ANAEROBIC OXIDATION OF METHANE IN FRESHWATER ECOSYSTEMS

Anaerobic oxidation of methane (AOM) is a biochemical process that plays an important role in aquatic ecosystems, as it significantly reduces the emission of methane (CH₄) to the atmosphere. Under anaerobic conditions, CH₄ can be oxidized with electron acceptors, such as sulphates (SO₄^2-), nitrates (NO₃^-) or nitrites (NO₂^-), iron (Fe³⁺), manganese (Mn⁴⁺) and humic substances. The anaerobic oxidation of methane is mainly regulated by anaerobic methanotrophic archaea (ANME) and sulphate reducing bacteria. The AOM process is crucial to understand the CH₄ cycle and anticipate future emissions of the gas from water reservoirs. The process is widely described in marine environments, however very little is known about its occurrence and importance in freshwater systems. There is a great demand for this kind of the research, especially in ecosystems exposed to long-term anaerobic conditions, which may be in degraded reservoirs.

Full text (pdf)

1. Alperin M.J., Reeburgh W.S., Whiticar M.J., Carbon and hydrogen isotope fractionation resulting from anaerobic methane oxidation, Global Biogeochem. Cycles, 2, 1988, 279–288.
2. Aquilina A., Knab N.J., Knittel K., Kaur G., Geissler A., Kelly S.P., Fossing H., Boot C.S., Parkes R.J., Mills R.A., Boetius A., Lloyd J.R., Pancost R.D., Biomarker indicators for anaerobic oxidizers of methane in brackish-marine sediments with diffusive methane fluxes, Organic Geochemistry 41, 2010, 414–426.
3. Bastviken D., Cole J.J., Michael L. Pace  Matthew C. Van de Bogert, Fates of methane from different lake habitats: Connecting whole‐lake budgets and CH₄ emissions, Journal of geophysical research, 113, 2008, doi:10.1029/2007JG000608.
4. Bastviken, D., Ejlertsson, J., Sundh, I., Tranvik, L., Methane as a source of carbon and energy for lake pelagic food webs, Ecology 84, 2003, 969–981.
5. Bastviken D., Ejlertsson J., and Tranvik L., Measurement of methane oxidation in lakes—A comparison of methods, Environ. Sci. Technol., 36, 2002, 3354–3361.
6. Beal E.J., House C.H., Orphan V.J., Manganese- and Iron-Dependent Marine Methane Oxidation, 325(5937), 2009, 184–187, DOI: 10.1126/science.1169984.
7. Boetius A., Ferdelman T., Lochtea K., Bacterial activity in sediments of the deep Arabian Sea in relation to vertical flux, Deep Sea Research Part II: Topical Studies in Oceanography, 47(14), 2000a, 2835–2875.
8. Boetius A., Ravenschlag K., Schubert C. J., Rickert D., Widdel F., Gieseke A., Amann R., Jørgensen B. B., Witte U., Pfannkuche O., A marine microbial consortium apparently mediating anaerobic oxidation of methane, Nature, 407, 2000b, 623–626, doi:10.1038/35036572.
9. Caldwell S.L., Laidler J.R., Brewer E.A., Eberly J.O., Sandborgh S.C., Colwell F.S., Anaerobic oxidation of methane: Mechanisms, bioenergetics, and the ecology of associated microorganisms, Environ Sci Technol. 42, 2008, 6791–6799.
10. Crowe S.A., Katsev S., Leslie K., et al., The methane cycle in ferruginous Lake Matano, Geobiology 9(1), 2011, 61–78.
11. Deutzmann J.S., Hoppert M., Schink B., Characterization and phylogeny of a novel methanotroph, Methyloglobulus morosus gen. nov., spec. nov. Sys. Appl. Microbiol. 37, 2014, 165–169, doi: 10.1016/j.syapm.2014.02.001.
12. Deutzmann, J. S., Schink B., Anaerobic Oxidation of Methane in Sediments of Lake Constance, an Oligotrophic Freshwater Lake, Applied and Environmental Microbiology, 77, 2011, 4429–4436.
