Skip to main content

Life Close to the Thermodynamic Limit: How Methanogenic Archaea Conserve Energy

  • Chapter
  • First Online:
Book cover Bioenergetics

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 45))

Abstract

Methane-forming archaea are strictly anaerobic, ancient microbes that are widespread in nature. These organisms are commonly found in anaerobic environments such as rumen, anaerobic sediments of rivers and lakes, hyperthermal deep sea vents and even hypersaline environments. From an evolutionary standpoint they are close to the origin of life. Common to all methanogens is the biological production of methane by a unique pathway currently only found in archaea. Methanogens can grow on only a limited number of substrates such as H2 + CO2, formate, methanol and other methyl group-containing substrates and some on acetate. The free energy change associated with methanogenesis from these compounds allows for the synthesis of 1 (acetate) to a maximum of only 2 mol of ATP under standard conditions while under environmental conditions less than one ATP can be synthesized. Therefore, methanogens live close to the thermodynamic limit. To cope with this problem, they have evolved elaborate mechanisms of energy conservation using both protons and sodium ions as the coupling ion in one pathway. These energy conserving mechanisms are comprised of unique enzymes, cofactors and electron carriers present only in methanogens. This review will summarize the current knowledge of energy conservation of methanogens and focus on recent insights into structure and function of ion translocating enzymes found in these organisms.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Abbott IA, Hollenberg GJ (1976) Marine algae of california. Stanford Univ Press, Stanford, CA, USA

    Google Scholar 

  • Abken HJ, Deppenmeier U (1997) Purification and properties of an F420H2 dehydrogenase from Methanosarcina mazei Gö1. FEMS Microbiol Lett 154:231–237

    CAS  Google Scholar 

  • Abken HJ, Tietze M, Brodersen J, Bäumer S, Beifuss U, Deppenmeier U (1998) Isolation and characterization of methanophenazine and the function of phenazines in membrane-bound electron transport of Methanosarcina mazei Gö1. J Bacteriol 180:2027–2032

    PubMed  CAS  Google Scholar 

  • Bäumer S, Murakami E, Brodersen J, Gottschalk G, Ragsdale SW, Deppenmeier U (1998) The F420H2:heterodisulfide oxidoreductase system from Methanosarcina species. FEBS Lett 428:295–298

    Article  PubMed  Google Scholar 

  • Bäumer S, Ide T, Jacobi C, Johann A, Gottschalk G, Deppenmeier U (2000) The F420H2 dehydrogenase from Methanosarcina mazei Gö1 is a redox-driven proton pump closely related to NADH dehydrogenases. J Biol Chem 275:17968–17973

    Article  PubMed  Google Scholar 

  • Becher B, Müller V (1994) ∆μNa+ drives the synthesis of ATP via an ∆μNa+-translocating F1FO-ATP synthase in membrane vesicles of the archaeon Methanosarcina mazei Gö1. J Bacteriol 176:2543–2550

    PubMed  CAS  Google Scholar 

  • Beifuss U, Tietze M, Bäumer S, Deppenmeier U (2000) Methanophenazine: Structure, total synthesis, and function of a new cofactor from methanogenic archaea. Angew Chem Int Ed 39:2470–2472

    Article  CAS  Google Scholar 

  • Beifuss U, Tietze M (2005) Methanophenazine and other natural biologically active phenazines. Top Curr Chem 244:77–113

    CAS  Google Scholar 

  • Bernhard M, Benelli B, Hochkoeppler A, Zannoni D, Friedrich B (1997) Functional and structural role of the cytochrome b subunit of the membrane-bound hydrogenase complex of Alcaligenes eutrophus H16. Eur J Biochem 248:179–186

    Article  PubMed  CAS  Google Scholar 

  • Boone DR, Whitman WB, Rouviere PE (1993) Diversity and taxonomy of methanogens. In: Ferry JG (ed) Methanogenesis. Chapman & Hall, New York, pp 35–80

    Google Scholar 

  • Brandt U, Kerscher S, Drose S, Zwicker K, Zickermann V (2003) Proton pumping by NADH:ubiquinone oxidoreductase. A redox driven conformational change mechanism? FEBS Lett 545:9–17

    Article  PubMed  CAS  Google Scholar 

  • Breas O, Guillou C, Reniero F, Wada E (2002) The global methane cycle: Isotopes and mixing ratios, sources and sinks. Isot Environ Healt S 37:257–379

