FTIR Investigations on Orientation of Protein Secondary Structures and Primary Reactions in Photosynthesis

  • E. Nabedryk
  • W. Mäntele
  • J. Breton
Part of the NATO ASI Series book series (NSSA, volume 168)

Abstract

In the field of photosynthesis, a variety of spectroscopic techniques have been used to investigate the physical properties of the components (pigments, charge carriers, proteins) in the intact photosynthetic membrane and in the isolated complexes as well as in model systems which were thought to mimic the in vivo environment. These techniques have revealed a very high level of organization of the membrane components in vivo (1–4). Although a wealth of spectroscopic data has been collected over the years, the problem of inferring from these measurements alone the most probable configuration of the pigments and proteins in vivo is extremely complex.

Keywords

Chlorophyll Cage Amide Carboxyl FTIR Spectroscopy 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Breton J. and Verméglio A. (1982) Orientation of photosynthetic pigments in vivo. in: ‘Photosynthesis: Energy Conversion by Plants and Bacteria’ (Govindjee, Ed.), Academic Press, New York, pp.153–194.Google Scholar
  2. 2.
    Breton J. and Nabedryk E. (1984) Transmembrane orientation of alpha-helices and the organization of chlorophylls in photosynthetic pigment-protein complexes. FEBS Lett. 176(2), 355–359.CrossRefGoogle Scholar
  3. 3.
    Lutz M. (1984) Resonance Raman studies in photosynthesis. in: ‘Advances in Infrared and Raman Spectroscopy,’ (Clark R.J.H, Hester R.E eds.), Wiley-Heyden, Londres, Vol. 11, pp. 211–300.Google Scholar
  4. 4.
    Breton J. and Nabedryk E. (1987) Pigment and protein organization in reaction center and antenna complexes. in: ‘Topics in Photosynthesis — The Light Reactions’, pp. 159–195, (Barber J., ed), Elsevier Science Publishers B.V.Google Scholar
  5. 5.
    Deisenhofer J., Epp O., Miki K., Huber R. and Michel H. (1984) X-ray structure analysis of a membrane protein complex. Electron density map at 3A resolution and a model of the chromophores of the photosynthetic reaction center of Rhodopseudomonas viridis. J. Mol. Biol. 180, 385–398.PubMedCrossRefGoogle Scholar
  6. 6.
    Allen J.P., Feher G., Yeates T.O., Komiya H. and Rees D.C. (1987) Structure of the reaction center from Rhodobacter sphaeroides R-26: The cofactors. Proc. Natl. Acad. Sci. USA 84, 5730–5734.PubMedCrossRefGoogle Scholar
  7. 7.
    Deisenhofer J., Epp O., Miki K., Huber R. and Michel H. (1985) Structure of the protein subunits in the photosynthetic reaction center of Rhodopseudomonas viridis at 3A resolution. Nature (Lond.) 318, 618–624.CrossRefGoogle Scholar
  8. 8.
    Allen J.P., Feher G., Yeates T.O., Komiya H. and Rees D.C. (1987) Structure of the reaction center from Rhodobacter sphaeroides R-26: The protein subunits. Proc. Natl. Acad. Sci. USA 84, 6162–6166.PubMedCrossRefGoogle Scholar
  9. 9.
    Zuber H. (1987) The structure of light-harvesting pigment-protein complexes. in: ‘Topics in Photosynthesis. The Light Reactions’, pp. 197–259. (J. Barber, ed.). Elsevier Science Publishers B.V.Google Scholar
  10. 10.
    Susi H. (1969) Infrared spectra of biological macromolecules and related systems. in: ‘Structure and Stability of Biological Macromolecules’, (Timasheff S.N. and Fasman G.D., eds.) pp. 575–663, Dekker, New York.Google Scholar
  11. 11.
