Widespread non-microbial methane production by organic ...

Earth-Science Reviews 127 (2013) 193–202

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Widespread non-microbial methane production by organic compounds and the impact of environmental stresses Zhi-Ping Wang a,b, Scott X. Chang b,⁎, Hua Chen c, Xing-Guo Han a,d,⁎ a

State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, Chinese Academy of Sciences, Nanxincun 20, Xiangshan, Beijing 100093, China Department of Renewable Resources, University of Alberta, Edmonton, Alberta T6G 2E3, Canada Biology Department, University of Illinois at Springfield, Springfield, IL 62703-5407, USA d State Key Laboratory of Forest and Soil Ecology, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang 110016, China b c

a r t i c l e

i n f o

Article history: Received 24 November 2012 Accepted 2 October 2013 Available online 22 October 2013 Keywords: CH4 source Methyl group Organic matter Organism Global warming

a b s t r a c t Non-microbial methane (CH4) production is more pervasive in nature than previously thought, but it has received less attention than microbial CH4 production. Non-microbial CH4 is produced commonly by an instantaneous reaction involving organic compounds under environmental stresses, without enzymatic catalysis by methanogenic archaea. In addition to the widely known sources of non-microbial CH4, i.e., energy usage, biomass burning, and geological emissions, non-microbial CH4 emissions from plants, animals, fungi, soils, and surface waters of oceans have been recently reported. In most ecosystems, microbial and non-microbial CH4 production co-occur and/or alternate depending on the conditions, and thus CH4 emission in terrestrial ecosystems represents a mixture of microbial and non-microbial CH4 production. Global CH4 emission was estimated at 582 Tg yr−1 over the 2000–2004 period, where geological sources of non-microbial CH4 were not included. When geological sources are included, total emissions will likely not increase but its partition among the individual sources would change, and emissions of non-microbial CH4 might account for approximately 40% of the global total. This fraction would slightly increase if non-microbial CH4 emissions of plants, animals, fungi and soils in terrestrial ecosystems and surface waters of oceans are considered, although no global estimates for those fractions currently exist. The stable isotope signatures of C and H in CH4 may be a useful tool for identifying the source of CH4. Based on this review of the literature, we conclude that non-microbial CH4 production may occur in any organism or dead organic matter when organic compounds are exposed to environmental stresses. © 2013 Elsevier B.V. All rights reserved.

Contents

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Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Established sources of non-microbial CH4 . . . . . . . . . . . . . . . . . . . . 2.1. Energy usage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Biomass burning . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3. Geological sources . . . . . . . . . . . . . . . . . . . . . . . . . . . . Potential sources of non-microbial CH4 . . . . . . . . . . . . . . . . . . . . . . 3.1. Plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Animals, fungi, and soils . . . . . . . . . . . . . . . . . . . . . . . . . 3.3. Mixed emissions of microbial and non-microbial CH4 in terrestrial ecosystems 3.4. Surface waters of most oceans . . . . . . . . . . . . . . . . . . . . . . The strengths of non-microbial CH4 sources . . . . . . . . . . . . . . . . . . . Mechanisms of non-microbial CH4 production . . . . . . . . . . . . . . . . . . 5.1. Functional groups of organic compounds as precursors . . . . . . . . . . .

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⁎ Corresponding authors. Correspondence should be addressed to S.X.C. (Tel.: +1 780 492 6375, E-mail address: [email protected]) or X.G.H. (Tel.: +86 10 6283 6635, E-mail address: [email protected]). 0012-8252/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.earscirev.2013.10.001

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5.2. The role of environmental stresses . . . 5.3. The end production of non-microbial CH4 6. Isotopic signatures of non-microbial CH4 . . . . 7. Future directions . . . . . . . . . . . . . . . Acknowledgments . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . .

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1. Introduction Methane (CH4) is the second most important anthropogenic greenhouse gas after carbon (C) dioxide (CO2) and exerts an important influence on the atmospheric chemistry and the climate (Denman et al., 2007). The CH4 concentration in the atmosphere has rapidly increased since the pre-industrial era, from 715 nL L− 1 in 1750 to 1774 nL L− 1 in 2005, resulting in a radiative forcing of 0.48 w m− 2 (Forster et al., 2007). Recently, the CH4 concentration in the atmosphere has increased to approximately1800 nL L−1 (Dlugokencky et al., 2009). In the Earth's crust, CH4 is largely of biogenic origin resulting from the microbial and thermochemical decompositions of organic matter (Schoell, 1983, 1988; Welhan, 1988). Methane may also be produced through inorganic reactions without involvement of organic matter and is consequently termed abiogenic (Schoell, 1983, 1988; Welhan, 1988). Abiogenic CH4 production is mainly controlled by geological processes (Horita and Berndt, 1999) and has three main sources: water–rock interactions, volcanic activities, and geothermal systems (Emmanuel and Ague, 2007). Research so far suggests that abiogenic CH4 emissions are quantitatively insignificant (Schoell, 1988; Emmanuel and Ague, 2007; Fiebig et al., 2009), accounting for approximately 0.4 (Emmanuel and Ague, 2007) to 1% (Fiebig et al., 2009) of the global total. These results indicate that about 99% of the CH4 in the atmosphere is ultimately derived from organic compounds. Thus, we need to focus on CH4 production from organic compounds. Methane has traditionally been considered an end product of organic matter degradation involving complex microbial processes. The microbes involved are a limited group of obligate prokaryotes called methanogenic archaea that thrive under anaerobic conditions and are phylogenetically distinct from bacteria and eukarya (Woese et al., 1990; Conrad, 1996; Schimel, 2004; Conrad, 2005). Accordingly, CH4 produced by methanogenic archaea should be termed microbial rather than bacterial. On the other hand, the term biogenic CH4 describes methane that is biologically formed from organic matter (Schoell, 1988; Welhan, 1988) and is not based on the mechanism of CH4 production. As a result, the term biogenic CH4 might be easily misunderstood as microbial CH4. Here we propose to use microbial and non-microbial CH4 as unifying terms for CH4 production in nature. Microbial CH4 production has been extensively studied over the past several decades (Conrad, 1996, 2005) and was previously considered to account for more than 70% of the global total, with non-microbial CH4 production accounting for less than 30% of the global total (Hein et al., 1997; Quay et al., 1999; Denman et al., 2007). As a result of the smaller proportion in the global total CH4 production, non-microbial CH4 production has received much less attention. When geological sources are considered (Table 1), emissions of non-microbial CH4 would be more important for the global total than previously thought. Recently, emissions of non-microbial CH4 have been reported in plants (Keppler et al., 2006), animals (Ghyczy et al., 2003; Ghyczy et al., 2008), fungi (Lenhart et al., 2012), soils (Hurkuck et al., 2012; Jugold et al., 2012; Wang et al., 2013), and the surface waters of oceans (Bange and Uher, 2005; Karl et al., 2008; Moore, 2008). These emissions of non-microbial CH4 might further increase the importance of emissions of non-microbial CH4 in the global CH4 total. In this paper, we review the production and emission of nonmicrobial CH4 in nature. When considering the emission of CH4, we