    Article  Google Scholar 

  • Brooks JM, Bryant WR, Bernard BB, Cameron NR (2000) The nature of gas hydrates on the Nigerian continental slope Gas hydrates. In: Challenges for the future. Ann NY Acad Sci 912:76–93

    Article  CAS  Google Scholar 

  • Coskun Ü, Grüber G, Koch MH, Godovac-Zimmermann J, Lemker T, Müller V (2002) Crosstalk in the A1-ATPase from Methanosarcina mazei Gö1 due to nucleotide-binding. J Biol Chem 277:17327–17333

    Article  PubMed  CAS  Google Scholar 

  • Coskun Ü, Chaban YL, Lingl A, Müller V, Keegstra W, Boekema EJ, Grüber G (2004a) Structure and subunit arrangement of the A-type ATP synthase complex from the archaeon Methanococcus jannaschii visualized by electron microscopy. J Biol Chem 279:38644–38648

    Article  PubMed  CAS  Google Scholar 

  • Coskun Ü, Radermacher M, Müller V, Ruiz T, Grüber G (2004b) Three-dimensional organization of the archaeal A1-ATPase from Methanosarcina mazei Gö1. J Biol Chem 279:22759–22764

    Article  PubMed  CAS  Google Scholar 

  • Deppenmeier U, Blaut M, Mahlmann A, Gottschalk G (1990) Reduced coenzyme F420H2-dependent heterodisulfide oxidoreductase: a proton-translocating redox system in methanogenic bacteria. Proc Natl Acad Sci USA 87:9449–9453

    Article  PubMed  CAS  Google Scholar 

  • Deppenmeier U, Blaut M, Gottschalk G (1991) H2 : heterodisulfide oxidoreductase, a second energy-conserving system in the methanogenic strain Gö1. Arch Microbiol 155:272–277

    Article  CAS  Google Scholar 

  • Deppenmeier U, Blaut M, Schmidt B, Gottschalk G (1992) Purification and properties of a F420-nonreactive membrane-bound hydrogenase from Methanosarcina strain Gö1. Arch Microbiol 157:505–511

    PubMed  CAS  Google Scholar 

  • Deppenmeier U, Blaut M, Lentes S, Herzberg C, Gottschalk G (1995) Analysis of the vhoGAC and vhtGAC operons from Methanosarcina mazei strain Gö1, both encoding a membrane-bound hydrogenase and a cytochrome b. Eur J Biochem 227:261–269

    Article  PubMed  CAS  Google Scholar 

  • Deppenmeier U, Lienard T, Gottschalk G (1999) Novel reactions involved in energy conservation by methanogenic archaea. FEBS Lett 457:291–297

    Article  PubMed  CAS  Google Scholar 

  • Deppenmeier U, Johann A, Hartsch T, Merkl R, Schmitz RA, Martinez-Arias R, Henne A, Wiezer A, Bäumer S, Jacobi C, Bruggemann H, Lienard T, Christmann A, Bomeke M, Steckel S, Bhattacharyya A, Lykidis A, Overbeek R, Klenk HP, Gunsalus RP, Fritz HJ, Gottschalk G (2002) The genome of Methanosarcina mazei: Evidence for lateral gene transfer between bacteria and archaea. J Mol Microbiol Biotechnol 4:453–461

    PubMed  CAS  Google Scholar 

  • Deppenmeier U (2002a) The unique biochemistry of methanogenesis. Prog Nucl Acid Res Mol Biol 71:223–283

    CAS  Google Scholar 

  • Deppenmeier U (2002b) Redox-driven proton translocation in methanogenic Archaea. Cell Mol Life Sci 59:1–21

    Google Scholar 

  • Deppenmeier U (2004) The membrane-bound electron transport system of Methano- sarcina species. J Bioenerg Biomembr 36:55–64

    Article  PubMed  CAS  Google Scholar 

  • Drennan CL, Doukov TI, Ragsdale SW (2004) The metalloclusters of carbon monoxide dehydrogenase/acetyl-CoA synthase: a story in pictures. J Biol Inorg Chem 9:511–515

    Article  PubMed  CAS  Google Scholar 

  • Ermler U (2005) On the mechanism of methyl-coenzyme M reductase. Dalton Trans 21:3451–3458

    Article  PubMed  CAS  Google Scholar 

  • Ferry JG (1997) Enzymology of the fermentation of acetate to methane by Methanosarcina thermophila. Biofactors 6:25–35

    PubMed  CAS  Google Scholar 

  • Fischer R, Gärtner P, Yeliseev A, Thauer RK (1992) N5-methyltetrahydromethanopterin:co- enzyme M methyltransferase in methanogenic archaebacteria is a membrane protein. Arch Microbiol 158:208–217