    Nabedryk E. and Breton J. (1981) Orientation of intrinsic proteins in photosynthetic membranes. Polarized infrared spectroscopy of chloroplasts and chromatophores. Biochim. Biophys. Acta 635, 515–524.PubMedCrossRefGoogle Scholar
  12. 12.
    Susi H. and Byler D.M. (1983) Protein structure by Fourier transform infrared spectroscopy: second derivative spectra. Biochem. Biophys. Res. Commun. 115, 391–397.PubMedCrossRefGoogle Scholar
  13. 13.
    Chen Y.H., Yang T. and Chau K.H. (1974) Determination of the alpha-helix and beta form of proteins in acqueous solution by circular dichroism. Biochemistry 13, 3350–3359.PubMedCrossRefGoogle Scholar
  14. 14.
    Henderson R. and Unwin P.N.T. (1975) Three-dimensional model of purple membrane obtained by electron microscopy. Nature (Lond.) 257, 28–32.CrossRefGoogle Scholar
  15. 15.
    Rothschild K.J. and Clark N.A. (1979) Polarized infrared spectroscopy of oriented purple membrane. Biophys. J. 25, 473–488.PubMedCrossRefGoogle Scholar
  16. 16.
    Nabedryk E., Bardin A.-M. and Breton J. (1985) Further characterization of protein secondary structures in purple membrane by circular dichroism and polarized infrared spectroscopies. Biophys. J. 48, 873–876,PubMedCrossRefGoogle Scholar
  17. 17.
    Kieffel B.R., Garavito M., Baumeister W. and Rosenbusch J.P. (1985) Secondary structure of a channel-forming protein: porin from E. coli outer membranes. EMBO J. 4, 1589–1592.Google Scholar
  18. 18.
    Nabedryk E., Garavito R.M. and Breton J. (1988) The orientation of beta-sheets in porin. A polarized Fourier transform infrared spectroscopic investigation. Biophys. J. 53, 671–676.PubMedCrossRefGoogle Scholar
  19. 19.
    Mao D. and Wallace B.A. (1984) Differential light scattering and absorption flattening optical effects are minimal in the circular dichroism spectra of small unilamellar vesicles. Biochemistry 23, 2667–2673.PubMedCrossRefGoogle Scholar
  20. 20.
    Nabedryk E., Tiede D.M., Dutton P.L. and Breton J. (1982) Conformation and orientation of the protein in the bacterial photosynthetic reaction center. Biochim. Biophys. Acta 682, 273–280.CrossRefGoogle Scholar
  21. 21.
    Byler D.M. and Susi H. (1986) Examination of the secondary structure of proteins by deconvolved FTIR spectra. Biopolymers. 25, 469–487.PubMedCrossRefGoogle Scholar
  22. 22.
    Trewhella J., Popot J.-L., Zaccai G. and Engelman D.M. (1986) Localization of two chymotryptic fragments in the structure of renatured bacteriorhodopsin by neutron diffraction. EMBO J. 5, 3045–3049.PubMedGoogle Scholar
  23. 23.
    Tsygannik I.N. and Baldwin J.M. (1987) Three-dimensional structure of deoxycholate-treated purple membrane at 6A resolution and molecular averaging of three crystals forms of bacteriorhodopsin. Eur. Biophys. J. 14, 263–272.CrossRefGoogle Scholar
  24. 24.
    Williams J.C., Steiner L.A., Ogden R.C., Simon M.I. and Feher G. (1983) Primary structure of the M subunit of the reaction center from Rhodopseudomonas sphaeroides. Proc. Natl. Acad. Sci., USA 80, 6505–6509.PubMedCrossRefGoogle Scholar
  25. 25.
    Williams J.C., Steiner L.A., Feher G. and Simon M.I. (1984) Primary structure of the L subunit of the reaction center from Rhodopseudomonas sphaeroides. Proc. Natl. Acad. Sci USA 81, 7303–7307.PubMedCrossRefGoogle Scholar
  26. 26.
    Nabedryk E., Berger G., Andrianambinintsoa S. and Breton J. (1985) Comparison of alpha-helix orientation in the chromatophore, quantasome and reaction centre of Rhodopseudomonas viridis by circular dichroism and polarized infrared spectroscopy. Biochim. Biophys. Acta 809, 271–276.CrossRefGoogle Scholar
