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Aerobic methane production

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Methane

Aerobic methane production is a potential biological pathway for atmospheric methane (CH4) production under oxygenated conditions. The existence of this pathway was first theorized in 2006.[1] While significant evidence suggests the existence of this pathway,[1][2][3][4][5] it remains poorly understood and its existence is controversial.[2][6][7] Naturally occurring methane is mainly produced by the process of methanogenesis, a form of anaerobic respiration used by microorganisms as an energy source.[8] Methanogenesis usually only occurs under anoxic conditions. By contrast, aerobic methane production is thought to occur in oxygenated environments under near-ambient conditions. The process involves non-microbial methane generation from terrestrial plant-matter. Temperature and ultraviolet light are thought to be key factors in this process.[1] Methane may also be produced under aerobic conditions in near-surface ocean water, a process which likely involves the degradation of methylphosphonate.[9]

From terrestrial plants

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Global atmospheric methane distribution
Part of a series on the
Carbon cycle
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Carbon dioxide
Forms of carbon
Metabolic pathways
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Initial discovery

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In 2005, Frankenberg et al. published the findings of a global methane distribution study in which they used space-borne near-infrared absorption spectroscopy. The study identified significantly elevated CH4 mixing ratios in tropical regions above evergreen forests.[10] The data indicated an additional tropical source of 30–40 Tg[10] over the time period of the investigation (August–November). This contribution could not be adequately explained within the currently accepted global budget of CH4.[10] These findings prompted Keppler et al. to conduct their study to investigate the possibility of methane formation by plant material. Their study included glass vial incubation experiments with detached leaves and Plexiglas chamber experiments with intact plants. In both cases the material was sealed in a controlled environment with CH4-free air in order to analyze the production of CH4. Since the tests were conducted under aerobic conditions it was unlikely that any CH4 produced would be related to methanogenic bacteria.[1] This possibility was further excluded by measuring CH4 production by leaf tissue sterilized with γ-radiation. They theorized that "the structural component pectin plays a prominent role in the in situ formation of CH4 in plants"[1] but were unable to identify a chemical mechanism for this CH4 production.

Further study

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Wang et al. (2008) found that methane emissions varied greatly by plant species, noting that shrub species were much more likely to produce methane than herbaceous species.[4] They also noted that among herbaceous species which they tested, those that emitted methane did so from stems, but not from detached leaves, while shrub species typically emitted higher methane concentrations from detached leaves.[4] A follow-up study by Keppler et al. reconfirmed their earlier findings and found "unambiguous isotope evidence that methoxyl groups of pectin can act as a source of atmospheric CH4 under aerobic conditions",[3] but again failed to identify the chemical mechanism.

Influence of temperature and light

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Keppler et al.. observed that the release of CH4 was "very temperature sensitive—concentrations approximately doubled with every 10 °C increase over the range 30–70 °C suggesting a non-enzymic rather than an enzyme-mediated process".[1] They also remarked that "emission rates were found to increase dramatically, by a factor of 3–5 (up to 870 ng per g (dry weight) h−1), when chambers were exposed to natural sunlight".[1] Vigano et al.. found that "emissions from UV irradiation are almost instantaneous, indicating a direct photochemical process".[2]

Potential environmental significance

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Keppler et al.. calculated a "first estimate" for the newly established CH4 source. Their calculations were based on broad assumptions, which they admitted neglected "the complexity of terrestrial ecosystems".[1] They estimated methane released by living vegetation to be in the range 62–236 Tg yr−1 (average 149 Tg yr−1) with the main contribution assigned to tropical forests and grasslands.[1] They believed that "the detection of an additional source of this magnitude, some 10-30% of the present annual source strength, would necessitate reconsideration of the global CH4 budget".[1] Later estimates, using Keppler et al.'s data as well as data produced by later studies suggested a lesser global significance.[3] One study suggested that the maximum global emissions of methane from terrestrial plants might only be on the order of 0.2–1.0 Tg CH4 yr−1 compared with total global emissions of 550 Tg CH4 yr−1, a significantly smaller contribution.[5]

Criticism and conflicting data

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Following the publication of Keppler et al.'s (2006) findings, there was a substantial response from the scientific community. Many questioned the findings, pointing to flaws in Keppler et al.'s methodology. In particular, their up-scaling method for calculating global estimates for methane emissions by terrestrial plants was criticized.[2] A number of follow-up publications presented conflicting data, generating significant uncertainty in the role of terrestrial plants to the global methane budget.

