Structural Asymmetry and Kinetic Limping of Single Rotary F-ATP Synthases

Overview

Journal Molecules

Publisher MDPI

Specialty Biology

Date 2019 Feb 2

PMID 30704145

Citations 8

Authors

Hendrik Sielaff

Seiga Yanagisawa

Wayne D Frasch

Wolfgang Junge

Michael Borsch

Affiliations

Soon will be listed here.

Abstract

F-ATP synthases use proton flow through the F domain to synthesize ATP in the F₁ domain. In , the enzyme consists of rotor subunits γε and stator subunits (αβ)₃δ₂. Subunits or (αβ)₃ alone are rotationally symmetric. However, symmetry is broken by the ₂ homodimer, which together with subunit δ, forms a single eccentric stalk connecting the membrane embedded F domain with the soluble F₁ domain, and the central rotating and curved stalk composed of subunit γε. Although each of the three catalytic binding sites in (αβ)₃ catalyzes the same set of partial reactions in the time average, they might not be fully equivalent at any moment, because the structural symmetry is broken by contact with ₂δ in F₁ and with ₂ in F. We monitored the enzyme's rotary progression during ATP hydrolysis by three single-molecule techniques: fluorescence video-microscopy with attached actin filaments, Förster resonance energy transfer between pairs of fluorescence probes, and a polarization assay using gold nanorods. We found that one dwell in the three-stepped rotary progression lasting longer than the other two by a factor of up to 1.6. This effect of the structural asymmetry is small due to the internal elastic coupling.

Citing Articles

Changes within the central stalk of E. coli FF ATP synthase observed after addition of ATP.

Sobti M, Zeng Y, Walshe J, Brown S, Ishmukhametov R, Stewart A Commun Biol. 2023; 6(1):26.

PMID: 36631659 PMC: 9834311. DOI: 10.1038/s42003-023-04414-z.

Direct observation of stepping rotation of V-ATPase reveals rigid component in coupling between V and V motors.

Otomo A, Iida T, Okuni Y, Ueno H, Murata T, Iino R Proc Natl Acad Sci U S A. 2022; 119(42):e2210204119.

PMID: 36215468 PMC: 9586324. DOI: 10.1073/pnas.2210204119.

F-F coupling and symmetry mismatch in ATP synthase resolved in every F rotation step.

Kubo S, Niina T, Takada S Biophys J. 2022; 122(14):2898-2909.

PMID: 36171725 PMC: 10397808. DOI: 10.1016/j.bpj.2022.09.034.

FF ATP synthase molecular motor mechanisms.

Frasch W, Bukhari Z, Yanagisawa S Front Microbiol. 2022; 13:965620.

PMID: 36081786 PMC: 9447477. DOI: 10.3389/fmicb.2022.965620.

F-ATPase Rotary Mechanism: Interpreting Results of Diverse Experimental Modes With an Elastic Coupling Theory.

Volkan-Kacso S, Marcus R Front Microbiol. 2022; 13:861855.

PMID: 35531282 PMC: 9072658. DOI: 10.3389/fmicb.2022.861855.

References

Brandt K, Maiwald S, Herkenhoff-Hesselmann B, Gnirss K, Greie J, Dunn S . Individual interactions of the b subunits within the stator of the Escherichia coli ATP synthase. J Biol Chem. 2013; 288(34):24465-79. PMC: 3750146. DOI: 10.1074/jbc.M113.465633. View

Girvin M, Rastogi V, Abildgaard F, Markley J, Fillingame R . Solution structure of the transmembrane H+-transporting subunit c of the F1F0 ATP synthase. Biochemistry. 1998; 37(25):8817-24. DOI: 10.1021/bi980511m. View

Pogoryelov D, Yildiz O, Faraldo-Gomez J, Meier T . High-resolution structure of the rotor ring of a proton-dependent ATP synthase. Nat Struct Mol Biol. 2009; 16(10):1068-73. DOI: 10.1038/nsmb.1678. View

Toei M, Noji H . Single-molecule analysis of F0F1-ATP synthase inhibited by N,N-dicyclohexylcarbodiimide. J Biol Chem. 2013; 288(36):25717-25726. PMC: 3764779. DOI: 10.1074/jbc.M113.482455. View

Hahn A, Vonck J, Mills D, Meier T, Kuhlbrandt W . Structure, mechanism, and regulation of the chloroplast ATP synthase. Science. 2018; 360(6389). PMC: 7116070. DOI: 10.1126/science.aat4318. View

