Methane oxidation by anaerobic archaea for conversion to liquid fuels

Abstract

Given the recent increases in natural gas reserves and associated drawbacks of current gas-to-liquids technologies, the development of a bioconversion process to directly convert methane to liquid fuels would generate considerable industrial interest. Several clades of anaerobic methanotrophic archaea (ANME) are capable of performing anaerobic oxidation of methane (AOM). AOM carried out by ANME offers carbon efficiency advantages over aerobic oxidation by conserving the entire carbon flux without losing one out of three carbon atoms to carbon dioxide. This review highlights the recent advances in understanding the key enzymes involved in AOM (i.e., methyl-coenzyme M reductase), the ecological niches of a number of ANME, the putative metabolic pathways for AOM, and the syntrophic consortia that they typically form.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. 1.

    Alberty RA (2001) Standard apparent reduction potentials for biochemical half reactions as a function of pH and ionic strength. Arch Biochem Biophys 389(1):94–109. doi:10.1006/Abbi.2001.2318

    CAS  PubMed  Article  Google Scholar 

  2. 2.

    Allen KD, Wegener G, White RH (2014) Discovery of multiple modified F430 coenzymes in methanogens and anaerobic methanotrophic archaea suggests possible new roles for F430 in Nature. Appl Environ Microbiol. doi:10.1128/AEM.02202-14

    Google Scholar 

  3. 3.

    Alperin M, Hoehler T (2010) Biogeochemistry the ongoing mystery of sea-floor methane. Science 329(5989):288–289. doi:10.1126/Science.1189966

    CAS  PubMed  Article  Google Scholar 

  4. 4.

    Alperin MJ, Hoehler TM (2009) Anaerobic methane oxidation by archaea/sulfate-reducing bacteria aggregates: 1. Thermodynamic and physical constraints. Am J Sci 309(10):869–957. doi:10.2475/10.2009.01

    CAS  Article  Google Scholar 

  5. 5.

    Annual energy outlook2014 (2014). U S Energy Information Administration

  6. 6.

    Beal EJ, House CH, Orphan VJ (2009) Manganese- and iron-dependent marine methane oxidation. Science 325(5937):184–187. doi:10.1126/science.1169984

    CAS  PubMed  Article  Google Scholar 

  7. 7.

    Beasley KK, Nanny MA (2012) Potential energy surface for anaerobic oxidation of methane via fumarate addition. Environ Sci Technol 46(15):8244–8252. doi:10.1021/es3009503

    CAS  PubMed  Article  Google Scholar 

  8. 8.

    Boetius A, Holler T, Knittel K, Felden J, Wenzhofer F (2009) The seabed as natural laboratory: lessons from uncultivated methanotrophs. Microbiol Monogr 10:59–82. doi:10.1007/7171_2008_15

    Article  Google Scholar 

  9. 9.

    Brandstetter H, Whittington DA, Lippard SJ, Frederick CA (1999) Mutational and structural analyses of the regulatory protein B of soluble methane monooxygenase from methylococcus capsulatus (Bath). Chem Biol 6(7):441–449

    CAS  PubMed  Article  Google Scholar 

  10. 10.

    Brazelton WJ, Schrenk MO, Kelley DS, Baross JA (2006) Methane- and sulfur-metabolizing microbial communities dominate the lost city hydrothermal field ecosystem. Appl Environ Microbiol 72(9):6257–6270. doi:10.1128/Aem.0057406

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  11. 11.

    Buffett B, Archer D (2004) Global inventory of methane clathrate: sensitivity to changes in the deep ocean. Earth Planet Sci Lett 227:185–199

    CAS  Article  Google Scholar 

  12. 12.

    Callaghan AV (2013) Enzymes involved in the anaerobic oxidation of n-alkanes: from methane to long-chain paraffins. Front microbiol 4:89. doi:10.3389/fmicb.2013.00089

    PubMed Central  PubMed  Article  Google Scholar 

  13. 13.