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emphasize the areas/sites and the strength of the emission; when considering the production of CH4, we focus on the underlying mechanisms. We summarize the characteristics for non-microbial CH4 production, including the organic compounds, functional groups and environmental stresses involved. We also discuss the use of isotopic signatures of C and hydrogen (H) in CH4 for understanding nonmicrobial CH4 production. Finally, we provide perspectives on future research on non-microbial CH4 production and emission.

2. Established sources of non-microbial CH4 Currently, emissions of non-microbial CH4 have been established in energy usage, biomass burning and geological sources (Table 1). In considering the sources of CH4 as part of its inventory of greenhouse gases, the Intergovernmental Panel on Climate Change (IPCC) included energy usage and biomass burning but did not include geological sources, although geological sources were discussed in the report (Denman et al., 2007). The failure to include geological sources might be due to the large uncertainties in estimates of geological CH4 emissions. However, all of those sources have been widely studied in recent decades. Below, we provide a brief overview of those sources.

Table 1 The global emission of non-microbial methane (Tg CH4 yr−1). Sources Energy usage Biomass burning Geological sources Volcanoes Geothermal Mud volcanoes Seeps Micro-seepage Marine seepage Terrestrial ecosystems Plants

Animals Soils Fungi Surface waters of oceans

Emissions a

110 ± 13 89.5b 50 ± 8a 46.5b 60c b1 2.5–6.3 6–9 or 10–20 3–4 10–25 ~20 ? 62–236 10–60 53 85–125 20–69 0–213 34–56 Insignificant–60 0.2–1.0d ? ? ? ?

References Bousquet et al. (2006) Denman et al. (2007) Bousquet et al. (2006) Denman et al. (2007) Etiope (2012)

Keppler et al. (2006) Kirschbaum et al. (2006) Parsons et al. (2006) Houweling et al. (2006) Butenhoff and Khalil (2007) Ferretti et al. (2007) Megonigal and Guenther (2008) Keppler et al. (2009) Bloom et al. (2010)

The average emissions of non-microbial CH4 are calculated aover the 1984–2003 period using the online supplementary material in Bousquet et al. (2006) or bover the period of about recent three decades using the estimates cited in Denman et al. (2007). c Geological sources of CH4 are cited from the material in Etiope (2012), where the CH4 emitted from volcanoes is not ultimately derived from organic matter. d The estimate is the global CH4 emission driven by UV-irradiation from pectin in plant foliage. Question marks denote no available estimates in these potential sources.


2.1. Energy usage Energy usage, such as the use of coal, crude oil, and natural gas, is recognized as a dominant source of non-microbial CH4 (Table 1). Methane emissions consist of fuel combustion and fugitive emission from energy-related activities (USEPA, 2006). Methane emissions primarily come from fugitive sources such as leaking equipment, system upsets, deliberate flaring and venting at production fields, processing and storage facilities, and along transmission and distribution lines; these sources account for about 80% of energyrelated emissions (USEPA, 2006). Because newer equipment tends to leak less than older equipment, fugitive emissions of CH4 are likely to be reduced when oil and gas facilities are modernized (USEPA, 2006). Global energy usage is increasing (IPCC, 2011). Decreasing the share of usage of coal, crude oil and natural gas may also slow down CH4 emissions in energy usage. Greenhouse gas emissions resulting from energy usage have significantly contributed to the historic increase in atmospheric greenhouse gas concentrations. There are multiple options for lowering greenhouse gas emissions from energy usage, of which increasing the share of renewable energy is an available option. Renewable energy sources, such as bioenergy, solar energy, geothermal energy, hydropower, ocean energy and wind energy, have a large potential to displace emissions of greenhouse gases from the combustion of fossil fuels and thereby mitigate climate change (IPCC, 2011). Therefore, non-microbial CH4 emissions from energy usage may be retarded by increasing the use of renewable energy.

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much greater depths and temperatures (Etiope, 2012). As indicated by the isotopic signature (Quay et al., 1999; Whiticar and Schaefer, 2007), geological CH4 is mainly thermogenic (Etiope, 2012). Thus, geological CH4 may be classified as non-microbial. Among geological sources, micro-seepage is an important source of non-microbial CH4 emissions. Micro-seepage is pervasive and constitutes continual emissions of CH4 over dry soil areas in hydrocarbon-rich sedimentary basins, with rates ranging from a few units to hundreds of mg m−2 d−1; this form of CH4 emission has been recently observed at an increasing number of sites (Etiope and Klusman, 2010). In general, dry soils are a net sink for atmospheric CH4. However, micro-seepage can easily mask the strength of the soil CH4 sink. Therefore, microseepage should be further studied. Because some of the CH4 from micro-seepage is oxidized in aerobic soils, the extent of the oxidation should also be quantified. 3. Potential sources of non-microbial CH4 In addition to the established sources of non-microbial CH4 discussed above, emissions of non-microbial CH4 have recently been observed from plants, animals, fungi, soils, and surface waters of oceans. To be considered a CH4 source by the IPCC, the source's CH4 emission must be substantial and result in a large global total. Similarly, to be considered a potential source, the source's CH4 emission may be substantial or only detectable but its global amount is uncertain. When the total amount generated by a potential source is confirmed to be large globally, the potential source would be upgraded and accepted as a source that may be listed in the IPCC greenhouse gas inventories.

