- Access by Xinjiang University
Design principles and optimal performance for molecular motors under realistic constraints
Phys. Rev. E 97, 022403 – Published 9 February, 2018
DOI: https://doi.org/10.1103/PhysRevE.97.022403
Abstract
The performance of a molecular motor, characterized by its power output and energy efficiency, is investigated in the motor design space spanned by the stepping rate function and the motor-track interaction potential. Analytic results and simulations show that a gating mechanism that restricts forward stepping in a narrow window in configuration space is needed for generating high power at physiologically relevant loads. By deriving general thermodynamics laws for nonequilibrium motors, we find that the maximum torque (force) at stall is less than its theoretical limit for any realistic motor-track interactions due to speed fluctuations. Our study reveals a tradeoff for the motor-track interaction: while a strong interaction generates a high power output for forward steps, it also leads to a higher probability of wasteful spontaneous back steps. Our analysis and simulations show that this tradeoff sets a fundamental limit to the maximum motor efficiency in the presence of spontaneous back steps, i.e., loose-coupling. Balancing this tradeoff leads to an optimal design of the motor-track interaction for achieving a maximum efficiency close to 1 for realistic motors that are not perfectly coupled with the energy source. Comparison with existing data and suggestions for future experiments are discussed.
Physics Subject Headings (PhySH)
Article Text
References (55)
- H. C. Berg and R. A. Anderson, Bacteria swim by rotating their flagellar filaments, Nature 245, 380 (1973).
- S. H. Larsen, J. Adler, J. J. Gargus, and R. W. Hogg, Chemomechanical coupling without atp: The source of energy for motility and chemotaxis in bacteria, Proc. Natl. Acad. Sci. USA 71, 1239 (1974).
- N. Hirota, M. Kitada, and Y. Imae, Flagellar motors of alkalophilic bacillus are powered by an electrochemical potential gradient of , FEBS Lett. 132, 278 (1981).
- H. C. Berg, The rotatory motor of bacterial flagella, Annu. Rev. Biochem. 72, 19 (2003).
- A. Parmeggiani, F. Julicher, A. Ajdari, and J. Prost, Energy transduction of isothermal ratchets: Generic aspects and specific examples close to and far from equilibrium, Phys. Rev. E 60, 2127 (1999).
- J. M. R. Parrondo and B. J. de Cisneros, Energetics of Brownian motors: A review, Appl. Phys. A 75, 179 (2002).
- R. D. Astumian, Thermodynamics and kinetics of molecular motors, Biophys. J. 98, 2401 (2010).
- Y. V. Morimoto and T. Minamino, Structure and function of the bi-directional bacterial flagellar motor, Biomolecules 4, 217 (2014).
- M. A. B. Baker, R. M. G. Hynson, L. A. Ganuelas, N. S. Mohammadi, C. W. Liew, A. A. Rey, A. P. Duff, A. E. Whitten, C. M. Jeffries, N. J. Delalez, Y. V. Morimoto, D. Stock, J. P. Armitage, A. J. Turberfield, K. Namba, R. M. Berry, and L. K. Lee, Domain-swap polymerization drives the self-assembly of the bacterial flagellar motor, Nat. Struct. Mol. Biol. 23, 197 (2016).
- Y. Asai, S. Kojima, H. Kato, N. Nishioka, I. Kawagishi, and M. Homma, Putative channel components for the fast-rotating sodium-driven flagellar motor of a marine bacterium, J. Bacteriol. 179, 5104 (1997).
- D. F. Blair and H. C. Berg, The mota protein of E. coli is a proton-conducting component of the flagellar motor, Cell 60, 439 (1990).
- K. Sato and M. Homma, Functional reconstitution of the -driven polar flagellar motor component of vibrio alginolyticus, J. Biol. Chem. 275, 5718 (2000).
- S. Kojima and D. F. Blair, Solubilization and purification of the MotA/MotB complex of Escherichia coli, Biochemistry 43, 26 (2004).
