Skip to main content
SpringerLink
Log in

Basic Aspects of Electron and Proton Transfer Reactions with Applications to Photosynthesis

  • Chapter
Oxygenic Photosynthesis: The Light Reactions

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 4))

Summary

Starting with a discussion of the dependence of the activation energy of electron transport on reorganization energy, conclusions that apply to charge transfer in photosynthetic membrane proteins are: (i) a relatively low reorganization energy is anticipated from the low dielectric constant of the protein and membrane interior; (ii) the rate of intraprotein electron transfer in theory depends on the detailed pathway, but empirically a first-order rate-distance dependence for electron transfer holds over twelve orders of magnitude in rates, a factor of ten decrease for each 1.7 Å increase in center-center separation. Most of the data apply to the photosynthetic reaction center. (iii) The theories of the distance dependence of intraprotein electron transfer do not provide an explanation for the asymmetry of electron transfer, i.e., the far greater rate through the ‘L’ compared to the ‘M’ branch of the photosynthetic reaction center. (iv) The existence of long distance intraprotein electron transfer implies that the redox poise between centers separated by as much as 20 Å must be carefully regulated in vivo to avoid ‘promiscuous’ transfer events. (v) Special aspects of intramembrane electron transfer include (a) consideration of a three layer membrane model that includes a 10–15 Å thick interfacial layer of intermediate (ε=10–20) dielectric constant; and (b) in the case of the reaction center, a time-dependent ps→μs) increase in effective dielectric constant that is needed to keep the reaction activationless. (vi) Long distance transmembrane H+ translocation is likely to involve extended water chains, as inferred from recent atomic structure data on the n-side peripheral domain of the reaction center and the p-side peripheral domain of cytochrome f of the integral cytochrome b 6 f complex.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 259.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 329.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 329.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Applequist J and Mahr TG (1966) The conformation of poly-L-tyrosine in quinoline from dielectric dispersion studies. J Amer Chem Soc 88: 5419–5429

    CAS  Google Scholar 

  • Bashford D (1991) Electrostatic effects in biological molecules. Curr Op Struct Biol 1: 175–184

    Article  CAS  Google Scholar 

  • Beratan DN and Onuchic JN (1989) Electron tunneling pathways in proteins: Influences on the transfer rate. Photosynth Res 22: 173–186

    Article  CAS  Google Scholar 

  • Beratan DN, Betts JN and Onuchic JN (1991) Protein electron transfer rates set by the bridging secondary and tertiary structure. Science 252: 1285–1288

    PubMed  CAS  Google Scholar 

  • Betts JN, Beratan DN and Onuchic JN (1992) Mapping electron tunneling pathways: An algorithm that finds the minimum length/maximum coupling pathway between electron donors and acceptors in proteins. J Amer Chem Soc 114: 4043–4046

    CAS  Google Scholar 

  • Bowler BE, Raphael AL and Gray HB (1990) Long range electron transfer in donor (spacer) acceptor molecules and proteins. Prog Inorg Chem: Bioinorg Chem 38: 259–322

    CAS  Google Scholar 

  • Boxer SG (1990) Mechanism of long-distance electron transfer in proteins: Lessons from photosynthetic reaction centers. Ann Rev Biophys Biophys Chem 19: 267–299

    Article  CAS  Google Scholar 

  • Cave RJ, Siders P and Marcus RA (1986) Mutual orientation effects on electron transfer between porphyrins. J Phys Chem 90: 1436–1444

    Article  CAS  Google Scholar 

  • Cherepanov D and Krishtalik LI (1990) Intramembrane electric fields: A single charge, protein α-helix, photosynthetic reaction center. Bioelectrochem Bioenerg 24: 113–127

    Article  CAS  Google Scholar 

  • Christensen HEM, Conrad LS, Mikkelsen KV, Nielsen MK and Ulstrup J (1990) Direct and superexchange electron tunneling at the adjacent and remote sites of higher plant plastocyanins. Inorg Chem 29: 2808–2816

    Article  CAS  Google Scholar 

  • Churg AK, Weiss RM, Warshel A and Takano T (1983) On the action of cytochrome c: Correlating geometry change upon oxidation with activation energies of electron transfer. J Phys Chem 87: 1683–1694

    Article  CAS  Google Scholar 

  • Cramer WA and Knaff DB (1991) Energy Transduction in Biological Membranes, Chap. 2. Springer Study Edition, Springer-Verlag, New York