    Article  PubMed  CAS  Google Scholar 

  • Fox JD, Kerby RL, Roberts GP, Ludden PW (1996) Characterization of the CO-induced, CO-tolerant hydrogenase from Rhodospirillum rubrum and the gene encoding the large subunit of the enzyme. J Bacteriol 178:1515–1524

    PubMed  CAS  Google Scholar 

  • Friedrich T, Scheide D (2000) The respiratory complex I of bacteria, archaea and eukarya and its module common with membrane-bound multisubunit hydrogenases. FEBS Lett 479:1–5

    Article  PubMed  CAS  Google Scholar 

  • Friedrich T, Stolpe S, Schneider D, Barquera B, Hellwig P (2005) Ion translocation by the Escherichia coli NADH:ubiquinone oxidoreductase (complex I). Biochem Soc Trans 33:836–839

    Article  PubMed  CAS  Google Scholar 

  • Galagan JE, Nusbaum C, Roy A, Endrizzi MG, Macdonald P, FitzHugh W, Calvo S, Engels R, Smirnov S, Atnoor D, Brown A, Allen N, Naylor J, Stange-Thomann N, DeArellano K, Johnson R, Linton L, McEwan P, McKernan K, Talamas J, Tirrell A, Ye WJ, Zimmer A, Barber RD, Cann I, Graham DE, Grahame DA, Guss AM, Hedderich R, Ingram-Smith C, Kuettner HC, Krzycki JA, Leigh JA, Li WX, Liu JF, Mukhopadhyay B, Reeve JN, Smith K, Springer TA, Umayam LA, White O, White RH, de Macario EC, Ferry JG, Jarrell KF, Jing H, Macario AJL, Paulsen I, Pritchett M, Sowers KR, Swanson RV, Zinder SH, Lander E, Metcalf WW, Birren B (2002) The genome of Methanosarcina acetivorans reveals extensive metabolic and physiological diversity. Genome Res 12:532–542

    Article  PubMed  CAS  Google Scholar 

  • Garcia JL, Patel BKC, Ollivier B (2000) Taxonomy, phylogenetic, and ecological diversity of methanogenic Archaea. Anaerobe 6:205–226

    Article  PubMed  CAS  Google Scholar 

  • Gärtner P, Ecker A, Fischer R, Linder D, Fuchs G, Thauer RK (1993) Purification and properties of N5-methyltetrahydromethanopterin:coenzyme M methyltransferase from Methanobacterium thermoautotrophicum. Eur J Biochem 213:537–545

    Article  PubMed  Google Scholar 

  • Gärtner P, Weiss DS, Harms U, Thauer RK (1994) N5-methyltetrahydromethanopterin:co- enzyme M methyltransferase from Methanobacterium thermoautotrophicum—catalytic mechanism and sodium ion dependence. Eur J Biochem 226:465–472

    Article  PubMed  Google Scholar 

  • Gottschalk G, Thauer RK (2001) The Na+-translocating methyltransferase complex from methanogenic archaea. Biochim Biophys Acta 1505:28–36

    Article  PubMed  CAS  Google Scholar 

  • Grüber G, Svergun DI, Coskun Ü, Lemker T, Koch MH, Schägger H, Müller V (2001) Structural insights into the A1 ATPase from the archaeon, Methanosarcina mazei Gö1. Biochemistry 40:1890–1896

    Article  PubMed  CAS  Google Scholar 

  • Haase P, Deppenmeier U, Blaut M, Gottschalk G (1992) Purification and characterization of F420H2-dehydrogenase from Methanolobus tindarius. Eur J Biochem 203:527–531

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Harms U, Weiss DS, Gärtner P, Linder D, Thauer RK (1995) The energy conserving N5-methyltetrahydromethanopterin:coenzyme M methyltransferase complex from Methanobacterium thermoautotrophicum is composed of eight different subunits. Eur J Biochem 228:640–648

    Article  PubMed  CAS  Google Scholar 

  • Harms U, Thauer RK (1996) Methylcobalamin:coenzyme M methyltransferase isoenzymes MtaA and MtbA from Methanosarcina barkeri—Cloning, sequencing and differential transcription of the encoding genes, and functional overexpression of the mtaA gene in Escherichia coli. Eur J Biochem 235:653–659