    Cedervall PE, Dey M, Li XH, Sarangi R, Hedman B, Ragsdale SW, Wilmot CM (2011) Structural analysis of a Ni-methyl species in methyl-coenzyme M reductase from methanothermobacter marburgensis. J Am Chem Soc 133(15):5626–5628. doi:10.1021/Ja110492p

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  14. 14.

    Chen SL, Blomberg MRA (2012) Siegbahn PEM (2012) How Is methane formed and oxidized reversibly when catalyzed by Ni-containing methyl-coenzyme M reductase? Chem Eur J 18(39):6309–6315. doi:10.1002/Chem.201203134

    CAS  PubMed  Article  Google Scholar 

  15. 15.

    Chen SL, Blomberg MRA, Siegbahn PEM (2014) An investigation of possible competing mechanisms for Ni-containing methyl-coenzyme M reductase. Phys Chem Chem Phys 16(27):14029–14035. doi:10.1039/C4cp01483a

    CAS  PubMed  Article  Google Scholar 

  16. 16.

    Coleman ML, Hedrick DB, Lovley DR, White DC, Pye K (1993) Reduction of Fe(III) in sediments by sulfate-reducing bacteria. Nature 361(6411):436–438. doi:10.1038/361436a0

    CAS  Article  Google Scholar 

  17. 17.

    Deangelis MA, Lilley MD (1987) Methane in surface waters of oregon estuaries and rivers. Limnol Oceanogr 32(3):716–722

    CAS  Article  Google Scholar 

  18. 18.

    Dey M, Kunz RC, Lyons DM, Ragsdale SW (2007) Characterization of alkyl-nickel adducts generated by reaction of methyl-coenzyme M reductase with brominated acids. Biochemistry 46(42):11969–11978. doi:10.1021/Bi700925n

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  19. 19.

    Dickens GR (2003) A methane trigger for rapid warming? Science 299

  20. 20.

    Dimitrov L (2002) Contribution to atmospheric methane by natural seepages on the Bulgarian continental shelf. Cont Shelf Res 22(16):2429–2442 S0278-4343(02)00055-9[Pii]

    Article  Google Scholar 

  21. 21.

    Dominik U, Kyra P, Schaub G (2010) Fischer-Tropsch synfuels from biomass: maximizing carbon efficiency and hydrocarbon yield. Energy Fuels 24:2634–2641

    Article  Google Scholar 

  22. 22.

    Ermler U, Grabarse W, Shima S, Goubeaud M, Thauer RK (1997) Crystal structure of methyl coenzyme M reductase: the key enzyme of biological methane formation. Science 278(5342):1457–1462. doi:10.1126/Science.278.5342.1457

    CAS  PubMed  Article  Google Scholar 

  23. 23.

    Ettwig KF, Butler MK, Le Paslier D, Pelletier E, Mangenot S, Kuypers MM, Schreiber F, Dutilh BE, Zedelius J, de Beer D, Gloerich J, Wessels HJ, van Alen T, Luesken F, Wu ML, van de Pas-Schoonen KT, Op den Camp HJ, Janssen-Megens EM, Francoijs KJ, Stunnenberg H, Weissenbach J, Jetten MS, Strous M (2010) Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature 464(7288):543–548. doi:10.1038/nature08883

    CAS  PubMed  Article  Google Scholar 

  24. 24.

    Ettwig KF, Shima S, van de Pas-Schoonen KT, Kahnt J, Medema MH, op den Camp HJM, Jetten MSM, Strous M (2008) Denitrifying bacteria anaerobically oxidize methane in the absence of Archaea. Environ microbiol 10(11):3164–3173. doi:10.1111/J.1462-2920.2008.01724.X

    CAS  PubMed  Article  Google Scholar 

  25. 25.

    Goenrich M, Duin EC, Mahlert F, Thauer RK (2005) Temperature dependence of methyl-coenzyme M reductase activity and of the formation of the methyl-coenzyme M reductase red2 state induced by coenzyme B. J Biol Inorg Chem 10(4):333–342. doi:10.1007/S00775-005-0636-6

    CAS  PubMed  Article  Google Scholar 

  26. 26.