2.2. Biomass burning 3.1. Plants Biomass burning is very common in terrestrial ecosystems. Biomass burning produces large amounts of trace gases and aerosol particles that can greatly affect atmospheric chemistry and the climate (Crutzen and Andreae, 1990) and makes important contributions to the global budgets of trace gases (Andreae and Merlet, 2001). Methane is produced by thermogenic reactions and thus is non-microbial. Methane emission rates depend mainly upon the stage of combustion reached, the C content of the biomass, and the amount of biomass burned (Levine et al., 2000). When combustion is complete, most emissions are in the form of CO2. When combustion is incomplete, however, a significant amount of CH4 and other higher-order hydrocarbons may be produced (Levine et al., 2000). Biomass burning might explain the anomalous growth rates of atmospheric CH4 concentration (Dlugokencky et al., 2001; Simpson et al., 2006). There were large interannual variations in the growth rates of CH4 (Dlugokencky et al., 2001). The mechanisms causing these variations were poorly understood but biomass burning was thought to significantly contribute to the anomalous growths of atmospheric CH4 concentration in 1993 to 1994 and 1997 to 1998 (Langenfelds et al., 2002; Butler et al., 2004; Morimoto et al., 2006). It is likely that with global warming the frequency of wildland fire will increase in arid and semiarid regions. The increased CH4 might lead to a positive feedback on climate change. 2.3. Geological sources Geological sources are defined as the CH4 emitted into the atmosphere through natural events: eruptions of volcanoes and mud volcanoes, geothermal activities, marine seepage, seepage, and microseepage (Etiope and Klusman, 2002; Kvenvolden and Rogers, 2005; Solomon et al., 2009; Etiope and Klusman, 2010; Anthony et al., 2012; Etiope, 2012). Geological CH4 may be produced by microbial and thermogenic degradation of organic matter (Schoell, 1983, 1988; Welhan, 1988; Horita and Berndt, 1999; Osborn et al., 2011; Etiope, 2012; Tassi et al., 2012). Generally, microbial CH4 is produced at shallow depths and low temperatures, while thermogenic production occurs at

Traditionally, plants have been thought to provide a transport pathway for belowground microbial CH4 emissions. However, plants have recently been found to produce non-microbial CH4 (Keppler et al., 2006). Several other studies reported non-detectable or negligible CH4 emissions from plants (Dueck et al., 2007; Beerling et al., 2008; Kirschbaum and Walcroft, 2008; Nisbet et al., 2009). On the other hand, most subsequent studies confirmed that non-microbial CH4 production in plants does indeed occur (Keppler et al., 2008; McLeod et al., 2008; Vigano et al., 2008; Wang et al., 2008; Brüggemann et al., 2009; Bruhn et al., 2009; Messenger et al., 2009; Qaderi and Reid, 2009; Vigano et al., 2009; Wang et al., 2009; Qaderi and Reid, 2011; Wang et al., 2011a,b; Wishkerman et al., 2011; Bruhn et al., 2012). The mechanisms of CH4 production by plants and the contribution of this production to the global total remain poorly understood (Wang et al., 2011a,b). Researchers have suggested that substantial CH4 production by plants is linked to environmental stresses (Dueck and van der Werf, 2008; Keppler et al., 2009; Nisbet et al., 2009; Qaderi and Reid, 2009, 2011; Wang et al., 2011a,b). Plants respond to environmental stresses via defense strategies that include the production of both catabolic products and by-products such as volatile organic compounds (Laothawornkitkul et al., 2009). Plant CH4 production might be an integral part of the defense strategies of plants in response to environmental stresses. Physical injury and anaerobic conditions are common stresses experienced by plants. Such stresses may stimulate plants to produce non-microbial CH4 (Wang et al., 2009, 2011a). In nature, plants are commonly grazed by herbivores, and then the wounded plant matter is stressed within the herbivores' hypoxic gastrointestinal tracts. In addition to supporting microbial CH4 production in the gastrointestinal tracts, the plant matter could support non-microbial CH4 production as a consequence of being cut and chewed and then slowly degraded in the hypoxic environment of the herbivore digestive system. Insect grazing might stimulate plant matter to produce non-microbial CH4. Insects are the largest class of arthropods and the most diverse group