13. Egger M., Jilbert T., Behrends T., Rivard C., Slomp C. P., Vivianite is a major sink for phosphorus in methanogenic coastal surface sediments, Geochimica et Cosmochimica Acta, 169, 2015, 217–235.
14. Ettwig K.F., Butler M.K., Le Paslier D. et al., Nitrite-driven anaerobic methane oxidation by oxygenic bacteria, Nature 464(7288), 2010, 543–548.
15. Ettwig K.F., Shima S., van de Pas-Schoonen K.T., Kahnt J., Medema M.H., op den Camp H.J.M., Jetten M.S.M., Strous M., Denitrifying bacteria anaerobically oxidize methane in the absence of Archaea, Environmental Microbiology, 10(11), 2008, 3164–3173, doi:10.1111/j.1462-2920.2008.01724.x.
16. Ettwig K.F., van Alen T., van de Pas-Schoonen K.T., Jetten M.S.M., Strous M., Enrichment and molecular detection of denitrifying methanotrophic bacteria of the NC10 phylum, Appl. Environ. Microbiol., 75, 2009, 3656–3662.
17. Ettwig K., Zhu B., Speth D., Keltjens J.T., Jetten M.S.M., Kartal B., Archaea catalyze iron-dependent anaerobic oxidation of methane, PNAS, 113, 45, 2016, 12792–12796, www.pnas.org/cgi/doi/10.1073/pnas.1609534113.
18. Harder, J., Anaerobic methane oxidation by bacteria employing (super 14) C-methane uncontaminated with (super 14) C-carbon monoxide, In T. C. E. van Weering, G. T. Klaver, and R. A. Prins (ed.), Marine geology, Elsevier, Amsterdam, The Netherlands, vol. 137, 1997, 13–23.
19. Haroon MF, et al., Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage, Nature 500(7464), 2013, 567–570.
20. Hinrichs K.-U., Boetius A., The Anaerobic Oxidation of Methane: New Insights in Microbial Ecology and Biogeochemistry, Ocean Margin Systems, 2002, 457–477.
21. Hinrichs K.-U., Hayes J.M., Sylva S.P., Brewer P.G., DeLong E.F., Methane-consuming archaebacteria in marine sediments, Nature, 398, 1999, 802–805.
22. Hoehler T., M.J. Alperin, D.B. Albert, C.S. Martens, Field and laboratory studies of methane oxidation in an anoxic marine sediment: Evidence for a methanogen-sulfate reducer consortium, Global Biogeochemical Cycles 8(4), 1994, 451–463.
23. Hu B., Shen L., Lian X., Zhu Q., Liu S., Huang Q., He Z., Geng S., Cheng D., Lou L., Xu X., Zheng P., He Y., Evidence for nitrite-dependent anaerobic methane oxidation as a previously overlooked microbial methane sink in wetlands, PNAS 111(22), 2014, 4495–4500.
24. Intergovernmental Panel on Climate Change, Climate Change 2014, Mitigation of Climate Change, Summary for Policymakers and Technical Summary, 2015.
25. Islas-Lima S., Thalasso, F., Gomez-Hernandez, J., Evidence of anoxic methane oxidation coupled to denitrification, Water Res., 38, 2004, 13–16.
26. Iversen N., Jørgensen B.B., Anaerobic methane oxidation rates at the sulfate-methane transition in marine sediments from Kattegat and Skagerrak (Denmark), Limnology and Oceanography 30(5), 1985, 944–955, DOI: 10.4319/lo.1985.30.5.0944.
27. Jones, R. I., Grey, J., Biogenic methane in freshwater food webs, Freshw. Biol. 56, 2011, 213–229. doi: 10.1111/j.1365-2427.2010.02494.x.
28. Jones R.L.I., Whatley R.C., Cronin T.M., Dowsett H.J., Reconstructing late Quaternary deep-water masses in the eastern Arctic Ocean using benthonic ostracoda, Marine Micropaleontology, 37(3–4), 1999, 251–272, https://doi.org/10.1016/S0377-8398(99)00022-5.
29. Kankaala, P., Eller G., Jones R.I., Could bacterivorous zooplankton affect lake pelagic methanotrophic activity, Fundamental and Applied Limnology, 169, 2007a, 203–209.
