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Inventing the dynamo machine: the evolution of the F-type and V-type ATPases - Nature Reviews Microbiology

  • ️Koonin, Eugene V.
  • ️Thu Nov 01 2007
  • Nelson, N. Structure, function, and evolution of proton-ATPases. Plant Physiol. 86, 1–3 (1988).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drory, O. & Nelson, N. The emerging structure of vacuolar ATPases. Physiology (Bethesda) 21, 317–325 (2006).

    Article  CAS  PubMed  Google Scholar 

  • Gogarten, J. P. et al. Evolution of the vacuolar H+-ATPase: implications for the origin of eukaryotes. Proc. Natl Acad. Sci. USA 86, 6661–6665 (1989).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gogarten, J. P., Starke, T., Kibak, H., Fishman, J. & Taiz, L. Evolution and isoforms of V-ATPase subunits. J. Exp. Biol. 172, 137–147 (1992).

    CAS  PubMed  Google Scholar 

  • Boyer, P. D. The ATP synthase — a splendid molecular machine. Annu. Rev. Biochem. 66, 717–749 (1997).

    Article  CAS  PubMed  Google Scholar 

  • Junge, W. & Nelson, N. Nature's rotary electromotors. Science 308, 642–644 (2005).

    Article  CAS  PubMed  Google Scholar 

  • Perzov, N., Padler-Karavani, V., Nelson, H. & Nelson, N. Features of V-ATPases that distinguish them from F-ATPases. FEBS Lett. 504, 223–228 (2001).

    Article  CAS  PubMed  Google Scholar 

  • Nakanishi-Matsui, M. & Futai, M. Stochastic proton pumping ATPases: from single molecules to diverse physiological roles. IUBMB Life 58, 318–322 (2006).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hilario, E. & Gogarten, J. P. Horizontal transfer of ATPase genes — the tree of life becomes a net of life. Biosystems 31, 111–119 (1993).

    Article  CAS  PubMed  Google Scholar 

  • Hilario, E. & Gogarten, J. P. The prokaryote-to-eukaryote transition reflected in the evolution of the V/F/A-ATPase catalytic and proteolipid subunits. J. Mol. Evol. 46, 703–715 (1998).

    Article  CAS  PubMed  Google Scholar 

  • Nesbo, C. L. & Doolittle, W. F. Targeting clusters of transferred genes in Thermotoga maritima. Environ. Microbiol. 5, 1144–1154 (2003).

    Article  CAS  PubMed  Google Scholar 

  • Stock, D., Gibbons, C., Arechaga, I., Leslie, A. G. & Walker, J. E. The rotary mechanism of ATP synthase. Curr. Opin. Struct. Biol. 10, 672–679 (2000).

    Article  CAS  PubMed  Google Scholar 

  • Iwata, M. et al. Crystal structure of a central stalk subunit C and reversible association/dissociation of vacuole-type ATPase. Proc. Natl Acad. Sci. USA 101, 59–64 (2004).

    Article  CAS  PubMed  Google Scholar 

  • Bernal, R. A. & Stock, D. Three-dimensional structure of the intact Thermus thermophilus H+-ATPase/synthase by electron microscopy. Structure 12, 1789–1798 (2004).

    Article  CAS  PubMed  Google Scholar 

  • Makyio, H. et al. Structure of a central stalk subunit F of prokaryotic V-type ATPase/synthase from Thermus thermophilus. EMBO J. 24, 3974–3983 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Schafer, I. B. et al. Crystal structure of the archaeal A1A0 ATP synthase subunit B from Methanosarcina mazei Go1: implications of nucleotide-binding differences in the major A1A0 subunits A and B. J. Mol. Biol. 358, 725–740 (2006).

    Article  PubMed  CAS  Google Scholar 

  • Wilkens, S. Rotary molecular motors. Adv. Protein Chem. 71, 345–382 (2005).

    Article  CAS  PubMed  Google Scholar 

  • Gibbons, C., Montgomery, M. G., Leslie, A. G. & Walker, J. E. The structure of the central stalk in bovine F1-ATPase at 2.4 Å resolution. Nature Struct. Biol. 7, 1055–1061 (2000).