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of animals on the planet. Over one million insect species have been described (Chapman, 2006), of which herbivorous species constitute about 50% (Bernays and Chapman, 1994). The large numbers of herbivores mean that they consume a huge amount of plant biomass. For instance, herbivores can consume over 15% of the biomass produced annually in temperate and tropical ecosystems (Johnson, 2011). It is likely that the grazing on plant matter by herbivores stimulates substantial emissions of non-microbial CH4 at the global scale but this hypothesis remains to be further tested. A number of field studies have reported substantial CH4 emissions from xerophytes (Rusch and Rennenberg, 1998; do Carmo et al., 2006; Megonigal and Guenther, 2008; Rice et al., 2010; Mukhin and Voronin, 2011; Covey et al., 2012) and hydrophytes (Whiting and Chanton, 1993; Joabsson et al., 1999). CH4 emissions from terrestrial plants have traditionally been attributed to the dissolved CH4 in the water drawn into the plants and subsequently emitted through diffusion (Dueck et al., 2007) and/or transpiration (Nisbet et al., 2009). But plants may produce non-microbial CH4 under aerobic or anaerobic conditions (Wang et al., 2011a,b). Plant roots are distributed in soils with widely varying oxygen concentrations. The fluctuation in the oxygen concentration likely represents an environmental stress that stimulates the physiological activities of plant roots and that could stimulate the production of non-microbial CH4. Accordingly, non-microbial and microbial CH4 production might simultaneously occur in plant roots. The biomass of plant roots is huge, and roots are estimated to contain 160 Pg C at the global scale (Saugier et al., 2001) or 241 Pg C (Mokany et al., 2006). Although plant roots might be as important as aboveground plant biomass for nonmicrobial CH4 production, the contribution of plant roots to nonmicrobial CH4 production has not been estimated. It is likely that certain plant species harbor methanogens (Zeikus and Ward, 1974) and/or methanotrophs (Keppler et al., 2009). For example, Raghoebarsing et al. (2005) reported that Sphagnum spp. (mosses) consumed CH4 by symbiosis, part of the CH4 consumption was by endophytic methanotrophs. The CO2 produced from oxidation of CH4 is then fixed by the plant during photosynthesis (Raghoebarsing et al., 2005). More recently, Sundqvist et al. (2012) observed a net uptake of CH4 by all of the plants that they studied (Picea abies, Betula pubescens, Sorbus aucuparia, and Pinus sylvestris) both in situ and in the laboratory. All these reports indicate that gross production of non-microbial CH4 in plants might be greater than indicated by net emission rates observed in previous studies and this might have important implications for the global CH4 budget.

3.3. Mixed emissions of microbial and non-microbial CH4 in terrestrial ecosystems Microbial and non-microbial CH4 production co-occur and/or alternate in nature. For a microbial CH4 source/site, microbial CH4 production occurs on most temporal and spatial scales, while nonmicrobial CH4 production at the same source/site can be transitory and patchy. Similarly, for a non-microbial CH4 source/site, non-microbial CH4 production occurs on most temporal and spatial scales, while microbial CH4 production at the same site or from the same source can be transitory and patchy. The responses of microbial and non-microbial CH4 production to temperature provide a good example of the co-occurrence and/or alternation of microbial versus non-microbial CH4 production. Microbial CH4 production in soils usually shows a parabolic relationship with temperature, with an emission peak at 25–30 °C, which is the optimal temperature range for enzymatic metabolism by methanogenic archaea (Dunfield et al., 1993). In contrast, non-microbial CH4 production in soils was found to increase with increasing temperature between 30 and 70 °C (Hurkuck et al., 2012) or between 30 and 90 °C (Jugold et al., 2012). Methane produced in geological sediments is primarily a product of the conversion of organic matter under different temperature regimes (Schoell, 1988), with microbial CH4 production at low temperatures and thermogenic CH4 production at high temperatures (Welhan, 1988; Etiope, 2012; Tassi et al., 2012). In general, the upper threshold of temperature for enzymatic metabolism is about 50 °C because microbial enzymes are denatured at high temperatures. Thus, CH4 production in response to temperature would roughly follow the following pattern: no CH4 production below 0 °C, microbial CH4 production between 0 and 30 °C, concurrent microbial and non-microbial CH4 production between 30 and 50 °C, and non-microbial CH4 production above 50 °C. The co-occurrence and/or alternation of microbial and nonmicrobial CH4 production implies a mixed emission of microbial and non-microbial CH4 in terrestrial ecosystems. Given that plants, animals, fungi, and soils are important components of terrestrial ecosystems and are capable of non-microbial CH4 production under laboratory conditions, we may infer that in situ non-microbial CH4 production should occur in terrestrial ecosystems. It follows that in situ measurements of CH4 fluxes in the field may reflect mixed emissions of microbial and non-microbial CH4. This is counter to the traditional idea that the CH4 emission measured in the field is solely microbial. With current technology, however, it is difficult to distinguish between microbial and non-microbial CH4 production in terrestrial ecosystems. 3.4. Surface waters of most oceans

3.2. Animals, fungi, and soils Animals, fungi, and soils also produce non-microbial CH4. For instance, the production of CH4 in animals was found to originate not solely from the intestinal microbial flora (Boros et al., 1999). Hypoxia-induced production of non-microbial CH4 was found in rat mitochondria and eukaryotic cells (Ghyczy et al., 2003, 2008). Fungi are a large group of eukaryotic organisms that are distinct from plants, animals, and bacteria. More recently, fungi have also been found to produce non-microbial CH4 (Lenhart et al., 2012). With respect to soils, non-microbial CH4 was produced in aerobic soils under heating, UV irradiation, and drying–rewetting cycles (Hurkuck et al., 2012; Jugold et al., 2012) and in anaerobic soils under heating (Wang et al., 2013), and the CH4 was derived from organic matter rather than mineral components (Hurkuck et al., 2012). Soils are frequently exposed to environmental stresses, such as high temperature, drought, flooding and UV radiation, and it is therefore likely that soils are commonly a source of non-microbial CH4. Only a few studies have investigated non-microbial CH4 production by animals, fungi and soils; however, more research is urgently needed.