    Google Scholar 

  • Creighton S, Hwang JK, Warshel A, Parson WW and Norris J (1988) Simulating the dynamics of the primary charge separation process in bacterial photosynthesis. Biochemistry 27: 774–781

    CAS  Google Scholar 

  • Crofts AR (1985) The mechanism of ubiquinol:cytochrome c oxidoreductases of mitochondria and Rb. sphaeroides. In: Martonosi A (ed) The Enzymes of Biological Membranes, Vol 4, pp 347–382. Plenum, New York

    Google Scholar 

  • Deisenhofer J and Michel H (1989) The photosynthetic reaction center from the purple bacterium, Rps. viridis. EMBO J 8: 2149–2169

    PubMed  CAS  Google Scholar 

  • DeVault D (1984) Quantum-Mechanical Tunneling in Biological Systems, 2nd Ed, Cambridge University Press, Cambridge

    Google Scholar 

  • DeVault D (1986) Vibronic coupling to electron transfer and the structure of the R. viridis reaction center. Photosynth Res 10: 125–137

    Google Scholar 

  • Dogonadze RR (1971) Theory of molecular electrode kinetics. In: Hush NS (ed) Reactions of Molecules at Electrodes, pp 135–227. J Wiley, Intersci, London-New York

    Google Scholar 

  • Dogonadze RR and Kuznetsov AM (1967) Effect of the changes in the first coordination sphere upon the reaction rate. Elektrokhimiya 3: 1324–1330

    CAS  Google Scholar 

  • Dogonadze RR and Kuznetsov AM (1975) Theory of charge transfer kinetics at solid-polar liquid interfaces. Progress in Surface Science 6: 1–42

    Article  CAS  Google Scholar 

  • Ermler U, Fritzsch G, Buchanan SK and Michel H (1994) Structure of the photosynthetic reaction center from Rhodobacter sphaeroides at 2.65 Å resolution: Cofactors and protein-cofactor interactions. Structure 2: 925–936

    Article  CAS  PubMed  Google Scholar 

  • Farid RS, Moser CC and Dutton PL (1993) Electron transfer in proteins. Curr Op Struct Biol 3: 225–233

    Article  CAS  Google Scholar 

  • Feher G, Allen JP, Okamura MY and Rees DC (1989) Structure and function of bacterial photosynthetic reaction centers. Nature 339: 111–116

    Article  CAS  Google Scholar 

  • Frauenfelder H, Sligar SG and Wolynes PG (1991) The energy landscapes and motions of proteins. Science 254: 1598–1603

    PubMed  CAS  Google Scholar 

  • Furbacher PN and Cramer WA (1989) On the question of interheme electron transfer in the chloroplast cytochrome b 6 in situ. Biochemistry 28: 8990–8998

    Article  PubMed  CAS  Google Scholar 

  • Gilson M and Honig B (1985) The dielectric constant of a folded protein. Biopolymers 25: 2097–2119

    Google Scholar 

  • Golbeck JH and Bryant DA (1991) Photosystem I. In: Lee CP (ed) Curr Topics Bioenerg, Vol 16, pp 83–177. Academic Press, Orlando

    Google Scholar 

  • Goldstein RA, Takiff L and Boxer SG (1988) Energetics of initial charge separation in bacterial photosynthesis: The triplet decay rate in very high magnetic fields. Biochim Biophys Acta 934: 253–263

    CAS  Google Scholar 

  • Gray HB and Malmstrom BG (1989) Long range electron transfer in multisite metalloproteins. Biochemistry 28: 7499–7505

    Article  PubMed  CAS  Google Scholar 

  • Harvey SC (1989) Treatment of electrostatic effects in macromolecular modeling. Proteins: Structure, Function, Genetics 5: 78–92

    Article  CAS  Google Scholar 

  • Honig BH, Hubbell WL and Flewelling RF (1986) Electrostatic interactions in membranes and proteins. Ann Rev Biophys Biophys Chem 15: 163–193

    Article  CAS  Google Scholar 

  • Horton P, Whitmarsh J and Cramer WA (1976) On the specific site of action of 3-(3,4-dichlorophenyl)-1,1-dimethylurea in chloroplasts: Inhibition of a dark acid-induced decrease in midpoint potential of cytochrome b-559. Arch Biochem Biophys 176: 519–524

    Article  PubMed  CAS  Google Scholar 

  • Khorana HG (1988) Bacteriorhodopsin, a membrane protein that uses light to translocate protons. J Biol Chem 263: 7439–7442