    Article  PubMed  CAS  Google Scholar 

  • Hedderich R, Berkessel A, Thauer RK (1990) Purification and properties of heterodisulfide reductase from Methanobacterium thermoautotrophicum (strain Marburg). Eur J Biochem 193:255–261

    Article  PubMed  CAS  Google Scholar 

  • Hedderich R, Koch J, Linder D, Thauer RK (1994) The heterodisulfide reductase from Methanobacterium thermoautotrophicum contains sequence motifs characteristic of pyridine nucleotide-dependent thioredoxin reductases. Eur J Biochem 225:253–261

    Article  PubMed  CAS  Google Scholar 

  • Hedderich R, Klimmek O, Kröger A, Dirmeier R, Keller M, Stetter KO (1998) Anaerobic respiration with elemental sulfur and with disulfides. FEMS Microbiol Rev 22:353–381

    Article  CAS  Google Scholar 

  • Hedderich R (2004) Energy-converting [NiFe] hydrogenases from archaea and extremophiles: ancestors of complex I. J Bioenerg Biomembr 36:65–75

    Article  PubMed  CAS  Google Scholar 

  • Hedderich R, Hamann N, Bennati M (2005) Heterodisulfide reductase from methanogenic archaea: a new catalytic role for an iron-sulfur cluster. Biol Chem 386:961–970

    Article  PubMed  CAS  Google Scholar 

  • Hedderich R, Forzi L (2005) Energy-converting [NiFe] hydrogenases: more than just H2 activation. J Mol Microbiol Biotechnol 10:92–104

    Article  PubMed  CAS  Google Scholar 

  • Heiden S, Hedderich R, Setzke E, Thauer RK (1994) Purification of a two-subunit cytochrome b-containing heterodisulfide reductase from methanol-grown Methano- sarcina barkeri. Eur J Biochem 221:855–861

    Article  PubMed  CAS  Google Scholar 

  • Hendrickson EL, Kaul R, Zhou Y, Bovee D, Chapman P, Chung J, de Macario EC, Dodsworth JA, Gillett W, Graham DE, Hackett M, Haydock AK, Kang A, Land ML, Levy R, Lie TJ, Major TA, Moore BC, Porat I, Palmeiri A, Rouse G, Saenphimmachak C, Soll D, Van Dien S, Wang T, Whitman WB, Xia Q, Zhang Y, Larimer FW, Olson MV, Leigh JA (2004) Complete genome sequence of the genetically tractable hydrogenotrophic methanogen Methanococcus maripaludis. J Bacteriol 186:6956–6969

    Article  PubMed  CAS  Google Scholar 

  • Hughes PE, Tove SB (1982) Occurrence of alpha-tocopherolquinone and alpha-tocopherolquinol in microorganisms. J Bacteriol 151:1397–1402

    PubMed  CAS  Google Scholar 

  • Ide T, Bäumer S, Deppenmeier U (1999) Energy conservation by the H2:heterodisulfide oxidoreductase from Methanosarcina mazei Gö1: identification of two proton-translocating segments. J Bacteriol 181:4076–4080

    PubMed  CAS  Google Scholar 

  • Jouanneau Y, Jeong HS, Hugo N, Meyer C, Willison JC (1998) Overexpression in Escherichia coli of the rnf genes from Rhodobacter capsulatus – characterization of two membrane-bound iron-sulfur proteins. Eur J Biochem 251:54–64

    Article  PubMed  CAS  Google Scholar 

  • Kaesler B, Schönheit P (1989) The role of sodium ions in methanogenesis. Formaldehyde oxidation to CO2 and 2 H2 in methanogenic bacteria is coupled with primary electrogenic Na+ translocation at a stoichiometry of 2–3 Na+/CO2. Eur J Biochem 184:223–232

    Article  PubMed  CAS  Google Scholar 

  • Kashyap DR, Dadhich KS, Sharma SK (2003) Biomethanation under psychrophilic conditions: a review. Bioresour Technol 87:147–153

    Article  PubMed  CAS  Google Scholar 

  • Kemner JM, Zeikus JG (1994) Purification and characterization of membrane-bound hydrogenase from Methanosarcina barkeri MS. Arch Microbiol 161:47–54

    Article  CAS  Google Scholar 

  • Khalil MAK, Rasmussen RA (1994) Global emission of methane during the last several centuries. Chemosphere 29:833–842

    Article  CAS  Google Scholar 

  • Krzycki JA (2004) Function of genetically encoded pyrrolysine in corrinoid-dependent methylamine methyltransferases. Curr Opin Chem Biol 8:484–491

