Advertisement

Photosynthesis Research

, Volume 92, Issue 1, pp 35–53 | Cite as

Heliobacterial photosynthesis

  • Mark Heinnickel
  • John H. Golbeck
Review Paper

Abstract

Heliobacteria contain Type I reaction centers (RCs) and a homodimeric core, but unlike green sulfur bacteria, they do not contain an extended antenna system. Given their simplicity, the heliobacterial RC (HbRC) should be ideal for the study of a prototypical homodimeric RC. However, there exist enormous gaps in our knowledge, particularly with regard to the nature of the secondary and tertiary electron acceptors. To paraphrase S. Neerken and J. Amesz (2001 Biochim Biophys Acta 1507:278–290): with the sole exception of primary charge separation, little progress has been made in recent years on the HbRC, either with respect to the polypeptide composition, or the nature of the electron acceptor chain, or the kinetics of forward and backward electron transfer. This situation, however, has changed. First, the low molecular mass polypeptide that contains the terminal FA and FB iron-sulfur clusters has been identified. The change in the lifetime of the flash-induced kinetics from 75 ms to 15 ms on its removal shows that the former arises from the P798+ [FA/FB] recombination, and the latter from P798+ FX recombination. Second, FX has been identified in HbRC cores by EPR and Mössbauer spectroscopy, and shown to be a [4Fe–4S]1+,2+ cluster with a ground spin state of S = 3/2. Since all of the iron in HbRC cores is in the FX cluster, a ratio of ∼22 Bchl g/P798 could be calculated from chemical assays of non-heme iron and Bchl g. Third, the N-terminal amino acid sequence of the FA/FB-containing polypeptide led to the identification and cloning of its gene. The expressed protein can be rebound to isolated HbRC cores, thereby regaining both the 75 ms kinetic phase resulting from P798+ [FA/FB] recombination and the light-induced EPR resonances of FA and FB . The gene was named ‘pshB’ and the protein ‘PshB’ in keeping with the accepted nomenclature for Type I RCs. This article reviews the current state of knowledge on the structure and function of the HbRC.

Keywords

Photosynthesis Heliobacteria FX FA FB Iron–sulfur cluster PshA PshB Type I RC Fe/S-type RC 

Notes

Acknowledgments

The authors thank Drs. Rufat Agalarov, Robert Blankenship, Donald Bryant, and Michael Madigan for stimulating discussions. The author’s work was funded by a grant from the US Department of Energy (DE-FG02-98ER20314). The Phototrophic Prokaryote Sequencing Project <http://genomes.tgen.org/funded>http://genomes.tgen.org/ was funded by the NSF Microbial Genome Sequencing Program.