Although oceans are traditionally thought to be a source of microbial CH4 (Denman et al., 2007), surface waters of most oceans are aerobic, and aerobic conditions do not generally favor microbial CH4 production (Karl and Tilbrook, 1994). In surface waters of most oceans, CH4 may be produced by photochemical reactions under aerobic conditions (Bange and Uher, 2005; Moore, 2008) or may be due to the formation of methyl radicals (Moore, 2008). Furthermore, CH4 concentrations in surface waters of most oceans are supersaturated relative to the CH4 concentration in the atmosphere, where the CH4 is aerobically produced as a by-product of methylphosphonate decomposition (Karl et al., 2008). The importance of surface waters of most oceans in the global production of non-microbial CH4 is presently unclear. 4. The strengths of non-microbial CH4 sources The global emissions of CH4 from energy usage and biomass burning have been widely estimated and are recognized as the major sources of non-microbial CH4. On average, non-microbial CH4 emissions were estimated at about 100 and 48 Tg yr−1 in energy usage and biomass


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Fig. 1. Processes involving reactions of organic compounds and microbial and non-microbial CH4 production. (a) organic sediments from ancient ecosystems; (b) fresh tissues, metabolic products, and dead organic matter from contemporary ecosystems; (c) organic compounds go through further transformations and reactions (solid yellow arrows) under ambient conditions (circle) and/or environmental stresses (star); (d) non-microbial CH4 production under environmental stresses (star); and (e) microbial CH4 production under ambient conditions (circle). The organic compounds that serve as substrates in the production of non-microbial CH4 may be living tissues and metabolic products without involvement of microbes (solid green arrow), dead organic materials that do not further react in the environment (dashed green arrow), and/or organic compounds that undergo additional reactions (dotted green arrow). Organic compounds may undergo complicated reactions before microbial CH4 is produced (dotted blue arrow).

burning, respectively (Table 1). Global geological CH4 emissions have been recently estimated to be approximately 60 to 80 Tg yr−1 (Etiope, 2012). This estimate is much higher than those reported in previous studies (Houweling et al., 2000; Wuebbles and Hayhoe, 2002). Although the emission rates for specific geological sources are reasonably well known, the global seepage area and the number of seepage sites are uncertain (Etiope, 2012). Therefore, obtaining an accurate estimate of the global CH4 emission from geological sources is challenging, and more measurements are needed. Non-microbial CH4 emissions from plants have been widely estimated based on global plant biomass, stable isotope mass balance, and modeling (Table 1). The emissions reported in an earliest study (Keppler et al., 2006) should have been overestimated and were not accepted by subsequent studies, even Keppler et al. (2009) themselves updated the emissions from insignificant to 60 Tg yr−1 (Table 1). The recent literature indicates that almost all plants produce nonmicrobial CH4 (Wang et al., 2011a,b; Bruhn et al., 2012). Whether non-microbial CH4 emissions can be detected from plants depends on the limits of the analytical system employed. For instance, even very low emission rates of non-microbial CH4 can be detected by stable isotope analysis (Vigano et al., 2008; Brüggemann et al., 2009; Wishkerman et al., 2011). But these cannot indicate that plants are a significant source of non-microbial CH4. Currently, it is difficult to provide a confident estimate of non-microbial CH4 emissions from plants (Keppler et al., 2009; Bruhn et al., 2012). More measurements are needed. In the future, the following two points (Wang et al., 2011a) might be important for estimating nonmicrobial CH4 emissions from plants. First, in nature about 10% of plant species are considered to have substantial emissions of nonmicrobial CH4 under environmental stresses; most notable are fragrant species such as Lavandula angustifolia and species in the family Asteraceae. Second, short-lived pulse emissions of CH4 by plants immediately following environmental stresses might be quantitatively significant. At present, non-microbial CH4 emissions from animals, fungi, soils and surface waters of oceans have not been estimated because data

are lacking (Table 1). When non-microbial CH4 emissions from these potential sources are estimated in the future, the global total of nonmicrobial CH4 emissions might be updated. The total amount of global CH4 emissions has been estimated but the strengths of individual sources remain highly uncertain (Denman et al., 2007). Global CH4 emissions were estimated at 525 ± 8 Tgyr−1 over the 1984–2003 period (Bousquet et al., 2006) or 582 Tg yr−1 over the 2000–2004 period (Denman et al., 2007), where geological sources of non-microbial CH4 were not included. When contribution from geological sources of 60 Tg yr−1 (Table 1) is included, total emissions are likely not increasing according to the current growth rate and sink strength of atmospheric CH4 (Denman et al., 2007), but the partitioning among the individual sources would have changed. The 60 Tg yr−1 of geological emissions is equal to approximately 10–11% of the global total emission of 525 Tg yr−1 (Bousquet et al., 2006) or 582 Tg yr−1 (Denman et al., 2007). Adding that to the estimated non-microbial CH4 that accounts for about 30% of the global total, the emissions of non-microbial CH4 would account for about 40% of the global total. This fraction might further increase if non-microbial CH4 emissions of plants, animals, fungi and soils in terrestrial ecosystems and surface waters of most oceans are included, although their estimates are currently not available. This indicates that non-microbial CH4 emissions for the global total are more important than previously thought. As stated above, non-microbial CH4 sources may be coarsely classified into established ones (energy usage, biomass burning and geological sources) and potential ones (plants, animals, fungi and soils in the terrestrial ecosystems, and surface waters of most oceans). With the current knowledge, the established sources have large emissions whereas the potential sources are very likely small sources. 5. Mechanisms of non-microbial CH4 production Various mechanisms have been proposed to explain non-microbial CH4 production, and these include thermogenesis in the Earth's crust (Schoell, 1988; Welhan, 1988; Etiope and Klusman, 2002), thermogenic reactions in biomass burning (Fischer et al., 2008), free radical attacks in

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plant tissues (Sharpatyi, 2007; McLeod et al., 2008; Messenger et al., 2009), the disturbance of the electron transport chain in the cells of animals (Ghyczy et al., 2008) and plants (Wishkerman et al., 2011), chemical reactions in soils (Hurkuck et al., 2012; Jugold et al., 2012), and biochemical reactions within fungi (Lenhart et al., 2012). These mechanisms produce non-microbial CH4 from organic compounds (especially when the organic compounds are subjected to environmental stresses), without catalytic involvement by the enzymes of methanogenic archaea. Here, we summarize the key characteristics of these mechanisms.