    Article  PubMed  CAS  Google Scholar 

  • Krzycki JA (2005) The direct genetic encoding of pyrrolysine. Curr Opin Microbiol 8:706–712

    PubMed  CAS  Google Scholar 

  • Kumagai H, Fujiwara T, Matsubara H, Saeki K (1997) Membrane localization, topology, and mutual stabilization of the rnfABC gene products in Rhodobacter capsulatus and implications for a new family of energy coupling NADH oxidoreductases. Biochemistry 36:5509–5521

    Article  PubMed  CAS  Google Scholar 

  • Künkel A, Vaupel M, Heim S, Thauer RK, Hedderich R (1997) Heterodisulfide reductase from methanol-grown cells of Methanosarcina barkeri is not a flavoenzyme. Eur J Biochem 244:226–234

    Article  PubMed  Google Scholar 

  • Kunow K, Linder D, Stetter KO, Thauer RK (1994) F420H2:quinone oxidoreductase from Archaeoglobus fulgidus. Eur J Biochem 223:503–511

    Article  PubMed  CAS  Google Scholar 

  • Kvenvolden KA (1999) Potential effects of gas hydrate on human welfare. Proc Natl Acad Sci USA 96:3420–3426

    Article  PubMed  CAS  Google Scholar 

  • Lemker T, Ruppert C, Stöger H, Wimmers S, Müller V (2001) Overproduction of a functional A1 ATPase from the archaeon Methanosarcina mazei Gö1 in Escherichia coli. Eur J Biochem 268:3744–3750

    Article  PubMed  CAS  Google Scholar 

  • Lemker T, Schmid R, Grüber G, Müller V (2003) Subcomplexes of the heterologously produced archaeal A1 ATPase from Methanosarcina mazei Gö1: subunit composition and redox modulation. FEBS Lett 544:206–209

    Article  PubMed  CAS  Google Scholar 

  • Lewalter K, Müller V (2006) Bioenergetics of archaea: ancient energy conserving mechanisms developed in the early history of life. Biochim Biophys Acta 1757:437–445

    Article  PubMed  CAS  Google Scholar 

  • Li O, Li L, Rejtar T, Lessner DJ, Karger BL, Ferry JG (2006) Electron transport in the pathway of acetate conversion to methane in the marine archaeon Methanosarcina acetivorans. J Bacteriol 188:702–710

    Article  PubMed  CAS  Google Scholar 

  • Lienard T, Gottschalk G (1998) Cloning and expression of the genes encoding the sodium translocating N5-methyltetrahydromethanopterin:coenzyme M methyltransferase of the methylotrophic archaeon Methanosarcina mazei Gö1. FEBS Lett 425:204–208

    Article  PubMed  CAS  Google Scholar 

  • Lienard T, Becher B, Marschall M, Bowien S, Gottschalk G (1996) Sodium ion translocation by N5-methyltetrahydromethanopterin:coenzyme M methyltransferase from Methanosarcina mazei Gö1 reconstituted in ether lipid liposomes. Eur J Biochem 239:857–864

    Article  PubMed  CAS  Google Scholar 

  • Lingl A, Huber H, Stetter KO, Mayer F, Kellermann J, Müller V (2003) Isolation of a complete A1AO ATP synthase comprising nine subunits from the hyperthermophile Methanococcus jannaschii. Extremophiles 7:249–257

    PubMed  CAS  Google Scholar 

  • Lu WP, Becher B, Gottschalk G, Ragsdale SW (1995) Electron paramagnetic resonance spectroscopic and electrochemical characterization of the partially purified N5-methyltetrahydromethanopterin:coenzyme M methyltransferase from Methanosarcina mazei Gö1. J Bacteriol 177:2245–2250

    PubMed  CAS  Google Scholar 

  • Lübben M, Lünsdorf H, Schäfer G (1988) Archaebacterial ATPase: studies on subunit composition and quaternary structure of the F1-analogous ATPase from Sulfolobus acidocaldarius. Biol Chem Hoppe Seyler 369:1259–1266

    PubMed  Google Scholar 

  • Maegawa Y, Morita H, Iyaguchi D, Yao M, Watanabe N, Tanaka I (2006) Structure of the catalytic nucleotide-binding subunit A of A-type ATP synthase from Pyrococcus horikoshii reveals a novel domain related to the peripheral stalk. Acta Crystallogr D Biol Crystallogr 62:483–488

    Article  PubMed  CAS  Google Scholar 

  • Meier T, Polzer P, Diederichs K, Welte W, Dimroth P (2005) Structure of the rotor ring of F-Type Na+-ATPase from Ilyobacter tartaricus. Science 308:659–662