References

  1. Adman ET, Siefker LC, Jensen LH (1976) Structure of Peptococcus aerogenes ferredoxin. Refinement at 2 Å resolution. J Biol Chem 251:3801–3806PubMedGoogle Scholar
  2. Albert I, Rutherford AW, Grav H, Kellermann J, Michel H (1998) The 18 kDa cytochrome c553 from Heliobacterium gestii: gene sequence and characterization of the mature protein. Biochemistry 37:9001–9008PubMedCrossRefGoogle Scholar
  3. Amesz J (1995) The heliobacteria, a new group of photosynthetic bacteria. J Photochem Photobiol B: Biol 30:89–96CrossRefGoogle Scholar
  4. Antonkine ML, Jordan P, Fromme P, Krauß N, Golbeck JH, Stehlik D (2003) Assembly of protein subunits within the stromal ridge of Photosystem I. Structural changes between unbound and sequentially PS I-bound polypeptides and correlated changes of the magnetic properties of the terminal iron sulfur clusters. J Mol Biol 327:671–697PubMedCrossRefGoogle Scholar
  5. Antonkine ML, Liu G, Bentrop D, Bryant DA, Bertini I, Luchinat C, Golbeck JH, Stehlik D (2002) Solution structure of the unbound, oxidized Photosystem I subunit PsaC, containing [4Fe–4S] clusters FA and FB: a conformational change occurs upon binding to Photosystem I. J Biol Inorg Chem 7:461–472PubMedCrossRefGoogle Scholar
  6. Aono S, Bentrop D, Bertini I, Cosenza G, Luchinat C (1998a) Solution structure of an artificial Fe8S8 ferredoxin: the D13C variant of Bacillus schlegelii Fe7S8 ferredoxin. Eur J Biochem 258:502–514PubMedCrossRefGoogle Scholar
  7. Aono S, Bentrop D, Bertini I, Donaire A, Luchinat C, Niikura Y, Rosato A (1998b) Solution structure of the oxidized Fe7S8 ferredoxin from the thermophilic bacterium Bacillus schlegelii by 1H NMR spectroscopy. Biochemistry 37:9812–9826PubMedCrossRefGoogle Scholar
  8. Barber J (1985) A new type of photosynthetic reaction centre. Trends Biochem Sci 10:17–19CrossRefGoogle Scholar
  9. Beck H, Hegeman G, White D (1990) Fatty acid and lipopolysaccharide analysis of three Heliobacterium spp. FEMS Microbiol Lett 69:229–232CrossRefGoogle Scholar
  10. Beer-Romero P, Gest H (1987) Heliobacillus mobilis, a peritrichously flagellated anoxyphototroph containing bacteriochlorophyll g. FEMS Microbiol Lett 41:109–114CrossRefGoogle Scholar
  11. Bertini I, Donaire A, Feinberg BA, Luchinat C, Piccioli M, Yuan HP (1995) Solution structure of the oxidized 2[4Fe–4S] ferredoxin from Clostridium pasteurianum. Eur J Biochem 232:192–205PubMedCrossRefGoogle Scholar
  12. Brettel K, Leibl W (2001) Electron transfer in Photosystem I. Biochim Biophys Acta 1507:100–114PubMedCrossRefGoogle Scholar
  13. Brettel K, Leibl W, Liebl U (1998) Electron transfer in the heliobacterial reaction center: evidence against a quinone-type electron acceptor functioning analogous to A1 in Photosystem I. Biochim Biophys Acta 1363:175–181PubMedCrossRefGoogle Scholar
  14. Brockmann H Jr, Lipinski A (1983) Bacteriochlorophyll g. A new bacteriochlorophyll from Heliobacterium chlorum. Arch Microbiol 136:17–19CrossRefGoogle Scholar
  15. Brok M, Vasmel H, Horikx JTG, Hoff AJ (1986) Electron transport components of Heliobacterium chlorum investigated by EPR spectroscopy at 9 and 35 GHz. FEBS Lett 194:322–326CrossRefGoogle Scholar
  16. Bryant DA, Frigaard NU (2006) Prokaryotic photosynthesis and phototrophy illuminated. Trends Microbiol 14:488–496PubMedGoogle Scholar
