bacterial proton translocating atpases


Summary: Membrane-bound proton-translocating ATPases that serve two important physiological functions in bacteria. One function is to generate ADENOSINE TRIPHOSPHATE by utilizing the energy provided by an electrochemical gradient of protons across the cellular membrane. A second function is to counteract a loss of the transmembrane ion gradient by pumping protons at the expense of adenosine triphosphate hydrolysis.

Top Publications

  1. Liu J, Fujisawa M, Hicks D, Krulwich T. Characterization of the Functionally Critical AXAXAXA and PXXEXXP Motifs of the ATP Synthase c-Subunit from an Alkaliphilic Bacillus. J Biol Chem. 2009;284:8714-25 pubmed publisher
    ..The results highlight the requirement for c-subunit adaptations to achieve alkaliphile ATP synthesis with minimal cytoplasmic proton loss and suggest partial suppression of some mutations by changes outside the atp operon. ..
  2. Pogoryelov D, Yildiz O, Faraldo Gómez J, Meier T. High-resolution structure of the rotor ring of a proton-dependent ATP synthase. Nat Struct Mol Biol. 2009;16:1068-73 pubmed publisher
    ..Proton exchange would occur in a more hydrophilic and electrostatically distinct environment upon contact with the a subunit interface. ..
  3. Meier T, Krah A, Bond P, Pogoryelov D, Diederichs K, Faraldo Gómez J. Complete ion-coordination structure in the rotor ring of Na+-dependent F-ATP synthases. J Mol Biol. 2009;391:498-507 pubmed publisher
    ..Given the evolutionary ascendancy of sodium over proton bioenergetics, this structure uncovers an ancient strategy for selective ion coupling in ATP synthases...
  4. von Ballmoos C, Dimroth P. Two distinct proton binding sites in the ATP synthase family. Biochemistry. 2007;46:11800-9 pubmed
    ..The concept of two different binding sites in the ATP synthase family is supported by the ATP hydrolysis pH profiles of the investigated enzymes...
  5. Meier T, Ferguson S, Cook G, Dimroth P, Vonck J. Structural investigations of the membrane-embedded rotor ring of the F-ATPase from Clostridium paradoxum. J Bacteriol. 2006;188:7759-64 pubmed
    ..On the basis of these results, it was determined that the F-ATPase from C. paradoxum contains an undecameric c ring. ..
  6. Steed P, Fillingame R. Aqueous accessibility to the transmembrane regions of subunit c of the Escherichia coli F1F0 ATP synthase. J Biol Chem. 2009;284:23243-50 pubmed publisher
  7. Akopian M, Poladian A, Bagramian K. [Energy transformation coupled to formate oxidation during anaerobic fermentation]. Biofizika. 2006;51:466-71 pubmed
  8. Minamino T, Imada K, Namba K. Mechanisms of type III protein export for bacterial flagellar assembly. Mol Biosyst. 2008;4:1105-15 pubmed publisher
  9. Langemeyer L, Engelbrecht S. Essential arginine in subunit a and aspartate in subunit c of FoF1 ATP synthase: effect of repositioning within helix 4 of subunit a and helix 2 of subunit c. Biochim Biophys Acta. 2007;1767:998-1005 pubmed
    ..Mutant cD61N/cM65D grew on succinate, retained the ability to synthesize ATP and supported passive proton conduction but apparently not ATP hydrolysis-driven proton pumping. ..

More Information


  1. Palese L, Gaballo A, Technikova Dobrova Z, Labonia N, Abbrescia A, Scacco S, et al. Characterization of plasma membrane respiratory chain and ATPase in the actinomycete Nonomuraea sp. ATCC 39727. FEMS Microbiol Lett. 2003;228:233-9 pubmed
    ..The H+-ATPase activity reaches, as the respiratory chain, a maximal activity at the end of the exponential growth phase and then remains constant in the stationary phase. ..