    Article  PubMed  CAS  Google Scholar 

  • Meuer J, Bartoschek S, Koch J, Künkel A, Hedderich R (1999) Purification and catalytic properties of Ech hydrogenase from Methanosarcina barkeri. Eur J Biochem 265:325–335

    Article  PubMed  CAS  Google Scholar 

  • Meuer J, Kuettner HC, Zhang JK, Hedderich R, Metcalf WW (2002) Genetic analysis of the archaeon Methanosarcina barkeri Fusaro reveals a central role for Ech hydrogenase and ferredoxin in methanogenesis and carbon fixation. Proc Natl Acad Sci USA 99:5632–5637

    Article  PubMed  CAS  Google Scholar 

  • Meyerdierks A, Kube M, Lombardot T, Knittel K, Bauer M, Glockner FO, Reinhardt R, Amann R (2005) Insights into the genomes of archaea mediating the anaerobic oxidation of methane. Environ Microbiol 7:1937–1951

    Article  PubMed  CAS  Google Scholar 

  • Müller V, Blaut M, Gottschalk G (1988a) The transmembrane electrochemical gradient of Na+ as driving force for methanol oxidation in Methanosarcina barkeri. Eur J Biochem 172:601–606

    Article  PubMed  Google Scholar 

  • Müller V, Winner C, Gottschalk G (1988b) Electron transport-driven sodium extrusion during methanogenesis from formaldehyde + H2 by Methanosarcina barkeri. Eur J Biochem 178:519–525

    Article  PubMed  Google Scholar 

  • Müller V, Grüber G (2003) ATP synthases: structure, function and evolution of unique energy converters. Cell Mol Life Sci 60:474–494

    Article  PubMed  Google Scholar 

  • Müller V (2004) An exceptional variability in the motor of archaeal A1AO ATPases: from multimeric to monomeric rotors comprising 6–13 ion binding sites. J Bioenerg Biomembr 36:115–125

    Article  PubMed  Google Scholar 

  • Müller V, Lemker T, Lingl A, Weidner C, Coskun U, Grüber G (2005a) Bioenergetics of archaea: ATP synthesis under harsh environmental conditions. J Mol Microbiol Biotechnol 10:167–180

    Article  PubMed  CAS  Google Scholar 

  • Müller V, Lingl A, Lewalter K, Fritz M (2005b) ATP synthases with novel rotor subunits: new insights into structure, function and evolution of ATPases. J Bioenerg Biomembr 37:455–460

    Article  PubMed  CAS  Google Scholar 

  • Murata T, Yamato I, Kakinuma Y, Leslie AG, Walker JE (2005) Structure of the rotor of the V-Type Na+-ATPase from Enterococcus hirae. Science 308:654–659

    Article  PubMed  CAS  Google Scholar 

  • Paul L, Ferguson DJ, Krzycki JA (2000) The trimethylamine methyltransferase gene and multiple dimethylamine methyltransferase genes of Methanosarcina barkeri contain in-frame and read-through amber codons. J Bacteriol 182:2520–2529

    Article  PubMed  CAS  Google Scholar 

  • Peinemann S (1989) Kopplung von ATP-Synthese und Methanogenese in Vesikelpräparationen des methanogenen Bakteriums Stamm Gö1. PhD Thesis, University of Göttingen, Germany

    Google Scholar 

  • Perski HJ, Moll J, Thauer RK (1981) Sodium dependence of growth and methane formation in Methanobacterium thermoautotrophicum. Arch Microbiol 130:319–321

    Article  CAS  Google Scholar 

  • Perski HJ, Schönheit P, Thauer RK (1982) Sodium dependence of methane formation in methanogenic bacteria. FEBS Lett 143:323–326

    Article  CAS  Google Scholar 

  • Poirot CM, Kengen SW, Valk E, Keltjens JT, van der Drift C, Vogels GD (1987) Formation of methylcoenzyme M from formaldehyde by cell free extracts of Methanobacterium thermoautotrophicum. Evidence for the involvement of a corrinoid-containing methyltransferase. FEMS Microbiol Lett 40:7–13

    Article  CAS  Google Scholar 

  • Porat I, Kim W, Hendrickson EL, Xia QW, Zhang Y, Wang TS, Taub F, Moore BC, Anderson IJ, Hackett M, Leigh JA, Whitman WB (2006) Disruption of the operon encoding Ehb hydrogenase limits anabolic CO2 assimilation in the archaeon Methanococcus maripaludis. J Bacteriol 188:1373–1380

