Photosynthesis Research

, Volume 85, Issue 1, pp 115–131 | Cite as

High potential iron–sulfur proteins and their role as soluble electron carriers in bacterial photosynthesis: tale of a discovery

  • Stefano Ciurli
  • Francesco Musiani


This review is an attempt to retrace the chronicle of the discovery of the role of high-potential iron–sulfur proteins (HiPIPs) as electron carriers in the photosynthetic chain of bacteria. Data and facts are presented through the magnifying lenses of the authors, using their best judgment to filter and elaborate on the many facets of the research carried out on this class of proteins over the years. The tale is divided into four main periods: the seeds, the blooming, the ripening, and the harvest, representing the times from the discovery of these proteins to the most recent advancements in the understanding of the relationship between their structure and their function.


bacterial photosynthesis electron transfer high potential iron–sulfur protein molecular modeling photosynthetic reaction center protein docking tetraheme cytochrome subunit 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Alric, J, Yoshida, M, Nagashima, KV, Hienerwadel, R, Parot, P, Vermeglio, A, Chen, SW, Pellequer, JL 2004Two distinct binding sites for high potential iron–sulfur protein and cytochrome c on the reaction center-bound cytochrome of Rubrivivax gelatinosusJ Biol Chem2793254532553Google Scholar
  2. Bartsch, RG 1963Non-heme iron proteins and Chromatium iron proteinGest, HSan Pietro, AVerdon, LP eds. Bacterial PhotosynthesisAntioch PressYellow Springs, OH315326Google Scholar
  3. Bartsch, RG 1991The distribution of soluble metallo-redox proteins in purple phototrophic bacteriaBiochim Biophys Acta10582830Google Scholar
  4. Borsari, M, Benini, S, Marchesi, D, Ciurli, S 1997Cyclic voltammetry and spectroelectrochemistry of cytochrome c8 from Rubrivivax gelatinosus Implications in photosynthetic electron transferInorg Chim Acta263379384Google Scholar
  5. Carter, CW,Jr 2001High potential iron–sulfur proteinsMesserschmidt, AHuber, RWieghardt, KPoulos, T eds. Handbook of MetalloproteinsJohn WileyChichester, UK602609Google Scholar
  6. Carter, CW,Jr, Kraut, J, Freer, ST, Alden, RA, Sieker, LC, Adman, E, Jensen, LH 1972A comparison of [Fe4S4] clusters in high potential iron protein and in ferredoxinProc Natl Acad Sci USA6935263529Google Scholar
  7. Carter, CW,Jr, Kraut, J, Freer, ST, Xoung, NH, Alden, RA, Bartsch, RG 1974Two-Ångstrom crystal structure of oxydized Chromatium high potential iron proteinJ Biol Chem24942124225Google Scholar
  8. De Klerk, H, Kamen, MD 1966A high potential non-haem iron protein from the facultative photoheterotroph Rhodopseudomonas gelatinosaBiochim Biophys Acta2175178Google Scholar
  9. Dus, K, De Klerk, H, Sletten, K, Bartsch, RG 1967Chemical characterization of high potential iron proteins from Chromatium and Rhodopseudomonas gelatinosaBiochim Biophys Acta140291311Google Scholar
  10. Dutton, PL, Leigh, JS 1973Electron spin resonance characterization of Chromatium D hemes, non-heme irons and the components involved in primary photosynthesisBiochim Biophys Acta314178190Google Scholar
  11. Evans, MCW, Lord, AV, Reeves, SG 1974The detection and characterization by electron paramagnetic resonance spectroscopy of iron–sulfur proteins and other electron-transport components in chromatophores from the purple bacterium ChromatiumBiochem J138177183Google Scholar
  12. Fukumori, Y, Yamanaka, T 1979A high-potential non-heme iron protein (HiPIP)-linked thiosulfate-oxidizing enzyme derived from Chromatium vinosumCurr Microbiol3117120Google Scholar
  13. Hiraishi, A, Hoshino, Y, Satoh, T 1991Rhodoferax fermentans gen. nov., sp. nov., a phototrophic purple non-sulfur bacterium previously referred to as the ‘Rhodocyclus gelatinosus-like’ groupArch Microbiol155330336Google Scholar
  14. Hochkoeppler, A, Ciurli, S, Venturoli, G, Zannoni, D 1995The high potential iron–sulfur protein (HiPIP). from Rhodoferax fermentans is competent in photosynthetic electron transferFEBS Lett3577074Google Scholar