  17. Dauter Z, Wilson KS, Sieker LC, Meyer J, Moulis JM (1997) Atomic resolution (0.94 Å) structure of Clostridium acidurici ferredoxin. Detailed geometry of [4Fe–4S] clusters in a protein. Biochemistry 36:16065–16073PubMedCrossRefGoogle Scholar
  18. Deisenhofer J, Epp O, Miki K, Huber R, Michel H (1984) X-ray structure analysis of a membrane protein complex. Electron density map at 3 Å resolution and a model of the chromophores of the photosynthetic reaction center from Rhodopseudomonas viridis. J Mol Biol 180:385–398PubMedCrossRefGoogle Scholar
  19. Duee ED, Fanchon E, Vicat J, Sieker LC, Meyer J, Moulis JM (1994) Refined crystal structure of the 2[4Fe–4S] ferredoxin from Clostridium acidurici at 1.84 Å resolution. J Mol Biol 243:683–695PubMedCrossRefGoogle Scholar
  20. Enkh-Amgalan J, Kawasaki H, Seki T (2005) NifH and NifD sequences of heliobacteria: a new lineage in the nitrogenase phylogeny. FEMS Microbiol Lett 243:73–79PubMedCrossRefGoogle Scholar
  21. Enkh-Amgalan J, Kawasaki H, Seki T (2006) Molecular evolution of the nif gene cluster carrying nifI 1 and nifI 2 genes in the Gram-positive phototrophic bacterium Heliobacterium chlorum. Int J Syst Evol Microbiol 56:65–74PubMedCrossRefGoogle Scholar
  22. Fischer MR (1990) Photosynthetic electron transfer in Heliobacterium chlorum studied by EPR spectroscopy. Biochim Biophys Acta 1015:471–481CrossRefGoogle Scholar
  23. Fischer N, Hippler M, Sétif P, Jacquot JP, Rochaix JD (1998) The PsaC subunit of Photosystem I provides an essential lysine residue for fast electron transfer to ferredoxin. EMBO J 17:849–858PubMedCrossRefGoogle Scholar
  24. Fischer N, Sétif P, Rochaix JD (1999) Site-directed mutagenesis of the PsaC subunit of Photosystem I. FB is the cluster interacting with soluble ferredoxin. J Biol Chem 274:23333–23340PubMedCrossRefGoogle Scholar
  25. Fuller RC, Sprague SG, Gest H, Blankenship RE (1985) A unique photosynthetic reaction center from Heliobacterium chlorum. FEBS Lett 182:345–349CrossRefGoogle Scholar
  26. Gest H (1994) Discovery of heliobacteria. Photosynth Res 41:17–21CrossRefGoogle Scholar
  27. Gest H, Favinger JL (1983) Heliobacterium chlorum, an anoxygenic brownish-green photosynthetic bacterium containing a “new” form of bacteriochlorophyll. Arch Microbiol 136:11–16CrossRefGoogle Scholar
  28. Golbeck JH (1999) A comparative analysis of the spin state distribution of in vitro and in vivo mutants of PsaC. A biochemical argument for the sequence of electron transfer in Photosystem I as FX → FA → FB → ferredoxin/flavodoxin. Photosynth Res 61:107–144CrossRefGoogle Scholar
  29. Golbeck JH, Bryant DA (1991) Photosystem I. In: Lee CP (ed) Current topics in bioenergetics, vol 16. Academic Press, San Diego, CA, pp 83–177Google Scholar
  30. Hans M, Buckel W, Bill E (2000) The iron–sulfur clusters in 2-hydroxyglutaryl-CoA dehydratase from Acidaminococcus fermentans. Eur J Biochem 267:7082–7093PubMedCrossRefGoogle Scholar
  31. Hatano A, Seo D, Kitashima M, Sakurai H, Inoue K (2005) Purification of two ferredoxins and cloning of these genes from the photosynthetic bacterium Heliobacillus mobilis. In: van der Est A, Bruce D (eds) 13th International congress on photosynthesis. Allen Press Inc., Lawrence, Kansas, pp 83–85Google Scholar
  32. Hauska G, Schoedl T, Remigy H, Tsiotis G (2001) The reaction center of green sulfur bacteria. Biochim Biophys Acta 1507:260–277PubMedCrossRefGoogle Scholar