    Goenrich M, Mahlert F, Duin EC, Bauer C, Jaun B, Thauer RK (2004) Probing the reactivity of Ni in the active site of methyl-coenzyme M reductase with substrate analogues. J Biol Inorg Chem 9(6):691–705. doi:10.1007/S00775-004-0552-1

    CAS  PubMed  Article  Google Scholar 

  27. 27.

    Grabarse W, Mahlert F, Duin EC, Goubeaud M, Shima S, Thauer RK, Lamzin V, Ermler U (2001) On the mechanism of biological methane formation: structural evidence for conformational changes in methyl-coenzyme M reductase upon substrate binding. J Mol Biol 309(1):315–330. doi:10.1006/Jmbi.2001.4647

    CAS  PubMed  Article  Google Scholar 

  28. 28.

    Grabarse WG, Mahlert F, Shima S, Thauer RK, Ermler U (2000) Comparison of three methyl-coenzyme M reductases from phylogenetically distant organisms: unusual amino acid modification, conservation and adaptation. J Mol Biol 303(2):329–344. doi:10.1006/Jmbi.2000.4136

    CAS  PubMed  Article  Google Scholar 

  29. 29.

    Green-Saxena A, Dekas AE, Dalleska NF, Orphan VJ (2014) Nitrate-based niche differentiation by distinct sulfate-reducing bacteria involved in the anaerobic oxidation of methane. ISME J 8(1):150–163. doi:10.1038/ismej.2013.147

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  30. 30.

    Hallam SJ, Girguis PR, Preston CM, Richardson PM, DeLong EF (2003) Identification of methyl coenzyme M reductase A (mcrA) genes associated with methane-oxidizing archaea. Appl Environ Microb 69(9):5483–5491. doi:10.1128/Aem.69.9.5483-5491.2003

    CAS  Article  Google Scholar 

  31. 31.

    Hallam SJ, Putnam N, Preston CM, Detter JC, Rokhsar D, Richardson PM, DeLong EF (2004) Reverse methanogenesis: testing the hypothesis with environmental genomics. Science 305(5689):1457–1462. doi:10.1126/Science.1100025

    CAS  PubMed  Article  Google Scholar 

  32. 32.

    Haroon MF, Hu S, Shi Y, Imelfort M, Keller J, Hugenholtz P, Yuan Z, Tyson GW (2013) Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage. Nature 500(7464):567–570. doi:10.1038/nature12375

    CAS  PubMed  Article  Google Scholar 

  33. 33.

    Haynes CA, Gonzalez R (2014) Rethinking biological activation of methane and conversion to liquid fuels. Nat Chem Biol 10(5):331–339. doi:10.1038/nchembio.1509

    CAS  PubMed  Article  Google Scholar 

  34. 34.

    Hoehler TM, Alperin MJ, Albert DB, Martens CS (1994) Field and laboratory studies of methane oxidation in an anaerobic marine sediment: evidence for a methanogenic-sulfate reducer consortium. Glob Biogeochem Cycles 8(4):451–463

    CAS  Article  Google Scholar 

  35. 35.

    Huo ZX, Hester K, Sloan ED, Miller KT (2003) Methane hydrate nonstoichiometry and phase diagram. AIChE J 49(5):1300–1306. doi:10.1002/Aic.690490521

    CAS  Article  Google Scholar 

  36. 36.

    Inagaki F, Kuypers MMM, Tsunogai U, Ishibashi J, Nakamura K, Treude T, Ohkubo S, Nakaseama M, Gena K, Chiba H, Hirayama H, Nunoura T, Takai K, Jorgensen BB, Horikoshi K, Boetius A (2006) Microbial community in a sediment-hosted CO2 lake of the southern Okinawa trough hydrothermal system. Proc Natl Acad Sci USA 103(38):14164–14169. doi:10.1073/Pnas.0606083103

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  37. 37.

    U.S. Energy Information Administration (2013) International Energy Statistics

  38. 38.