Dueck et al. conducted similar experiments to the intact-plant chamber experiments conducted by Keppler et al.. They found "no evidence for substantial methane emissions from terrestrial plants".[7] They suggested that the supposed emissions observed by Keppler et al. may have been related to "ambient methane concentrations in inter-cellular air spaces and air spaces in the soil system".[7] Vigano et al. later responded to this criticism by suggesting that, if UV light is in fact an important factor in aerobic methane emissions, "then it is not surprising that no emissions were found by Dueck et al. (2007), who used metal halide HPI-T lamps and glass chambers for their measurements".[2] Other studies suggested that the detected methane emissions were related to transport of dissolved methane from the soil in water, or to the spontaneous breakdown of plant matter under certain stress conditions.[6]

In aquatic environments

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See also: Methane § Geological routes

Supersaturation of methane in oxygenated, near-surface water in oceans, lakes and rivers is a phenomenon which has been widely observed, but which is still poorly understood.[11] Methane is often 10–75% supersaturated in the oxygenated surface mixed layer of oceans, and up to 1000% in lakes causing aquatic envirionments to contribute methane to the atmosphere.[11][12][13]

Several sources and mechanisms have been identified for the production of methane in aquatic environments. One such source is the degradation of dissolved water column methylphosphonate.[9] The importance of the degradation of methylphosphonate in the production of CH4 in the ocean is likely variable and may be related to the availability of Fe, N, and P in the water column[11] and to the presence and nature of the enzymatic machinery that processes the methylphosphonates.[14]

A second source which appears not to depend on any substrate is the emission of methane by phytoplankton (algae and cyanobacteria) during the process of photosynthesis.[15][16]

The presence of algae and cyanobacteria in all illuminated aquatic environments on Earth likely makes this process a significant contributor to aquatic methane emissions. In the last decades we have been witnessing an increase in cyanobacterial and algal blooms as a result of anthropogenic pollution and global warming.[17][18]

Since Atmospheric methane is a very potent greenhouse gas, a feedback loop was hypothesized in which algae and cyanobacteria produced methane, enhance warming, and subsequently enhance blooms.[19] Dimethylsulfoniopropionate (DMSP) is a common compound in marine environments used by algae as an osmoprotectant. Several studies have revealed that the degradation of DMSP by bacteria results in the release of methane.[20][21]

Methylamines are a known source of methane from anoxic environments. In 2018, Bizic et al. published results showing that degradation of methylamines result in methane emissions also under oxic conditions.[22] The mechanism responsible for this process was later identified by Wang et al. and was attributed to a single, very common gene.[23][24]

Several other mechanisms have been since then recognized. In 2022, Perez-Coronel & Beman analyzed methane production in fresh water and found an association with "(bacterio)chlorophyll metabolism and photosynthesis,[25] Keppler and colleagues identified a mechanism through which reactive oxygen species result in the production of methane by potentially organism utilizing oxygen.[26][27]

