Abstract
The molecular mechanism for proton conduction along hydrogen-bonded chains, or "proton wires," is studied with free energy simulations. The complete transport of a charge along a proton wire requires two complementary processes: 1) translocation of an excess proton (propagation of an ionic defect), and 2) reorientation of the hydrogen-bonded chain (propagation of a bonding defect). The potential of mean force profile for these two steps is computed in model systems comprising a single-file chain of nine dissociable and polarizable water molecules represented by the PM6 model of Stillinger and co-workers. Results of molecular dynamics simulations with umbrella sampling indicate that the unprotonated chain is preferably polarized, and that the inversion of its total dipole moment involves an activation free energy of 8 kcal/mol. In contrast, the rapid translocation of an excess H+ across a chain extending between two spherical solvent droplets is an activationless process. These results suggest that the propagation of a bonding defect constitutes a limiting step for the passage of several protons along single-file chains of water molecules, whereas the ionic translocation may be fast enough to occur within the lifetime of transient hydrogen-bonded water chains in biological membranes.
Full Text
The Full Text of this article is available as a PDF (140.0 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Akeson M., Deamer D. W. Proton conductance by the gramicidin water wire. Model for proton conductance in the F1F0 ATPases? Biophys J. 1991 Jul;60(1):101–109. doi: 10.1016/S0006-3495(91)82034-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Baciou L., Michel H. Interruption of the water chain in the reaction center from Rhodobacter sphaeroides reduces the rates of the proton uptake and of the second electron transfer to QB. Biochemistry. 1995 Jun 27;34(25):7967–7972. doi: 10.1021/bi00025a001. [DOI] [PubMed] [Google Scholar]
- Breed J., Sankararamakrishnan R., Kerr I. D., Sansom M. S. Molecular dynamics simulations of water within models of ion channels. Biophys J. 1996 Apr;70(4):1643–1661. doi: 10.1016/S0006-3495(96)79727-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chiu S. W., Subramaniam S., Jakobsson E., McCammon J. A. Water and polypeptide conformations in the gramicidin channel. A molecular dynamics study. Biophys J. 1989 Aug;56(2):253–261. doi: 10.1016/S0006-3495(89)82671-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- DeCoursey T. E., Cherny V. V. Deuterium isotope effects on permeation and gating of proton channels in rat alveolar epithelium. J Gen Physiol. 1997 Apr;109(4):415–434. doi: 10.1085/jgp.109.4.415. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Deamer D. W., Nichols J. W. Proton flux mechanisms in model and biological membranes. J Membr Biol. 1989 Feb;107(2):91–103. doi: 10.1007/BF01871715. [DOI] [PubMed] [Google Scholar]
- Duca K. A., Jordan P. C. Ion-water and water-water interactions in a gramicidinlike channel: effects due to group polarizability and backbone flexibility. Biophys Chem. 1997 Apr 22;65(2-3):123–141. doi: 10.1016/s0301-4622(96)02233-8. [DOI] [PubMed] [Google Scholar]
- Marrink S. J., Jähnig F., Berendsen H. J. Proton transport across transient single-file water pores in a lipid membrane studied by molecular dynamics simulations. Biophys J. 1996 Aug;71(2):632–647. doi: 10.1016/S0006-3495(96)79264-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Martinez S. E., Huang D., Ponomarev M., Cramer W. A., Smith J. L. The heme redox center of chloroplast cytochrome f is linked to a buried five-water chain. Protein Sci. 1996 Jun;5(6):1081–1092. doi: 10.1002/pro.5560050610. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nagle J. F., Morowitz H. J. Molecular mechanisms for proton transport in membranes. Proc Natl Acad Sci U S A. 1978 Jan;75(1):298–302. doi: 10.1073/pnas.75.1.298. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nagle J. F. Theory of passive proton conductance in lipid bilayers. J Bioenerg Biomembr. 1987 Oct;19(5):413–426. doi: 10.1007/BF00770027. [DOI] [PubMed] [Google Scholar]
- Nagle J. F., Tristram-Nagle S. Hydrogen bonded chain mechanisms for proton conduction and proton pumping. J Membr Biol. 1983;74(1):1–14. doi: 10.1007/BF01870590. [DOI] [PubMed] [Google Scholar]
- Paula S., Volkov A. G., Van Hoek A. N., Haines T. H., Deamer D. W. Permeation of protons, potassium ions, and small polar molecules through phospholipid bilayers as a function of membrane thickness. Biophys J. 1996 Jan;70(1):339–348. doi: 10.1016/S0006-3495(96)79575-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pomès R., Roux B. Structure and dynamics of a proton wire: a theoretical study of H+ translocation along the single-file water chain in the gramicidin A channel. Biophys J. 1996 Jul;71(1):19–39. doi: 10.1016/S0006-3495(96)79211-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Roux B., Karplus M. Molecular dynamics simulations of the gramicidin channel. Annu Rev Biophys Biomol Struct. 1994;23:731–761. doi: 10.1146/annurev.bb.23.060194.003503. [DOI] [PubMed] [Google Scholar]
- Sagnella D. E., Laasonen K., Klein M. L. Ab initio molecular dynamics study of proton transfer in a polyglycine analog of the ion channel gramicidin A. Biophys J. 1996 Sep;71(3):1172–1178. doi: 10.1016/S0006-3495(96)79321-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Woolf T. B., Roux B. The binding site of sodium in the gramicidin A channel: comparison of molecular dynamics with solid-state NMR data. Biophys J. 1997 May;72(5):1930–1945. doi: 10.1016/S0006-3495(97)78839-8. [DOI] [PMC free article] [PubMed] [Google Scholar]