  33. Heinnickel M, Agalarov R, Svensen N, Krebs C, Golbeck JH (2006) Identification of FX in the heliobacterial reaction center as a [4Fe–4S] cluster with an S = 3/2 ground spin state. Biochemistry 45:6756–6764PubMedCrossRefGoogle Scholar
  34. Heinnickel M, Shen G, Agalarov R, Golbeck JH (2005) Resolution and reconstitution of a bound Fe–S protein from the photosynthetic reaction center of Heliobacterium modesticaldum. Biochemistry 44:9950–9960PubMedCrossRefGoogle Scholar
  35. Heinnickel M, Shen G, Golbeck JH (2007) Identification and characterization of PshB the dicluster ferredoxin that harbors the terminal electron acceptors FA and FB in Heliobacterium modesticaldum. Biochemistry 46:2530–2536PubMedCrossRefGoogle Scholar
  36. Hiraishi A (1989) Occurrence of menaquinone as the sole isoprenoid quinone in the photosynthetic bacterium Heliobacterium chlorum. Arch Microbiol 151:378–379CrossRefGoogle Scholar
  37. Jordan P, Fromme P, Witt HT, Klukas O, Saenger W, Krauß N (2001) Three dimensional structure of cyanobacterial Photosystem I at 2.5 Å resolution. Nature 411:909–917PubMedCrossRefGoogle Scholar
  38. Kandrashkin YE, Salikhov KM, van der Est A, Stehlik D (1998) Electron spin polarization in consecutive spin-correlated radical pairs: application to short-lived and long-lived precursors in type 1 photosynthetic reaction centres. Appl Magn Reson 15:417–447CrossRefGoogle Scholar
  39. Ke B (1973) The primary electron acceptor of Photosystem I. Biochim Biophys Acta 301:1–33PubMedGoogle Scholar
  40. Kern J, Loll B, Zouni A, Saenger W, Irrgang KD, Biesiadka J (2005) Cyanobacterial Photosystem II at 3.2 Å resolution—the plastoquinone binding pockets. Photosynth Res 84:153–159PubMedCrossRefGoogle Scholar
  41. Kimble LK, Madigan MT (1992a) Evidence for an alternative nitrogenase in Heliobacterium gestii. FEMS Microbiol Lett 100:255–260CrossRefGoogle Scholar
  42. Kimble LK, Madigan MT (1992b) Nitrogen fixation and nitrogen metabolism in heliobacteria. Arch Microbiol 158:155–161CrossRefGoogle Scholar
  43. Kimble LK, Mandelco L, Woese CR, Madigan MT (1995) Heliobacterium modesticaldum, sp. nov., a thermophilic heliobacterium of hot springs and volcanic soils. Arch Microbiol 163:259–267Google Scholar
  44. Kimble LK, Stevenson AK, Madigan MT (1994) Chemotrophic growth of heliobacteria in darkness. FEMS Microbiol Lett 115:51–56PubMedCrossRefGoogle Scholar
  45. Kleinherenbrink FAM, Aartsma TJ, Amesz J (1991) Charge separation and formation of bacteriochlorophyll triplets in Heliobacterium chlorum. Biochim Biophys Acta 1057:346–352CrossRefGoogle Scholar
  46. Kleinherenbrink FAM, Chiou HC, LoBrutto R, Blankenship RE (1994a) Spectroscopic evidence for the presence of an iron–sulfur center similar to FX of Photosystem I in Heliobacillus mobilis. Photosynth Res 41:115–123PubMedCrossRefGoogle Scholar
  47. Kleinherenbrink FAM, Hastings G, Wittmershaus BP, Blankenship RE (1994b) Delayed fluorescence from Fe–S type photosynthetic reaction centers at low redox potential. Biochemistry 33:3096–3105PubMedCrossRefGoogle Scholar
  48. Kleinherenbrink FAM, Ikegami I, Hiraishi A, Otte SCM, Amesz J (1993a) Electron transfer in menaquinone depleted membranes of Heliobacterium chlorum. Biochim Biophys Acta 1142:69–73CrossRefGoogle Scholar
  49. Kleinherenbrink FAM, Amesz J. (1993b) Stoichiometries and rates of electron transfer and charge recombination in Heliobacterium chlorum. Biochim Biophys Acta 1143:77–83CrossRefGoogle Scholar