  2. Petersen K, Christensen H, Bisgaard M, Olsen J. Genetic diversity of Pasteurella multocida fowl cholera isolates as demonstrated by ribotyping and 16S rRNA and partial atpD sequence comparisons. Microbiology. 2001;147:2739-48 pubmed
    ..The considerable genetic diversity of P. multocida fowl cholera isolates is probably related to the clonal nature of this organism, resulting in many divergent lines...
  3. Ganti S, Vik S. Chemical modification of mono-cysteine mutants allows a more global look at conformations of the epsilon subunit of the ATP synthase from Escherichia coli. J Bioenerg Biomembr. 2007;39:99-107 pubmed
    ..The results indicate that the two C-terminal alpha-helices do not adopt a fixed conformation under resting conditions, but rather exhibit intrinsic flexibility. ..
  4. Dimroth P, von Ballmoos C, Meier T, Kaim G. Electrical power fuels rotary ATP synthase. Structure. 2003;11:1469-73 pubmed
    ..Here, we incorporate recent results on structure and function of the F(0) domain and present a mechanism for torque generation with the fundamental nature of the membrane potential as driving force in the core. ..
  5. Hersch G, Burton R, Bolon D, Baker T, Sauer R. Asymmetric interactions of ATP with the AAA+ ClpX6 unfoldase: allosteric control of a protein machine. Cell. 2005;121:1017-27 pubmed
    ..These studies further emphasize commonalities between distant AAA+ family members, including protein and DNA translocases, helicases, motor proteins, clamp loaders, and other ATP-dependent enzymes. ..
  6. Ahmad Z, Senior A. Mutagenesis of residue betaArg-246 in the phosphate-binding subdomain of catalytic sites of Escherichia coli F1-ATPase. J Biol Chem. 2004;279:31505-13 pubmed
    ..Phosphate protected against NBD-Cl inhibition in wild type but not in mutants. The results show that phosphate can bind in the betaE catalytic site of E. coli F(1) and that betaArg-246 is an important phosphate-binding residue. ..
  7. Tadevosyan H, Kalantaryan V, Trchounian A. Extremely high frequency electromagnetic radiation enforces bacterial effects of inhibitors and antibiotics. Cell Biochem Biophys. 2008;51:97-103 pubmed publisher
    ..The radiation of bacteria might lead to changed metabolic pathways and to antibiotic resistance. It may also give bacteria with a specific role in biosphere. ..
  8. Gueguen E, Savitzky D, Darwin A. Analysis of the Yersinia enterocolitica PspBC proteins defines functional domains, essential amino acids and new roles within the phage-shock-protein response. Mol Microbiol. 2009;74:619-33 pubmed publisher
    ..These data provide compelling support for the proposal that these two functions are independent...
  9. Weber T, Widger W, Kohn H. Metal dependency for transcription factor rho activation. Biochemistry. 2003;42:1652-9 pubmed
  10. Fillingame R, Jiang W, Dmitriev O. The oligomeric subunit C rotor in the fo sector of ATP synthase: unresolved questions in our understanding of function. J Bioenerg Biomembr. 2000;32:433-9 pubmed
    ..The H+-transport coupled rotation of this helix is proposed to drive the stepwise movement of the c-oligomeric rotor. The model is testable and provides a useful framework for addressing questions raised by other experiments. ..
  11. Vik S. What is the role of epsilon in the Escherichia coli ATP synthase?. J Bioenerg Biomembr. 2000;32:485-91 pubmed
    ..In light of recent work by our group and that of others, the role of epsilon in the ATP synthase from E. coli is discussed. ..
  12. Cipriano D, Wood K, Bi Y, Dunn S. Mutations in the dimerization domain of the b subunit from the Escherichia coli ATP synthase. Deletions disrupt function but not enzyme assembly. J Biol Chem. 2006;281:12408-13 pubmed
    ..This function is proposed to depend on proper, specific interactions between the b subunits and F1. ..
