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PMID: 22353718 Published · epublish English Journal Article Research Support, Non-U.S. Gov't

The dynamic stator stalk of rotary ATPases.

Nature communications ·Vol. 3 ·2012-02-21 ·Pages 687

Stewart AG, Lee LK, Donohoe M, Chaston JJ, Stock D

Abstract

Rotary ATPases couple ATP hydrolysis/synthesis with proton translocation across biological membranes and so are central components of the biological energy conversion machinery. Their peripheral stalks are essential components that counteract torque generated by rotation of the central stalk during ATP synthesis or hydrolysis. Here we present a 2.25-Å resolution crystal structure of the peripheral stalk from Thermus thermophilus A-type ATPase/synthase. We identify bending and twisting motions inherent within the structure that accommodate and complement a radial wobbling of the ATPase headgroup as it progresses through its catalytic cycles, while still retaining azimuthal stiffness necessary to counteract rotation of the central stalk. The conformational freedom of the peripheral stalk is dictated by its unusual right-handed coiled-coil architecture, which is in principle conserved across all rotary ATPases. In context of the intact enzyme, the dynamics of the peripheral stalks provides a potential mechanism for cooperativity between distant parts of rotary ATPases.

MeSH Terms
Adenosine Triphosphatases/chemistry,metabolism Crystallography, X-Ray Models, Molecular Protein Structure, Quaternary Protein Structure, Tertiary Protein Subunits/chemistry,metabolism Thermus thermophilus/cytology,enzymology
Chemicals
Protein Subunits Adenosine Triphosphatases
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Stewart Alastair G
Structural and Computational Biology Division, The Victor Chang Cardiac Research Institute, Darlinghurst, Australia.
Lee Lawrence K
Donohoe Mhairi
Chaston Jessica J
Stock Daniela
References (60)
60 references, click to expand
  1. Solubilization of green plant thylakoid membranes with n-dodecyl-alpha,D-maltoside. Implications for the structural organization of the Photosystem II, Photosystem I, ATP synthase and cytochrome b6 f complexes.
    Photosynth Res. 2000;64(2-3):155-66 PMID: 16228454
  2. Scaling and assessment of data quality.
    Acta Crystallogr D Biol Crystallogr. 2006 Jan;62(Pt 1):72-82 PMID: 16369096
  3. A change in the radius of rotation of F1-ATPase indicates a tilting motion of the central shaft.
    Biophys J. 2011 Nov 2;101(9):2201-6 PMID: 22067159
  4. A different conformation for EGC stator subcomplex in solution and in the assembled yeast V-ATPase: possible implications for regulatory disassembly.
    Structure. 2008 Dec 10;16(12):1789-98 PMID: 19081055
  5. Structural divergence of the rotary ATPases.
    Q Rev Biophys. 2011 Aug;44(3):311-56 PMID: 21426606
  6. Structure of the mitochondrial ATP synthase by electron cryomicroscopy.
    EMBO J. 2003 Dec 1;22(23):6182-92 PMID: 14633978
  7. Structure of the ATP synthase catalytic complex (F(1)) from Escherichia coli in an autoinhibited conformation.
    Nat Struct Mol Biol. 2011 Jun;18(6):701-7 PMID: 21602818
  8. Optimal description of a protein structure in terms of multiple groups undergoing TLS motion.
    Acta Crystallogr D Biol Crystallogr. 2006 Apr;62(Pt 4):439-50 PMID: 16552146
  9. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions.
    Acta Crystallogr D Biol Crystallogr. 2004 Dec;60(Pt 12 Pt 1):2256-68 PMID: 15572779
  10. Three-dimensional structure of A1A0 ATP synthase from the hyperthermophilic archaeon Pyrococcus furiosus by electron microscopy.
    J Biol Chem. 2009 Apr 10;284(15):10110-9 PMID: 19203996
  11. VMD: visual molecular dynamics.
    J Mol Graph. 1996 Feb;14(1):33-8, 27-8 PMID: 8744570
  12. UCSF Chimera--a visualization system for exploratory research and analysis.
    J Comput Chem. 2004 Oct;25(13):1605-12 PMID: 15264254