References

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  1. ^ a b c d e f g h i j Keppler, Frank; Hamilton, John T. G.; Braß, Marc; Röckmann, Thomas (12 January 2006). "Methane emissions from terrestrial plants under aerobic conditions". Nature. 439 (7073): 187–191. Bibcode:2006Natur.439..187K. doi:10.1038/nature04420. PMID 16407949. S2CID 2870347.
  2. ^ a b c d e Vigano, I.; van Weelden, H.; Holzinger, R.; Keppler, F.; McLeod, A.; Röckmann, T. (26 June 2008). "Effect of UV radiation and temperature on the emission of methane from plant biomass and structural components". Biogeosciences. 5 (3): 937–947. Bibcode:2008BGeo....5..937V. doi:10.5194/bg-5-937-2008. hdl:20.500.11820/c41a0c2c-a7c2-43b3-a4c2-189ba201438f.
  3. ^ a b c Keppler, Frank; Hamilton, John T. G.; McRoberts, W. Colin; Vigano, Ivan; Braß, Marc; Röckmann, Thomas (June 2008). "Methoxyl groups of plant pectin as a precursor of atmospheric methane: evidence from deuterium labelling studies". New Phytologist. 178 (4): 808–814. doi:10.1111/j.1469-8137.2008.02411.x. PMID 18346110.
  4. ^ a b c Wang, ZP; Han, XG; Wang, GG; Song, Y; Gulledge, J (1 January 2008). "Aerobic methane emission from plants in the Inner Mongolia steppe". Environmental Science & Technology. 42 (1): 62–8. Bibcode:2008EnST...42...62W. doi:10.1021/es071224l. PMID 18350876.
  5. ^ a b Bloom, A. Anthony; Lee-Taylor, Julia; Madronich, Sasha; Messenger, David J.; Palmer, Paul I.; Reay, David S.; McLeod, Andy R. (July 2010). "Global methane emission estimates from ultraviolet irradiation of terrestrial plant foliage". New Phytologist. 187 (2): 417–425. doi:10.1111/j.1469-8137.2010.03259.x. PMID 20456057.
  6. ^ a b Nisbet, R.E.R; Fisher, R; Nimmo, R.H; Bendall, D.S; Crill, P.M; Gallego-Sala, A.V; Hornibrook, E.R.C; Lopez-Juez, E; Lowry, D; Nisbet, P.B.R; Shuckburgh, E.F; Sriskantharajah, S; Howe, C.J; Nisbet, E.G (13 January 2009). "Emission of methane from plants". Proceedings of the Royal Society B: Biological Sciences. 276 (1660): 1347–1354. doi:10.1098/rspb.2008.1731. PMC 2660970. PMID 19141418.
  7. ^ a b c Dueck, TA; de Visser, R; Poorter, H; Persijn, S; Gorissen, A; de Visser, W; Schapendonk, A; Verhagen, J; Snel, J; Harren, FJ; Ngai, AK; Verstappen, F; Bouwmeester, H; Voesenek, LA; van der Werf, A (2007). "No evidence for substantial aerobic methane emission by terrestrial plants: a 13C-labelling approach". The New Phytologist. 175 (1): 29–35. doi:10.1111/j.1469-8137.2007.02103.x. PMID 17547664.
  8. ^ Thauer, R. K. (1998). "Biochemistry of Methanogenesis: a Tribute to Marjory Stephenson". Microbiology. 144 (9): 2377–2406. doi:10.1099/00221287-144-9-2377. PMID 9782487.
  9. ^ a b Karl, David M.; Beversdorf, Lucas; Björkman, Karin M.; Church, Matthew J.; Martinez, Asuncion; Delong, Edward F. (29 June 2008). "Aerobic production of methane in the sea". Nature Geoscience. 1 (7): 473–478. Bibcode:2008NatGe...1..473K. doi:10.1038/ngeo234.
  10. ^ a b c Frankenberg, C.; Meirink, J. F.; van Weele, M.; Platt, U.; Wagner, T. (13 May 2005). "Assessing Methane Emissions from Global Space-Borne Observations". Science. 308 (5724): 1010–1014. Bibcode:2005Sci...308.1010F. doi:10.1126/science.1106644. PMID 15774724. S2CID 14987357.
  11. ^ a b c del Valle, DA; Karl, DM (2 October 2014). "Aerobic production of methane from dissolved water-column methylphosphonate and sinking particles in the North Pacific Subtropical Gyre". Aquatic Microbial Ecology. 73 (2): 93–105. doi:10.3354/ame01714.
  12. ^ Rosentreter, Judith A.; Borges, Alberto V.; Deemer, Bridget R.; Holgerson, Meredith A.; Liu, Shaoda; Song, Chunlin; Melack, John; Raymond, Peter A.; Duarte, Carlos M.; Allen, George H.; Olefeldt, David; Poulter, Benjamin; Battin, Tom I.; Eyre, Bradley D. (April 2021). "Half of global methane emissions come from highly variable aquatic ecosystem sources". Nature Geoscience. 14 (4): 225–230. Bibcode:2021NatGe..14..225R. doi:10.1038/s41561-021-00715-2. hdl:10754/668712. S2CID 233030781.
  13. ^ Günthel, Marco; Donis, Daphne; Kirillin, Georgiy; Ionescu, Danny; Bizic, Mina; McGinnis, Daniel F.; Grossart, Hans-Peter; Tang, Kam W. (2 December 2019). "Contribution of oxic methane production to surface methane emission in lakes and its global importance". Nature Communications. 10 (1): 5497. Bibcode:2019NatCo..10.5497G. doi:10.1038/s41467-019-13320-0. PMC 6888895. PMID 31792203.