    Article  CAS  PubMed  Google Scholar 

  • Noji, H., Yasuda, R., Yoshida, M. & Kinosita, K. Jr. Direct observation of the rotation of F1-ATPase. Nature 386, 299–302 (1997).

    Article  CAS  PubMed  Google Scholar 

  • Junge, W., Lill, H. & Engelbrecht, S. ATP synthase: an electrochemical transducer with rotatory mechanics. Trends Biochem. Sci. 22, 420–423 (1997).

    Article  CAS  PubMed  Google Scholar 

  • Panke, O., Gumbiowski, K., Junge, W. & Engelbrecht, S. F-ATPase: specific observation of the rotating c subunit oligomer of EF0EF1 . FEBS Lett. 472, 34–38 (2000).

    Article  CAS  PubMed  Google Scholar 

  • Xing, J., Liao, J. C. & Oster, G. Making ATP. Proc. Natl Acad. Sci. USA 102, 16539–16546 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cherepanov, D. A., Mulkidjanian, A. Y. & Junge, W. Transient accumulation of elastic energy in proton translocating ATP synthase. FEBS Lett. 449, 1–6 (1999).

    Article  CAS  PubMed  Google Scholar 

  • Feniouk, B. A. et al. The proton-driven rotor of ATP synthase: ohmic conductance (10 fS), and absence of voltage gating. Biophys. J. 86, 4094–4109 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mulkidjanian, A. Y. Proton in the well and through the desolvation barrier. Biochim. Biophys. Acta 1757, 415–427 (2006).

    Article  CAS  PubMed  Google Scholar 

  • Deckers-Hebestreit, G., Greie, J., Stalz, W. & Altendorf, K. The ATP synthase of Escherichia coli: structure and function of F0 subunits. Biochim. Biophys. Acta 1458, 364–373 (2000).

    Article  CAS  PubMed  Google Scholar 

  • Fillingame, R. H., Jiang, W. & Dmitriev, O. Y. Coupling H+ transport to rotary catalysis in F-type ATP synthases: structure and organization of the transmembrane rotary motor. J. Exp. Biol. 203, 9–17 (2000).

    CAS  PubMed  Google Scholar 

  • Beyenbach, K. W. & Wieczorek, H. The V-type H+ ATPase: molecular structure and function, physiological roles and regulation. J. Exp. Biol. 209, 577–589 (2006).

    Article  CAS  PubMed  Google Scholar 

  • Walker, J. E. & Cozens, A. L. Evolution of ATP synthase. Chem. Scr. 26B, 263–272 (1986).

    CAS  Google Scholar 

  • Walker, J. E. ATP synthesis by rotary catalysis (Nobel lecture). Angew. Chem. Int. Ed. Engl. 37, 2309–2319 (1998).

    Article  Google Scholar 

  • Supekova, L., Supek, F. & Nelson, N. The Saccharomyces cerevisiae VMA10 is an intron-containing gene encoding a novel 13-kDa subunit of vacuolar H+-ATPase. J. Biol. Chem. 270, 13726–13732 (1995).

    Article  CAS  PubMed  Google Scholar 

  • Pallen, M. J., Bailey, C. M. & Beatson, S. A. Evolutionary links between FliH/YscL-like proteins from bacterial type III secretion systems and second-stalk components of the F0F1 and vacuolar ATPases. Protein Sci. 15, 935–941 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lolkema, J. S., Chaban, Y. & Boekema, E. J. Subunit composition, structure, and distribution of bacterial V-type ATPases. J. Bioenerg. Biomembr. 35, 323–335 (2003).

    Article  CAS  PubMed  Google Scholar 

  • Kawano, M., Igarashi, K., Yamato, I. & Kakinuma, Y. Arginine residue at position 573 in Enterococcus hirae vacuolar-type ATPase NtpI subunit plays a crucial role in Na+ translocation. J. Biol. Chem. 277, 24405–24410 (2002).