    PubMed  CAS  Google Scholar 

  • King G, Lee FS and Warshel A (1991) Microscopic simulations of macroscopic dielectric constants of solvated proteins. J Chem Phys 95: 4366–4377

    Article  CAS  Google Scholar 

  • Knapp EW, Fischer SF, Zinth W, Sanler M, Kaiser W, Deisenhofer J and Michel H (1985) Analysis of optical spectra from single crystals of Rps. viridis reaction centers. Proc Natl Acad Sci, USA 82: 8463–8467

    CAS  PubMed  Google Scholar 

  • Krishtalik LI (1979) Globule size and activation energy of an enzymatic process. Molekulyarnaya Biologiya (Moscow) 13: 577–581

    CAS  Google Scholar 

  • Krishtalik LI (1980) Catalytic acceleration of reactions by enzymes. Effect of screening of a polar medium by a protein globule. J Theor Biol 86: 757–771

    Article  PubMed  CAS  Google Scholar 

  • Krishtalik LI (1986a) Charge Transfer Reactions in Electrochemical and Chemical Processes. Plenum Press, New York

    Google Scholar 

  • Krishtalik LI (1986b) Energetics of multielectron reactions. Photosynthetic oxygen evolution. Biochim Biophys Acta 849: 162–171

    CAS  Google Scholar 

  • Krishtalik LI (1988) Charge-medium interactions in biological charge transfer reactions. In: Dogonadze RR, Kalman E, Kornyshev AA and Ulstrup J (eds) The Chemical Physics of Solvation, part C, pp 707–739. Elsevier, Amsterdam

    Google Scholar 

  • Krishtalik LI (1989) Activationless electron transfer in the reaction center of photosynthesis. Biochim Biophys Acta 977: 200–206

    CAS  Google Scholar 

  • Krishtalik LI (1990) Activation energy of photosynthetic oxygen evolution: An attempt at theoretical analysis. Bioelectrochem Bioenerg 23: 249–263

    Article  CAS  Google Scholar 

  • Krishtalik LI (1992) Intramembrane charge transfer reactions. The membrane as a dielectric medium. Molekularnaya Biologiya 26: 1377–1388

    CAS  Google Scholar 

  • Krishtalik LI (1995) Fast electron transfers in the photosynthetic reaction centre: Effect of the time-evolution of the dielectric response. Biochim Biophys Acta 1228: 58–66

    Google Scholar 

  • Krishtalik LI and Kuznetsov AM (1986) Energetics of the elementary act and ‘configurational’ electrode potential. Elektrokhimiya 22: 246–248

    CAS  Google Scholar 

  • Krishtalik LI and Topolev VV (1983) Intraglobular electric field. The primary electric field set up by the polypeptide back bone, functional groups, and ions of the α-chymotrypsin molecule. Molekulyarnaya Biologiya (Moscow) 17: 1034–1041

    CAS  Google Scholar 

  • Krishtalik LI, Tae GS, Cherepanov D and Cramer WA (1993) The redox properties of cytochromes b imposed by the membrane electrostatic environment. Biophys J 65: 1–12

    Google Scholar 

  • Lanyi J (1993) Proton translocation mechanism and energetics in the light-driven pump bacteriorhodopsin. Biochim Biophys Acta 1183: 241–261

    PubMed  CAS  Google Scholar 

  • Levine RP (1969) A light-induced absorbance change at 564 nm in wild-type and mutant strains of Chlamydomonas reinhardtii. In: Metzner H (ed) Progress in Photosynthesis Research, pp 971–977. Int Union Biol Sci, Tübingen

    Google Scholar 

  • Marchi M, Gehelen JN, Chandler D and Newton M (1993) Diabatic surfaces and the pathway for primary electron transfer in a photosynthetic reaction center. J Am Chem Soc 115: 4178–4190

    Article  CAS  Google Scholar 

  • Marcus RA (1956) On the theory of oxidation-reduction reactions involving electron transfer. I. J Chem Phys 24: 966–978

    CAS  Google Scholar 

  • Marcus RA (1964) Chemical and electrochemical electron transfer theory. Ann Rev Phys Chem 15: 155–196

    Article  CAS  Google Scholar 

  • Marcus RA and Sutin N (1985) Electron transfers in chemistry and biology. Biochim Biophys Acta 811: 265–322

    CAS  Google Scholar 

  • Maricíc S, Pifat G and Pravdic V (1964) Proton conductivity in solid hydrated haemoglobin. Biochim Biophys Acta 79: 293–300

