Home Life Sciences Hybrid rotors in F1Fo ATP synthases: subunit composition, distribution, and physiological significance
Article
Licensed
Unlicensed Requires Authentication

Hybrid rotors in F1Fo ATP synthases: subunit composition, distribution, and physiological significance

  • Karsten Brandt and Volker Müller EMAIL logo
Published/Copyright: April 1, 2015
Biological Chemistry
From the journal Biological Chemistry Volume 396 Issue 9-10

Abstract

The c ring of the Na+ F1Fo ATP synthase from the anaerobic acetogenic bacterium Acetobacterium woodii is encoded by three different genes: atpE1, atpE2 and atpE3. Subunit c1 is similar to typical V-type c subunits and has four transmembrane helices with one ion binding site. Subunit c2 and c3 are identical at the amino acid level and are typical F-type c subunits with one ion binding site in two transmembrane helices. All three constitute a hybrid FoVoc ring, the first found in nature. To analyze whether other species may have similar hybrid rotors, we searched every genome sequence publicly available as of 23 February 2015 for F1Fo ATPase operons that have more than one gene encoding the c subunit. This revealed no other species that has three different c subunit encoding genes but twelve species that encode one Fo- and one Vo-type c subunit in one operon. Their c subunits have the conserved binding motif for Na+. The organisms are all anaerobic. The advantage of hybrid c rings for the organisms in their environments is discussed.

Keywords: ATP synthesis; bioenergetics; electrochemical sodium ion potential; Rnf
Corresponding author: Volker Müller, Molecular Microbiology and Bioenergetics, Institute of Molecular Biosciences, Johann Wolfgang Goethe University Frankfurt, Max-von-Laue-Str. 9, D-60438 Frankfurt/Main, Germany, e-mail:

Acknowledgments

This work was supported by grants from the Deutsche Forschungsgemeinschaft (SFB 807).

References

Biegel, E. and Müller, V. (2010). Bacterial Na+-translocating ferredoxin:NAD+ oxidoreductase. Proc. Natl. Acad. Sci. USA 107, 18138–18142.10.1073/pnas.1010318107Search in Google Scholar

Biegel, E., Schmidt, S., González, J.M., and Müller, V. (2011). Biochemistry, evolution and physiological function of the Rnf complex, a novel ion-motive electron transport complex in prokaryotes. Cell. Mol. Life Sci. 68, 613–634.10.1007/s00018-010-0555-8Search in Google Scholar

Cai, S. and Dong, X. (2010). Cellulosilyticum ruminicola gen. nov., sp. nov., isolated from the rumen of yak, and reclassification of Clostridium lentocellum as Cellulosilyticum lentocellum comb. nov. Int. J. Syst. Evol. Microbiol. 60, 845–849.10.1099/ijs.0.014712-0Search in Google Scholar

Cato, E.P., Moore, L.V.H., and Moore, W.E.C. (1985). Fusobacterium alocis sp. nov. and Fusobacterium sulci sp. nov. from the human gingival sulcus. Int. J. Syst. Bacteriol. 35, 475–477.10.1099/00207713-35-4-475Search in Google Scholar

Dimroth, P. (1997). Primary sodium ion translocating enzymes. Biochim. Biophys. Acta 1318, 11–51.10.1016/S0005-2728(96)00127-2Search in Google Scholar

Dimroth, P., von Ballmoos, C., and Meier, T. (2006). Catalytic and mechanical cycles in F-ATP synthases. EMBO Rep. 7, 276–282.10.1038/sj.embor.7400646Search in Google Scholar

Dmitriev, O.Y., Jones, P.C., and Fillingame, R.H. (1999). Structure of the subunit c oligomer in the F1Fo ATP synthase: model derived from solution structure of the monomer and cross-linking in the native enzyme. Proc. Natl. Acad. Sci. USA 96, 7785–7790.10.1073/pnas.96.14.7785Search in Google Scholar