5.1. Functional groups of organic compounds as precursors In nature, organic compounds such as pectins, lignins, celluloses, lipids, fatty acids, nucleic acids, proteins, and amino acids are ubiquitous. Organic compounds undergo reactions as part of complex microbial metabolism and/or in response to environmental stresses (Fig. 1a–c). Decomposition of plant matter, for example, begins with depolymerization, in which extracellular enzymes break down polymers into monomers (Schimel, 2004). Various organic compounds in different stages of reaction may serve as substrates for non-microbial CH4 production (Fig. 1b–d). These organic compounds may come from living organisms and/or dead organic matter and include hydrocarbons (Schoell, 1988; Welhan, 1988; Etiope and Klusman, 2002), pectins (Keppler et al., 2006), lignins and celluloses (Vigano et al., 2008), ascorbic acid (Althoff et al., 2010), organic matter (Hurkuck et al., 2012; Jugold et al., 2012), and methionine (Lenhart et al., 2012). The kinds of organic compounds that may serve as substrates for non-microbial CH4 production primarily depend on the nature of their available functional groups. Functional groups are specific units of atoms and/or bonds in organic compounds that are responsible for characteristic chemical reactions associated with those molecules (March, 1992). Methyl (\CH3) or methoxyl (\O\CH3) groups in pectins and lignins of plants may serve as the precursor for non-microbial CH4 production under UV irradiation and heating (Keppler et al., 2008; Vigano et al., 2008; Messenger et al.,

2009). Methoxyl groups have two types of chemical bonds: the ester methoxyl group mainly appears in pectins, and the ether methoxyl group mainly exists in lignins (Vigano et al., 2009). But cellulose, which does not contain methyl groups, may also produce non-microbial CH4 (Vigano et al., 2008). Cellulose is the polymer of D-glucose molecules, which contains the hydroxymethyl group (\CH2\OH) that chemically differs from the methoxyl group. When CH4 is produced from such functional groups, two H atoms are added to the hydroxymethyl group instead of one in the case of the methyl group (Vigano et al., 2009). The acetyl group (\CO\CH3) is also a potential precursor for non-microbial CH4 production (Messenger et al., 2009). Methionine is a nonpolar α-amino acid that can play a major role in sulfur metabolism and trans-methylation reactions in organisms. Research suggested that the thiomethyl group (\S\CH3) of methionine might be a precursor for CH4 production in living plants (Bruhn et al., 2012). This was also confirmed in fungi, in which the thiomethyl group of methionine was found to be a precursor for nonmicrobial CH4 production (Lenhart et al., 2012). Additional functional groups that can serve as precursors for non-microbial CH4 production are likely to be found in the future. The methyl group is a type of hydrocarbon group. The C\H bonds and/or C\C bonds are common characteristics of organic compounds (Robert et al., 1992). Methyl groups usually occur in the C chains of organic compounds. The organic compounds with methyl groups are very diverse and are far from being limited to those listed in Fig. 2. The methyl group or its analogue (such as \CH2\) is contained in other functional groups such as methoxyl, acetyl, thiomethyl, and hydroxymethyl groups. A high availability of methyl type of functional groups may provide a large reservoir of precursors for non-microbial CH4 production. Thus, the methyl type of functional groups should be the focus for future research on non-microbial CH4 production.

5.2. The role of environmental stresses Organic compounds in nature are frequently subjected to various environmental stresses, such as high temperature, freeze/thaw, high

Fig. 2. The methyl group is ubiquitous in organic compounds. The methyl group is colored red. Short dotted lines (- -) usually denote a hydrocarbon chain of any length but may sometimes refer to any group of atoms. (a) hydrocarbons; (b) haloalkane, where X is a halogen: fluorine (F), chlorine (Cl), bromine (Br), or iodine (I); (c) organic compounds containing nitrogen; and (d) organic compounds containing sulfur. This figure was compiled using materials in en.wikipedia.org.


pressure, hypoxia/hyperoxia, reductive/oxidative conditions, water deficit/flooding, physical injury, solar UV radiation, and herbicides. Some stresses on one organism that are imposed by another organism can be considered environmental. For example, grazing by herbivores physically injures plant tissue. Plants, animals, and fungi often experience internal reductive or oxidative stresses that are also environmental. Microbial and non-microbial CH4 production have very different mechanisms (Fig. 1d,e). Microbial CH4 production is a multistep process in which CH4 is eventually produced by the precursors of acetate (CH3COOH), CO2, and H2 under the catalysis of the methyl coenzyme-M reductase of methanogenic archaea (Conrad, 1996; Schimel, 2004; Conrad, 2005). In contrast, non-microbial CH4 production is an instantaneous process that occurs when environmental stresses break down organic compounds, cleave functional groups (similar to decomposition by microbes in microbial CH4 production), and ‘catalyze’ the production of non-microbial CH4 (similar to enzymatic catalysis by methanogenic archaea in microbial CH4 production). Non-microbial CH4 was found to be produced from different components of plants under UV radiation and heating (Keppler et al., 2008; Vigano et al., 2008; Messenger et al., 2009). Plants, animals and fungi may also produce low quantities of non-microbial CH4 under ambient conditions (Ghyczy et al., 2003; Keppler et al., 2006; Ghyczy et al., 2008; Wang et al., 2011a; Lenhart et al., 2012), likely as a consequence of internal reductive or oxidative stress, which is an integral part of their metabolism. Non-microbial CH4 may also be a by-product of reactions involving organic compounds in organisms. More research is needed on non-microbial CH4 production under both internal physiological stresses and external ambient conditions. 5.3. The end production of non-microbial CH4 Methyl groups may exist as anions, cations, or a radical such as + methanide anion (\CH− 3 ), methylium cation (\CH3 ), and methyl radical (\CH3•) (March, 1992). Depending on the kind of methyl group, the organic compound with the methyl group may be oxidative − (R\CH+ 3 ), reductive (R\CH3 ), or neutral (R•) (Fig. 1d). The production of non-microbial CH4 requires a cooperative reactant (H+) and an oxidative, reductive, or neutral medium (Fig. 1d). These may be provided by free radical reactions. Free radicals, particularly reactive oxygen species (ROS), may react with organic compounds such as carbohydrates, nucleic acids, lipids, and proteins to generate a wide range of products (Møller et al., 2007). Free radicals, with three forms of charges (positive, negative, and neutral), are ubiquitous in nature. For example, environmental stresses on plants stimulate the formation of ROS, such as •OH, H2O2, O2•−, HO2•, and 1O2 (Thompson et al., 1987; Fry et al., 2001; Apel and Hirt, 2004). Non-microbial CH4 production involves ROS cleavage of methyl groups from plant pectin and/or lignin (Sharpatyi, 2007; Keppler et al., 2008; McLeod et al., 2008; Messenger et al., 2009). Free radicals are short-lived and highly reactive (March, 1992; Fry et al., 2001), which is consistent with the instantaneous production of non-microbial CH4 production in response to environmental stress. Redox (reduction–oxidation) reactions may provide a link between microbial and non-microbial CH4 production. Previous studies showed that microbial CH4 may be produced under aerobic or anaerobic conditions (DeGroot et al., 1994; Yavitt et al., 1995; Grossart et al., 2011). Non-microbial CH4 production in plant matter may also occur under aerobic or anaerobic conditions (Wang et al., 2011a,b). Whether nonmicrobial CH4 production is enhanced or inhibited under certain aerobic or anaerobic conditions presumably depends on which organic compounds interact in an environment. It has been clearly shown that CH4 production, whether microbial or non-microbial, does not completely depend on aeration conditions. Redox reactions resulting from the co-occurrence of electron acceptors and donors are fundamental for CH4 production.

