Methane oxidation by anaerobic archaea for conversion to liquid fuels

  • Thomas J. Mueller
  • Matthew J. Grisewood
  • Hadi Nazem-Bokaee
  • Saratram Gopalakrishnan
  • James G. Ferry
  • Thomas K. Wood
  • Costas D. Maranas
Bioenergy/Biofuels/Biochemicals

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.

Keywords

Archaea Anaerobic oxidation of methane Anaerobic methanotrophic archaea ANME 

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 PubMedCrossRefGoogle 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 PubMedCrossRefGoogle 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 CrossRefGoogle Scholar
  5. 5.
    Annual energy outlook2014 (2014). U S Energy Information AdministrationGoogle Scholar
  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 PubMedCrossRefGoogle 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 PubMedCrossRefGoogle 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 CrossRefGoogle 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):441–449PubMedCrossRefGoogle 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 PubMedCentralPubMedCrossRefGoogle Scholar
  11. 11.
    Buffett B, Archer D (2004) Global inventory of methane clathrate: sensitivity to changes in the deep ocean. Earth Planet Sci Lett 227:185–199CrossRefGoogle 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 PubMedCentralPubMedCrossRefGoogle 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 PubMedCentralPubMedCrossRefGoogle 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 PubMedCrossRefGoogle 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 PubMedCrossRefGoogle 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 CrossRefGoogle Scholar
  17. 17.
    Deangelis MA, Lilley MD (1987) Methane in surface waters of oregon estuaries and rivers. Limnol Oceanogr 32(3):716–722CrossRefGoogle 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 PubMedCentralPubMedCrossRefGoogle Scholar
  19. 19.
    Dickens GR (2003) A methane trigger for rapid warming? Science 299Google Scholar
  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]CrossRefGoogle Scholar
  21. 21.
    Dominik U, Kyra P, Schaub G (2010) Fischer-Tropsch synfuels from biomass: maximizing carbon efficiency and hydrocarbon yield. Energy Fuels 24:2634–2641CrossRefGoogle 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 PubMedCrossRefGoogle 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 PubMedCrossRefGoogle 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 PubMedCrossRefGoogle 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 PubMedCrossRefGoogle 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 PubMedCrossRefGoogle 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 PubMedCrossRefGoogle 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 PubMedCrossRefGoogle 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 PubMedCentralPubMedCrossRefGoogle 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 CrossRefGoogle 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 PubMedCrossRefGoogle 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 PubMedCrossRefGoogle 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 PubMedCrossRefGoogle 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):451–463CrossRefGoogle 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 CrossRefGoogle 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 PubMedCentralPubMedCrossRefGoogle Scholar
  37. 37.
    U.S. Energy Information Administration (2013) International Energy StatisticsGoogle Scholar
  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.ch8Google Scholar
  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 PubMedCrossRefGoogle 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 CrossRefGoogle 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 PubMedCrossRefGoogle 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 CrossRefGoogle 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 PubMedCentralPubMedCrossRefGoogle 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 PubMedGoogle 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 PubMedCrossRefGoogle 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 CrossRefGoogle 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 PubMedCentralPubMedCrossRefGoogle 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 PubMedCentralPubMedCrossRefGoogle 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 CrossRefGoogle 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 148:3521–3530Google 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 PubMedCentralPubMedCrossRefGoogle 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 PubMedCrossRefGoogle 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 PubMedCrossRefGoogle 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 PubMedCrossRefGoogle 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 PubMedCentralPubMedCrossRefGoogle 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 PubMedCrossRefGoogle 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):162–173PubMedGoogle 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):303–309PubMedCentralPubMedCrossRefGoogle 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 PubMedCrossRefGoogle 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 PubMedGoogle Scholar
  61. 61.
    U.S. Energy Information Administration (2014) Natural gas exploration and reservesGoogle Scholar
  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):296–305PubMedCrossRefGoogle 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 PubMedCrossRefGoogle 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):1587–1599CrossRefGoogle 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 PubMedCentralPubMedCrossRefGoogle 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 PubMedCrossRefGoogle 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 PubMedCentralPubMedCrossRefGoogle 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 PubMedCrossRefGoogle 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 PubMedCentralPubMedCrossRefGoogle 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 PubMedCrossRefGoogle Scholar
  71. 71.
    Reeburgh WS (2007) Oceanic methane biogeochemistry. Chem Rev 107(2):486–513. doi:10.1021/cr050362v PubMedCrossRefGoogle 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 PubMedCrossRefGoogle 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 CrossRefGoogle 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 PubMedCrossRefGoogle 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 PubMedCrossRefGoogle 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 PubMedCentralPubMedCrossRefGoogle 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 PubMedGoogle 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 PubMedCrossRefGoogle 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 CrossRefGoogle 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 CrossRefGoogle 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 PubMedCrossRefGoogle 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 CrossRefGoogle 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 PubMedCrossRefGoogle 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 CrossRefGoogle 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 AdministrationGoogle Scholar
  86. 86.
    Thauer RK (1998) Biochemistry of methanogenesis: a tribute to marjory stephenson. Microbiol Uk 144:2377–2406CrossRefGoogle 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 PubMedCrossRefGoogle 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.ch24Google Scholar
  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 PubMedCrossRefGoogle 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 PubMedCentralPubMedCrossRefGoogle 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 PubMedCentralPubMedCrossRefGoogle 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 CrossRefGoogle 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 CrossRefGoogle Scholar
  94. 94.
    Valentine DL, Reeburgh WS (2000) New perspectives on anaerobic methane oxidation. Environ Microbiol 2(5):477–484PubMedCrossRefGoogle 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 PubMedCrossRefGoogle Scholar
  96. 96.
    Zehnder AJB, Brock TD (1979) Methane formation and methane oxidation by methanogenic bacteria. J Bacteriol 137(1):420–432PubMedCentralPubMedGoogle Scholar

Copyright information

© Society for Industrial Microbiology and Biotechnology 2014

Authors and Affiliations

  • Thomas J. Mueller
    • 1
  • Matthew J. Grisewood
    • 1
  • Hadi Nazem-Bokaee
    • 1
  • Saratram Gopalakrishnan
    • 1
  • James G. Ferry
    • 2
  • Thomas K. Wood
    • 1
    • 2
  • Costas D. Maranas
    • 1
  1. 1.Department of Chemical EngineeringThe Pennsylvania State UniversityUniversity ParkUSA
  2. 2.Department of Biochemistry and Molecular BiologyThe Pennsylvania State UniversityUniversity ParkUSA

Personalised recommendations