1 .

85 Tg year−1

Leaf emission rates of Keppler et al.[7] scaled by biome leaf biomass. Leafy biomass, 42 Tg year−1 ; non-leafy biomass, 11 Tg year−1 .

Kirschbaum et al.[15] 10–60 Leaf emission rates of Keppler et al.[7] scaled by biome leaf biomass – mean 36 Tg year−1 (range 15–60 Tg year−1 ); or by leaf photosynthesis, 10 Tg year−1 .

Keppler et al.[7] 62–236 Sunlit and dark leaf emission rate scaled by daylength, season length and biome net primary production. Mean rate of 149 Tg year−1 based on emission rates 374 ng g−1 dry weight (DW) h−1 (sunlight) and 119 ng g−1 DW h−1 (no sun). Range of 62–236 Tg year−1 was based on emission rates 198–598 ng g−1 DW h−1 (sunlight) and 30–207 ng g−1 DW h−1 (no sun).

Global methane emission (Tg year−1 ) Scaling method

Table 1. Estimates of global aerobic methane emissions by vegetation (adapted from Megonigal and Guenther[12] )

Reference

Methane formation in aerobic environments

Why do plants host methane-consuming bacteria? The aerobic production of CH4 by plant tissues provides one potential explanation for the discovery of methanotrophic bacteria living within plant tissues. Methanotrophs are divided into two main groups by phylogenetic affiliation, the method of formaldehyde fixation, and membrane structure, and both types are found inside plants. Specifically, type II methanotrophs of the genus Methylocystis have been isolated from bud and leaf tissues of linden and spruce trees[41] and knotgrass.[42] Methylosinus sp., belonging to type II, and an unknown type I methanotroph were identified in maize stem and root tissues respectively.[43,44] Methanotrophs have previously been identified only in soil, freshwater and marine environments[45] and in the aerenchyma of emergent wetland plants,[46–48] which represent the expected CH4 -rich environments for these bacteria. In general, methanotrophic bacteria oxidise CH4 as the sole source of carbon and energy in aerobic conditions. Practically all methanotrophs are obligate CH4 consumers as only the genus Methylocella is known to contain facultative methanotroph strains.[49] Little information exists on the distribution of methanotrophs in the range of plant tissues or between different plant species but the data collected so far suggests that many individual plant species harbour methanotrophs to a variable degree. It is an interesting and challenging question whether a highly variable aerobic CH4 formation could provide selective niches for the methanotrophs colonising plant internal tissues. 461

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Environmental stress factors Microbial Heat and attack water stress

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(plus ethane, ethylene, CO2) Fig. 2. Environmental stress factors known to generate reactive oxygen species (microbial attack, heat and water stress, UV radiation, herbivory, nutrient deficiency, salinity, tropospheric ozone) and their potential role in aerobic methane formation in plants, showing the inter-relationship of reactive oxygen species.[35]

Non-microbial methane formation in animals

chloroplasts. Indeed, it has been demonstrated that alternative electron acceptors in plants may help to prevent the overreduction of electron carriers (reductive stress) in fluctuating light or in light-induced stress conditions.[54] Using an in vitro exothermic reaction model it is possible to generate CH4 from a mixture of hydrogen peroxide, iron, ascorbate and choline.[52] Indeed it was demonstrated that in the presence of ROS, CH4 was released in proportion to the number of methyl groups present in choline and demethylated choline metabolites.[33] Moreover, it is clear that temporary oxygen deprivation or interruption of the respiratory chain in aerobic cells can lead to the generation of CH4 from biomolecules with EMGs in the mitochondrial matrix.[33] Further details suggest that this pathway may function to correct an abnormal rise in electron-donor activity, as CH4 -generating choline metabolites counteract ROS generation and have the potential to inhibit production of hydroxyl radicals.[33] In summary, methane formation in animal or plant mitochondria may be a common consequence of redox conditions with a negative redox potential in the presence of oxygen or reactive oxygen species. In this respect, hypoxia-induced CH4 generation may be a necessary phenomenon of aerobic life, and perhaps a surviving evolutionary trait in animals, as well as in plants.