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6. Isotopic signatures of non-microbial CH4 The formation of organic compounds and the production of CH4 cause the fractionation of isotopes, leading to the depletion or enrichment of C and H isotopes in the emitted CH4 (Schoell, 1988; Phillips and Gregg, 2001; Keppler et al., 2006; Whiticar and Schaefer, 2007; Vigano et al., 2008). Organic compounds obtain their isotopic signatures predominantly through plant biosynthesis. The δ13C of plant matter depends directly on atmospheric δ13CO2, photosynthetic pathways, and environmental parameters (Whiticar and Schaefer, 2007). When CH4 is produced from organic compounds that are derived from C3 or C4 plants, the δ13C\CH4 values are also distinctive. Therefore, the proportion of organic compounds derived from C3 versus C4 plants affects the isotopic signatures of the CH4 produced. On average, δ13C\CH4 ranges from −63‰ (termites) to −24‰ (biomass burning) while δD\CH4 ranges from −390‰ (termites) to −140‰ (coal mining) (Fig. 3). The isotopic signatures of CH4 would have much wider ranges if individual measurements are considered. Generally, the C and H isotopes in CH4 are more enriched when the CH4 is from non-microbial rather than microbial sources (Fig. 3), largely because the fractionation of the isotopes depends on the mechanism of CH4 production. The ranges of isotopic signatures of CH4 in the nonmicrobial sources are considerably larger than those in the microbial sources, partly due to the wide ranges in environmental conditions and organic precursor compounds involved in the non-microbial production (Keppler et al., 2004). In contrast, microbial CH4 is usually produced at ambient conditions from acetate and CO2, under relatively narrow ranges of environmental conditions that favor the enzymatic metabolism of methanogenic archaea, which results in the small ranges in the isotopic signatures of microbial CH4. It is likely that the isotopic signatures of CH4 are related to the strength of environmental stresses if other conditions are similar. However, this needs to be examined in future studies.

Fig. 3. Typical carbon and hydrogen isotopic signatures of CH4 in non-microbial (stars) and microbial (solid circles) sources. Isotopic signatures of atmospheric CH4 are indicated with an open circle. Red and green plots denote potential ranges of isotopic signatures of CH4 in the non-microbial and microbial sources, respectively. The colored arrow represents a hypothesized increase in environmental stresses. Isotopic signatures of CH4 in wetlands, ruminants, rice paddies, landfills, natural gas, coal mining, and biomass burning are from Quay et al. (1999). The error bars indicate the variation of reported values. Average isotopic signatures of CH4 in termites, ocean, freshwater, gas hydrates, and geological sources are from Whiticar and Schaefer (2007). The δ13C\CH4 in plants 1 are from Keppler et al. (2006) while the δD\CH4 are in the range of the projections by Whiticar and Schaefer (2007) and Fischer et al. (2008). The UV-derived isotopic signatures of CH4 in plants 2 are from Vigano et al. (2009). The average δ13C\CH4 in the organic matter of the bulk soil samples under heating, UV irradiation, and drying–rewetting cycles are from Jugold et al. (2012), while the δD\CH4 values in soils are assumed to have the same ranges as in plants.