  15. Hochkoeppler, A, Kofod, P, Ferro, G, Ciurli, S 1995Isolation, characterization, and functional role of the high-potential iron–sulfur protein (HiPIP). from Rhodoferax fermentansArch Biochem Biophys322313318Google Scholar
  16. Hochkoeppler, A, Moschettini, G, Zannoni, D 1995The electron transport system of the facultative phototroph Rhodoferax fermentans. I. A functional, thermodynamic␣and spectroscopic study of the respiratory chain of dark- and light-grown cellsBiochim Biophys Acta12297380Google Scholar
  17. Hochkoeppler, A, Zannoni, D, Ciurli, S, Meyer, TE, Cusanovich, MA, Tollin, G 1996Kinetics of photo-induced electron transfer from high-potential iron–sulfur protein to the photosynthetic reaction center of the purple phototroph Rhodoferax fermentansProc Natl Acad Sci USA9369987002Google Scholar
  18. Hochkoeppler, A, Zannoni, D, Venturoli, G 1995The electron transport system of the facultative phototroph Rhodoferax fermentans. II. Flash-induced oxidation of membrane-bound cytochromes cBiochim. Biophys. Acta12298188Google Scholar
  19. Hochkoeppler, A, Ciurli, S, Kofod, P, Venturoli, G, Zannoni, D 1997On the role of cytochrome c8 in photosynthetic electron transfer of the purple non-sulfur bacterium Rhodoferax fermentansPhotosynth Res531321Google Scholar
  20. Hori, K 1961Electron transporting components partecipating in nitrate and oxygen respirations from a halotolerant Micrococcus. II. Properties of cytochrome c551 and brown proteinJ Biochem50481485Google Scholar
  21. Hori, K 1961Electron transporting components participating in nitrate and oxygen respirations from a halotolerant Micrococcus. I. Purification and properties of cytochromes b4 (I). and b4 (II)J Biochem50440449Google Scholar
  22. Kennel, SJ, Bartsch, RG, Kamen, MD 1972Observations on light-induced oxidation reactions in the electron transport system of ChromatiumBiophys J12882896Google Scholar
  23. Knaff, DB, Whetstone, R, Carr, JW 1980The role of soluble cytochrome c-551 in cyclic electron flow-driven active transport in Chromatium vinosumBiochim Biophys Acta5905058Google Scholar
  24. Kurnikov IV (2000). HARLEM Molecular Modeling Package, 1.0 edn. Department of Chemistry, University of Pittsburgh, Pittsburgh, PAGoogle Scholar
  25. Lange, C, Hunte, C 2002Crystal structure of the yeast cytochrome bc1 complex with its bound substrate cytochrome cProc Natl Acad Sci USA9928002805Google Scholar
  26. Lieutaud, C, Nitschke, W, Vermeglio, A, Parot, P, Schoepp-Cothenet, B 2003HiPIP in Rubrivivax gelatinosus is firmly associated to the membrane in a conformation efficient for electron transfer towards the photosynthetic reaction centerBiochim Biophys Acta15578390Google Scholar
  27. Matsuura, K, Fukushima, A, Shimada, K, Satoh, T 1988Direct and indirect electron transfer from cytochromes c and c2 to the photosynthetic reaction center in pigment-protein complexes isolated from Rhodocyclus gelatinosusFEBS Lett.2372125Google Scholar
  28. Menin, L, Schoepp, B, Parot, P, Vermeglio, A 1997Photoinduced cyclic electron transfer in Rhodocyclus tenuis cells: participation of HiPIP or cytochrome c8 depending on the ambient redox potentialBiochemistry361218312188Google Scholar
  29. Menin, LG, Parot, P, Schoepp, B, Nitschke, W, Vermeglio, A 1998Role of HiPIP as electron-donor to the RC-bound cytochrome in photosynthetic purple bacteriaPhotosynth Res55343348Google Scholar
  30. Menin, L, Yoshida, M, Jaquinod, M, Nagashima, KV, Matsuura, K, Parot, P, Vermeglio, A 1999Dark aerobic growth conditions induce the synthesis of a high midpoint potential cytochrome c8 in the photosynthetic bacterium Rubrivivax gelatinosusBiochemistry381523815244Google Scholar
  31. Nagashima, KV, Matsuura, K, Shimada, K, Vermeglio, A 2002High-potential iron–sulfur protein (HiPIP). is the major electron donor to the reaction center complex in photosynthetically growing cells of the purple bacterium Rubrivivax gelatinosusBiochemistry411402814032Google Scholar