  50. Kobayashi M, Hamano T, Akiyama M, Watanabe T, Inoue K, Oh-Oka H, Amesz J, Yamamura M, Kise H (1998) Light-independant isomerization of bacteriochlorophyll g to chlorophyll a catalyzed by weak acid in vitro. Anal Chim Acta 365:199–203CrossRefGoogle Scholar
  51. Kobayashi M, van de Meent EJ, Erkelens C, Amesz J, Ikegami I, Watanabe T (1991a) Bacteriochlorophyll g epimer as a possible reaction center component of heliobacteria. Biochim Biophys Acta 1057:89–96CrossRefGoogle Scholar
  52. Kobayashi M, Watanabe T, Ikegami I, van de Meent EJ, Amesz J (1991b) Enrichment of bacteriochlorophyll g(′ in membranes of Heliobacterium chlorum by ether extraction. Unequivocal evidence for its existence in vivo. FEBS Lett 284:129–131PubMedCrossRefGoogle Scholar
  53. Kramer DM, Schoepp B, Liebl U, Nitschke W (1997) Cyclic electron transfer in Heliobacillus mobilis involving a menaquinol-oxidizing cytochrome bc complex and an RCI-type reaction center. Biochemistry 36:4203–4211PubMedCrossRefGoogle Scholar
  54. Liebl U, Lambry JC, Breton J, Martin JL, Vos MH (1997) Spectral equilibration and primary photochemistry in Heliobacillus mobilis at cryogenic temperature. Biochemistry 36:5912–5920PubMedCrossRefGoogle Scholar
  55. Liebl U, Lambry JC, Leibl W, Breton J, Martin JL, Vos MH (1996) Energy and electron transfer upon selective femtosecond excitation of pigments in membranes of Heliobacillus mobilis. Biochemistry 35:9925–9934PubMedCrossRefGoogle Scholar
  56. Liebl U, Mockensturm-Wilson M, Trost JT, Brune DC, Blankenship RE, Vermaas W (1993) Single core polypeptide in the reaction center of the photosynthetic bacterium Heliobacillus mobilis: structural implications and relations to other photosystems. Proc Natl Acad Sci USA 90:7124–7128PubMedCrossRefGoogle Scholar
  57. Liebl U, Rutherford AW, Nitschke W (1990) Evidence for a unique Rieske iron–sulphur centre in Heliobacterium chlorum. FEBS Lett 261:427–430CrossRefGoogle Scholar
  58. Lin S, Chiou HC, Blankenship RE (1995) Secondary electron transfer processes in membranes of Heliobacillus mobilis. Biochemistry 34:12761–12767PubMedCrossRefGoogle Scholar
  59. Lin S, Chiou HC, Kleinherenbrink FAM, Blankenship RE (1994) Time-resolved spectroscopy of energy and electron transfer processes in the photosynthetic bacterium Heliobacillus mobilis. Biophys J 66:437–445PubMedCrossRefGoogle Scholar
  60. Lindahl PA, Day EP, Kent TA, Orme-Johnson WH, Münck E (1985) Mössbauer, EPR, and magnetization studies of the Azotobacter vinelandii Fe protein. Evidence for a [4Fe–4S]1+ cluster with spin S = 3/2. J Biol Chem 260:11160–11173PubMedGoogle Scholar
  61. Locher KP, Hans M, Yeh AP, Schmid B, Buckel W, Rees DC (2001) Crystal structure of the Acidaminococcus fermentans 2-hydroxyglutaryl-CoA dehydratase component A. J Mol Biol 307:297–308PubMedCrossRefGoogle Scholar
  62. Loll B, Kern J, Zouni A, Saenger W, Biesiadka J, Irrgang KD (2005) The antenna system of Photosystem II from Thermosynechococcus elongatus at 3.2 Å resolution. Photosynth Res 86:175–184PubMedCrossRefGoogle Scholar
  63. Madigan MT (2001) Heliobacteriaceae. In: Boone E, Castenholz RW, Garrity GM (eds) Bergy's manual of systematic bacteriology, 2nd edn., vol 1. Springer-Verlag, New York, NY, pp 625–630Google Scholar
  64. Madigan MT, Ormerod JG (1995) Taxonomy, physiology, and ecology of heliobacteria. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic photosynthetic bacteria. Kluwer Academic Publishers, Dordrecht, pp 17–30Google Scholar