  13. Two rotary motors in F-ATP synthase are elastically coupled by a flexible rotor and a stiff stator stalk.
    Proc Natl Acad Sci U S A. 2011 Mar 8;108(10):3924-9 PMID: 21368147
  14. MolProbity: all-atom structure validation for macromolecular crystallography.
    Acta Crystallogr D Biol Crystallogr. 2010 Jan;66(Pt 1):12-21 PMID: 20057044
  15. The structure of the membrane extrinsic region of bovine ATP synthase.
    Proc Natl Acad Sci U S A. 2009 Dec 22;106(51):21597-601 PMID: 19995987
  16. Three-dimensional structure of the intact Thermus thermophilus H+-ATPase/synthase by electron microscopy.
    Structure. 2004 Oct;12(10):1789-98 PMID: 15458628
  17. REFMAC5 dictionary: organization of prior chemical knowledge and guidelines for its use.
    Acta Crystallogr D Biol Crystallogr. 2004 Dec;60(Pt 12 Pt 1):2184-95 PMID: 15572771
  18. Normal mode analysis of macromolecular motions in a database framework: developing mode concentration as a useful classifying statistic.
    Proteins. 2002 Sep 1;48(4):682-95 PMID: 12211036
  19. ATP synthase--a marvellous rotary engine of the cell.
    Nat Rev Mol Cell Biol. 2001 Sep;2(9):669-77 PMID: 11533724
  20. The evolution of A-, F-, and V-type ATP synthases and ATPases: reversals in function and changes in the H+/ATP coupling ratio.
    FEBS Lett. 2004 Oct 8;576(1-2):1-4 PMID: 15473999
  21. Structure-function relationships of A-, F- and V-ATPases.
    J Exp Biol. 2001 Aug;204(Pt 15):2597-605 PMID: 11533110
  22. Structure of intact Thermus thermophilus V-ATPase by cryo-EM reveals organization of the membrane-bound V(O) motor.
    Proc Natl Acad Sci U S A. 2010 Jan 26;107(4):1367-72 PMID: 20080582
  23. Structural changes linked to proton translocation by subunit c of the ATP synthase.
    Nature. 1999 Nov 18;402(6759):263-8 PMID: 10580496
  24. Novel features of the rotary catalytic mechanism revealed in the structure of yeast F1 ATPase.
    EMBO J. 2006 Nov 15;25(22):5433-42 PMID: 17082766
  25. Rotor architecture in the yeast and bovine F1-c-ring complexes of F-ATP synthase.
    J Struct Biol. 2012 Feb;177(2):490-7 PMID: 22119846
  26. Scalable molecular dynamics with NAMD.
    J Comput Chem. 2005 Dec;26(16):1781-802 PMID: 16222654
  27. Novel features in the structure of bovine ATP synthase.
    J Mol Biol. 1999 Jul 9;290(2):379-84 PMID: 10390338
  28. ATP hydrolysis and synthesis of a rotary motor V-ATPase from Thermus thermophilus.
    J Biol Chem. 2008 Jul 25;283(30):20789-96 PMID: 18492667
  29. Domain architecture of the stator complex of the A1A0-ATP synthase from Thermoplasma acidophilum.
    J Biol Chem. 2009 May 1;284(18):12031-40 PMID: 19234304
  30. Dodecamer rotor ring defines H+/ATP ratio for ATP synthesis of prokaryotic V-ATPase from Thermus thermophilus.
    Proc Natl Acad Sci U S A. 2007 Dec 18;104(51):20256-61 PMID: 18077374
  31. ElNemo: a normal mode web server for protein movement analysis and the generation of templates for molecular replacement.
    Nucleic Acids Res. 2004 Jul 1;32(Web Server issue):W610-4 PMID: 15215461
  32. On the structure of the stator of the mitochondrial ATP synthase.
    EMBO J. 2006 Jun 21;25(12):2911-8 PMID: 16791136
  33. ATP synthase's second stalk comes into focus.
    Nature. 1998 May 7;393(6680):29 PMID: 9590688
  34. Presenting your structures: the CCP4mg molecular-graphics software.
    Acta Crystallogr D Biol Crystallogr. 2011 Apr;67(Pt 4):386-94 PMID: 21460457
  35. Crystal structure of the cytoplasmic N-terminal domain of subunit I, a homolog of subunit a, of V-ATPase.
    J Mol Biol. 2011 Sep 9;412(1):14-21 PMID: 21787787
  36. ATP synthase b subunit dimerization domain: a right-handed coiled coil with offset helices.
    J Mol Biol. 2006 Dec 8;364(4):735-46 PMID: 17028022
  37. Function, structure and regulation of the vacuolar (H+)-ATPases.
    Arch Biochem Biophys. 2008 Aug 1;476(1):33-42 PMID: 18406336