30. Kankaala P., Taipale S., Grey J., Sonninen E., Arvola L., Jones R.I., Experimental δ¹³C evidence for a contribution of methane to pelagic food webs in lakes, Limnol. Oceanogr. 51(6), 2006, 2821–2827.
31. Kankaala, P., Taipale S., Nykänen H., Jones R. I., Oxidation, efflux and isotopic fractionation of methane during autumnal turnover in a polyhumic, boreal lake, Journal of Geophysical Research–Biogeosciences, 112, 2007b, doi: 10.1029/2006JG000336.
32. Knittel K., Boetius A., Anaerobic oxidation of methane: Progress with an unknown process. Annual Reviews of Microbiology, 63, 2009, 311–334.
33. Knittel K., Lösekann T., Boetius A., Kort R., Amann R., Diversity and Distribution of Methanotrophic Archaea at Cold Seeps, Applied and Environmental Microbiology, 71(1), 2005, 467–479, https://doi.org/10.1128/AEM.71.1.467-479.2005.
34. Lofton D., Whalen S. C., Hershey A. E., Effect of temperature on methane dynamics and evaluation of methane oxidation kinetics in shallow Arctic Alaskan lakes, Hydrobiologia 721(1), 2014, DOI: 10.1007/s10750-013-1663-x.
35. Lösekann T., Knittel K., Nadalig T., Fuchs B., Niemann H., Boetius A. et al., Diversity and abundance of aerobic and anaerobic methane oxidizers at the Haakon Mosby mud volcano, Barents Sea, Appl. Environ. Microbiol., 73, 2007, 3348–3362.
36. Maignien L., Parkes R.J., Cragg B., Niemann H., Knittel K., Coulon S., Akhmetzhanov A., Boon N., Anaerobic oxidation of methane in hypersaline cold seep sediments, FEMS Microbiol. Ecol, 83, 2013, 214–231.
37. Martinez-Cruz K., Leewis M.-C., Herriott I. C., Sepulveda-Jauregui A., Anthony K. W., Thalasso F., Leigh M. B., Anaerobic oxidation of methane by aerobic methanotrophs in sub-Arctic, Science of the Total Environment, 607–608, 2017, 23–31.
38. Milucka J., et al., Zero-valent sulphur is a key intermediate in marine methane oxidation. Nature, 491(7425), 2012, 541–546.
39. Moran J.J., House C.H., Freeman K.H., Ferry J.G., Trace methane oxidation studied in several Euryarchaeota under diverse conditions, Archaea, 1, 2005, 303–309.
40. Niemann H., Duarte J., Hensen C., Omoregie E., Magalhaes V.H., Elvert M., Pinheiro L.M., Kopf A., Boetius A., Microbial methane turnover at mud volcanoes of the Gulf of Cadiz, Geochimica et Cosmochimica Acta, 70, 2006, 5336–5355.
41. Nordi K.A., Thamdrup B., Nitrate-dependent anaerobic methane´oxidation in a freshwater sediment, Geochim Cosmochim Acta, 132, 2014, 141–150.
42. Nordi K., Thamdrup B., Schubert C. J., Anaerobic oxidation of methane in an iron-rich Danish freshwater Lake sediment, Limnol. Oceanogr., 58(2), 2013, 546–554, doi:10.4319/lo.2013.58.2.0546.
43. Oni O., Miyatake T., Kasten S., Richter-Heitmann T., Fischer D., Wagenknecht L., et al., Distinct microbial populations are tightly linked to the profile of dissolved iron in the methanic sediments of the Helgoland mud area, North Sea. Front. Microbiol, 6(365), 2015, doi: 10.3389/fmicb.2015.00365.
44. Pancost R.D., Sinninghe Damsté J.S., de Lint S., van der Maarel M.J., Gottschal J.C., Biomarker evidence for widespread anaerobic methane oxidation in Mediterranean sediments by a consortium of methanogenic archaea and bacteria, Applied and Environmental Microbiology, 66, 2000, 1126–1132.