  65. Michalski TJ, Hunt JE, Bowman MK, Smith U, Bardeen K, Gest H, Norris JR, Katz JJ (1987) Bacteriopheophytin g: properties and some speculations on a possible primary role for bacteriochlorophylls b and g in the biosynthesis of chlorophylls. Proc Natl Acad Sci USA 84:2570–2574PubMedCrossRefGoogle Scholar
  66. Miller K, Jacob JS, Smith U, Kolaczkowski S, Bowman MK (1986) Heliobacterium chlorum: cell organization and structure. Arch Microbiol 146:111–114PubMedCrossRefGoogle Scholar
  67. Miyamoto R, Iwaki M, Mino H, Harada J, Itoh S, Oh-Oka H (2006) ESR signal of the iron–sulfur center FX and its function in the homodimeric reaction center of Heliobacterium modesticaldum. Biochemistry 45:6306–6316PubMedCrossRefGoogle Scholar
  68. Mizoguchi T, Oh-oka H, Tamiaki H (2005) Determination of stereochemistry of bacteriochlorophyll g F and 81-hydroxy-chlorophyll a F from Heliobacterium modesticaldum. Photochem Photobiol 81:666–673PubMedCrossRefGoogle Scholar
  69. Moulis JM, Sieker LC, Wilson KS, Dauter Z (1996) Crystal structure of the 2[4Fe–4S] ferredoxin from Chromatium vinosum: evolutionary and mechanistic inferences for [3/4Fe–4S] ferredoxins. Protein Sci 5:1765–1775PubMedGoogle Scholar
  70. Muhiuddin IP, Rigby SEJ, Evans MCW, Amesz J, Heathcote P (1999) ENDOR and special TRIPLE resonance spectroscopy of photoaccumulated semiquinone electron acceptors in the reaction centers of green sulfur bacteria and heliobacteria. Biochemistry 38:7159–7167PubMedCrossRefGoogle Scholar
  71. Neerken S, Amesz J (2001) The antenna reaction center complex of heliobacteria: composition, energy conversion and electron transfer. Biochim Biophys Acta 1507:278–290PubMedCrossRefGoogle Scholar
  72. Nitschke W, Liebl U, Matsuura K, Kramer DM (1995) Membrane-bound c-type cytochromes in Heliobacillus mobilis. In vivo study of the hemes involved in electron donation to the photosynthetic reaction center. Biochemistry 34:11831–11839PubMedCrossRefGoogle Scholar
  73. Nitschke W, Rutherford AW (1991) Photosynthetic reaction centres: variations on a common structural theme? Trends Biochem Sci 16:241–245PubMedCrossRefGoogle Scholar
  74. Nitschke W, Schoepp B, Floss B, Schricker A, Rutherford AW, Liebl U (1996) Membrane-bound c-type cytochromes in Heliobacillus mobilis. Characterisation by EPR and optical spectroscopy in membranes and detergent-solubilised material. Eur J Biochem 242:695–702PubMedCrossRefGoogle Scholar
  75. Nitschke W, Sétif P, Liebl U, Feiler U, Rutherford AW (1990) Reaction center photochemistry of Heliobacterium chlorum. Biochemistry 29:11079–11088PubMedCrossRefGoogle Scholar
  76. Noguchi T, Fukami Y, Oh-oka H amd Inoue Y (1997) Fourier transform infrared study on the primary donor P798 of Heliobacterium modesticaldum: cysteine S–H coupled to P798 and molecular interactions of carbonyl groups. Biochemistry 36:12329–12336PubMedCrossRefGoogle Scholar
  77. Nuijs AM, Van Dorssen RJ, Duysens LNM, Amesz J (1985) Excited states and primary photochemical reactions in the photosynthetic bacterium Heliobacterium chlorum. Proc Natl Acad Sci USA 82:6865–6868PubMedCrossRefGoogle Scholar
  78. Oh-Oka H (2006) Type 1 reaction center of photosynthetic heliobacteria. Photochem Photobiol  DOI: 10.1562/2006-03-29-IR-860
  79. Oh-Oka H, Iwaki M, Itoh S (2002) Electron donation from membrane-bound cytochrome c to the photosynthetic reaction center in whole cells and isolated membranes of Heliobacterium gestii. Photosynth Res 71:137–147PubMedCrossRefGoogle Scholar