    Article  CAS  PubMed  Google Scholar 

  • Kawasaki-Nishi, S., Nishi, T. & Forgac, M. Arg-735 of the 100-kDa subunit a of the yeast V-ATPase is essential for proton translocation. Proc. Natl Acad. Sci. USA 98, 12397–12402 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Adelman, J. L. et al. Mechanochemistry of transcription termination factor Rho. Mol. Cell 22, 611–621 (2006).

    Article  CAS  PubMed  Google Scholar 

  • Skordalakes, E. & Berger, J. M. Structure of the Rho transcription terminator: mechanism of mRNA recognition and helicase loading. Cell 114, 135–146 (2003).

    Article  CAS  PubMed  Google Scholar 

  • Patel, S. S. & Picha, K. M. Structure and function of hexameric helicases. Annu. Rev. Biochem. 69, 651–697 (2000).

    Article  CAS  PubMed  Google Scholar 

  • Gomis-Ruth, F. X. et al. The bacterial conjugation protein TrwB resembles ring helicases and F1-ATPase. Nature 409, 637–641 (2001).

    Article  CAS  PubMed  Google Scholar 

  • Cabezon, E. & de la Cruz, F. TrwB: an F1-ATPase-like molecular motor involved in DNA transport during bacterial conjugation. Res. Microbiol. 157, 299–305 (2006).

    Article  CAS  PubMed  Google Scholar 

  • Aussel, L. et al. FtsK is a DNA motor protein that activates chromosome dimer resolution by switching the catalytic state of the XerC and XerD recombinases. Cell 108, 195–205 (2002).

    Article  CAS  PubMed  Google Scholar 

  • Iyer, L. M., Makarova, K. S., Koonin, E. V. & Aravind, L. Comparative genomics of the FtsK-HerA superfamily of pumping ATPases: implications for the origins of chromosome segregation, cell division and viral capsid packaging. Nucleic Acids Res. 32, 5260–5279 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Juuti, J. T., Bamford, D. H., Tuma, R. & Thomas, G. J. Jr. Structure and NTPase activity of the RNA-translocating protein (P4) of bacteriophage phi 6. J. Mol. Biol. 279, 347–359 (1998).

    Article  CAS  PubMed  Google Scholar 

  • Pirttimaa, M. J., Paatero, A. O., Frilander, M. J. & Bamford, D. H. Nonspecific nucleoside triphosphatase P4 of double-stranded RNA bacteriophage phi6 is required for single-stranded RNA packaging and transcription. J. Virol. 76, 10122–10127 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kainov, D. E. et al. RNA packaging device of double-stranded RNA bacteriophages, possibly as simple as hexamer of P4 protein. J. Biol. Chem. 278, 48084–48091 (2003).

    Article  CAS  PubMed  Google Scholar 

  • Wall, D. & Kaiser, D. Type IV pili and cell motility. Mol. Microbiol. 32, 1–10 (1999).

    Article  CAS  PubMed  Google Scholar 

  • Merz, A. J., So, M. & Sheetz, M. P. Pilus retraction powers bacterial twitching motility. Nature 407, 98–102 (2000).

    Article  CAS  PubMed  Google Scholar 

  • Kainov, D. E., Tuma, R. & Mancini, E. J. Hexameric molecular motors: P4 packaging ATPase unravels the mechanism. Cell. Mol. Life Sci. 63, 1095–1105 (2006).

    Article  CAS  PubMed  Google Scholar 

  • Laskey, R. A. & Madine, M. A. A rotary pumping model for helicase function of MCM proteins at a distance from replication forks. EMBO Rep. 4, 26–30 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee, J. Y. & Yang, W. UvrD helicase unwinds DNA one base pair at a time by a two-part power stroke. Cell 127, 1349–1360 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Skordalakes, E. & Berger, J. M. Structural insights into RNA-dependent ring closure and ATPase activation by the Rho termination factor. Cell 127, 553–564 (2006).