- T. Yorimitsu, M. Kojima, T. Yakushi, and M. Homma, Multimeric structure of the PomA/PomB channel complex in the -driven flagellar motor of Vibrio alginolyticus, J. Biochem. 135, 43 (2004).
- S. Y. Chun and J. S. Parkinson, Bacterial motility: Membrane topology of the Escherichia coli MotB protein, Science 239, 276 (1988).
- A. Roujeinikova, Crystal structure of the cell wall anchor domain of MotB, a stator component of the bacterial flagellar motor: Implications for peptidoglycan recognition, Proc. Natl. Acad. Sci. USA 105, 10348 (2008).
- S. M. Block and H. C. Berg, Successive incorporation of force-generating units in the bacterial rotary motor, Nature 309, 470 (1984).
- D. F. Blair and H. C. Berg, Restoration of torque in defective flagellar motors, Science 242, 1678 (1988).
- M. D. Manson, P. M. Tedesco, and H. C. Berg, Energetics of flagellar rotation in bacteria, J. Mol. Biol. 138, 541 (1980).
- S. Khan and H. C. Berg, Isotope and thermal effects in chemiosmotic coupling to the flagellar motor of streptococcus, Cell 32, 913 (1983).
- G. Lowe, M. Meister, and H. C. Berg, Rapid rotation of flagellar bundles in swimming bacteria, Nature 325, 637 (1987).
- X. Chen and H. C. Berg, Torque-speed relationship of the flagellar rotary motor of Escherichia coli, Biophys. J. 78, 1036 (2000).
- J. Yuan, K. A. Fahrner, L. Turner, and H. C. Berg, Asymmetry in the clockwise and counterclockwise rotation of the bacterial flagellar motor, Proc. Natl. Acad. Sci. USA 107, 12846 (2010).
- P. Läuger, Torque and rotation rate of the bacterial flagellar motor, Biophys. J. 53, 53 (1988).
- R. M. Berry, Torque and switching in the bacterial flagellar motor: An electrostatic model, Biophys. J. 64, 961 (1993).
- J. Xing, F. Bai, R. Berry, and G. Oster, Torque-speed relationship of the bacterial flagellar motor, Proc. Natl. Acad. Sci. USA 103, 1260 (2006).
- T. Mora, H. Yu, Y. Sowa, and N. S. Wingreen, Steps in the bacterial flagellar motor, PLOS Comput. Biol. 5, e1000540 (2009).
- G. Meacci and Y. Tu, Dynamics of the bacterial flagellar motor with multiple stators, Proc. Natl. Acad. Sci. USA 106, 3746 (2009).
- S. B. van Albada, S. Tănase-Nicola, and P. R. ten Wolde, The switching dynamics of the bacterial flagellar motor, Mol. Syst. Biol. 5, 316 (2009).
- G. Meacci, G. Lan, and Y. Tu, Dynamics of the bacterial flagellar motor: The effects of stator compliance, back steps, temperature, and rotational asymmetry, Biophys. J. 100, 1986 (2011).
- R. Boschert, F. R. Adler, and D. F. Blair, Loose coupling in the bacterial flagellar motor, Proc. Natl. Acad. Sci. USA 112, 4755 (2015).
- K. K. Mandadapu, J. A. Nirody, R. M. Berry, and G. Oster, Mechanics of torque generation in the bacterial flagellar motor, Proc. Natl. Acad. Sci. USA 112, E4381 (2015).
- M. Meister, G. Lowe, and H. C. Berg, The proton flux through the bacterial flagellar motor, Cell 49, 643 (1987).
- S. Nakamura, N. Kami-ike, P. Y. Jun-ichi, T. Minamino, and K. Namba, Evidence for symmetry in the elementary process of bidirectional torque generation by the bacterial flagellar motor, Proc. Natl. Acad. Sci. USA 107, 17616 (2010).
- M. Meister, S. R. Caplan, and H. C. Berg, Dynamics of a tightly coupled mechanism for flagellar rotation. bacterial motility, chemiosmotic coupling, proton motive force, Biophys. J. 55, 905 (1989).