    Jaun B, Thauer RK (2007) Methyl-coenzyme M reductase and its nickel corphin coenzyme F430 in methanogenic archaea. In: nickel and its surprising impact in nature. Wiley pp 323–356. doi:10.1002/9780470028131.ch8

  39. 39.

    Katz ME, Pak DK, Dickens GR, Miller KG (1999) The source and fate of massive carbon input during the latest paleocene thermal maximum. Science 286(5444):1531–1533. doi:10.1126/Science.286.5444.1531

    CAS  PubMed  Article  Google Scholar 

  40. 40.

    Kirschke S, Bousquet P, Ciais P, Saunois M, Canadell JG, Dlugokencky EJ, Bergamaschi P, Bergmann D, Blake DR, Bruhwiler L, Cameron-Smith P, Castaldi S, Chevallier F, Feng L, Fraser A, Heimann M, Hodson EL, Houweling S, Josse B, Fraser PJ, Krummel PB, Lamarque JF, Langenfelds RL, Le Quere C, Naik V, O’Doherty S, Palmer PI, Pison I, Plummer D, Poulter B, Prinn RG, Rigby M, Ringeval B, Santini M, Schmidt M, Shindell DT, Simpson IJ, Spahni R, Steele LP, Strode SA, Sudo K, Szopa S, van der Werf GR, Voulgarakis A, van Weele M, Weiss RF, Williams JE, Zeng G (2013) Three decades of global methane sources and sinks. Nat Geosci 6(10):813–823. doi:10.1038/Ngeo1955

    CAS  Article  Google Scholar 

  41. 41.

    Knittel K, Boetius A (2009) Anaerobic oxidation of methane: progress with an unknown process. Annu Rev Microbiol 63:311–334. doi:10.1146/annurev.micro.61.080706.093130

    CAS  PubMed  Article  Google Scholar 

  42. 42.

    Knittel K, Boetius A, Lemke A, Eilers H, Lochte K, Pfannkuche O, Linke P, Amann R (2003) Activity, distribution, and diversity of sulfate reducers and other bacteria in sediments above gas hydrate (Cascadia margin, Oregon). Geomicrobiol J 20(4):269–294. doi:10.1080/01490450303896

    CAS  Article  Google Scholar 

  43. 43.

    Knittel K, Losekann T, Boetius A, Kort R, Amann R (2005) Diversity and distribution of methanotrophic archaea at cold seeps. Appl Environ Microbiol 71(1):467–479. doi:10.1128/Aem.71.1.467-479.2005

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  44. 44.

    Kojima H, Moll J, Kahnt J, Fukui M, Shima S (2014) A reversed genetic approach reveals the coenzyme specificity and other catalytic properties of three enzymes putatively involved in anaerobic oxidation of methane with sulfate. Environ Microbiol. doi:10.1111/1462-2920.12475

    PubMed  Google Scholar 

  45. 45.

    Kruger M, Meyerdierks A, Glockner FO, Amann R, Widdel F, Kube M, Reinhardt R, Kahnt J, Bocher R, Thauer RK, Shima S (2003) A conspicuous nickel protein in microbial mats that oxidize methane anaerobically. Nature 426(6968):878–881. doi:10.1038/nature02207

    PubMed  Article  Google Scholar 

  46. 46.

    Kruger M, Treude T, Wolters H, Nauhaus K, Boetius A (2005) Microbial methane turnover in different marine habitats. Palaeogeogr Palaeocl 227(1–3):6–17. doi:10.1016/J.Palaeo.04.031

    Article  Google Scholar 

  47. 47.

    Li XH, Telser J, Kunz RC, Hoffman BM, Gerfen G, Ragsdale SW (2010) Observation of organometallic and radical intermediates formed during the reaction of methyl-coenzyme M reductase with bromoethanesulfonate. Biochemistry 49(32):6866–6876. doi:10.1021/Bi100650m

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  48. 48.