    PubMed  Google Scholar 

  • Maróti P, Kirmaier C, Wraight C, Holten D and Pearlstein RM (1985) Photochemistry and electron transfer in borohydride-treated reaction centers. Biochim Biophys Acta 810: 132–139

    Google Scholar 

  • Martinez SE, Cramer WA and Smith JL (1995) An internal H2O chain in cytochrome f. Biophys J 68: 246a

    Google Scholar 

  • Michel-Beyerle M, Plato M, Deisenhofer J, Michel H, Bixon M and Jortner J (1988) Unidirectionality of charge separation in reaction centers of photosynthetic bacteria. Biochim Biophys Acta 932: 52–70

    CAS  Google Scholar 

  • Moser CC and Dutton PL (1992) Engineering protein structure for electron transfer function in photosynthetic reaction centers. Biochim Biophys Acta 1101: 171–176

    PubMed  CAS  Google Scholar 

  • Moser CC, Keske JM, Warncke K, Farid RS and Dutton PL (1992) Nature of biological electron transfer. Nature 355: 796–802

    Article  PubMed  CAS  Google Scholar 

  • Nagle JF and Morowitz H (1978) Molecular mechanisms for proton transport in membranes. Proc Natl Acad Sci, USA 75: 298–302

    PubMed  CAS  Google Scholar 

  • Nagle JF and Tristram-Nagle S (1983) Hydrogen bonded chain mechanisms for proton conduction and proton pumping. J Mem Biol 74: 1–14

    CAS  Google Scholar 

  • Nakamura H, Sakamoto T and Wada A (1988) A theoretical study of the dielectric constant of proteins. Prot Eng 2: 177–183

    CAS  Google Scholar 

  • Naleway CA, Curtiss LA and Miller JR (1991) Super-exchange pathway model for long distance electronic couplings. J Phys Chem 95: 8434–8437

    Article  CAS  Google Scholar 

  • Onuchic JN, Beratan DN, Winkler JR and Gray HB (1992) Pathway analysis of protein electron transfer reactions. Ann Rev Biophys Biomol Struct 21: 349–377

    CAS  Google Scholar 

  • Paddock ML, Rongey SH, McPherson PH, Juth A, Feher G and Okamura MY (1994) Pathway of proton transfer in bacterial reaction centers: Role of aspartate-L213 in proton transfers associated with reduction of quinone to hydroquinone. Biochemistry 33: 734–745

    Article  PubMed  CAS  Google Scholar 

  • Papadopoulos G, Deneher NA, Zaccai G and Büldt G (1990) Water molecules and exchangeable hydrogen ions at the active centre of bacteriorhodopsin localized by neutron diffraction. J Mol Biol 214: 15–19

    Article  PubMed  CAS  Google Scholar 

  • Pethig R (1979) Dielectric and Electronic Properties of Biological Materials. Wiley, Chichester

    Google Scholar 

  • Regan JJ, Risser SM, Beratan DN and Onuchic JN (1993) Protein electron transport: Single vs. multiple pathways. J Phys Chem 97: 13083–13088

    Article  CAS  Google Scholar 

  • Rothschild KJ, He YW, Sonar A, Marti T and Khorana HG (1992) Vibrational spectroscopy of bacteriorhodopsin mutants. Evidence that Thr-46 and Thr-89 form part of a transient network of hydrogen bonds. J Biol Chem 267: 1615–1622

    PubMed  CAS  Google Scholar 

  • Sharp KA and Honig BH (1990) Electrostatic interactions in macromolecules: Theory and applications. Ann Rev Biophys Biophys Chem 19: 301–332

    Article  CAS  Google Scholar 

  • Shinkarev VP and Wraight CA (1993) Electron and proton transfer in the acceptor-quinone complex of reaction centers of phototrophic bacteria. In: Deisenhofer J and Norris JR (eds) The Photosynthetic Reaction Center, Vol 1, pp 193–255. Academic Press, Orlando

    Google Scholar 

  • Shopes RJ and Wraight CA (1987) Charge recombination from the P+QA − state in reaction centers from Rps. viridis. Biochim Biophys Acta 893: 409–425

    PubMed  CAS  Google Scholar 

  • Siddarth P and Marcus RA (1990) Comparison of experimental and theoretical electronic matrix elements for long-range electron transfer. J Phys Chem 94: 2985–2989

    CAS  Google Scholar 

  • Simonson T, Perahia D and Bricogne G (1991a) Intramolecular dielectric screening in proteins, J Mol Biol 218: 1859–1886