Downie, J.A., Langman, L., Cox, G.B., Yanofsky, C., and Gibson, F. (1980). Subunits of the adenosine triphosphatase complex translated in vitro from the Escherichia coli unc operon. J. Bacteriol. 143, 8–17.10.1128/jb.143.1.8-17.1980Search in Google Scholar

Drake, H.L., Hu, S.I., and Wood, H.G. (1981). Purification of five components from Clostridium thermoaceticum which catalyze synthesis of acetate from pyruvate and methyltetrahydrofolate. J. Biol. Chem. 56, 11137–11144.10.1016/S0021-9258(19)68568-6Search in Google Scholar

Fendrich, C., Hippe, H., and Gottschalk, G. (1990). Clostridium halophilium sp. nov. and C. litorale sp. nov., an obligate halophilic and a marine species degrading betaine in the Stickland reaction. Arch. Microbiol. 154, 127–132.10.1007/BF00423321Search in Google Scholar

Fillingame, R.H. (1997). Coupling H+ transport and ATP synthesis in F1F0-ATP synthases: Glimpses of interacting parts in a dynamic molecular machine. J. Exp. Biol. 200, 217–224.10.1242/jeb.200.2.217Search in Google Scholar PubMed

Forgac, M. (2007). Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nat. Rev. Mol. Cell. Biol. 8, 917–929.10.1038/nrm2272Search in Google Scholar PubMed

Fritz, M. and Müller, V. (2007). An intermediate step in the evolution of ATPases – the F1FO-ATPase from Acetobacterium woodii contains F-type and V-type rotor subunits and is capable of ATP synthesis. FEBS J. 274, 3421–3428.10.1111/j.1742-4658.2007.05874.xSearch in Google Scholar PubMed

Fritz, M., Klyszejko, A.L., Morgner, N., Vonck, J., Brutschy, B., Müller, D.J., Meier, T., Müller, V. (2008). An intermediate step in the evolution of ATPases: a hybrid F1FO rotor in a bacterial Na+ F1FO ATP synthase. FEBS J. 275, 1999–2007.10.1111/j.1742-4658.2008.06354.xSearch in Google Scholar PubMed

Gottschalk, G. (1986). Bacterial Metabolism, 2nd Ed, (Springer: Berlin, Germany).10.1007/978-1-4612-1072-6Search in Google Scholar

Hatch, L.P., Cox, G.B., and Howitt, S.M. (1995). The essential arginine residue at position 210 in the alpha subunit of the Escherichia coli ATP synthase can be transferred to position 252 with partial retention of activity. J. Biol. Chem. 270, 29407–29412.10.1074/jbc.270.49.29407Search in Google Scholar PubMed

Heise, R., Müller, V., and Gottschalk, G. (1992). Presence of a sodium-translocating ATPase in membrane vesicles of the homoacetogenic bacterium Acetobacterium woodii. Eur. J. Biochem. 206, 553–557.10.1111/j.1432-1033.1992.tb16959.xSearch in Google Scholar PubMed

Heise, R., Müller, V., and Gottschalk, G. (1993). Acetogenesis and ATP synthesis in Acetobacterium woodii are coupled via a transmembrane primary sodium ion gradient. FEMS Microbiol. Lett. 112, 261–268.10.1111/j.1574-6968.1993.tb06460.xSearch in Google Scholar

Hellmuth, K., Rex, G., Surin, B., Zinck, R., and McCarthy, J.E. (1991). Translational coupling varying in efficiency between different pairs of genes in the central region of the atp operon of Escherichia coli. Mol. Microbiol. 5, 813–824.10.1111/j.1365-2958.1991.tb00754.xSearch in Google Scholar PubMed

Hess, V., Schuchmann, K., and Müller, V. (2013). The ferredoxin:NAD+ oxidoreductase (Rnf) from the acetogen Acetobacterium woodii requires Na+ and is reversibly coupled to the membrane potential. J. Biol. Chem. 288, 31496–31502.10.1074/jbc.M113.510255Search in Google Scholar PubMed PubMed Central

