The two last overviews by Colin Allen Wraight (1945–2014) on energy conversion in photosynthetic bacteria

Abstract

Colin Allen Wraight (1945–2014) was a well-known biophysicist and biochemist of our times—formerly Professor of Biochemistry, Biophysics and Plant Biology, and Head of the Department of Biochemistry, University of Illinois at Urbana-Champaign, Urbana, IL, USA. (See a detailed Tribute to him by Govindjee et al., Photosynth Res, 2015.) During the latter part of his life, Colin had (1) given an excellent lecture in 2008 on the overall topic of the molecular mechanisms in biological energy conversion, focusing on how an ubiquinone is reduced to ubiquinol at the so-called “two electron gate”, and (2) presented a review poster on the design features of long distance proton transport in biological systems, with focus on photosynthetic bacteria (a pdf file of the original is available from one of us, Govindjee). We present here for historical purpose, a complete transcript of his 2008 lecture and his 2013 poster, which have been annotated and expanded by the authors of this paper. The major theme is: electron and proton transfer in biological systems, with emphasis on bacterial reaction centers. The figures, some of which were prepared by us, are presented in sequence for both the lecture and the poster. A common bibliography is provided at the end of the paper, which is divided into two parts: (I) The Lecture; and (II) The Poster.

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Notes

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    https://www.youtube.com/watch?v=2IB5e6FxH0M.

References

  1. Ädelroth P, Paddock ML, Tehrani A, Beatty JT, Feher G, Okamura MY (2001) Identification of the proton pathway in bacterial reaction centers: decrease of proton transfer rate by mutation of surface histidines at H126 and H128 and chemical rescue by imidazole identifies the initial proton donors. Biochemistry 40:14538–14546

    PubMed  Article  Google Scholar 

  2. Berg JM, Tymoczko JL, Stryer L (2002) Chapter 18.4: a proton gradient powers the synthesis of ATP. In: Biochemistry, 5th edn. W. H. Freeman and Company, New York

  3. Crofts AR, Rose S (2007) Marcus treatment of endergonic reactions: a commentary. Biochim Biophys Acta 1767:1228–1232

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  4. Govindjee, Prince RC, Ort DR (2015) Colin A. Wraight (1945–2014). Photosynth Res :20. doi:10.1007/s11120-015-0174-1

  5. Junge W (2013) Half a century of molecular bioenergetics. Biochem Soc Trans 41:1207–1218

    PubMed  CAS  Article  Google Scholar 

  6. Kis M, Asztalos E, Sipka G, Maróti P (2014) Assembly of photosynthetic apparatus in Rhodobacter sphaeroides as revealed by functional assessments at different growth phases and in synchronized and greening cells. Photosynth Res 122:261–273

  7. Kochendoerfer GG, Lin SW, Sakmar TP, Mathies RA (1999) How color visual pigments are tuned? Trends Biochem Sci 24:300–305

    PubMed  CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  9. Mitchell P (1961) Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 191:141–148

    Article  Google Scholar 

  10. Mitchell P (1966) Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. Glynn Research Ltd., Research Report No. 66/1. Corwell, Bodmin; also see Biochim Biophys Acta 1807:1507–1538

  11. Mitchell P (1979) Keilin’s respiratory chain concept and its chemiosmotic consequences. Science 206:1148–1159

    PubMed  CAS  Article  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

  13. Moser CC, Page CC, Cogdell RJ, Barber J, Wraight CA, Dutton PL (2003) Length, time and energy scales of photosystems. Adv Protein Chem 63:71–109

    PubMed  CAS  Article  Google Scholar 

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

    PubMed  CAS  PubMed Central  Article  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

  16. Onsager L (1967) Ion passages in lipid bilayers. Science 156:541–543

    Google Scholar 

  17. Onsager L (1969) The motion of ions: principles and concepts. Science 166:1359–1364

    PubMed  CAS  Article  Google Scholar 

  18. Paddock ML, Ädelroth P, Feher G, Okamura MY, Beatty JT (2002) Determination of proton transfer rates by chemical rescue: application to bacterial reaction centers. Biochemistry 41:14716–14725

    PubMed  CAS  Article  Google Scholar 

  19. Paddock ML, Sagle L, Tehrani A, Beatty JT, Feher G, Okamura MY (2003) Mechanism of proton transfer inhibition by Cd(2+) binding to bacterial reaction centers: determination of the pK(A) of functionally important histidine residues. Biochemistry 42:9626–9632

