Skip to main content
Log in

Dissipation in bioenergetic electron transfer chains

  • Minireview/Hypothesis
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

This paper examines the processes by which wasteful dissipation of free energy may occur in bioenergetic electron transfer chains. Frictionless transfer requires high rate constants in order to achieve a quasi-equilibrium steady-state. Previous results concerning the maximum power available from a photochemical source are recalled. The energetic performance of the bacterial reaction center is discussed, characterizing the processes that decrease either the quantum yield (recombination and obstruction) or the chemical potential (friction and non-equilibrated mechanisms). Considering the whole chain, diffusive carriers are potentially weaker links, due to kinetic limitation and short-circuiting reactions. It is suggested that the evolutionary trend has been to limit their number by lumping them into tightly bound protein complexes or, in a more flexible way, into labile supercomplexes.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

Cyt:

cytochrome

F :

Faraday

H:

primary acceptor in the bacterial reaction center (bacteriopheophytin)

k B :

Boltzmann's constant

P:

primary photochemical donor (special bacteriochlorophyll pair)

RC:

reaction center

QA, QB :

primary, secondary quinone acceptor

References

  • Arata H and Parson WW (1981) Delayed fluorescence from Rhodopseudomonas sphaeroides reaction centers. Enthalpy and free energy changes accompanying electron transfer from P-870 to quinones. Biochim Biophys Acta 638: 201–209

    Google Scholar 

  • Arnold W (1949) A calorimetric determination of the quantum yield in photosynthesis. In: Franck J and Loomis WE (eds) Photosynthesis in Plants, pp 273–276. The Iowa State Press, Ames, IA

    Google Scholar 

  • Arnold WA (1991) Experiments. Photosynth Res 27: 73–82

    Google Scholar 

  • Barber J (1995) Molecular basis of the vulnerability of Photosystem II to damage by light. Austr J Plant Physiol 22: 201–208

    Google Scholar 

  • Berry EA and Trumpower BL (1985) Isolation of ubiquinol oxidase from Paracoccus denitrificans and resolution into cytochrome bc 1 and cytochrome aa 3 complexes. J Biol Chem 260: 2458–2467

    PubMed  Google Scholar 

  • Bolton JR (1977) Solar energy conversion efficiency in photosynthesis — or — why two photosystems? In: Hall DO, Coombs J and Goodwin TW (eds) Photosynthesis 77: Proceedings of the 4th International Congress on Photosynthesis, pp 621–634. Biochemical Society, London

    Google Scholar 

  • Bolton JR and Hall DO (1991) The maximum efficiency of photosynthesis. Photochem Photobiol 53: 545–548

    Google Scholar 

  • Bolton JR, Haught AF and Ross TR (1981) Photochemical energy storage: An analysis of limits. In: Connolly JS (ed) Photochemical Conversion and Storage of Solar Energy, pp 297–339. Academic Press, New York

    Google Scholar 

  • De Donder T (1936) L'affinité. Gauthier-Villars, Paris.

    Google Scholar 

  • Duysens LNM (1958) The path of light in photosynthesis. In: The Photochemical Apparatus; Its Structure and Function. Brookhaven Symp Biol No 11, pp 10–25

  • Emerson R and Lewis CM (1943) The dependence of the quantum yield of Chlorella photosynthesis on the wavelength of light. Am J Bot 30: 165–178

    Google Scholar 

  • Fernández-Velasco JG and Crofts AR (1991) Complex or supercomplexes: Inhibitor titration shows that electron transfer in chromatophores from Rhodobacter sphaeroides involves a dimeric UQH2: cytochrome c 2 oxidase, and is delocalized. Biochem Soc Trans 19: 588–593

    PubMed  Google Scholar 

  • Freiberg A (1995) Coupling of antennas to reaction centers. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 385–398. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Gunner MR and Dutton PL (1989) Temperature and-ΔG0 dependence of the electron transfer from BPheo to QA in reaction center protein from Rhodobacter sphaeroides with different quinones as QA. J Am Chem Soc 111: 3400–3412

    Google Scholar 

  • Haehnel W (1986) Plastocyanin. In: Staehelin LA and Arntzen CJ (eds) Encyclopedia of Plant Physiology; Photosynthesis III, pp 547–559. Springer-Verlag, Berlin, Heidelberg

    Google Scholar 

  • Joliot P, Joliot A and Kok B (1968) Analysis of the interactions between the two photosystems in isolated chloroplasts. Biochim Biophys Acta 153: 635–652

    PubMed  Google Scholar 

  • Joliot P, Verméglio A and Joliot A (1989) Evidence for supercomplexes between reaction centers, cytochrome c 2 and cytochrome bc 1 complex in Rhodobacter sphaeroides whole cells. Biochim Biophys Acta 975: 336–345

    Google Scholar 

  • Joliot P, Lavergne J and Beal D (1992) Plastoquinone compartmentation in chloroplasts. 1. Evidence for domains with different rates of photo-reduction. Biochim Biophys Acta 1101: 1–12

    Google Scholar 

  • Joliot P, Verméglio A and Joliot A (1993) Supramolecular membrane protein assemblies in photosynthesis and respiration. Biochim Biophys Acta 1141: 151–174

    Google Scholar 

  • Junge W and Jackson JB (1982) The development of electrochemical gradient across the photosynthetic membranes. In: Govindjee (ed) Photosynthesis, Vol 1, pp 589–646. Academic Press, New York

    Google Scholar 

  • Knox RS (1969) Thermodynamics and the primary processes of photosynthesis. Biophys J 9: 1351–1362