    Article  CAS  PubMed  Google Scholar 

  • Vogler, A. P., Homma, M., Irikura, V. M. & Macnab, R. M. Salmonella typhimurium mutants defective in flagellar filament regrowth and sequence similarity of FliI to F0F1, vacuolar, and archaebacterial ATPase subunits. J. Bacteriol. 173, 3564–3572 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aizawa, S. I. Bacterial flagella and type III secretion systems. FEMS Microbiol. Lett. 202, 157–164 (2001).

    Article  CAS  PubMed  Google Scholar 

  • Blocker, A., Komoriya, K. & Aizawa, S. Type III secretion systems and bacterial flagella: insights into their function from structural similarities. Proc. Natl Acad. Sci. USA 100, 3027–3030 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tato, I., Zunzunegui, S., de la Cruz, F. & Cabezon, E. TrwB, the coupling protein involved in DNA transport during bacterial conjugation, is a DNA-dependent ATPase. Proc. Natl Acad. Sci. USA 102, 8156–8161 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Philippe, H. & Laurent, J. How good are deep phylogenetic trees? Curr. Opin. Genet. Dev. 8, 616–623 (1998).

    Article  CAS  PubMed  Google Scholar 

  • Gribaldo, S. & Philippe, H. Ancient phylogenetic relationships. Theor. Popul. Biol. 61, 391–408 (2002).

    Article  PubMed  Google Scholar 

  • Yu, X. & Egelman, E. H. The RecA hexamer is a structural homologue of ring helicases. Nature Struct. Biol. 4, 101–104 (1997).

    Article  CAS  PubMed  Google Scholar 

  • Iyer, L. M., Leipe, D. D., Koonin, E. V. & Aravind, L. Evolutionary history and higher order classification of AAA+ ATPases. J. Struct. Biol. 146, 11–31 (2004).

    Article  CAS  PubMed  Google Scholar 

  • Pohlschroder, M., Hartmann, E., Hand, N. J., Dilks, K. & Haddad, A. Diversity and evolution of protein translocation. Annu. Rev. Microbiol. 59, 91–111 (2005).

    Article  CAS  PubMed  Google Scholar 

  • Wilharm, G., Dittmann, S., Schmid, A. & Heesemann, J. On the role of specific chaperones, the specific ATPase, and the proton motive force in type III secretion. Int. J. Med. Microbiol. 297, 27–36 (2007).

    Article  CAS  PubMed  Google Scholar 

  • Wilharm, G., Lehmann, V., Neumayer, W., Trcek, J. & Heesemann, J. Yersinia enterocolitica type III secretion: evidence for the ability to transport proteins that are folded prior to secretion. BMC Microbiol. 4, 27 (2004).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Koonin, E. V. & Gorbalenya, A. E. Autogenous translation regulation by Escherichia coli ATPase SecA may be mediated by an intrinsic RNA helicase activity of this protein. FEBS Lett. 298, 6–8 (1992).

    Article  CAS  PubMed  Google Scholar 

  • Keramisanou, D. et al. Disorder-order folding transitions underlie catalysis in the helicase motor of SecA. Nature Struct. Mol. Biol. 13, 594–602 (2006).

    Article  CAS  Google Scholar 

  • Martin, W. & Russell, M. J. On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells. Phil. Trans. R. Soc. Lond. B 358, 59–85 (2003).

    Article  CAS  Google Scholar 

  • Pereto, J., Lopez-Garcia, P. & Moreira, D. Ancestral lipid biosynthesis and early membrane evolution. Trends Biochem. Sci. 29, 469–477 (2004).

    Article  CAS  PubMed  Google Scholar 

  • Mushegian, A. R. & Koonin, E. V. A minimal gene set for cellular life derived by comparison of complete bacterial genomes. Proc. Natl Acad. Sci. USA 93, 10268–10273 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edgell, D. R. & Doolittle, W. F. Archaea and the origin(s) of DNA replication proteins. Cell 89, 995–998 (1997).