    Lloyd KG, Lapham L, Teske A (2006) An anaerobic methane-oxidizing community of ANME-1b archaea in hypersaline Gulf of Mexico sediments. Appl Environ Microbiol 72(11):7218–7230. doi:10.1128/AEM.00886-06

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  49. 49.

    Losekann T, Knittel K, Nadalig T, Fuchs B, Niemann H, Boetius A, Amann R (2007) Diversity and abundance of aerobic and anaerobic methane oxidizers at the Haakon Mosby Mud Volcano. Barents Sea Appl Environ Microbiol 73(10):3348–3362. doi:10.1128/AEM.00016-07

    Article  Google Scholar 

  50. 50.

    Luton PE, Wayne JM, Sharp RJ, Riley PW (2002) The mcrA gene as an alternative to 16S rRNA in the phylogenetic analysis of methanogen populations in landfill. Microbiol Sgm 148:3521–3530

    CAS  Google Scholar 

  51. 51.

    Martinho M, Choi DW, Dispirito AA, Antholine WE, Semrau JD, Munck E (2007) Mossbauer studies of the membrane-associated methane monooxygenase from methylococcus capsulatus bath: evidence for a diiron center. J Am Chem Soc 129(51):15783–15785. doi:10.1021/ja077682b

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  52. 52.

    Mayr S, Latkoczy C, Kruger M, Gunther D, Shima S, Thauer RK, Widdel F, Jaun B (2008) Structure of an F430 variant from archaea associated with anaerobic oxidation of methane. J Am Chem Soc 130(32):10758–10767. doi:10.1021/Ja802929z

    CAS  PubMed  Article  Google Scholar 

  53. 53.

    Meyerdierks A, Kube M, Kostadinov I, Teeling H, Glockner FO, Reinhardt R, Amann R (2010) Metagenome and mRNA expression analyses of anaerobic methanotrophic archaea of the ANME-1 group. Environ Microbiol 12(2):422–439. doi:10.1111/j.1462-2920.2009.02083.x

    CAS  PubMed  Article  Google Scholar 

  54. 54.

    Michaelis W, Seifert R, Nauhaus K, Treude T, Thiel V, Blumenberg M, Knittel K, Gieseke A, Peterknecht K, Pape T, Boetius A, Amann R, Jorgensen BB, Widdel F, Peckmann J, Pimenov NV, Gulin MB (2002) Microbial reefs in the Black Sea fueled by anaerobic oxidation of methane. Science 297(5583):1013–1015. doi:10.1126/science.1072502

    CAS  PubMed  Article  Google Scholar 

  55. 55.

    Mills HJ, Martinez RJ, Story S, Sobecky PA (2005) Characterization of microbial community structure in Gulf of Mexico gas hydrates: comparative analysis of DNA- and RNA-derived clone libraries. Appl Environ Microbiol 71(6):3235–3247. doi:10.1128/AEM.71.6.3235-3247.2005

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  56. 56.

    Milucka J, Ferdelman TG, Polerecky L, Franzke D, Wegener G, Schmid M, Lieberwirth I, Wagner M, Widdel F, Kuypers MM (2012) Zero-valent sulphur is a key intermediate in marine methane oxidation. Nature 491(7425):541–546. doi:10.1038/nature11656

    CAS  PubMed  Article  Google Scholar 

  57. 57.

    Moran JJ, Beal EJ, Vrentas JM, Orphan VJ, Freeman KH, House CH (2008) Methyl sulfides as intermediates in the anaerobic oxidation of methane. Environ Microbiol 10(1):162–173

    CAS  PubMed  Google Scholar 

  58. 58.

    Moran JJ, House CH, Freeman KH, Ferry JG (2005) Trace methane oxidation studied in several euryarchaeota under diverse conditions. Archaea 1(5):303–309

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  59. 59.

    Murrell JC, Gilbert B, McDonald IR (2000) Molecular biology and regulation of methane monooxygenase. Arch Microbiol 173(5–6):325–332. doi:10.1007/S002030000158

    CAS  PubMed  Article  Google Scholar 

  60. 60.