  27. 27.
    Yeates T.O, Komiya H., Rees D.C., Allen J.P. and Feher G. (1987) Structure of the reaction center from Rhodobacter sphaeroides R-26: membrane-protein interactions. Proc. Natl. Acad. Sci. USA 84, 6438–6442.PubMedCrossRefGoogle Scholar
  28. 28.
    Nabedryk E., Tiede D.M., Dutton P.L. and Breton J. (1984) Polarized infrared spectroscopy of bacterial reaction centers; the LMH and LM complexes in reconstituted membranes in: ‘Advances in Photosynthesis Research’, Vol. II, 177–180. (Sybesma C, ed.), Nijhoff M, Junk D.W. Publ.Google Scholar
  29. 29.
    Nabedryk E., Andrianambinintsoa S. and Breton J. (1984) Transmembrane orientation of alpha-helices in the thylakoid membrane and in the light-harvesting complex. A polarized infrared spectroscopy study. Biochim. Biophys. Acta 765, 380–387.CrossRefGoogle Scholar
  30. 30.
    Hiller R.G., Bardin A.-M. and Nabedryk E. (1987) The secondary structure content of pigment-protein complexes from the thylakoids of two chromophyte algae. Biochim. Biophys. Acta 894, 365–369.CrossRefGoogle Scholar
  31. 31.
    Nabedryk E., Biaudet P., Darr S., Arntzen C.J. and Breton J., Breton J. (1984) Conformation and orientation of chlorophyll-proteins in Photosystem-I by circular dichroism and polarized infrared spectroscopies. Biochim. Biophys. Acta 767, 640–647.CrossRefGoogle Scholar
  32. 32.
    Mäntele W., Nabedryk E., Tavitian B.A., Kreutz W. and Breton J. (1985) Light-Induced Fourier transform infrared (FTIR) spectroscopic investigations of the primary donor oxidation in bacterial photosynthesis. FEBS Lett. 187, 227–232.CrossRefGoogle Scholar
  33. 33.
    Nabedryk E., Mäntele W., Tavitian B.A. and Breton J. (1986) Light-induced Fourier transform infrared (FTIR) spectroscopic investigations of the intermediary electron acceptor reduction in bacterial photosynthesis. Photochem. Photobiol. 43, 461–465.CrossRefGoogle Scholar
  34. 34.
    Nabedryk E., Tavitian B.A., Mäntele W., Kreutz W. and Breton J. (1987) Fourier transform infrared (FTIR) spectroscopic investigations of the primary reaction in purple photosynthetic bacteria, in ‘Progress in Photosynthesis Research’, Vol. I, pp. 177–180. (Biggins J., ed.). Martinus Nijhoff Publ., Dordrecht.Google Scholar
  35. 35.
    Mäntele W.G., Wollenweber A., Nabedryk E. and Breton J. (198 Infrared spectroelectrochemistry of bacteriochlorophylls and bacteriopheophytins: implications for the binding of the pigments in the reaction center from photosynthetic bacteria. Proc. Natl. Acad. Sci. USA. 8468–8472.Google Scholar
  36. 36.
    Tavitian B.A., Nabedryk E., Mäntele W. and Breton J. (1986) Light-induced Fourier transform infrared (FTIR) spectroscopic investigations of primary reactions in Photosystem I and Photosystem II. FEBS Lett. 201, 151–157.CrossRefGoogle Scholar
  37. 37.
    Tavitian B.A., Nabedryk E., Wollenweber A., Mäntele W. and Breton J. (1988) FTIR spectroscopy of primary photosynthetic reactions in the two photosystems of green plants. Comparison with spectroelectrochemistry of chlorophyll models, in: ‘Spectroscopy of Biological Molecules New Advances’, (Schmidt E.D., Schneider F.W. & Siebert F., eds.), Wiley & Sons Chichester, UK, pp. 297–300.Google Scholar
  38. 38.
    Ballschmiter K. and Katz J.J. (1969) An infrared study of chlorophyll-chlorophyll and chlorophyll-water interactions. J. Am. Chem. Soc. 91, 2661–2677.CrossRefGoogle Scholar