  14. ^ Sosa, Oscar A.; Casey, John R.; Karl, David M. (July 2019). "Methylphosphonate Oxidation in Prochlorococcus Strain MIT9301 Supports Phosphate Acquisition, Formate Excretion, and Carbon Assimilation into Purines". Applied and Environmental Microbiology. 85 (13). Bibcode:2019ApEnM..85E.289S. doi:10.1128/AEM.00289-19. PMC 6581173. PMID 31028025.
  15. ^ Williams, R. (2020) Blue-green algae produce methane, The Scientist Magazine®. Available at: https://www.the-scientist.com/blue-green-algae-produce-methane-66971 (Accessed: 12 March 2024).
  16. ^ Klintzsch, Thomas; Langer, Gerald; Nehrke, Gernot; Wieland, Anna; Lenhart, Katharina; Keppler, Frank (28 October 2019). "Methane production by three widespread marine phytoplankton species: release rates, precursor compounds, and potential relevance for the environment". Biogeosciences. 16 (20): 4129–4144. Bibcode:2019BGeo...16.4129K. doi:10.5194/bg-16-4129-2019.
  17. ^ Climate warming may increase algal blooms caused by sediment nutrient release in lakes – management must adapt(2023) Environment. Available at: https://environment.ec.europa.eu/news/climate-warming-may-increase-algal-blooms-caused-sediment-nutrient-release-lakes-management-must-2023-01-18_en (Accessed: 12 March 2024).
  18. ^ Colm, R. (2024) EPA: Agriculture the ‘biggest driver’ of algal blooms in rural areas, Agriland.ie. Available at: https://www.agriland.ie/farming-news/epa-agriculture-the-biggest-driver-of-algal-blooms-in-rural-areas (Accessed: 12 March 2024).
  19. ^ Bizic, Mina (23 November 2021). "Phytoplankton photosynthesis: an unexplored source of biogenic methane emission from oxic environments". Journal of Plankton Research. 43 (6): 822–830. doi:10.1093/plankt/fbab069.
  20. ^ Florez-Leiva, Lennin; Damm, Ellen; Farías, Laura (May 2013). "Methane production induced by dimethylsulfide in surface water of an upwelling ecosystem" (PDF). Progress in Oceanography. 112–113: 38–48. Bibcode:2013PrOce.112...38F. doi:10.1016/j.pocean.2013.03.005.
  21. ^ Damm, E.; Kiene, R.P.; Schwarz, J.; Falck, E.; Dieckmann, G. (February 2008). "Methane cycling in Arctic shelf water and its relationship with phytoplankton biomass and DMSP". Marine Chemistry. 109 (1–2): 45–59. Bibcode:2008MarCh.109...45D. doi:10.1016/j.marchem.2007.12.003.
  22. ^ Bižić-Ionescu, Mina; Ionescu, Danny; Günthel, Marco; Tang, Kam W.; Grossart, Hans-Peter (2018). "Oxic Methane Cycling: New Evidence for Methane Formation in Oxic Lake Water". Biogenesis of Hydrocarbons. pp. 1–22. doi:10.1007/978-3-319-53114-4_10-1. ISBN 978-3-319-53114-4.
  23. ^ Montana State University (2021) Research team publishes groundbreaking methane synthesis discovery, Phys.org - News and Articles on Science and Technology. Available at: https://phys.org/news/2021-07-team-publishes-groundbreaking-methane-synthesis.amp (Accessed: 13 March 2024).
  24. ^ Wang, Qian; Alowaifeer, Abdullah; Kerner, Patricia; Balasubramanian, Narayanaganesh; Patterson, Angela; Christian, William; Tarver, Angela; Dore, John E.; Hatzenpichler, Roland; Bothner, Brian; McDermott, Timothy R. (6 July 2021). "Aerobic bacterial methane synthesis". Proceedings of the National Academy of Sciences. 118 (27). Bibcode:2021PNAS..11819229W. doi:10.1073/pnas.2019229118. PMC 8271786. PMID 34183407.
  25. ^ Perez-Coronel, Elisabet; Michael Beman, J. (29 October 2022). "Multiple sources of aerobic methane production in aquatic ecosystems include bacterial photosynthesis". Nature Communications. 13 (1): 6454. Bibcode:2022NatCo..13.6454P. doi:10.1038/s41467-022-34105-y. PMC 9617973. PMID 36309500.
  26. ^ Ernst, Leonard; Steinfeld, Benedikt; Barayeu, Uladzimir; Klintzsch, Thomas; Kurth, Markus; Grimm, Dirk; Dick, Tobias P.; Rebelein, Johannes G.; Bischofs, Ilka B.; Keppler, Frank (17 March 2022). "Methane formation driven by reactive oxygen species across all living organisms". Nature. 603 (7901): 482–487. Bibcode:2022Natur.603..482E. doi:10.1038/s41586-022-04511-9. PMID 35264795.
  27. ^ Liu, Chang; Zhang, Jingyao (17 March 2022). "Methane might be made by all living organisms". Nature. 603 (7901): 396–397. Bibcode:2022Natur.603..396L. doi:10.1038/d41586-022-00206-3. PMID 35264800. S2CID 247362071.
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