Aerobic CH4 emission is not restricted to the plant kingdom. Almost a decade ago it was shown that animals exhale enhanced levels of CH4 after reoxygenisation of previously hypoxic tissues and occasionally the methane-producing status does not change after antibiotic treatments targeting the intestinal methanogenic bacterial flora.[50,51] Hypoxia-induced generation of CH4 has also been demonstrated in isolated liver mitochondria.[52] Further studies with cultured bovine endothelial cells under hypoxia, metabolic distress, or inhibition of the mitochondrial electron transport chain provided clear evidence of dose-dependent cellular CH4 production.[33] Based on these initial process studies it was proposed that electrophilic methyl groups (EMGs) bound to positively-charged nitrogen moieties (such as in choline molecules) may potentially act as electron acceptors, and that these reactions may entail the generation of CH4 in animal cells.[53] A continuous lack of the electron acceptor O2 will maintain an elevated mitochondrial NADH/NAD+ ratio, causing the formation of a nucleophilic hydride ion which is transferred to the EMG (Fig. 3). Such an anomalous increase in reducing power also occurs in pathologies involving the interruption of electron flow down the mitochondrial electron transport chain. It is possible that the same mechanisms occur in plant mitochondria and

Oceanic methane paradox

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The world’s oceans are considered to be a small source of CH4 to the atmosphere. Concentrations of CH4 in near-surface waters are often 5–75% supersaturated with respect to the atmosphere attributed to local methanogenesis and implying a net flux from the ocean to the atmosphere. As the surface ocean is also saturated or slightly supersaturated with oxygen, which does not favour methanogenesis, the observed CH4 supersaturation has been termed the ‘oceanic methane paradox’.[55]

H CH3

CH3

Fig. 3. Proposed reaction scheme for CH4 formation in hypoxic animal cells. The nucleophilic hydride-ion (H− ) is transferred to electrophilic methyl groups. This is followed by separation of the methyl group and the formation of CH4 .

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changes. A broad range of field measurements at different scales and satellite measurements at higher resolution are needed to support numerical modelling studies. The observation that some CH4 formation under aerobic conditions occurs in many eco- and bio-systems is robust and prevalent, and opens up new, interesting and very challenging avenues for future research in plant, animal and environmental sciences. It will require a considerable effort by researchers from different disciplines to complete and confirm our understanding of the biogeochemical cycling of CH4 and its importance for our atmosphere and climate.

The source of CH4 in surface waters has been suggested to be anoxic methanogenesis in microenvironments of organic aggregates.[56] A potential substrate in such aggregates is dimethylsulfoniopropionate (DMSP), an important algal product that is also the precursor of another climate-relevant gas, dimethylsulfide (DMS).[57] Although photochemical production of CH4 in oceans is thought to be negligible under oxic conditions,[58] an alternative non-biological CH4 formation in seawater might occur via a photochemical pathway due to the formation of methyl radicals as has been reported for methyl halides.[59] It came as a surprise when Karl et al.[60] recently demonstrated that CH4 is produced aerobically as a by-product of methylphosphonate decomposition in phosphatestressed waters. Although the mechanisms have not yet been fully identified, the authors suggest that methylphosphonate decomposition, and thus CH4 production, may be enhanced by the activity of nitrogen-fixing microorganisms. The global importance of this newly identified source is unclear. However, the recent advances from the plant and animal investigations might stimulate marine researchers to search for alternative CH4 sources particularly in environmentally stressed algae and coastal upwelling regions that have been identified as areas with enhanced CH4 emissions.[61]

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).

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Outlook Until recently only combustion processes were considered to form CH4 in the presence of limited amounts of oxygen. Independent observations from several research fields now show that plants, animals and the marine environment produce CH4 under aerobic conditions. The collective evidence from these unexpected findings suggests that aerobic CH4 formation may not be an exotic process, but widespread in nature. The immediate challenge is to test the proposed new hypotheses for aerobic CH4 formation from different biomolecules and cellular structures, and to draw a comprehensive picture of plausible CH4 sources and their specific importance in plants, animals and algae. The results published to date imply that aerobic methane formation may be an integral part of cellular responses towards changes in oxidative status present in all eukaryotes and that it is highly variable in time and source strength. Future research should answer the question whether CH4 generation is solely a by-product of abiotic degradation of biomolecules, e.g. induced by UV irradiation, increased temperatures, or hypoxia, or whether it also plays a more general physiological role. It appears that in plants, CH4 generation may be linked to environmental stress. Similar mechanisms might be active in animals and probably, also humans, producing CH4 when the organisms are under external or internal (e.g. inflammation) stress. With modern approaches in molecular biology, biochemistry and stable isotope research new tools are available to identify the reaction mechanisms of aerobic CH4 formation and estimate their contribution to the global CH4 budget, whilst not neglecting the consumption of CH4 by methanotrophs. Techniques for locating methanotrophs in various plant tissues and plant species may also become an indicator of co-evolution, plant stress status or simply used as an index of plant CH4 emissions. Atmospheric scientists should revisit the biogenic sources of CH4 (including wetlands and plants) in view of possible global change feedbacks. These may include links with stratospheric ozone depletion, changing humidity and temperature regimes, rising CO2 concentrations, land-use change and ecosystem responses, which are relevant for both modern and paleo-climatic 463

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