Hirata, R., Graham, L.A., Takatsuki, A., Stevens, T.H., and Anraku, Y. (1997). VMA11 and VMA16 encode second and third proteolipid subunits of the Saccharomyces cerevisiae vacuolar membrane H+-ATPase. J. Biol. Chem. 272, 4795–4803.10.1074/jbc.272.8.4795Search in Google Scholar

Imkamp, F. and Müller, V. (2002). Chemiosmotic energy conservation with Na+ as the coupling ion during hydrogen-dependent caffeate reduction by Acetobacterium woodii. J. Bacteriol. 184, 1947–1951.10.1128/JB.184.7.1947-1951.2002Search in Google Scholar

Junge, W., Lill, H., and Engelbrecht, S. (1997). ATP synthase: an electrochemical transducer with rotatory mechanics. Trends Biochem. Sci. 22, 420–423.10.1016/S0968-0004(97)01129-8Search in Google Scholar

Junge, W., Sielaff, H., and Engelbrecht, S. (2009). Torque generation and elastic power transmission in the rotary FOF1-ATPase. Nature 459, 364–370.10.1038/nature08145Search in Google Scholar

Kaim, G., Wehrle, F., Gerike, U., and Dimroth, P. (1997). Molecular basis for the coupling ion selectivity of F1FO ATP synthases: probing the liganding groups for Na+ and Li+ in the c subunit of the ATP synthase from Propionigenium modestum. Biochem. 36, 9185–9194.10.1021/bi970831qSearch in Google Scholar

Kivistö, A.T. and Karp, M.T. (2011). Halophilic anaerobic fermentative bacteria. J. Biotechnol. 152, 114–124.10.1016/j.jbiotec.2010.08.014Search in Google Scholar

Konings, W.N., Lolkema, J.S., and Poolman, B. (1995). The generation of metabolic energy by solute transport. Arch. Microbiol. 164, 235–242.10.1007/BF02529957Search in Google Scholar

Krulwich, T.A., Ito, M., and Guffanti, A.A. (2001). The Na+-dependence of alkaliphily in Bacillus. Biochim. Biophys. Acta 1505, 158–168.10.1016/S0005-2728(00)00285-1Search in Google Scholar

Li, F., Hinderberger, J., Seedorf, H., Zhang, J., Buckel, W., and Thauer, R.K. (2008). Coupled ferredoxin and crotonyl coenzyme A (CoA) reduction with NADH catalyzed by the butyryl-CoA dehydrogenase/Etf complex from Clostridium kluyveri. J. Bacteriol. 190, 843–850.10.1128/JB.01417-07Search in Google Scholar

Maloney, P.C. (1994). Bacterial transporters. Curr. Opin. Cell Biol. 6, 571–582.10.1016/0955-0674(94)90079-5Search in Google Scholar

Mandel, M., Moriyama, Y., Hulmes, J.D., Pan, Y.C.E., Nelson, H., and Nelson, N. (1988). cDNA sequence encoding the 16-kDa proteolipid of chromaffin granules implies gene duplication in the evolution of H+-ATPases. Proc. Natl. Acad. Sci. USA 85, 5521–5524.10.1073/pnas.85.15.5521Search in Google Scholar

Matthies, D., Zhou, W., Klyszejko, A.L., Anselmi, C., Yildiz, Ö., Brandt, K., Müller, V., Faraldo-Gomez, J.D. and Meier, T. (2014). High-resolution structure and mechanism of Na+-coupled F/V-hybrid ATP synthase rotor ring. Nat. Commun. 5, 5286.10.1038/ncomms6286Search in Google Scholar

Mayer, F. and Müller, V. (2013). Adaptations of anaerobic archaea to life under extreme energy limitation. FEMS Microbiol. Rev. 38, 449–472.10.1111/1574-6976.12043Search in Google Scholar

McCarthy, J.E. (1988). Expression of the unc genes in Escherichia coli. J. Bioenerg. Biomembr. 20, 19–39.10.1007/BF00762136Search in Google Scholar