- C.-J. Lo, Y. Sowa, T. Pilizota, and R. M. Berry, Mechanism and kinetics of a sodium-driven bacterial flagellar motor, Proc. Natl. Acad. Sci. USA 110, E2544 (2013).
- Y. Sowa, A. D. Rowe, M. C. Leake, T. Yakushi, M. Homma, A. Ishijima, and R. M. Berry, Direct observation of steps in rotation of the bacterial flagellar motor, Nature 437, 916 (2005).
- N. R. Francis, V. M. Irikura, S. Yamaguchi, D. J. De Rosier, and R. M. Macnab, Localization of the salmonella typhimurium flagellar switch protein flig to the cytoplasmic m-ring face of the basal body, Proc. Natl. Acad. Sci. USA 89, 6304 (1992).
- D. R. Thomas, N. R. Francis, C. Xu, and D. J. DeRosier, The three-dimensional structure of the flagellar rotor from a clockwise-locked mutant of Salmonella enterica serovar typhimurium, J. Bacteriol. 188, 7039 (2006).
- R. P. Feynman, R. B. Leighton, and M. Sands, The Feynman Lectures on Physics, Vol. I (Addison-Wesley, Reading, MA, 1966).
- J. M. R. Parrondo, J. M. Blanco, F. Cao, and R. Brito, Efficiency of Brownian motors, Europhys. Lett. 43, 248 (1998).
- N. Golubeva, A. Imparato, and L. Peliti, Efficiency of molecular machines with continuous phase space, Europhys. Lett. 97, 60005 (2012).
- F. Jülicher, A. Ajdari, and J. Prost, Modeling molecular motors, Rev. Mod. Phys. 69, 1269 (1997).
- T. Schmiedl and U. Seifert, Efficiency of molecular motors at maximum power, Europhys. Lett. 83, 30005 (2008).
- M. Esposito, K. Lindenberg, and C. Van den Broeck, Universality of Efficiency at Maximum Power, Phys. Rev. Lett. 102, 130602 (2009).
- K. Svoboda, C. F. Schmidt, B. J. Schnapp, and S. M. Block, Direct observation of kinesin stepping by optical trapping interferometry, Nature 365, 721 (1993).
- R. Bowater and J. Sleep, Demembranated muscle fibers catalyze a more rapid exchange between phosphate and adenosine triphosphate than actomyosin subfragment, Biochemistry 27, 5314 (1988).
- N. J. Carter and R. A. Cross, Mechanics of the kinesin step, Nature 435, 308 (2005).
- S. Liepelt and R. Lipowsky, Kinesin's Network of Chemomechanical Motor Cycles, Phys. Rev. Lett. 98, 258102 (2007).
- D. F. Blair and H. C. Berg, Mutations in the MotA protein of Escherichia coli reveal domains critical for proton conduction, J. Mol. Biol. 221, 1433 (1991).
- T. F. Braun, S. Poulson, J. B. Gully, J. C. Empey, S. Van Way, A. Putnam, and D. F. Blair, Function of proline residues of MotA in torque generation by the flagellar motor of Escherichia coli, J. Bacteriol. 181, 3542 (1999).
- H. Wang and G. Oster, The Stokes efficiency for molecular motors and its applications, Europhys. Lett. 57, 134 (2002).
- E. Zimmermann and U. Seifert, Efficiencies of a molecular motor: A generic hybrid model applied to the -ATPase, New J. Phys. 14, 103023 (2012).
- R. M. Berry and H. C. Berg, Absence of a barrier to backwards rotation of the bacterial flagellar motor demonstrated with optical tweezers, Proc. Natl. Acad. Sci. USA 94, 14433 (1997).
- C. Cheng, P. R. McGonigal, J. F. Stoddart, and R. D. Astumian, Design and synthesis of nonequilibrium systems, ACS Nano 9, 8672 (2015).