  38. Stoichiometry of the peripheral stalk subunits E and G of yeast V1-ATPase determined by mass spectrometry.
    J Biol Chem. 2008 Feb 8;283(6):3329-3337 PMID: 18055462
  39. Crystal structure of the Mg·ADP-inhibited state of the yeast F1c10-ATP synthase.
    J Biol Chem. 2010 Sep 17;285(38):29502-10 PMID: 20610387
  40. The integration of macromolecular diffraction data.
    Acta Crystallogr D Biol Crystallogr. 2006 Jan;62(Pt 1):48-57 PMID: 16369093
  41. Coot: model-building tools for molecular graphics.
    Acta Crystallogr D Biol Crystallogr. 2004 Dec;60(Pt 12 Pt 1):2126-32 PMID: 15572765
  42. Structure of the yeast vacuolar ATPase.
    J Biol Chem. 2008 Dec 19;283(51):35983-95 PMID: 18955482
  43. [27] Maximum-likelihood heavy-atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods.
    Methods Enzymol. 1997;276:472-494 PMID: 27799110
  44. PHENIX: a comprehensive Python-based system for macromolecular structure solution.
    Acta Crystallogr D Biol Crystallogr. 2010 Feb;66(Pt 2):213-21 PMID: 20124702
  45. Structure of bovine mitochondrial F(1)-ATPase with nucleotide bound to all three catalytic sites: implications for the mechanism of rotary catalysis.
    Cell. 2001 Aug 10;106(3):331-41 PMID: 11509182
  46. The structure of the peripheral stalk of Thermus thermophilus H+-ATPase/synthase.
    Nat Struct Mol Biol. 2010 Mar;17(3):373-8 PMID: 20173764
  47. XDS.
    Acta Crystallogr D Biol Crystallogr. 2010 Feb;66(Pt 2):125-32 PMID: 20124692
  48. A rotary molecular motor that can work at near 100% efficiency.
    Philos Trans R Soc Lond B Biol Sci. 2000 Apr 29;355(1396):473-89 PMID: 10836501
  49. Connecting stalks in V-type ATPase.
    Nature. 1999 Sep 2;401(6748):37-8 PMID: 10485704
  50. Subunit arrangement in V-ATPase from Thermus thermophilus.
    J Biol Chem. 2003 Oct 24;278(43):42686-91 PMID: 12913005
  51. Bioenergetic cost of making an adenosine triphosphate molecule in animal mitochondria.
    Proc Natl Acad Sci U S A. 2010 Sep 28;107(39):16823-7 PMID: 20847295
  52. Cryo-electron microscopy of the vacuolar ATPase motor reveals its mechanical and regulatory complexity.
    J Mol Biol. 2009 Mar 6;386(4):989-99 PMID: 19244615
  53. Inter-subunit interaction and quaternary rearrangement defined by the central stalk of prokaryotic V1-ATPase.
    EMBO Rep. 2009 Nov;10(11):1228-34 PMID: 19779483
  54. Crystal structure of a central stalk subunit C and reversible association/dissociation of vacuole-type ATPase.
    Proc Natl Acad Sci U S A. 2004 Jan 6;101(1):59-64 PMID: 14684831
  55. Stoichiometry and localization of the stator subunits E and G in Thermus thermophilus H+-ATPase/synthase.
    J Biol Chem. 2008 Feb 1;283(5):2595-603 PMID: 18055467
  56. Torque generation and elastic power transmission in the rotary F(O)F(1)-ATPase.
    Nature. 2009 May 21;459(7245):364-70 PMID: 19458712
  57. Regulatory interplay between proton motive force, ADP, phosphate, and subunit epsilon in bacterial ATP synthase.
    J Biol Chem. 2007 Jan 5;282(1):764-72 PMID: 17092944
  58. Direct visualisation of conformational changes in EF(0)F(1) by electron microscopy.
    J Mol Biol. 2000 Feb 18;296(2):449-57 PMID: 10669600
  59. Toward the structural genomics of complexes: crystal structure of a PE/PPE protein complex from Mycobacterium tuberculosis.
    Proc Natl Acad Sci U S A. 2006 May 23;103(21):8060-5 PMID: 16690741
  60. Molecular architecture of the rotary motor in ATP synthase.
    Science. 1999 Nov 26;286(5445):1700-5 PMID: 10576729
Article Info
Journal
Nature communications
Abbr.
Nat Commun
ISSN
2041-1723
DOI
10.1038/ncomms1693
Published
2012-02-21
Epub
2012-00-21
Pages
687
Language
English
Region
England
NLM ID
101528555
PMCID
PMC3293630
Subset
IM
Databases
PDB
3V6I
External Links
PubMed source DOI: 10.1038/ncomms1693 PMC Full Text View journal details
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