    Article  Google Scholar 

  • Simonson T, Perahia D and Brunger AT (1991b) Microscopic theory of the dielectric properties of proteins. Biophys J 59: 670–690

    Article  PubMed  CAS  Google Scholar 

  • Steffen MA, Lao K and Boxer SG (1994) Dielectric asymmetry in the photosynthetic reaction center. Science 264: 810–816

    CAS  PubMed  Google Scholar 

  • Takashima S and Schwan HP (1965) Dielectric dispersion of crystalline powders of amino acids, peptides, and proteins. J Phys Chem 69: 4176–4182

    PubMed  CAS  Google Scholar 

  • Treutlein M, Schulten K, Brunger AT, Karplus M, Deisenhofer J and Michel H (1992) Chromophore-protein interactions and the function of the photosynthetic reaction center: A molecular dynamics simulation. Proc Natl Acad Sci USA 89: 75–79

    PubMed  CAS  Google Scholar 

  • Ulstrup J (1979) Charge Transfer Processes in Condensed Media; Lecture Notes in Chemistry. Springer-Verlag, Berlin

    Google Scholar 

  • van Duijnen PT and Thole BT (1982) Cooperative effects in α-helices: An ab initio molecular orbital study. Biopolymers 21: 1749–1754

    Google Scholar 

  • Wada A (1976) The α-helix as an electric macro-dipole. In: Kotani M (ed) Advances in Biophysics, Vol 9, pp 1–63. University of Tokyo Press, Tokyo

    Google Scholar 

  • Warshel A and Aqvist J (1991) Electrostatic energies and macromolecular function. Ann Rev Biophys Biophys Chem 20: 267–298

    Article  CAS  Google Scholar 

  • Warshel A and Russel ST (1984) Calculations of electrostatic interactions in biological systems and in solutions. Quart Rev Biophys 17: 283–422

    Article  CAS  Google Scholar 

  • Winkler JR and Gray HB (1992) Electron transfer in ruthenium-modified proteins. Chem Rev 92: 369–379

    Article  CAS  Google Scholar 

  • Woodbury NW and Parson WW (1984) Nanosecond fluorescence from isolated photosynthetic reaction centers of Rb. sphaeroides. Biochim Biophys Acta 767: 345–361

    PubMed  CAS  Google Scholar 

  • Woodbury NW, Parson WW, Gunner MR, Prince RC and Dutton PL (1986) Radical pair energetics and decay mechanisms in reaction centers containing anthraquinones, naphthoquinones, or benzoquinones in place of ubiquinone. Biochim Biophys Acta 851: 6–22

    PubMed  CAS  Google Scholar 

  • Yadav A, Jackson RM, Holbrook JJ and Warshel A (1991) Role of solvent reorganization energies in the catalytic activity of enzymes. J Amer Chem Soc 113: 4800–4805

    Article  CAS  Google Scholar 

  • Zheng C, McCammon JC and Wolynes PG (1991) Quantum simulations of conformation reorganization in the electron transfer reactions of cytochrome c. Chem Phys 158: 261–270

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. The Frumkin Institute of Electrochemistry, Academy of Sciences, Moscow, 117 071, Russia

    Lev I. Krishtalik

  2. Dept. of Biological Sciences, Purdue University, West Lafayette, IN, 47907, USA

    William A. Cramer

Authors
  1. Lev I. Krishtalik
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. William A. Cramer
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. USDA/ARS, Photosynthesis Research Unit, University of Illinois, Urbana, Illinois, USA

    Donald R. Ort

  2. Department of Biology/Chemistry, University of Michigan, Ann Arbor, Michigan, USA

    Charles F. Yocum

  3. University of Illinois, USA

    Iris F. Heichel (Assistant Editor) (Assistant Editor)

Rights and permissions

Reprints and permissions

Copyright information

© 1996 Kluwer Academic Publishers

About this chapter

Cite this chapter

Krishtalik, L.I., Cramer, W.A. (1996). Basic Aspects of Electron and Proton Transfer Reactions with Applications to Photosynthesis. In: Ort, D.R., Yocum, C.F., Heichel, I.F. (eds) Oxygenic Photosynthesis: The Light Reactions. Advances in Photosynthesis and Respiration, vol 4. Springer, Dordrecht. https://doi.org/10.1007/0-306-48127-8_20

Download citation

  • DOI: https://doi.org/10.1007/0-306-48127-8_20

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-0-7923-3683-9

  • Online ISBN: 978-0-306-48127-7

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation