Advertisement

Photosynthesis Research

, Volume 137, Issue 3, pp 361–375 | Cite as

Remembering George Feher (1924–2017)

  • Melvin Y. OkamuraEmail author
  • Wolfgang Lubitz
  • James P. Allen
History and Biography

Abstract

We provide a tribute to George Feher, one of the founding scientists in the use of biophysical techniques to probe photosynthetic complexes, especially the bacterial reaction center. His early life is briefly reviewed followed by a description of the impact of his 30 years of photosynthesis research. We describe his pioneering work in bacterial photosynthesis that helped to provide a detailed picture of the molecular events responsible for light energy capture and the subsequent electron and proton transfer events in photosynthetic organisms. These studies had a profound and lasting impact on our understanding of the molecular mechanisms of photosynthesis. We also include some personal comments from his former students and colleagues.

Keywords

Photosynthetic bacteria Reaction centers Rhodobacter sphaeroides Electron paramagnetic resonance Electron-nuclear double resonance Electron transfer Proton transfer 

References

  1. Allen JP, Feher G, Yeates TO, Komiya H, Rees DC (1987) Structure of the reaction center from Rhodobacter sphaeroides R-26: the protein subunits. Proc Natl Acad Sci USA 84:6162–6166CrossRefPubMedGoogle Scholar
  2. Arnold W, Clayton RK (1960) The first step in photosynthesis: evidence for its electronic nature. Proc Natl Acad Sci USA 46:769–776CrossRefPubMedGoogle Scholar
  3. Axelrod HL, Abresch EC, Okamura MY, Yeh AP, Rees DC, Feher G (2002) X-ray structure determination of the cytochrome c 2: reaction center electron transfer complex from Rhodobacter sphaeroides. J Mol Biol 319:501–515CrossRefPubMedGoogle Scholar
  4. Clayton RK (1963) Toward the isolation of a photochemical reaction center in Rhodopseudomonas spheroides. Biochim Biophys Acta 75:312–323CrossRefPubMedGoogle Scholar
  5. Debus RJ, Feher G, Okamura MY (1986) Iron-depleted reaction centers from Rhodopseudomonas sphaeroides R-26.1: characterization and reconstitution with Fe2+, Mn2+, Co2+, Ni2+, Cu2+, and Zn2+. Biochemistry 25:2276–2287CrossRefPubMedGoogle Scholar
  6. Deisenhofer J, Epp O, Miki K, Huber R, Michel H (1984) Structure of the protein subunits in the photosynthetic reaction centre of Rhodopseudomonas viridis at 3 Å resolution. Nature 318:618–624CrossRefGoogle Scholar
  7. Feher G (1956) Observation of nuclear magnetic resonances via the electron spin resonance line. Phys Rev 103:834–835CrossRefGoogle Scholar
  8. Feher G (1957a) Sensitivity considerations in microwave paramagnetic resonance absorption techniques. Bell Syst Tech J 36:449–484CrossRefGoogle Scholar
  9. Feher G (1957b) Electronic structure of F centers in KCl by the electron spin double-resonance technique. Phys Rev 105:1122–1123CrossRefGoogle Scholar
  10. Feher G (1959) Electron spin resonance experiments on donors in silicon. I. Electronic structure of donors by the electron nuclear double resonance technique. Phys Rev 114:1219–1244CrossRefGoogle Scholar
  11. Feher G (1971) Some chemical and physical properties of a bacterial reaction center particle and its primary photochemical reactants. Photochem Photobiol 14:373–387CrossRefPubMedGoogle Scholar
  12. Feher G (1988) Light reflections. In: Breton J, Verméglio A (eds) The photosynthetic bacterial reaction center. Plenum Press, New York, pp 435–440CrossRefGoogle Scholar
  13. Feher G (1992) Light reflections II. In: Breton J, Verméglio A (eds) The photosynthetic bacterial reaction center II. Plenum Press, New York, pp 421–425CrossRefGoogle Scholar
  14. Feher G (1998a) Three decades of research in bacterial photosynthesis and the road leading to it: a personal account. Photosynth Res 55:1–40CrossRefGoogle Scholar
  15. Feher G (1998b) Light reflections III. Photosynth Res 55:375–378CrossRefGoogle Scholar
  16. Feher G (2002) My road to biophysics: picking flowers on the way to photosynthesis. Ann Rev Biophys Biomol Struct 31:1–44CrossRefGoogle Scholar
  17. Feher G (2017) Thoughts on the holocaust. Feher Publishing, La JollaGoogle Scholar
  18. Feher G, Hoff AJ, Isaacson RA, Ackerson LC (1975) ENDOR experiments on chlorophyll and bacteriochlorophyll in vitro and in the photosynthetic unit. Ann NY Acad Sci 244:239–259CrossRefPubMedGoogle Scholar
  19. Feher G, Allen JP, Okamura MY, Rees DC (1989) Structure and function of bacterial photosynthetic reaction centres. Nature 339:111–116CrossRefGoogle Scholar
  20. Flores M, Isaacson R, Abresch E, Calvo R, Lubitz W, Feher G (2007) Protein-cofactor interactions in bacterial reaction centers from Rhodobacter sphaeroides R-26: II. Geometry of the hydrogen bonds to the primary quinone QA ·− by 1H and 2H ENDOR spectroscopy. Biophys J 92:671–682CrossRefPubMedGoogle Scholar