    Article  PubMed  CAS  Google Scholar 

  • Rother M, Metcalf WW (2004) Anaerobic growth of Methanosarcina acetivorans C2A on carbon monoxide: An unusual way of life for a methanogenic archaeon. Proc Natl Acad Sci USA 101:16929–16934

    Article  PubMed  CAS  Google Scholar 

  • Ruppert C, Kavermann H, Wimmers S, Schmid R, Kellermann J, Lottspeich F, Huber H, Stetter KO, Müller V (1999) The proteolipid of the A1AO ATP synthase from Methanococcus jannaschii has six predicted transmembrane helices but only two proton-translocating carboxyl groups. J Biol Chem 274:25281–25284

    Article  PubMed  CAS  Google Scholar 

  • Ruppert C, Schmid R, Hedderich R, Müller V (2001) Selective extraction of subunit D of the Na+-translocating methyltransferase and subunit c of the A1AO ATPase from the cytoplasmic membrane of methanogenic archaea by chloroform/methanol and characterization of subunit c of Methanothermobacter thermoautotrophicus as a 16-kDa proteolipid. FEMS Microbiol Lett 195:47–51

    Article  PubMed  CAS  Google Scholar 

  • Sauter M, Böhm R, Böck A (1992) Mutational analysis of the operon (hyc) determining hydrogenase-3 formation in Escherichia coli. Mol Microbiol 6:1523–1532

    Article  PubMed  CAS  Google Scholar 

  • Schäfer G, Engelhard M, Müller V (1999) Bioenergetics of the Archaea. Microbiol Mol Biol Rev 63:570–620

    PubMed  Google Scholar 

  • Schäfer I, Rössle M, Biukovic G, Müller V, Grüber G (2006a) Structural and functional analysis of the coupling subunit F in solution and topological arrangement of the stalk domains of the methanogenic A1AO ATP synthase. J Bioenerg Biomembr 38:83–92

    Article  PubMed  CAS  Google Scholar 

  • Schäfer IB, Bailer SM, Düser MG, Börsch M, Bernal RA, Stock D, Grüber G (2006b) Crystal structure of the archaeal A1AO ATP synthase subunit B from Methanosarcina mazei Gö1: Implications of nucleotide-binding differences in the major A1AO subunits A and B. J Mol Biol 358:725–740

    Article  PubMed  CAS  Google Scholar 

  • Schink B (1997) Energetics of syntrophic cooperation in methanogenic degradation. Microbiol Mol Biol Rev 61:262–280

    PubMed  CAS  Google Scholar 

  • Setzke E, Hedderich R, Heiden S, Thauer RK (1994) H2:heterodisulfide oxidoreductase complex from Methanobacterium thermoautotrophicum. Composition and properties. Eur J Biochem 220:139–148

    Article  PubMed  CAS  Google Scholar 

  • Shima S, Warkentin E, Thauer RK, Ermler U (2002) Structure and function of enzymes involved in the methanogenic pathway utilizing carbon dioxide and molecular hydrogen. J Biosci Bioeng 93:519–530

    PubMed  CAS  Google Scholar 

  • Simianu M, Murakami E, Brewer JM, Ragsdale SW (1998) Purification and properties of the heme- and iron-sulfur containing heterodisulfide reductase from Methanosarcina thermophila. Biochemistry 37:10027–10039

    Article  PubMed  CAS  Google Scholar 

  • Slesarev AI, Mezhevaya KV, Makarova KS, Polushin NN, Shcherbinina OV, Shakhova VV, Belova GI, Aravind L, Natale DA, Rogozin IB, Tatusov RL, Wolf YI, Stetter KO, Malykh AG, Koonin EV, Kozyavkin SA (2002) The complete genome of hyperthermophile Methanopyrus kandleri AV19 and monophyly of archaeal methanogens. Proc Natl Acad Sci USA 99:4644–4649

    Article  PubMed  CAS  Google Scholar 

  • Smigan P, Majernik A, Greksak M (1994) Na+-driven ATP synthesis in Methanobacterium thermoautotrophicum and its differentiation from H+-driven ATP synthesis by rhodamine 6G. FEBS Lett 347:190–194

    Article  PubMed  CAS  Google Scholar 

  • Smigan P, Majernik A, Polak P, Hapala I, Greksak M (1995) The presence of H+ and Na+-translocating ATPases in Methanobacterium thermoautotrophicum and their possible function under alkaline conditions. FEBS Lett 371:119–122