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When the isotopic signatures of CH4 are near the upper and low ends of the range, they may be used as unambiguous fingerprints for nonmicrobial and microbial CH4 production. However, when the isotopic signatures of the two sources overlap, using them to distinguish between microbial vs. non-microbial production of CH4 will be difficult (Fig. 3). The CH4 produced from plant matter under UV irradiation, for example, was strongly depleted in both δ13C and δD, such that their values were close to or even overlapped with those from microbial sources (Vigano et al., 2009). The 13C and 2H of CH4 in landfills and oceans are usually slightly more enriched relative to the other microbial sources. Non-microbial CH4 produced from coal mining, natural gas, geological sources, soils, and gas hydrates are derived from dead organic matter. Non-microbial CH4 production may occur when fresh plant matter is burned but such production would obviously not include plant physiological activity. In the absence of burning, non-microbial CH4 production from plants, animals, and fungi is accompanied by physiological activity. The isotopic composition of non-microbial CH4 produced by dead organic matter may have unambiguous signatures, but that is not the case for non-microbial CH4 production by organisms (Fig. 3). At present, isotopic signature data of non-microbial CH4 produced in animals and fungi are lacking. Thus, multiple approaches must be used to determine the production of non-microbial CH4 by organisms. Molecular biology methods may be employed to pinpoint the presence or absence of microbial activity in CH4 production (Lenhart et al., 2012). State-of-the-art techniques of gas chromatography coupled to a combustion furnace and an isotope ratio mass spectrometer, and site-specific natural isotope fractionation nuclear magnetic resonance (SNIF-NMR) enable compound-specific isotope analysis at the molecular, functional group, and even atom levels (Lichtfouse, 2000); such techniques might help clarify the rates and mechanisms of non-microbial CH4 production. The isotopic signatures of atmospheric CH4 are the end result of the contributions of the different sources and sinks of CH4. The photochemical reactions in the troposphere and stratosphere involving CH4 and the CH4 uptake by aerated soils represent the most important sinks (Cicerone and Oremland, 1988; Prinn, 1994; Conrad, 2009). Typically, the reaction rate constants of CH4 sinks are faster for 12CH4 than for 13CH4 (Quay et al., 1999; Whiticar and Schaefer, 2007). As a result, the isotopic signatures of the residual CH4 are enriched relative to the source. In CH4 sinks, overall δ13C fractionation ranges from − 6.8 to − 10.8‰ while overall δD fractionation is − 218 ± 50‰ (Quay et al., 1999), leading to isotopic enrichment of CH4 in the atmosphere. Currently, atmospheric δ13C\CH4 and δD\CH4 are approximately − 48 and − 90‰, respectively (Fig. 3). Considerable uncertainties remain in the estimates on CH4 emissions from various sources to the atmosphere (Denman et al., 2007). The estimates can be constrained by the use of the tropospheric CH4 burden and the isotopic signatures of CH4 (Whiticar and Schaefer, 2007). On the global scale, however, it is difficult to obtain accurate isotopic signatures of non-microbial CH4. The question whether non-microbial CH4 emissions to the atmosphere can be confidently estimated using the isotopic signatures of CH4 is unanswered. Thus, it is essential that additional measurements are made so as to improve our understanding of the non-microbial CH4 budget. 7. Future directions Non-microbial CH4 production is an instantaneous response to environmental stresses and is more pervasive than previously thought. Even though non-microbial CH4 production is not characterized by the kinds of fixed mechanisms that characterize microbial CH4 production, its specific production processes should be better studied in organisms and dead organic matter. A key aspect of such studies is the identification of the functional groups of organic compounds that act as precursors to non-microbial CH4 production. Free radicals are widespread

and abundant in nature; their role in non-microbial CH4 production should receive increased attention in future research. Currently, no information is available on in situ emissions of nonmicrobial CH4 in terrestrial ecosystems. It is too early to draw conclusions on the extent and size of total non-microbial CH4 emissions in nature, because of the high uncertainties related to mechanisms, organic compounds and functional groups involved, and environmental stresses. Methylation is a common reaction involving many types of organic compounds, and organic compounds with a high degree of methylation should receive more attention in studying non-microbial CH4 emissions. Among all forms of emissions of non-microbial CH4, geological sources require the most attention in future research. The potentially large quantity of geological CH4 emission would warrant its inclusion in future IPCC greenhouse gas inventories. Additional measurements in a wide range of sites are essential for obtaining improved estimates of CH4 emissions from geological sources. Plants have been demonstrated to be a potential source of nonmicrobial CH4 production. However, all reported data concerning nonmicrobial CH4 production in plants have been obtained under controlled laboratory conditions. A few field studies failed to find in situ emissions of non-microbial CH4 from plants. For example, no substantial foliar CH4 emissions were found over a forest canopy under high UV irradiation (Bowling et al., 2009). Similarly, no CH4 emissions were detected from intact leaves and trunks of Japanese cypress (Chamaecyparis obtusa Sieb. et Zucc) in the field (Takahashi et al., 2012). No conclusive evidence was found for non-microbial CH4 emissions from the canopy in an upland tropical forest (Reserva Biológica Cuieiras), about 60 km north of Manaus, Brazil (Querino et al., 2011). This might reflect limitations of the traditional chamber and micro-meteorological methods or be essentially due to negligible emissions by plants in the field. Improved methods to measure in situ non-microbial CH4 production in the field are required. Soils are extensive and store a huge amount of organic matter, but non-microbial CH4 production in soils has rarely been studied. Even though non-microbial CH4 emission rates from the soil are small when compared with those in wetlands (Jugold et al., 2012), non-microbial CH4 emission from the soil could be globally significant because the global land area is very large. Non-microbial CH4 production might be highly sensitive to global change, such as global warming, land use change, stratospheric ozone depletion, spread of pests and atmospheric pollution. Environmental stresses drive non-microbial CH4 production in organisms and dead organic matter. Even though the evolution of non-microbial sources with respect to global change is not unique and microbial emissions may show even stronger dependencies at least on some factors, we believe global changes will increase the frequency and strength of environmental stresses imposed on organisms and dead organic matter and result in increased global emissions of non-microbial CH4. This topic should receive increased research and should be considered in models that simulate climatic change. Acknowledgments This research was supported by the National Natural Science Foundation of China (31370493), the Natural Science and Engineering Council of Canada (NSERC), the Rangeland Research Institute at the University of Alberta, and the State Key Laboratory of Vegetation and Environmental Change (2011zyts07). We thank the editor and anonymous reviewers for their constructive comments that improved an earlier version of the manuscript. References Althoff, F., Jugold, A., Keppler, F., 2010. Methane formation by oxidation of ascorbic acid using iron minerals and hydrogen peroxide. Chemosphere 80, 286–292. Andreae, M.O., Merlet, P., 2001. Emissions of trace gases and aerosols from biomass burning. Glob. Biogeochem. Cycles 15, 955–966.

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