  39. 39.
    Wollenweber A. (1986) Spektroelektrochemische Untersuchungen an den Bakteriochlorophyllen a und b, sowie den Bakteriophäophytinen a und b. Diplomarbeit Universität Freiburg, FRG.Google Scholar
  40. 40.
    Mäntele W., Wollenweber A., Rashwan F., Heinze J., Nabedryk Berger G. and Breton J. (1988) Fourier transform infrared spectroelectrochemistry of the bacteriochlorophyll a anion radical. Photochem. Photobiol. 47, 451–455.CrossRefGoogle Scholar
  41. 41.
    Mäntele W., Wollenweber A., Nabedryk E., Breton J., Rashwan Heinze J. and Kreutz W. (1987) Fourier-transform infrared (FTIR) spectroelectrochemistry of bacteriochlorophylls. in ‘Progress in Photosynthesis Research’. Vol. I, pp. 329–332. (Biggins J., ed.). Martinus Nijhoff Publ., Dordrecht.Google Scholar
  42. 42.
    Michel H., Epp O. and Deisenhofer J. (1986) Pigment-protein interactions in the photosynthetic reaction centre from Rhodopseudomonas viridis. EMBO J. 5, 2445–2451.PubMedGoogle Scholar
  43. 43.
    Tiede D.M., Budil D.E., Tang J., El-Kabbani O., Norris J.R., Chang C.H. and Schiffer M. (1988) Symmetry breaking structures involved in the docking of cytochrome c and primary electron transfer in reaction centers of Rhodobacter sphaeroides. in: ‘The Photosynthetic Bacterial Reaction Center: Structure and Dynamics’, (Breton J. and Vermeglio A., eds.) Vol. 149, pp. 13–20. NATO ASI Series, Plenum, N.Y.Google Scholar
  44. 44.
    Robert B. and Lutz M. (1986) Structure of the primary donor of Rhodopseudomonas sphaeroides: difference resonance Raman spectroscopy of reaction centers. Biochemistry 25(9), 2303–2309.CrossRefGoogle Scholar
  45. 45.
    Zhou Q., Robert B. and Lutz M. (1987) Interspecific structural variations of the primary donor in bacterial reaction centers. in: ‘Progress in Photosynthesis Research’, Vol. 1, pp. 395–398. (Biggins J., ed.), Martinus Nijhoff. Publ., Dordrecht.Google Scholar
  46. 46.
    Nabedryk E., Andrianambinintsoa S., Mäntele W. and Breton J. (1988) FTIR spectroscopic investigations of the intermediary electron acceptor photoreduction in purple photosynthetic bacteria and green plants. in: ‘The Photosynthetic Bacterial Reaction Centers: Structure and Dynamics’, (Breton J. and Vermeglio A., eds.), Vol. 149, pp. 237–250. NATO ASI Series, Series A: Life Sciences, Plenum, New York.Google Scholar
  47. 47.
    Allen J.P., Feher G., Yeates T.O., Komiya H. and Rees D.C. (1988) Structure of the reaction center from Rhodobacter sphaeroides R-26 and 2.4.1. in: ‘The Photosynthetic Bacterial Reaction Center: Structure and Dynamics’, (Breton J. and Vermeglio A., eds.) Vol. 149, pp. 5–11. NATO ASI Series, Plenum, N.Y.Google Scholar
  48. 48.
    Feher G., Isaacson R.A., Okamura M.Y. and Lubitz W. (1988) Endor of exchangeable protcns of the reduced intermediate acceptor in reaction cent rs from Rhodobacter sphaeroides R-26. in: ‘The Photosynthetic Bacterial Reaction Center: Structure and Dynamics’, (Breton J. and Vermeglio A., eds.) Vol. 149, pp. 229–235. NATO ASI Series, Plenum, N.Y.Google Scholar

Copyright information

© Plenum Press, New York 1989

Authors and Affiliations

  • E. Nabedryk
    • 1
  • W. Mäntele
    • 2
  • J. Breton
    • 1
  1. 1.Service de Biophysique, Département de BiologieCEN SaclayGif-sur-Yvette cedexFrance
  2. 2.Institut für Biophysik und StralhenbiologieUniversität FreiburgFreiburgGermany

Personalised recommendations