    Article  PubMed  CAS  Google Scholar 

  • Sowers KR, Baron SF, Ferry JG (1984) Methanosarcina acetivorans sp. nov., an acetotrophic methane-producing bacterium isolated from marine sediments. Appl Environ Microbiol 47:971–978

    PubMed  CAS  Google Scholar 

  • Steuber J, Rufibach M, Fritz G, Neese F, Dimroth P (2002) Inactivation of the Na+-translocating NADH:ubiquinone oxidoreductase from Vibrio alginolyticus by reactive oxygen species. Eur J Biochem 269:1287–1292

    Article  PubMed  CAS  Google Scholar 

  • Stojanowic A, Hedderich R (2004) CO2 reduction to the level of formylmethanofuran in Methanosarcina barkeri is non-energy driven when CO is the electron donor. FEMS Microbiol Lett 235:163–167

    Article  PubMed  CAS  Google Scholar 

  • Tersteegen A, Hedderich R (1999) Methanobacterium thermoautotrophicum encodes two multisubunit membrane-bound [NiFe] hydrogenases—transcription of the operons and sequence analysis of the deduced proteins. Eur J Biochem 264:930–943

    Article  PubMed  CAS  Google Scholar 

  • Thauer RK (1998) Biochemistry of methanogenesis: a tribute to Marjory Stephenson. Microbiology 144:2377–2406

    Article  PubMed  CAS  Google Scholar 

  • Thauer RK, Shima S (2006) Biogeochemistry: Methane and microbes. Nature 440:878–879

    Article  PubMed  CAS  Google Scholar 

  • Tietze M, Beuchle A, Lamla I, Orth N, Dehler M, Greiner G, Beifuss U (2003) Redox potentials of methanophenazine and CoB-S-S-CoM, factors involved in electron transport in methanogenic archaea. Chembiochem 4:333–335

    Article  PubMed  CAS  Google Scholar 

  • Van Beelen P, Labro JF, Keltjens JT, Geerts WJ, Vogels GD, Laarhoven WH, Guijt W, Haasnoot CA (1984) Derivatives of methanopterin, a coenzyme involved in methanogenesis. Eur J Biochem 139:359–365

    Article  PubMed  Google Scholar 

  • Vignais PM, Colbeau A (2004) Molecular biology of microbial hydrogenases. Curr Issue Mol Biol 6:159–188

    CAS  Google Scholar 

  • Volbeda A, Charon MH, Piras C, Hatchikian EC, Frey M, Fontecilla-Camps JC (1995) Crystal structure of the nickel-ion hydrogenase from Desulfovivrio gigas. Nature 373:580–587

    Article  PubMed  CAS  Google Scholar 

  • Walsh C (1986) Naturally occuring 5-deazaflavin coenzymes: Biological redox roles. Acc Chem Res 19:216–221

    Article  CAS  Google Scholar 

  • Weiss DS, Gärtner P, Thauer RK (1994) The energetics and sodium-ion dependence of N5-methyltetrahydromethanopterin:coenzyme M methyltransferase studied with cob(I)alamin as methyl acceptor and methylcob(III)alamin as methyl donor. Eur J Biochem 226:799–809

    Article  PubMed  CAS  Google Scholar 

  • Wilms R, Freiberg C, Wegerle E, Meier I, Mayer F, Müller V (1996) Subunit structure and organization of the genes of the A1AO ATPase from the archaeon Methanosarcina mazei Gö1. J Biol Chem 271:18843–18852

    Article  PubMed  CAS  Google Scholar 

  • Wolfe RS (1985) Unusual coenzymes of methanogenesis. TIBS 10:396–399

    CAS  Google Scholar 

  • Wood WT, Gettrust JF, Chapman NR, Spence GD, Hyndman RD (2002) Decreased stability of methane hydrates in marine sediments owing to phase-boundary roughness. Nature 420:656–660

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Volker Müller .

Editor information

Günter Schäfer Harvey S. Penefsky

Rights and permissions

Reprints and permissions

Copyright information

© 2007 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Deppenmeier, U., Müller, V. (2007). Life Close to the Thermodynamic Limit: How Methanogenic Archaea Conserve Energy. In: Schäfer, G., Penefsky, H.S. (eds) Bioenergetics. Results and Problems in Cell Differentiation, vol 45. Springer, Berlin, Heidelberg. https://doi.org/10.1007/400_2006_026

Download citation

Publish with us

Policies and ethics