  32. Nitschke, W, Dracheva, SM 1995Reaction center associated cytochromesBlankenship, REMadigan, MTBauer, CE eds. Anoxygenic Photosynthetic BacteriaKluwer Academic PublishersDordrecht, The Netherlands775805Google Scholar
  33. Osyczka, A, Yoshida, M, Nagashima, KVP, Shimada, K, Matsuura, K 1997Electron transfer from high potential iron–sulfur protein and low potential cytochrome c-551 to the primary donor of Rubrivivax gelatinosus reaction center mutationally devoid of the bound cytochrome subunitBiochim Biophys Acta13219399Google Scholar
  34. Osyczka, A, Nagashima, KVP, Sogabe, S, Miki, K, Yoshida, M, Shimada, K, Matsuura, K 1998Interaction site for soluble cytochromes on the tetraheme cytochrome subunit bound to the bacterial photosynthetic reaction center mapped by site-directed mutagenesisBiochemistry371173211744Google Scholar
  35. Osyczka, A, Nagashima, KV, Shimada, K, Matsuura, K 1999Interaction site for high potential iron–sulfur protein on the tetraheme cytochrome subunit bound to the photosynthetic reaction center of Rubrivivax gelatinosusBiochemistry3828612865Google Scholar
  36. Osyczka, A, Nagashima, KV, Sogabe, S, Miki, K, Shimada, K, Matsuura, K 1999Comparison of the binding sites for high potential iron–sulfur protein and cytochrome c on the tetraheme cytochrome subunit bound to the bacterial photosynthetic reaction centerBiochemistry381577915790Google Scholar
  37. Osyczka, A, Nagashima, KV, Sogabe, S, Miki, K, Shimada, K, Matsuura, K 2001Different mechanisms of the binding of soluble electron donors to the photosynthetic reaction center of Rubrivivax gelatinosus and Blastochloris viridisJ Biol Chem2762410824112Google Scholar
  38. Page, CC, Moser, CC, Chen, X, Dutton, PL 1999Natural engineering principles of electron tunnelling in biological oxidation-reductionNature4024752Google Scholar
  39. Samyn, B, De Smet, L, Driessche, G, Meyer, TE, Bartsch, RG, Cusanovich, MA, Van Beeumen, JJ 1996A high potential soluble cytochrome c-551 from the purple phototrophic bacterium Chromatium vinosum is homologous to cytochrome c8 from denitrifying PseudomonadsEur J Biochem236689696Google Scholar
  40. Strahs, G, Kraut, J 1968Low resolution electron-density and anomalous-scattering-density maps of Chromatium high-potential iron proteinJ Mol Biol35503512Google Scholar
  41. Tan, J, Corson, GE, Chen, YN, Garcia, MC, Güner, S, Knaff, DB 1993The uniquinol:cytochrome c2/c oxidoreductase of Chromatium vinosumBiochim Biophys Acta11446976Google Scholar
  42. Tedro, SV, Meyer, TE, Kamen, MD 1977Primary structure of a high potential iron–sulfur protein from a moderately halophilic denitrifying coccusJ Biol Chem25278267833Google Scholar
  43. Van Driessche, G, Vandenberghe, I, Devreese, B, Samyn, B, Meyer, TE, Leigh, R, Cusanovich, MA, Bartsch, RG, Fischer, U, Van Beeumen, JJ 2003Amino acid sequences and distribution of high potential iron–sulfur proteins that donate electrons to the photosynthetic reaction center in phototropic proteobacteriaJ Mol Evol57181199Google Scholar
  44. Grondelle, R, Duysens, LNM, Wel, JA, Wal, HN 1977Function and properties of a soluble c-type cytochrome c-551 in secondary photosynthetic electron transport in whole cells of Chromatium vinosum as studied with flash spectroscopyBiochim Biophys Acta461188201Google Scholar
  45. Venturoli, G, Mamedov, MD, Mansy, SS, Musiani, F, Strocchi, M, Francia, F, Semenov, AY, Cowan, JA, Ciurli, S 2004Electron transfer from HiPIP to the photooxidized tetraheme cytochrome subunit of Allochromatium vinosum reaction center: new insights from site-directed mutagenesis and computational studiesBiochemistry43437445Google Scholar
  46. Vermeglio, A, Li, J, Schoepp-Cothenet, B, Pratt, N, Knaff, DB 2002The role of high potential iron protein and cytochrome c8 as alternative electron donors to the reaction center of Chromatium vinosumBiochemistry4188688875Google Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  1. 1.Laboratory of Bioinorganic Chemistry, Department of Agro-Environmental Science and TechnologyUniversity of Bologna Viale Giuseppe Fanin 40BolognaItaly

Personalised recommendations