McCarthy, J.E. (1990). Post-transcriptional control in the polycistronic operon environment: studies of the atp operon of Escherichia coli. Mol. Microbiol. 4, 1233–1240.10.1111/j.1365-2958.1990.tb00702.xSearch in Google Scholar

McCarthy, J.E. and Bokelmann, C. (1988). Determinants of translational initiation efficiency in the atp operon of Escherichia coli. Mol. Microbiol. 2, 455–465.10.1111/j.1365-2958.1988.tb00051.xSearch in Google Scholar

McCarthy, J.E. and Gualerzi, C. (1990). Translational control of prokaryotic gene expression. Trends Genet. 6, 78–85.10.1016/0168-9525(90)90098-QSearch in Google Scholar

McCarthy, J.E., Schauder, B., and Ziemke, P. (1988). Post-transcriptional control in Escherichia coli: translation and degradation of the atp operon mRNA. Gene 72, 131–139.10.1016/0378-1119(88)90135-7Search in Google Scholar

Meier, T., Polzer, P., Diederichs, K., Welte, W., and Dimroth, P. (2005). Structure of the rotor ring of F-type Na+-ATPase from Ilyobacter tartaricus. Science 308, 659–662.10.1126/science.1111199Search in Google Scholar PubMed

Meier, T., Krah, A., Bond, P.J., Pogoryelov, D., Diederichs, K., and Faraldo-Gómez, J.D. (2009). Complete ion-coordination structure in the rotor ring of Na+-dependent F-ATP synthases. J. Mol. Biol. 391, 498–507.10.1016/j.jmb.2009.05.082Search in Google Scholar PubMed

Mesbah, N.M. and Wiegel, J. (2008). Life at extreme limits: the anaerobic halophilic alkalithermophiles. Ann. N. Y. Acad. Sci. 1125, 44–57.10.1196/annals.1419.028Search in Google Scholar PubMed

Mesbah, N.M. and Wiegel, J. (2011). The Na+-translocating F1FO-ATPase from the halophilic, alkalithermophile Natranaerobius thermophilus. Biochim. Biophys. Acta 1807, 1133–1142.10.1016/j.bbabio.2011.05.001Search in Google Scholar PubMed

Mesbah, N.M., Hedrick, D.B., Peacock, A.D., Rohde, M., and Wiegel, J. (2007). Natranaerobius thermophilus gen. nov., sp. nov., a halophilic, alkalithermophilic bacterium from soda lakes of the Wadi An Natrun, Egypt, and proposal of Natranaerobiaceae fam. nov. and Natranaerobiales ord. nov. Int. J. Syst. Evol. Microbiol. 57, 2507–2512.10.1099/ijs.0.65068-0Search in Google Scholar PubMed

Mitome, N., Ono, S., Sato, H., Suzuki, T., Sone, N., and Yoshida, M. (2010). Essential arginine residue of the FO-a subunit in FoF1-ATP synthase has a role to prevent the proton shortcut without c-ring rotation in the FO proton channel. Biochem. J. 430, 171–177.10.1042/BJ20100621Search in Google Scholar PubMed

Müller, V. (2003). Energy conservation in acetogenic bacteria. Appl. Environ. Microbiol. 69, 6345–6353.10.1128/AEM.69.11.6345-6353.2003Search in Google Scholar PubMed PubMed Central

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, 115–125.10.1023/B:JOBB.0000019603.68282.04Search in Google Scholar

Müller, V. (2008) Bacterial fermentation. In: Encyclopedia of Life Sciences. (Wiley-Blackwell: Hoboken, NJ, USA).Search in Google Scholar

Müller, V., Blaut, M., and Gottschalk, G. (1988). The transmembrane electrochemical gradient of Na+ as driving force for methanol oxidation in Methanosarcina barkeri. Eur. J. Biochem. 172, 601–606.10.1111/j.1432-1033.1988.tb13931.xSearch in Google Scholar PubMed

