Earth-Science Reviews 127 (2013) 193–202
Contents lists available at ScienceDirect
Earth-Science Reviews
journal homepage: www.elsevier.com/locate/earscirev
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
1.
2.
3.
4.
5.
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
194
Z.-P. Wang et al. / Earth-Science Reviews 127 (2013) 193–202
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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198
199
199
200
200
200
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.
Z.-P. Wang et al. / Earth-Science Reviews 127 (2013) 193–202
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.
195
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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Z.-P. Wang et al. / Earth-Science Reviews 127 (2013) 193–202
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
Z.-P. Wang et al. / Earth-Science Reviews 127 (2013) 193–202
197
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
198
Z.-P. Wang et al. / Earth-Science Reviews 127 (2013) 193–202
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.
Z.-P. Wang et al. / Earth-Science Reviews 127 (2013) 193–202
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.
199
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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Z.-P. Wang et al. / Earth-Science Reviews 127 (2013) 193–202
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.
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