45. Raghoebarsing A.A., Pol A., van de Pas-Schoonen K.T., Smolders A.J., Ettwig K.F., Rijpstra W.I., Schouten S., Damsté J.S., Op den Camp H.J., Jetten M.S., Strous M., A microbial consortium couples anaerobic methane oxidation to denitrification, Nature, 440(7086), 2006, 918–921.
46. Reeburgh, W., Oceanic methane biogeochemistry, Chem. Rev., 107, 2007, 486–513.
47. Riedinger N., Formolo M. J., Lyons T. W., Henkel S., Beck A., Kasten S., An inorganic geochemical argument for coupled anaerobic oxidation of methane and iron reduction in marine sediments, Geobiology, 12(2), 2014, 172–181.
48. Roland F. A. E., Morana C., Darchambeau F., Crowe S. A., Thamdrup B., Descy J.-P., Borges A. V., Anaerobic methane oxidation and aerobic methane production in an east African great lake (Lake Kivu), Journal of Great Lakes Research, 2018, (in press).
49. Scheller S., Yu H., Chadwick G. L., McGlynn S. E., Orphan V. J., Artificial electron acceptors decouple archaeal methane oxidation from sulfate reduction, Science, 351(6274), 2016, 703–707, DOI: 10.1126/science.aad7154.
50. Schlesinger W.H., Bernhardt E.S., Biogeochemistry: an analysis of global change, 2013.
51. Schubert C. J., et al., Oxidation and emission of methane in a monomictic lake (Rotsee, Switzerland), Aquat. Sci., 72, 2010, 455–466, doi:10.1007/s00027-010-0148-5.
52. Schubert C.J., Vazquez F., Lösekann-Behrens T., Knittel K., Tonolla M., Boetius A., Evidence for anaerobic oxidation of methane in sediments of a freshwater system (Lago di Cadagno), FEMS Microbiol Ecol., 76, 2011, 26–38.
53. Sivan O., Adler M., Pearson A. et al., Geochemical evidence for ironmediated anaerobic oxidation of methane, Limnol Oceanogr., 56, 2011, 1536–1544.
54. Smemo K.A., Yavitt J.B., Anaerobic oxidation of methane: an underappreciated aspect of methane cycling in peatland ecosystems?,  Biogeosciences, 8, 2011,
    779–793, https://doi.org/10.5194/bg-8-779-2011.
55. Taipale, S., Kankaala P., Jones R. I., Contributions of different organic carbon sources to Daphnia in the pelagic food web of a small polyhumic lake: Results from mesocosm ¹³C-additions, Ecosystems (N. Y., Print), 2008, doi:10.1007/s10021-007-9056-5.
56. Thauer R.K., Shima S., Methane as fuel for anaerobic microorganisms, Ann N Y Acad Sci., 1125, 2008, 158–170.
57. Timmers P.H., Suarez-Zuluaga D.A., van Rossem M. et al.,  Anaerobic oxidation of methane associated with sulfate reduction in a natural freshwater gas source, ISME J, 10, 2016, 1400–1412.
58. Timmers P.H., Welte C.U., Koehorst J.J., et al., Reverse methanogenesis and respiration in methanotrophic Archaea, Archaea, 2017.
59. Treude T., Knittel K., Blumenberg M., Seifert R., Boetius A., Subsurface microbial methanotrophic mats in the Black Sea, Appl. Environ. Microb., 71(10), 2005,
    6375–6378.
60. Trotsenko Y.A., Murrell J.C., Metabolic aspects of aerobic obligate methanotrophy, Advances in Applied Microbiology, 63, 2008, 183–229.
61. Wankel S.D., Adams M.M., Johnston D.T., Hansel C.M., Joye S.B., Girguis P.R., Anaerobic methane oxidation in metalliferous hydrothermal sediments: influence on carbon flux and decoupling from sulfate reduction, Environ. Microbiol., 14, 2012, 2726–2740.
62. Welte C.U., Nitrate- and nitrite-dependent anaerobic oxidation of methane, Environ. Microbiol. Rep., 8, 2016, 941–955.
63. Zehnder A.J., Brock T.D., Methane formation and methane oxidation by methanogenic bacteria, J Bacteriol., 137(1), 1979, 420–432.