Müller, V., Imkamp, F., Rauwolf, A., Küsel, K., and Drake, H.L. (2004) Molecular and cellular biology of acetogenic bacteria. In: Strict and Facultative Anaerobes. Medical and Environmental Aspects, MM. Nakano and P. Zuber, eds. (Horizon Biosciences: Norfolk, UK), pp. 251–281.Search in Google Scholar

Müller, V., Lemker, T., Lingl, A., Weidner, C., Coskun, Ü., and Grüber, G. (2005a). Bioenergetics of archaea: ATP synthesis under harsh environmental conditions. J. Mol. Microbiol. Biotechnol. 10, 167–180.10.1159/000091563Search in Google Scholar PubMed

Müller, V., Lingl, A., Lewalter, K., and Fritz, M. (2005b). ATP synthases with novel rotor subunits: new insights into structure, function and evolution of ATPases. J. Bioenerg. Biomembr. 37, 455–460.10.1007/s10863-005-9491-ySearch in Google Scholar PubMed

Nelson, N. and Harvey, W.R. (1999). Vacuolar and plasma membrane proton-adenosinetriphosphatases. Physiol. Rev. 79, 361–385.10.1152/physrev.1999.79.2.361Search in Google Scholar PubMed

Nelson, H. and Nelson, N. (1989). The progenitor of ATP synthases was closely related to the current vacuolar H+-ATPase. FEBS Lett. 247, 147–153.10.1016/0014-5793(89)81259-1Search in Google Scholar

Nishi, T., Kawasaki-Nishi, S., and Forgac, M. (2003). The first putative transmembrane segment of subunit c′ (Vma16p) of the yeast V-ATPase is not necessary for function. J. Biol. Chem. 278, 5821–5827.10.1074/jbc.M209875200Search in Google Scholar

Pikuta, E.V., Hoover, R.B., Marsic, D., Whitman, W.B., Lupa, B., Tang, J., and Krader, P. (2009). Proteocatella sphenisci gen. nov., sp. nov., a psychrotolerant, spore-forming anaerobe isolated from penguin guano. Int. J. Syst. Evol. Microbiol. 59, 2302–2307.10.1099/ijs.0.002816-0Search in Google Scholar

Poehlein, A., Schmidt, S., Kaster, A.K., Goenrich, M., Vollmers, J., Thürmer, A., Bertsch, J., Schuchmann, K., Voigt, B., Hecker, M., et al. (2012). An ancient pathway combining carbon dioxide fixation with the generation and utilization of a sodium ion gradient for ATP synthesis. PLoS One 7, e33439.10.1371/journal.pone.0033439Search in Google Scholar

Pogoryelov, D., Yildiz, O., Faraldo-Gómez, J.D., and Meier, T. (2009). High-resolution structure of the rotor ring of a proton-dependent ATP synthase. Nat. Struct. Mol. Biol. 16, 1068–1073.10.1038/nsmb.1678Search in Google Scholar

Preiss, L., Yildiz, O., Hicks, D.B., Krulwich, T.A., and Meier, T. (2010). A new type of proton coordination in an F1FO-ATP synthase rotor ring. PLoS Biol. 8, e1000443.10.1371/journal.pbio.1000443Search in Google Scholar

Ragsdale, S.W. (2008). Enzymology of the Wood-Ljungdahl pathway of acetogenesis. Ann. N. Y. Acad. Sci. 1125, 129–136.10.1196/annals.1419.015Search in Google Scholar

Ragsdale, S.W., Clark, J.E., Ljungdahl, L.G., Lundie, L.L., and Drake, H.L. (1983). Properties of purified carbon monoxide dehydrogenase from Clostridium thermoaceticum, a nickel, iron-sulfur protein. J. Biol. Chem. 258, 2364–2369.10.1016/S0021-9258(18)32932-6Search in Google Scholar

Rahlfs, S. and Müller, V. (1997). Sequence of subunit c of the Na+-translocating F1FO ATPase of Acetobacterium woodii: proposal for determinants of Na+ specificity as revealed by sequence comparisons. FEBS Lett. 404, 269–271.10.1016/S0014-5793(97)00088-4Search in Google Scholar