    PubMed  CAS  Article  Google Scholar 

  20. Takahashi E, Wraight CA (1992) Proton and electron transfer in the acceptor quinone complex of Rhodobacter sphaeroides reaction centers: characterization of site-directed mutants of the two ionizable residues, GluL212 and AspL213, in the QB binding site. Biochemistry 31:855–866

    PubMed  CAS  Article  Google Scholar 

  21. Takahashi E, Wraight CA (1996) Potentiation of proton transfer function by electrostatic interactions in photosynthetic reaction centers from Rhodobacter sphaeroides: first results from site-directed mutation of the H subunit. Proc Natl Acad Sci USA 93:2640–2645

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  22. Takahashi E, Wraight CA (2006) Small weak acids reactivate proton transfer in reaction centers from Rhodobacter sphaeroides mutated at AspL210 and AspM17. J Biol Chem 281:4413–4422

    PubMed  CAS  Article  Google Scholar 

  23. Wikström M, Ribacka C, Molin M, Laakkonen L, Verkhovsky M, Puustinen A (2005) Gating of proton and water transfer in the respiratory enzyme cytochrome c oxidase. Proc Natl Acad Sci USA 102:10478–10481

    PubMed  PubMed Central  Article  Google Scholar 

  24. Wraight CA (2004) Proton and electron transfer in the acceptor quinone complex of photosynthetic reaction centers from Rhodobacter sphaeroides. Front Biosci 9:309–337

    PubMed  CAS  Article  Google Scholar 

  25. Wraight CA (2005) Chapter 12: intraprotein proton transfer—concepts and realities from the bacterial photosynthetic reaction center. In: Wïkstrom M (ed) Biophysical and structural aspects of bioenergetics. RSC biomolecular science series. Royal Society of Chemistry, Cambridge

    Google Scholar 

  26. Wraight CA (2006) Chance and design—proton transfer in water, channels and bioenergetic proteins. Biochim Biophys Acta 1757:886–912

    PubMed  CAS  Article  Google Scholar 

  27. Wraight CA, Gunner MR (2009) The acceptor quinones of purple photosynthetic bacteria—structure and spectroscopy. In: Hunter CN, Daldal F, Thurnauer M, Beatty JT (eds) Advances in photosynthesis and respiration: the purple phototrophic bacteria. Springer, Dordrecht, pp 379–405

    Google Scholar 

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Acknowledgments

We are thankful to Debora Ann Lanter of the School of Integrative Biology, University of Illinois at Urbana-Champaign (UIUC) for transcribing Colin Wraight’s lecture that we have annotated, edited and presented here. Further, we are grateful to Joan Huber of UIUC for taking high-resolution photographs of the poster; and we thank Laura Thurlwell of the Department of Plant Biology, also of UIUC, for typing this poster from the photograph of the poster. We are indebted to Mary Wraight for her permission to use Colin’s poster and to disseminate it for historical and educational purpose. Most importantly, we are highly thankful to Tony Crofts for editing the text produced by two of us (PM and Gov). PM thanks a grant that supports his research: TÁMOP 4.2.2.D-15/1/KONV-2015-0024.

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Correspondence to Govindjee.

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Govindjee initiated the idea of making one of the last lectures and a single-authored poster of Colin Wraight (1945–2014) available to all for the history of research in photosynthesis. This paper is published with the permission of Mary, Colin Wraight’s wife. The current manuscript was read and edited by Antony (Tony) Crofts, who pointed out that since it is a lecture and a poster, it couldn’t be considered a review of the field, but a historical piece. This paper was approved for publication by Rienk van Grondelle, who serves on the Editorial Board of Photosynthesis Research; he added: It is beautiful, thanks a lot to both of you! Please publish it.

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Maróti, P., Govindjee The two last overviews by Colin Allen Wraight (1945–2014) on energy conversion in photosynthetic bacteria. Photosynth Res 127, 257–271 (2016). https://doi.org/10.1007/s11120-015-0175-0

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Keywords

  • Bioenergetics
  • Purple bacteria
  • Reaction center
  • Ubiquinones
  • Light induced electron and proton transfer
  • Two Electron Gate