    PubMed  Google Scholar 

  • Krieger A, Rutherford AW and Johnson GN (1995) On the determination of redox midpoint potential of the primary quinone electron acceptor, QA, in Photosystem II. Biochim Biophys Acta 1229: 193–201

    Google Scholar 

  • Lavergne J and Joliot P (1991) Restricted diffusion in photosynthetic membranes. Trends Biochem Sci 16: 129–134

    Article  PubMed  Google Scholar 

  • Lavergne J, Joliot P and Verméglio A (1989) Partial equilibration of photosynthetic electron carriers under weak illumination: A theoretical and experimental study. Biochim Biophys Acta 975: 346–354

    Google Scholar 

  • Lavergne J, Bouchaud JP and Joliot P (1992) Plastoquinone compartmentation in chloroplasts. 2. Theoretical aspects. Biochim Biophys Acta 1101: 13–22

    Google Scholar 

  • Lin X, Murchison HA, Nagarajan V, Parson WW, Allen JP and Williams JC (1994) Specific alterations of the oxidation potential of the electron donor in reaction centers from Rhodobacter sphaeroides. Proc Natl Acad Sci USA 91: 10265–10269

    PubMed  Google Scholar 

  • Lübben M, Kolmerer B and Saraste M (1992) An archaebacterial terminal oxidase combines core structures of two mitochondrial respiratory complexes EMBO J 11: 805–812

    PubMed  Google Scholar 

  • Maróti P and Wraight CA (1988) Flash-induced H+ binding by bacterial photosynthesis reaction centers: Influences of the redox states of the acceptor quinones and primary donor. Biochim Biophys Acta 934: 329–347

    Google Scholar 

  • McPherson PH, Okamura MY and Feher G (1988) Light-induced proton uptake by photosynthetic reaction centers from Rhodobacter sphaeroides R-26. I. Protonation of the one-electron-states. Biochim Biophys Acta 934: 348–368

    Google Scholar 

  • Parson WW (1978) Thermodynamics of the primary reactions of photosynthesis. Photochem Photobiol 28: 389–393

    Google Scholar 

  • Peloquin JM, Williams JC, Lin X, Alden RG, Murchison HA, Taguchi AKW, Allen JP and Woodbury NW (1994) Time-dependent thermodynamics during early electron transfer in reaction centers from Rhodobacter sphaeroides. Biochemistry 33, 8089–8100

    PubMed  Google Scholar 

  • Prigogine I (1955) Introduction to Thermodynamics of Irreversible Processes. Interscience, New York

    Google Scholar 

  • Prince RC and Dutton PL (1976) The primary acceptor of bacterial photosynthesis: Its operating midpoint potential. Arch Biochem Biophys 172: 329–334

    PubMed  Google Scholar 

  • Prince RC and Dutton PL (1978) Protonation and the reducing potential of the primary electron acceptor. In: Clayton RK and Sistrom WR (eds) The Photosynthetic Bacteria, pp 439–453. Plenum Press, New York

    Google Scholar 

  • Ross RT (1975) Radiative lifetime and thermodynamic potential of excited states. Photochem Photobiol 21: 401–406

    Google Scholar 

  • Ross RT and Calvin M (1967) Thermodynamics of light emission and free-energy storage in photosynthesis. Biophys J 7: 595–614

    PubMed  Google Scholar 

  • Sebban P, Robert B and Jolchine G (1985) Isolation and spectroscopic characterization of the B875 antenna complex of a mutant of Rhodopseudomonas sphaeroides. Photochem Photobiol 42: 573–578

    Google Scholar 

  • Sone N, Sekimachi M and Kutoh E (1987) Identification and properties of a quinol oxidase super-complex composed of abc 1 complex and cytochrome oxidase in the thermophilic bacterium PS3. J Biol Chem 262: 15386–15391

    PubMed  Google Scholar 

  • Thielen APGM and van Gorkom HJ (1981) Energy transfer and quantum yield in Photosystem II. Biochim Biophys Acta 637: 439–446

    Google Scholar 

  • Vass I, Styring S, Hundal T, Koivuniemi A, Aro E-M and Andersson B (1992) Reversible and irreversible intermediates during photoinhibition of Photosystem II: Stable reduced QA species promote chlorophyll triplet formation. Proc Natl Acad Sci USA 89: 1408–1412

    PubMed  Google Scholar 

  • Volk M, Ogrodnik A and Michel-Beyerle ME (1995) The recombination dynamics of the radical pair P+H in external magnetic and electric fields. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 595–626. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Wilson DF, Dutton PL and Wagner M (1973) Energy-transducing components in mitochondrial respiration. In: Sanadi DR and Vernon LP (eds) Current Topics in Bioenergetics, Vol 5, pp 233–265. Academic Press, New York

    Google Scholar 

  • Woodbury NW and Allen JP (1995) The pathway, kinetics and thermodynamics of electron transfer in wild type and mutant reaction centers of purple nonsulfur bacteria. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 527–557. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

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

    PubMed  Google Scholar 

  • Woodbury NW, Peloquin JM, Alden RG, Lin X, Taguchi AKW, Williams JC and Allen JP (1994) Relationship between thermodynamics and mechanism during photoinduced charge separation in reaction centers from Rhodobacter sphaeroides. Biochemistry 33: 8101–8112

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lavergne, J., Joliot, P. Dissipation in bioenergetic electron transfer chains. Photosynth Res 48, 127–138 (1996). https://doi.org/10.1007/BF00041003

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00041003

Key words

Navigation