Rahlfs, S., Aufurth, S., and Müller, V. (1999). The Na+-F1FO-ATPase operon from Acetobacterium woodii. Operon structure and presence of multiple copies of atpE which encode proteolipids of 8- and 18-kDa. J. Biol. Chem. 274, 33999–34004.10.1074/jbc.274.48.33999Search in Google Scholar PubMed

Reidlinger, J. and Müller, V. (1994). Purification of ATP synthase from Acetobacterium woodii and identification as a Na+-translocating F1FO-type enzyme. Eur. J. Biochem. 223, 275–283.10.1111/j.1432-1033.1994.tb18992.xSearch in Google Scholar

Roberts, D.L., James-Hagstrom, J.E., Garvin, D.K., Gorst, C.M., Runquist, J.A., Baur, J.R., Haase, F.C., and Ragsdale, S.W. (1989). Cloning and expression of the gene cluster encoding key proteins involved in acetyl-CoA synthesis in Clostridium thermoaceticum: CO dehydrogenase, the corrinoid/Fe-S protein, and methyltransferase. Proc. Natl. Acad. Sci. USA 86, 32–36.10.1073/pnas.86.1.32Search in Google Scholar

Sambongi, Y., Iko, Y., Tanabe, M., Omote, H., Iwamoto-Kihara, A., Ueda, I., Yanagida, T., Wada, Y., and Futai, M. (1999). Mechanical rotation of the c subunit oligomer in ATP synthase (FOF1): direct observation. Science 286, 1722–1724.10.1126/science.286.5445.1722Search in Google Scholar

Schauder, B. and McCarthy, J.E. (1989). The role of bases upstream of the Shine-Dalgarno region and in the coding sequence in the control of gene expression in Escherichia coli: translation and stability of mRNAs in vivo. Gene 78, 59–72.10.1016/0378-1119(89)90314-4Search in Google Scholar

Schmidt, S., Biegel, E., and Müller, V. (2009). The ins and outs of Na+ bioenergetics in Acetobacterium woodii. Biochim. Biophys. Acta 1787, 691–696.10.1016/j.bbabio.2008.12.015Search in Google Scholar PubMed

Schuchmann, K. and Müller, V. (2012). A bacterial electron bifurcating hydrogenase. J. Biol. Chem. 287, 31165–31171.10.1074/jbc.M112.395038Search in Google Scholar PubMed PubMed Central

Schuchmann, K. and Müller, V. (2014). Autotrophy at the thermodynamic limit of life: a model for energy conservation in acetogenic bacteria. Nat. Rev. Microbiol. 12, 809–821.10.1038/nrmicro3365Search in Google Scholar PubMed

Schulz, S., Iglesias-Cans, M., Krah, A., Yildiz, O., Leone, V., Matthies, D., Cook, G.M., Faraldo-Gomez, J.D. and Meier, T. (2013). A new type of Na+-driven ATP synthase membrane rotor with a two-carboxylate ion-coupling motif. PLoS Biol. 11, e1001596.10.1371/journal.pbio.1001596Search in Google Scholar PubMed PubMed Central

Seedorf, H., Fricke, W.F., Veith, B., Brüggemann, H., Liesegang, H., Strittmatter, A., Miethke, M., Buckel, W., Hinderberger, J., Li, F., et al. (2008). The genome of Clostridium kluyveri, a strict anaerobe with unique metabolic features. Proc. Natl. Acad. Sci. USA 105, 2128–2133.10.1073/pnas.0711093105Search in Google Scholar PubMed PubMed Central

Stock, D., Leslie, A.G., and Walker, J.E. (1999). Molecular architecture of the rotary motor in ATP synthase. Science 286, 1700–1705.10.1126/science.286.5445.1700Search in Google Scholar PubMed

Symersky, J., Pagadala, V., Osowski, D., Krah, A., Meier, T., Faraldo-Gomez, J.D., and Mueller, D.M. (2012). Structure of the c10 ring of the yeast mitochondrial ATP synthase in the open conformation. Nat. Struct. Mol. Biol. 19, 485–491.10.1038/nsmb.2284Search in Google Scholar

Toei, M., Gerle, C., Nakano, M., Tani, K., Gyobu, N., Tamakoshi, M., Sone, N., Yoshida, M., Fujiyoshi, Y., Mitsuoka, K., et al. (2007). Dodecamer rotor ring defines H+/ATP ratio for ATP synthesis of prokaryotic V-ATPase from Thermus thermophilus. Proc. Natl. Acad. Sci. USA 104, 20256–20261.10.1073/pnas.0706914105Search in Google Scholar

Valiyaveetil, F.I. and Fillingame, R.H. (1997). On the role of Arg-210 and Glu-219 of subunit a in proton translocation by the Escherichia coli FOF1-ATP synthase. J. Biol. Chem. 272, 32635–32641.10.1074/jbc.272.51.32635Search in Google Scholar

Vik, S.B. and Antonio, B.J. (1994). A mechanism of proton translocation by F1FO ATP synthases suggested by double mutants of the α subunit. J. Biol. Chem. 269, 30364–30369.10.1016/S0021-9258(18)43822-7Search in Google Scholar

Vollmar, M., Schlieper, D., Winn, M., Buchner, C., and Groth, G. (2009). Structure of the c14 rotor ring of the proton translocating chloroplast ATP synthase. J. Biol. Chem. 284, 18228–18235.10.1074/jbc.M109.006916Search in Google Scholar PubMed PubMed Central

von Ballmoos, C., Wiedenmann, A., and Dimroth, P. (2009). Essentials for ATP synthesis by F1FO ATP synthases. Annu. Rev. Biochem. 78, 649–672.10.1146/annurev.biochem.78.081307.104803Search in Google Scholar PubMed

Watt, I.N., Montgomery, M.G., Runswick, M.J., Leslie, A.G., and Walker, J.E. (2010). Bioenergetic cost of making an adenosine triphosphate molecule in animal mitochondria. Proc. Natl. Acad. Sci. USA 107, 16823–16827.10.1073/pnas.1011099107Search in Google Scholar PubMed PubMed Central

Wood, H.G. and Ljungdahl, L.G. (1991) Autotrophic character of the acetogenic bacteria. In: Variations in Autotrophic Life, JM. Shively and LL. Barton, eds. (Academic Press: San Diego, CA), pp. 201–250.Search in Google Scholar

Ye, Q., Roh, Y., Carroll, S.L., Blair, B., Zhou, J., Zhang, C.L., and Fields, M.W. (2004). Alkaline anaerobic respiration: isolation and characterization of a novel alkaliphilic and metal-reducing bacterium. Appl. Environ. Microbiol. 70, 5595–5602.10.1128/AEM.70.9.5595-5602.2004Search in Google Scholar PubMed PubMed Central

Zhilina, T.N. and Zavarzin, G.A. (1990). Extremely halophilic, methylotrophic, anaerobic bacteria. FEMS Microbiol. Lett. 87, 315–322.10.1111/j.1574-6968.1990.tb04930.xSearch in Google Scholar

Zhilina, T.N., Garnova, E.S., Turova, T.P., Kostrikina, N.A., and Zavarzin, G.A. (2001). Halonatronum saccharophilum gen. nov. sp. nov. – a new haloalkalophilic bacteria from the order Haloanaerobiales from Lake Magadi. Mikrobiology 70, 77–85.Search in Google Scholar

Received: 2015-3-2
Accepted: 2015-3-25
Published Online: 2015-4-1
Published in Print: 2015-9-1

©2015 by De Gruyter

Articles in the same Issue

  1. Frontmatter
  2. Meeting Report
  3. Membrane Transport and Communication in Frankfurt: Speakers’ Summary – Highlights
  4. HIGHLIGHT: MEMBRANE TRANSPORT AND COMMUNICATION
  5. Structure, function, evolution, and application of bacterial Pnu-type vitamin transporters
  6. Team work at its best – TAPL and its two domains
  7. The volume-regulated anion channel is formed by LRRC8 heteromers – molecular identification and roles in membrane transport and physiology
  8. Extending native mass spectrometry approaches to integral membrane proteins
  9. Functional diversity of the superfamily of K+ transporters to meet various requirements
  10. The structure of Na+-translocating of NADH:ubiquinone oxidoreductase of Vibrio cholerae: implications on coupling between electron transfer and Na+ transport
  11. Hybrid rotors in F1Fo ATP synthases: subunit composition, distribution, and physiological significance
  12. Homeostatic control of biological membranes by dedicated lipid and membrane packing sensors
  13. The transporter associated with antigen processing: a key player in adaptive immunity
  14. The pseudo-atomic structure of an RND-type tripartite multidrug efflux pump
  15. The assembly and disassembly of the AcrAB-TolC three-component multidrug efflux pump
  16. A universal mechanism for transport and regulation of CPA sodium proton exchangers
  17. Biosynthesis of membrane dependent proteins in insect cell lysates: identification of limiting parameters for folding and processing
  18. Fluorescence and excited state dynamics of the deprotonated Schiff base retinal in proteorhodopsin
  19. Regulatory role of charged clusters in the N-terminal domain of BetP from Corynebacterium glutamicum
  20. The contribution of methionine to the stability of the Escherichia coli MetNIQ ABC transporter-substrate binding protein complex
  21. The ABC exporter MsbA probed by solid state NMR – challenges and opportunities
  22. Functional properties of LptA and LptD in Anabaena sp. PCC 7120
https://doi.org/10.1515/hsz-2015-0137
Keywords for this article
ATP synthesis; bioenergetics; electrochemical sodium ion potential; Rnf

Articles in the same Issue

  1. Frontmatter
  2. Meeting Report
  3. Membrane Transport and Communication in Frankfurt: Speakers’ Summary – Highlights
  4. HIGHLIGHT: MEMBRANE TRANSPORT AND COMMUNICATION
  5. Structure, function, evolution, and application of bacterial Pnu-type vitamin transporters
  6. Team work at its best – TAPL and its two domains
  7. The volume-regulated anion channel is formed by LRRC8 heteromers – molecular identification and roles in membrane transport and physiology
  8. Extending native mass spectrometry approaches to integral membrane proteins
  9. Functional diversity of the superfamily of K+ transporters to meet various requirements
  10. The structure of Na+-translocating of NADH:ubiquinone oxidoreductase of Vibrio cholerae: implications on coupling between electron transfer and Na+ transport
  11. Hybrid rotors in F1Fo ATP synthases: subunit composition, distribution, and physiological significance
  12. Homeostatic control of biological membranes by dedicated lipid and membrane packing sensors
  13. The transporter associated with antigen processing: a key player in adaptive immunity
  14. The pseudo-atomic structure of an RND-type tripartite multidrug efflux pump
  15. The assembly and disassembly of the AcrAB-TolC three-component multidrug efflux pump
  16. A universal mechanism for transport and regulation of CPA sodium proton exchangers
  17. Biosynthesis of membrane dependent proteins in insect cell lysates: identification of limiting parameters for folding and processing
  18. Fluorescence and excited state dynamics of the deprotonated Schiff base retinal in proteorhodopsin
  19. Regulatory role of charged clusters in the N-terminal domain of BetP from Corynebacterium glutamicum
  20. The contribution of methionine to the stability of the Escherichia coli MetNIQ ABC transporter-substrate binding protein complex
  21. The ABC exporter MsbA probed by solid state NMR – challenges and opportunities
  22. Functional properties of LptA and LptD in Anabaena sp. PCC 7120
Sign up now to receive a 20% welcome discount
Institutional Access
How does access work?
Have an idea on how to improve our website?
Please write us.
© 2025 De Gruyter Brill
Downloaded on 22.12.2025 from https://www.degruyterbrill.com/document/doi/10.1515/hsz-2015-0137/html
Scroll to top button