  13. Watanabe S, Kobayashi N, Quiñones D, Hayakawa S, Nagashima S, Uehara N, et al. Genetic diversity of the low-level vancomycin resistance gene vanC-2/vanC-3 and identification of a novel vanC subtype (vanC-4) in Enterococcus casseliflavus. Microb Drug Resist. 2009;15:1-9 pubmed publisher
    ..These findings indicated that among E. casseliflavus there are at least two genetic lineages with the distinct vanC genes, that is, a single subtype including previously known vanC-2/C-3, and a novel subtype vanC-4. ..
  14. Ballhausen B, Altendorf K, Deckers Hebestreit G. Constant c10 ring stoichiometry in the Escherichia coli ATP synthase analyzed by cross-linking. J Bacteriol. 2009;191:2400-4 pubmed publisher
    ..Independent of the carbon source used for growth and independent of the presence of other FoF1 subunits, an equal pattern of cross-link formation stopping at the formation of decamers was obtained. ..
  15. von Ballmoos C, Meier T, Dimroth P. Membrane embedded location of Na+ or H+ binding sites on the rotor ring of F1F0 ATP synthases. Eur J Biochem. 2002;269:5581-9 pubmed
    ..The common membrane embedded location of the binding site of ATP synthases suggest a common mechanism for ion transfer across the membrane. ..
  16. Thompson C, Thompson F, Vicente A, Swings J. Phylogenetic analysis of vibrios and related species by means of atpA gene sequences. Int J Syst Evol Microbiol. 2007;57:2480-4 pubmed
    ..The intraspecies variation in the atpA gene sequence was about 99% sequence similarity. The results showed clearly that atpA gene sequences are a suitable alternative for the identification and phylogenetic study of vibrios...
  17. Gubellini F, Francia F, Turina P, Levy D, Venturoli G, Melandri B. Heterogeneity of photosynthetic membranes from Rhodobacter capsulatus: size dispersion and ATP synthase distribution. Biochim Biophys Acta. 2007;1767:1340-52 pubmed
  18. Fritz M, Klyszejko A, Morgner N, Vonck J, Brutschy B, Muller D, et al. An intermediate step in the evolution of ATPases: a hybrid F(0)-V(0) rotor in a bacterial Na(+) F(1)F(0) ATP synthase. FEBS J. 2008;275:1999-2007 pubmed publisher
    ..Furthermore, this stoichiometry was independent of the carbon source of the growth medium. These analyses clearly demonstrate, for the first time, an F(0)-V(0) hybrid motor in an ATP synthase...
  19. Sengupta D, Rampioni A, Marrink S. Simulations of the c-subunit of ATP-synthase reveal helix rearrangements. Mol Membr Biol. 2009;26:422-34 pubmed publisher
    ..The characterization of the monomer and ring presented in this work sheds light into the structural dynamics of the c-subunit and its functional relevance. ..
  20. Iino R, Hasegawa R, Tabata K, Noji H. Mechanism of inhibition by C-terminal alpha-helices of the epsilon subunit of Escherichia coli FoF1-ATP synthase. J Biol Chem. 2009;284:17457-64 pubmed publisher
    ..These results suggest that the C-terminal domain of the epsilon subunit of EFoF1 slows multiple elementary steps in both the ATP synthesis/hydrolysis reactions by restricting the rotation of the gamma subunit. ..
  21. Dmitriev O, Altendorf K, Fillingame R. Subunit A of the E. coli ATP synthase: reconstitution and high resolution NMR with protein purified in a mixed polarity solvent. FEBS Lett. 2004;556:35-8 pubmed
  22. Krebstakies T, Aldag I, Altendorf K, Greie J, Deckers Hebestreit G. The stoichiometry of subunit c of Escherichia coli ATP synthase is independent of its rate of synthesis. Biochemistry. 2008;47:6907-16 pubmed publisher
    ..Thus, these data clearly demonstrate that the stoichiometry of the subunit c rings remains constant even after reduction of the synthesis of subunit c. ..
  23. Wilkens S, Borchardt D, Weber J, Senior A. Structural characterization of the interaction of the delta and alpha subunits of the Escherichia coli F1F0-ATP synthase by NMR spectroscopy. Biochemistry. 2005;44:11786-94 pubmed
    ..On the basis of intermolecular contacts observed in (12)C/(13)C-filtered NOESY experiments, we describe structural details of the interaction of the delta-subunit N-terminal domain with the alpha-subunit N-terminal alpha helix. ..
  24. Kuhnert W, Zheng G, Faustoferri R, Quivey R. The F-ATPase operon promoter of Streptococcus mutans is transcriptionally regulated in response to external pH. J Bacteriol. 2004;186:8524-8 pubmed
    ..Fusions of the F-ATPase promoter to chloramphenicol acetyltransferase indicated that pH-dependent expression is still observed with a short promoter that contains a domain conserved between streptococcal ATPase operons. ..
  25. Arechaga I, Miroux B, Runswick M, Walker J. Over-expression of Escherichia coli F1F(o)-ATPase subunit a is inhibited by instability of the uncB gene transcript. FEBS Lett. 2003;547:97-100 pubmed
    ..Green fluorescent protein fusions with N- and C-ends of uncB helped to stabilize the mRNA and to obtain high yields of protein. ..
  26. Ozaki Y, Suzuki T, Kuruma Y, Ueda T, Yoshida M. UncI protein can mediate ring-assembly of c-subunits of FoF1-ATP synthase in vitro. Biochem Biophys Res Commun. 2008;367:663-6 pubmed publisher
    ..Fusion of the two kinds of liposomes, one containing only unassembled c-subunit and the other only UncI, resulted in gradual formation of c-ring. Thus, UncI alone can mediate in vitro post-translational c-ring assembly...
  27. Fry A, Wernegreen J. The roles of positive and negative selection in the molecular evolution of insect endosymbionts. Gene. 2005;355:1-10 pubmed
    ..In the course of this study, we reanalyzed variation at Buchnera groEL and found no evidence of positive selection that was previously reported. ..
  28. Lolkema J, Boekema E. The A-type ATP synthase subunit K of Methanopyrus kandleri is deduced from its sequence to form a monomeric rotor comprising 13 hairpin domains. FEBS Lett. 2003;543:47-50 pubmed
    ..The protein is likely to form the monomeric rotor of the ATP synthase that consists of 13 hairpin domains. ..
  29. Monticello R, Angov E, Brusilow W. Effects of inducing expression of cloned genes for the F0 proton channel of the Escherichia coli F1F0 ATPase. J Bacteriol. 1992;174:3370-6 pubmed
    ..Such induction did result in growth inhibition, but there was no correlation between growth inhibition and either increased membrane proton permeability or the presence of functional, reconstitutable F0. ..
  30. Vorburger T, Ebneter J, Wiedenmann A, Morger D, Weber G, Diederichs K, et al. Arginine-induced conformational change in the c-ring/a-subunit interface of ATP synthase. FEBS J. 2008;275:2137-50 pubmed publisher
    ..This mechanism allows efficient interaction between subunit a and the c-ring and simultaneously allows almost frictionless movement against each other. ..
  31. Priya R, Tadwal V, Roessle M, Gayen S, Hunke C, Peng W, et al. Low resolution structure of subunit b (b (22-156)) of Escherichia coli F(1)F(O) ATP synthase in solution and the b-delta assembly. J Bioenerg Biomembr. 2008;40:245-55 pubmed publisher
    ..The novel 3D structure of this peptide has been determined by NMR spectroscopy. The molecule adopts a stable helix formation in solution with a flexible tail between amino acid 140 to 145. ..
  32. Laughlin T, Ahmad Z. Inhibition of Escherichia coli ATP synthase by amphibian antimicrobial peptides. Int J Biol Macromol. 2010;46:367-74 pubmed publisher
    ..1, magainin II, or XT-7. Hence inhibition of F(1)-ATPase and E. coli cell growth by amphibian antimicrobial peptides suggests that their antimicrobial/anticancer properties are in part linked to their actions on ATP synthase. ..
  33. Rohlin L, Gunsalus R. Carbon-dependent control of electron transfer and central carbon pathway genes for methane biosynthesis in the Archaean, Methanosarcina acetivorans strain C2A. BMC Microbiol. 2010;10:62 pubmed publisher
    ..acetivorans are also present in other Methanosarcina species including M. mazei, and in M. barkeri, these findings provide a basis for predicting related control in these environmentally significant methanogens. ..
  34. Patel A, Dunn S. Degradation of Escherichia coli uncB mRNA by multiple endonucleolytic cleavages. J Bacteriol. 1995;177:3917-22 pubmed
    ..The rapid decay of uncB is expected to play a role in limiting expression of this gene relative to that of the other genes of the operon. ..
  35. Arechaga I, Butler P, Walker J. Self-assembly of ATP synthase subunit c rings. FEBS Lett. 2002;515:189-93 pubmed
    ..The results suggest that the ability of subunit c to form rings is determined by its primary structure...
  36. Yagi H, Kajiwara N, Tanaka H, Tsukihara T, Kato Yamada Y, Yoshida M, et al. Structures of the thermophilic F1-ATPase epsilon subunit suggesting ATP-regulated arm motion of its C-terminal domain in F1. Proc Natl Acad Sci U S A. 2007;104:11233-8 pubmed publisher
    ..These results suggest that the epsilon C-terminal domain can undergo an arm-like motion in response to an ATP concentration change and thereby contribute to regulation of F(o)F(1)-ATP synthase...
  37. Zimmermann B, Diez M, Zarrabi N, Graber P, Börsch M. Movements of the epsilon-subunit during catalysis and activation in single membrane-bound H(+)-ATP synthase. EMBO J. 2005;24:2053-63 pubmed
    ..The three states of the inactive enzyme were unequally populated. We conclude that the active-inactive transition was associated with a conformational change of epsilon within the central stalk. ..
  38. Imada K, Minamino T, Tahara A, Namba K. Structural similarity between the flagellar type III ATPase FliI and F1-ATPase subunits. Proc Natl Acad Sci U S A. 2007;104:485-90 pubmed
    ..These results imply an evolutionary relation between the flagellum and F0F1-ATPsynthase and a similarity in the mechanism between FliI and F1-ATPase despite the apparently different functions of these proteins. ..
  39. Bae L, Vik S. A more robust version of the Arginine 210-switched mutant in subunit a of the Escherichia coli ATP synthase. Biochim Biophys Acta. 2009;1787:1129-34 pubmed publisher
    ..This same unusual result was observed in the triple mutant background, P204T/R210Q/Q252R, suggesting that the Arginine-switched mutants are using the normal proton pathway from the periplasm. ..
  40. Galkin M, Ishmukhametov R, Vik S. A functionally inactive, cold-stabilized form of the Escherichia coli F1Fo ATP synthase. Biochim Biophys Acta. 2006;1757:206-14 pubmed
    ..The results suggest that thermohysteresis is a consequence of an inactive form of the enzyme that is stabilized by the binding of inhibitory Mg-ADP. ..
  41. Schwem B, Fillingame R. Cross-linking between helices within subunit a of Escherichia coli ATP synthase defines the transmembrane packing of a four-helix bundle. J Biol Chem. 2006;281:37861-7 pubmed
    ..Other key residues in TMHs 2, 4, and 5, which were concluded previously to compose a possible aqueous access pathway from the periplasm, were found to locate to the inside of the four-helix bundle. ..
  42. Thedei G, Leitão D, Bolean M, Paulino T, Spadaro A, Ciancaglini P. Toluene permeabilization differentially affects F- and P-type ATPase activities present in the plasma membrane of Streptococcus mutans. Braz J Med Biol Res. 2008;41:1047-53 pubmed
    ..The mild conditions used for the preparation of membrane fractions may be more suitable to study specific ATPase activity in the presence of biological agents, since this method preserves ATPase selectivity for standard inhibitors. ..
  43. Nakanishi Matsui M, Kashiwagi S, Ubukata T, Iwamoto Kihara A, Wada Y, Futai M. Rotational catalysis of Escherichia coli ATP synthase F1 sector. Stochastic fluctuation and a key domain of the beta subunit. J Biol Chem. 2007;282:20698-704 pubmed
    ..These results indicate that the domain between beta-sheet 4 (betaSer-174) and P-loop (betaGly-149) is important to drive rotation. ..
  44. Schumacher J, Zhang X, Jones S, Bordes P, Buck M. ATP-dependent transcriptional activation by bacterial PspF AAA+protein. J Mol Biol. 2004;338:863-75 pubmed
  45. Lee C, Revington M, Dunn S, Petersen N. The lateral diffusion of selectively aggregated peptides in giant unilamellar vesicles. Biophys J. 2003;84:1756-64 pubmed
    ..Comparisons with diffusion of lipids confirm that the diffusion of a transmembrane peptide is enhanced by coupling of density fluctuations between the two monolayers. ..
  46. Feniouk B, Yoshida M. Regulatory mechanisms of proton-translocating F(O)F (1)-ATP synthase. Results Probl Cell Differ. 2008;45:279-308 pubmed
    ..Inhibition by an additional regulatory protein (IF(1)) in mitochondrial enzyme In this review we summarize the information available on these regulatory mechanisms and discuss possible interplay between them. ..
  47. Kol S, Nouwen N, Driessen A. The charge distribution in the cytoplasmic loop of subunit C of the F1F0 ATPase is a determinant for YidC targeting. J Biol Chem. 2008;283:9871-7 pubmed publisher
    ..Positive charges in the cytoplasmic loop of F(0)c are important determinants for YidC binding and subsequent membrane insertion. These data support a model in which F(0)c binds directly to YidC prior to its membrane insertion. ..
  48. Claggett S, O Neil Plancher M, Dunn S, Cain B. The b subunits in the peripheral stalk of F1F0 ATP synthase preferentially adopt an offset relationship. J Biol Chem. 2009;284:16531-40 pubmed publisher
    ..Under less stringent reaction conditions, it was also possible to detect b subunits cross-linked through identical positions, suggesting that an in-register, nonstaggered parallel conformation may also exist. ..
  49. Fillingame R, Angevine C, Dmitriev O. Mechanics of coupling proton movements to c-ring rotation in ATP synthase. FEBS Lett. 2003;555:29-34 pubmed
    ..The concerted rotation of interacting helices in subunit a and subunit c is proposed to be the mechanical force driving rotation of the c-rotor, using a mechanism akin to meshed gears. ..
  50. Sievers M, Uermösi C, Fehlmann M, Krieger S. Cloning, sequence analysis and expression of the F1F0-ATPase beta-subunit from wine lactic acid bacteria. Syst Appl Microbiol. 2003;26:350-6 pubmed
    ..SDS-PAGE and Western blot analyses confirmed that O. oeni has an ATPase beta-subunit protein which is larger in size than the corresponding molecules from the investigated strains. ..
  51. Minoletti C, Santolini J, Haraux F, Pothier J, Andre F. Rebuilt 3D structure of the chloroplast f1 ATPase-tentoxin complex. Proteins. 2002;49:302-20 pubmed
    ..These results suggest a mechanism of CF1 inhibition by one molecule of tentoxin, by the impossibility of the alpha/beta interface bearing tentoxin to pass through the ATP-loaded state. ..
  52. Tozawa K, Yagi H, Hisamatsu K, Ozawa K, Yoshida M, Akutsu H. Functions and ATP-binding responses of the twelve histidine residues in the TF1-ATPase beta subunit. J Biochem. 2001;130:527-33 pubmed
    ..1999) Biophys. J. 77, 2175-2183]. This conformational change should be one of the essential driving forces in the rotation of the alpha3beta3gamma complex. ..
  53. Zhang Q, Atreya H, Kamen D, Girvin M, Szyperski T. GFT projection NMR based resonance assignment of membrane proteins: application to subunit C of E. coli F(1)F (0) ATP synthase in LPPG micelles. J Biomol NMR. 2008;40:157-63 pubmed publisher
    ..It is shown that the 4D and 5D spectral information obtained rapidly from GFT and G(2)FT NMR experiments enables one to efficiently obtain (nearly) complete resonance assignments of membrane proteins. ..