    Muyzer G, Stams AJM (2008) The ecology and biotechnology of sulphate-reducing bacteria. Nat Rev Microbiol 6(6):441–454. doi:10.1038/Nrmicro1892

    CAS  PubMed  Google Scholar 

  61. 61.

    U.S. Energy Information Administration (2014) Natural gas exploration and reserves

  62. 62.

    Nauhaus K, Boetius A, Kruger M, Widdel F (2002) In vitro demonstration of anaerobic oxidation of methane coupled to sulphate reduction in sediment from a marine gas hydrate area. Environ Microbiol 4(5):296–305

    CAS  PubMed  Article  Google Scholar 

  63. 63.

    Nauhaus K, Treude T, Boetius A, Kruger M (2005) Environmental regulation of the anaerobic oxidation of methane: a comparison of ANME-I and ANME-II communities. Environ Microbiol 7(1):98–106. doi:10.1111/j.1462-2920.2004.00669.x

    CAS  PubMed  Article  Google Scholar 

  64. 64.

    Orcutt B, Meile C (2008) Constraints on mechanisms and rates of anaerobic oxidation of methane by microbial consortia: process-based modeling of ANME-2 archaea and sulfate reducing bacteria interactions. Biogeosciences 5(6):1587–1599

    CAS  Article  Google Scholar 

  65. 65.

    Orphan VJ, Hinrichs KU, Ussler W 3rd, Paull CK, Taylor LT, Sylva SP, Hayes JM, Delong EF (2001) Comparative analysis of methane-oxidizing archaea and sulfate-reducing bacteria in anoxic marine sediments. Appl Environ Microbiol 67(4):1922–1934. doi:10.1128/AEM.67.4.1922-1934.2001

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  66. 66.

    Orphan VJ, House CH, Hinrichs KU, McKeegan KD, DeLong EF (2001) Methane-consuming archaea revealed by directly coupled isotopic and phylogenetic analysis. Science 293(5529):484–487. doi:10.1126/science.1061338

    CAS  PubMed  Article  Google Scholar 

  67. 67.

    Orphan VJ, House CH, Hinrichs KU, McKeegan KD, DeLong EF (2002) Multiple archaeal groups mediate methane oxidation in anoxic cold seep sediments. Proc Natl Acad Sci USA 99(11):7663–7668. doi:10.1073/pnas.072210299

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  68. 68.

    Pelmenschikov V, Siegbahn PEM (2003) Catalysis by methyl-coenzyme M reductase: a theoretical study for heterodisulfide product formation. J Biol Inorg Chem 8(6):653–662. doi:10.1007/S00775-003-0461-8

    CAS  PubMed  Article  Google Scholar 

  69. 69.

    Pernthaler A, Dekas AE, Brown CT, Goffredi SK, Embaye T, Orphan VJ (2008) Diverse syntrophic partnerships from-deep-sea methane vents revealed by direct cell capture and metagenomics. Proc Natl Acad Sci USA 105(19):7052–7057. doi:10.1073/Pnas.0711303105

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  70. 70.

    Raghoebarsing AA, Pol A, van de Pas-Schoonen KT, Smolders AJP, Ettwig KF, Rijpstra WIC, Schouten S, Damste JSS, Op den Camp HJM, Jetten MSM, Strous M (2006) A microbial consortium couples anaerobic methane oxidation to denitrification. Nature 440(7086):918–921. doi:10.1038/Nature04617

    CAS  PubMed  Article  Google Scholar 

  71. 71.

    Reeburgh WS (2007) Oceanic methane biogeochemistry. Chem Rev 107(2):486–513. doi:10.1021/cr050362v

    CAS  PubMed  Article  Google Scholar 

  72. 72.

    Reguera G, McCarthy KD, Mehta T, Nicoll JS, Tuominen MT, Lovley DR (2005) Extracellular electron transfer via microbial nanowires. Nature 435(7045):1098–1101. doi:10.1038/Nature03661

    CAS  PubMed  Article  Google Scholar 

  73. 73.