  21. Gopher A, Blatt Y, Schönfeld M, Okamura MY, Feher G, Montal M (1985) The effect of an applied electric field on the charge recombination kinetics in reaction centers reconstituted in planar lipid bilayers. Biophys J 48:311–320CrossRefPubMedPubMedCentralGoogle Scholar
  22. Graige MS, Feher G, Okamura MY (1998) Conformational gating of the electron transfer reaction QA –·QB → QAQB –· in bacterial reaction centers of Rhodobacter sphaeroides determined by a driving force assay. Proc Natl Acad Sci USA 95:11679–11684CrossRefPubMedGoogle Scholar
  23. Kleinfeld D, Okamura MY, Feher G (1984) Electron-transfer kinetics in photosynthetic reaction centers cooled to cryogenic temperatures in the charge-separated state: evidence for light-induced structural changes. Biochemistry 23:5780–5786CrossRefPubMedGoogle Scholar
  24. Lendzian F, Huber M, Isaacson RA, Endeward B, Plato M, Bönigk B, Möbius K, Lubitz W, Feher G (1993) The electronic structure of the primary donor cation radical in Rhodobacter sphaeroides R-26: ENDOR and TRIPLE resonance studies in single crystals of reaction centers. Biochim Biophys Acta 1183:139–160CrossRefGoogle Scholar
  25. Loach PA, Hall RL (1972) The question of the primary electron acceptor in bacterial photosynthesis. Proc Natl Acad Sci USA 69:786–790CrossRefPubMedGoogle Scholar
  26. Lubitz W, Feher G (1999) The primary and secondary acceptors in bacterial photosynthesis III. Characterization of the quinone radicals QA –· and QB –· by EPR and ENDOR. Appl Magn Reson 17:1–48CrossRefGoogle Scholar
  27. McElroy JD, Feher G, Mauzerall DC (1972) Characterization of primary reactants in bacterial photosynthesis: I. Comparison of the light-induced EPR signal (g = 2.0026) with that of a bacteriochlorophyll radical. Biochim Biophys Acta 267:363–374CrossRefPubMedGoogle Scholar
  28. Mitchell P (1966) Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. Biol Rev 41:445–502CrossRefPubMedGoogle Scholar
  29. Norris JR, Uphaus RA, Crespi HL, Katz JJ (1971) Electron spin resonance of chlorophyll and the origin of signal I in photosynthesis. Proc Natl Acad Sci USA 68:625–628CrossRefPubMedGoogle Scholar
  30. Norris JR, Druyan ME, Katz JJ (1973) Electron nuclear double resonance of bacteriochlorophyll free radical in vitro and in vivo. J Am Chem Soc 95:1680–1682CrossRefPubMedGoogle Scholar
  31. Okamura M (2014) George Feher: a pioneer in reaction center research. Photosyn Res 120:29–42CrossRefPubMedGoogle Scholar
  32. Okamura MY, Isaacson RA, Feher G (1975) Primary acceptor in bacterial photosynthesis: obligatory role of ubiquinone in photoactive reaction centers of Rhodopseudomonas spheroides. Proc Natl Acad Sci USA 72:3491–3495CrossRefPubMedGoogle Scholar
  33. Paddock ML, Feher G, Okamura MY (2003) Proton transfer pathways and mechanism in bacterial reaction centers. FEBS Lett 555:45–50CrossRefPubMedGoogle Scholar
  34. Reed DW, Clayton RK (1968) Isolation of a reaction center fraction from Rhodopseudomonas spheroides. Biochem Biophys Res Commun 30:471–475CrossRefPubMedGoogle Scholar
  35. Sienkiewicz A, Smith BG, Veselov A, Scholes CP (1996) Tunable Q-band resonator for low temperature electron paramagnetic resonance/electron nuclear double resonance measurements. Rev Sci Instrum 67:2134–2138CrossRefGoogle Scholar
  36. Slichter CP (1990) Principles of magnetic resonance, 3rd edn. Springer, Berlin, p 266CrossRefGoogle Scholar
  37. Steiner LA, Okamura MY, Lopes AD, Moskowitz E, Feher G (1974) Characterization of reaction centers from photosynthetic bacteria. II. Amino acid composition of the reaction center protein and its subunits in Rhodopseudomonas spheroides R-26. Biochem 13:1403–1410CrossRefGoogle Scholar
  38. Stowell MHB, McPhillips TM, Rees DC, Soltis SM, Abresch E, Feher G (1997) Light-induced structural changes in photosynthetic reaction center: Implications for mechanism of electron-proton transfer. Science 276:812–816CrossRefPubMedGoogle Scholar
  39. Sutton MR, Rosen D, Feher G, Steiner LA (1982) Amino-terminal sequences of the L, M, and H subunits of reaction centers from the photosynthetic bacterium Rhodopseudomonas sphaeroides R-26. Biochemistry 21:3842–3849CrossRefPubMedGoogle Scholar
  40. Valkirs GE, Feher G (1982) Topography of reaction center subunits in the membrane of the photosynthetic bacterium, Rhodopseudomonas sphaeroides. J Cell Biol 95:179–188CrossRefPubMedGoogle Scholar
  41. Williams JC, Steiner LA, Feher G (1986) Primary structure of the reaction center from Rhodopseudomonas sphaeroides. Proteins 1:312–325CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of PhysicsUniversity of California San DiegoLa JollaUSA
  2. 2.Max Planck Institute for Chemical Energy ConversionMülheim an der RuhrGermany
  3. 3.School of Molecular SciencesArizona State UniversityTempeUSA

Personalised recommendations