    Article  CAS  PubMed  Google Scholar 

  • Leipe, D. D., Aravind, L. & Koonin, E. V. Did DNA replication evolve twice independently? Nucleic Acids Res. 27, 3389–3401 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koonin, E. V. & Martin, W. On the origin of genomes and cells within inorganic compartments. Trends Genet. 21, 647–654 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jekely, G. Did the last common ancestor have a biological membrane? Biol. Direct 1, 35 (2006).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Deamer, D. W. The first living systems: a bioenergetic perspective. Microbiol. Mol. Biol. Rev. 61, 239–261 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ourisson, G. & Nakatani, Y. The terpenoid theory of the origin of cellular life: the evolution of terpenoids to cholesterol. Chem. Biol. 1, 11–23 (1994).

    Article  CAS  PubMed  Google Scholar 

  • Gotoh, M. et al. Membrane properties of branched polyprenyl phosphates, postulated as primitive membrane constituents. Chem. Biodivers. 3, 434–455 (2006).

    Article  CAS  PubMed  Google Scholar 

  • Woese, C. R. On the evolution of cells. Proc. Natl Acad. Sci. USA 99, 8742–8747 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vetsigian, K., Woese, C. & Goldenfeld, N. Collective evolution and the genetic code. Proc. Natl Acad. Sci. USA 103, 10696–10701 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koonin, E. V., Senkevich, T. G. & Dolja, V. V. The ancient virus world and evolution of cells. Biol. Direct 1, 29 (2006).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kainov, D. E., Lisal, J., Bamford, D. H. & Tuma, R. Packaging motor from double-stranded RNA bacteriophage phi12 acts as an obligatory passive conduit during transcription. Nucleic Acids Res. 32, 3515–3521 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ouzounis, C. A., Kunin, V., Darzentas, N. & Goldovsky, L. A minimal estimate for the gene content of the last universal common ancestor — exobiology from a terrestrial perspective. Res. Microbiol. 157, 57–68 (2006).

    Article  CAS  PubMed  Google Scholar 

  • Koonin, E. V., Mushegian, A. R. & Bork, P. Non-orthologous gene displacement. Trends Genet. 12, 334–336 (1996).

    Article  CAS  PubMed  Google Scholar 

  • Senior, A. E., Muharemagic, A. & Wilke-Mounts, S. Assembly of the stator in Escherichia coli ATP synthase. Complexation of α subunit with other F1 subunits is prerequisite for δ subunit binding to the N-terminal region of α. Biochemistry 45, 15893–15902 (2006).

    Article  CAS  PubMed  Google Scholar 

  • Mueller, D. M. Partial assembly of the yeast mitochondrial ATP synthase. J. Bioenerg. Biomembr. 32, 391–400 (2000).

    Article  CAS  PubMed  Google Scholar 

  • Puri, N., Lai-Zhang, J., Meier, S. & Mueller, D. M. Expression of bovine F1-ATPase with functional complementation in yeast Saccharomyces cerevisiae. J. Biol. Chem. 280, 22418–22424 (2005).

    Article  CAS  PubMed  Google Scholar 

  • Minamino, T. & Namba, K. Self-assembly and type III protein export of the bacterial flagellum. J. Mol. Microbiol. Biotechnol. 7, 5–17 (2004).

    Article  CAS  PubMed  Google Scholar 

  • 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. USA 104, 485–490 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Adachi, J. & Hasegawa, M. MOLPHY: programs for Molecular Phylogenetics (Institute of Statistical Mathematics, Tokyo, 1992).

    Google Scholar 

  • Hasegawa, M., Kishino, H. & Saitou, N. On the maximum likelihood method in molecular phylogenetics. J. Mol. Evol. 32, 443–445.

  • Cuff, J. A., Clamp, M. E., Siddiqui, A. S., Finlay, M. & Barton, G. J. J Pred: a consensus secondary structure prediction server. Bioinformatics 14, 892–893 (1998).

    Article  CAS  PubMed  Google Scholar 

  • Rost, B., Yachdav, G. & Liu, J. The PredictProtein server. Nucleic Acids Res. 32, W321–326 (2004).

    CAS  Google Scholar