    Reitner J, Peckmann J, Blumenberg M, Michaelis W, Reimer A, Thiel V (2005) Concretionary methane-seep carbonates and associated microbial communities in Black Sea sediments. Palaeogeogr Palaeocl 227(1–3):18–30. doi:10.1016/J.Palaeo.04.033

    Article  Google Scholar 

  74. 74.

    Scheller S, Goenrich M, Boecher R, Thauer RK, Jaun B (2010) The key nickel enzyme of methanogenesis catalyses the anaerobic oxidation of methane. Nature 465(7298):606–608. doi:10.1038/nature09015

    CAS  PubMed  Article  Google Scholar 

  75. 75.

    Scheller S, Goenrich M, Thauer RK, Jaun B (2013) Methyl-coenzyme M reductase from methanogenic archaea: isotope effects on the formation and anaerobic oxidation of methane. J Am Chem Soc 135(40):14975–14984. doi:10.1021/Ja406485z

    CAS  PubMed  Article  Google Scholar 

  76. 76.

    Schouten S, Wakeham SG, Hopmans EC, Damste JSS (2003) Biogeochemical evidence that thermophilic archaea mediate the anaerobic oxidation of methane. Appl Environ Microbiol 69(3):1680–1686. doi:10.1128/Aem.69.3.1680-1686.2003

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  77. 77.

    Schreiber L, Holler T, Knittel K, Meyerdierks A, Amann R (2010) Identification of the dominant sulfate-reducing bacterial partner of anaerobic methanotrophs of the ANME-2 clade. Environ Microbiol 12(8):2327–2340. doi:10.1111/J.1462-2920.2010.02275.X

    CAS  PubMed  Google Scholar 

  78. 78.

    Schubert CJ, Coolen MJ, Neretin LN, Schippers A, Abbas B, Durisch-Kaiser E, Wehrli B, Hopmans EC, Damste JS, Wakeham S, Kuypers MM (2006) Aerobic and anaerobic methanotrophs in the Black Sea water column. Environ Microbiol 8(10):1844–1856. doi:10.1111/j.1462-2920.2006.01079.x

    CAS  PubMed  Article  Google Scholar 

  79. 79.

    Scranton MI, Mcshane K (1991) Methane fluxes in the Southern north-sea—the role of European rivers. Cont Shelf Res 11(1):37–52. doi:10.1016/0278-4343(91)90033-3

    Article  Google Scholar 

  80. 80.

    Shima S, Krueger M, Weinert T, Demmer U, Kahnt J, Thauer RK, Ermler U (2012) Structure of a methyl-coenzyme M reductase from Black Sea mats that oxidize methane anaerobically. Nature 481(7379):98–101. doi:10.1038/nature10663

    CAS  Article  Google Scholar 

  81. 81.

    Shima S, Thauer RK (2005) Methyl-coenzyme M reductase and the anaerobic oxidation of methane in methanotrophic archaea. Curr Opin Microbiol 8(6):643–648. doi:10.1016/J.Mib.10.002

    CAS  PubMed  Article  Google Scholar 

  82. 82.

    Sivan O, Schrag DP, Murray RW (2007) Rates of methanogenesis and methanotrophy in deep-sea sediments. Geobiology 5(2):141–151. doi:10.1111/J.1472-4669.2007.00098.X

    CAS  Article  Google Scholar 

  83. 83.

    Stams AJM, de Bok FAM, Plugge CM, van Eekert MHA, Dolfing J, Schraa G (2006) Exocellular electron transfer in anaerobic microbial communities. Environ Microbiol 8(3):371–382. doi:10.1111/J.1462-2920.2006.00989.X

    CAS  PubMed  Article  Google Scholar 

  84. 84.

    Tebo BM, Obraztsova AY (1998) Sulfate-reducing bacterium grows with Cr(VI), U(VI), Mn(IV), and Fe(III) as electron acceptors. FEMS Microbiol Lett 162(1):193–198. doi:10.1111/J.1574-6968.1998.Tb12998.X

    CAS  Article  Google Scholar 

  85. 85.