Martin J, Ishmukhametov R, Hornung T, Ahmad Z, Frasch W . Anatomy of F1-ATPase powered rotation. Proc Natl Acad Sci U S A. 2014; 111(10):3715-20. PMC: 3956197. DOI: 10.1073/pnas.1317784111. View

Meier T, Krah A, Bond P, Pogoryelov D, Diederichs K, Faraldo-Gomez J . Complete ion-coordination structure in the rotor ring of Na+-dependent F-ATP synthases. J Mol Biol. 2009; 391(2):498-507. DOI: 10.1016/j.jmb.2009.05.082. View

Mao H, Weber J . Identification of the betaTP site in the x-ray structure of F1-ATPase as the high-affinity catalytic site. Proc Natl Acad Sci U S A. 2007; 104(47):18478-83. PMC: 2141802. DOI: 10.1073/pnas.0709322104. View

von Ballmoos C, Wiedenmann A, Dimroth P . Essentials for ATP synthesis by F1F0 ATP synthases. Annu Rev Biochem. 2009; 78:649-72. DOI: 10.1146/annurev.biochem.78.081307.104803. View

10.

Hirata T, Iwamoto-Kihara A, Sun-Wada G, Okajima T, Wada Y, Futai M . Subunit rotation of vacuolar-type proton pumping ATPase: relative rotation of the G and C subunits. J Biol Chem. 2003; 278(26):23714-9. DOI: 10.1074/jbc.M302756200. View

11.

Weber J, Senior A . Catalytic mechanism of F1-ATPase. Biochim Biophys Acta. 1997; 1319(1):19-58. DOI: 10.1016/s0005-2728(96)00121-1. View

12.

Borsch M, Diez M, Zimmermann B, Reuter R, Graber P . Stepwise rotation of the gamma-subunit of EF(0)F(1)-ATP synthase observed by intramolecular single-molecule fluorescence resonance energy transfer. FEBS Lett. 2002; 527(1-3):147-52. DOI: 10.1016/s0014-5793(02)03198-8. View

13.

Singh D, Sielaff H, Sundararaman L, Bhushan S, Gruber G . The stimulating role of subunit F in ATPase activity inside the A1-complex of the Methanosarcina mazei Gö1 A1AO ATP synthase. Biochim Biophys Acta. 2015; 1857(2):177-187. DOI: 10.1016/j.bbabio.2015.12.003. View

14.

Martin J, Hudson J, Hornung T, Frasch W . Fo-driven Rotation in the ATP Synthase Direction against the Force of F1 ATPase in the FoF1 ATP Synthase. J Biol Chem. 2015; 290(17):10717-28. PMC: 4409238. DOI: 10.1074/jbc.M115.646430. View

15.

Panke O, Cherepanov D, Gumbiowski K, Engelbrecht S, Junge W . Viscoelastic dynamics of actin filaments coupled to rotary F-ATPase: angular torque profile of the enzyme. Biophys J. 2001; 81(3):1220-33. PMC: 1301604. DOI: 10.1016/S0006-3495(01)75780-3. View

16.

Weber J, Muharemagic A, Wilke-Mounts S, Senior A . Analysis of sequence determinants of F1Fo-ATP synthase in the N-terminal region of alpha subunit for binding of delta subunit. J Biol Chem. 2004; 279(24):25673-9. DOI: 10.1074/jbc.M402738200. View

17.

Sambongi Y, Iko Y, Tanabe M, Omote H, Ueda I, Yanagida T . Mechanical rotation of the c subunit oligomer in ATP synthase (F0F1): direct observation. Science. 1999; 286(5445):1722-4. DOI: 10.1126/science.286.5445.1722. View

18.

Guo H, Rubinstein J . Cryo-EM of ATP synthases. Curr Opin Struct Biol. 2018; 52:71-79. DOI: 10.1016/j.sbi.2018.08.005. View

19.

Duser M, Bi Y, Zarrabi N, Dunn S, Borsch M . The proton-translocating a subunit of F0F1-ATP synthase is allocated asymmetrically to the peripheral stalk. J Biol Chem. 2008; 283(48):33602-10. PMC: 2662277. DOI: 10.1074/jbc.M805170200. View

20.

Noji H, Nishiura M, Muneyuki E, Hara K, Yasuda R, Kinosita Jr K . Pause and rotation of F(1)-ATPase during catalysis. Proc Natl Acad Sci U S A. 2001; 98(24):13649-54. PMC: 61095. DOI: 10.1073/pnas.241365698. View