    Technically recoverable shale oil and shale gas resources: an assessment of 137 shale formations in 41 countries outside the United States (2013). US Energy Information Administration

  86. 86.

    Thauer RK (1998) Biochemistry of methanogenesis: a tribute to marjory stephenson. Microbiol Uk 144:2377–2406

    CAS  Article  Google Scholar 

  87. 87.

    Thauer RK (2011) Anaerobic oxidation of methane with sulfate: on the reversibility of the reactions that are catalyzed by enzymes also involved in methanogenesis from CO2. Curr Opin Microbiol 14(3):292–299. doi:10.1016/j.mib.2011.03.003

    CAS  PubMed  Article  Google Scholar 

  88. 88.

    Thauer RK, Shima S (2006) Methyl-coenzyme M reductase in methanogens and methanotrophs. In: archaea. Blackwell pp 275–283. doi:10.1002/9780470750865.ch24

  89. 89.

    Thauer RK, Shima S (2008) Methane as fuel for anaerobic microorganisms. Ann N Y Acad Sci 1125:158–170. doi:10.1196/annals.1419.000

    CAS  PubMed  Article  Google Scholar 

  90. 90.

    Treude T, Knittel K, Blumenberg M, Seifert R, Boetius A (2005) Subsurface microbial methanotrophic mats in the Black Sea. Appl Environ Microbiol 71(10):6375–6378. doi:10.1128/AEM.71.10.6375-6378.2005

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  91. 91.

    Treude T, Orphan V, Knittel K, Gieseke A, House CH, Boetius A (2007) Consumption of methane and CO2 by methanotrophic microbial mats from gas seeps of the anoxic Black Sea. Appl Environ Microbiol 73(7):2271–2283. doi:10.1128/AEM.02685-06

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  92. 92.

    Tryon MD, Brown KM, Torres ME (2002) Fluid and chemical flux in and out of sediments hosting methane hydrate deposits on Hydrate Ridge, OR, II: hydrological processes. Earth Planet Sci Lett 201(3–4):541–557. doi:10.1016/s0012-821x(02)00732-x

    CAS  Article  Google Scholar 

  93. 93.

    Valentine DL (2002) Biogeochemistry and microbial ecology of methane oxidation in anoxic environments: a review. Anton Leeuw Int J G 81(1–4):271–282. doi:10.1023/A:1020587206351

    CAS  Article  Google Scholar 

  94. 94.

    Valentine DL, Reeburgh WS (2000) New perspectives on anaerobic methane oxidation. Environ Microbiol 2(5):477–484

    CAS  PubMed  Article  Google Scholar 

  95. 95.

    Wang FP, Zhang Y, Chen Y, He Y, Qi J, Hinrichs KU, Zhang XX, Xiao X, Boon N (2014) Methanotrophic archaea possessing diverging methane-oxidizing and electron-transporting pathways. ISME J 8(5):1069–1078. doi:10.1038/Ismej.2013.212

    CAS  PubMed  Article  Google Scholar 

  96. 96.

    Zehnder AJB, Brock TD (1979) Methane formation and methane oxidation by methanogenic bacteria. J Bacteriol 137(1):420–432

    CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

Supported by funding from The Advanced Research Projects Agnecy-Energy (ARPA-E), U S Department of Energy to Drs. Costas D. Maranas, Thomas K. Wood, and James G. Ferry, grant DE-AR0000431.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Costas D. Maranas.

Additional information

Special Issue: Metabolic Engineering.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Mueller, T.J., Grisewood, M.J., Nazem-Bokaee, H. et al. Methane oxidation by anaerobic archaea for conversion to liquid fuels. J Ind Microbiol Biotechnol 42, 391–401 (2015). https://doi.org/10.1007/s10295-014-1548-7

Download citation

Keywords

  • Archaea
  • Anaerobic oxidation of methane
  • Anaerobic methanotrophic archaea
  • ANME