  80. Olson JM, Blankenship RE (2004) Thinking about the evolution of photosynthesis. Photosynth Res 80:373–386PubMedCrossRefGoogle Scholar
  81. Ormerod JG, Kimble LK, Nesbakken T, Torgersen YA, Woese CR, Madigan MT (1996) Heliophilum fasciatum gen. nov. sp. nov. and Heliobacterium gestii sp. nov. endospore-forming heliobacteria from rice field soil. Arch Microbiol 165:226–234PubMedCrossRefGoogle Scholar
  82. Parrett KG, Mehari T, Warren P, Golbeck JH (1989) Purification and properties of the intact P-700 and FX containing Photosystem I core protein. Biochim Biophys Acta 973:324–332PubMedGoogle Scholar
  83. Pickett MW, Weiss N, Kelly DJ (1994a) Gram-positive cell wall structure of the A3γ type in heliobacteria. FEMS Microbiol Lett 122:7–12PubMedCrossRefGoogle Scholar
  84. Pickett MW, Williamson MP, Kelly DJ (1994b) An enzyme and 13C-NMR study of carbon metabolism in heliobacteria. Photosynth Res 41:75–88CrossRefGoogle Scholar
  85. Prince RC, Gest H, Blankenship RE (1985) Thermodynamic properties of the photochemical reaction center of Heliobacterium chlorum. Biochim Biophys Acta 810:377–384CrossRefGoogle Scholar
  86. Rémigy HW, Stahlberg H, Fotiadis D, Müller SA, Wolpensinger B, Engel A, Hauska G, Tsiotis G (1999) The reaction center complex from the green sulfur bacterium Chlorobium tepidum: a structural analysis by scanning transmission electron microscopy. J Mol Biol 290:851–858PubMedCrossRefGoogle Scholar
  87. Smit HWJ, Amesz J, van der Hoeven MFR (1987) Electron transport and triplet formation in membranes of the photosynthetic bacterium Heliobacterium chlorum. Biochim Biophys Acta 893:232–240CrossRefGoogle Scholar
  88. Stevenson AK, Kimble LK, Woese CR, Madigan MT (1997) Characterization of new phototrophic heliobacteria and their habitats. Photosynth Res 53:1–12CrossRefGoogle Scholar
  89. Stout CD (1993) Crystal structures of oxidized and reduced Azotobacter vinelandii ferredoxin at pH 8 and pH 6. J Biol Chem 268:25920–25927PubMedGoogle Scholar
  90. Takaichi S, Inoue K, Akaike M, Kobayashi M, Oh-oka H, Madigan MT (1997) The major carotenoid in all known species of heliobacteria is the C30 carotenoid 4,4′-diaponeurosporene, not neurosporene. Arch Microbiol 168:277–281PubMedCrossRefGoogle Scholar
  91. Tranqui D, Jesior JC (1995) Structure of the ferredoxin from Clostridium acidiurici—model at 1.8 Å resolution. Acta Crystallogr D Biol Crystallogr 51:155–159PubMedCrossRefGoogle Scholar
  92. Trost JT, Blankenship RE (1989) Isolation of a photoactive photosynthetic reaction center-core antenna complex from Heliobacillus mobilis. Biochemistry 28:9898–9904PubMedCrossRefGoogle Scholar
  93. Trost JT, Brune DC, Blankenship RE (1992) Protein sequences and redox titrations indicate that the electron acceptors in reaction centers from heliobacteria are similar to Photosystem I. Photosynth Res 32:11–22PubMedCrossRefGoogle Scholar
  94. Unciuleac M, Boll M, Warkentin E, Ermler U (2004) Crystallization of 4-hydroxybenzoyl-CoA reductase and the structure of its electron donor ferredoxin. Acta Crystallogr D Biol Crystallogr 60:388–391PubMedCrossRefGoogle Scholar
  95. van de Meent EJ, Kobayashi M, Erkelens C, van Veelen PA, Amesz J, Watanabe T (1991) Identification of 81-hydroxychlorophyll a as a functional reaction center pigment in heliobacteria. Biochim Biophys Acta 1058:356–362CrossRefGoogle Scholar
  96. van de Meent EJ, Kleinherenbrink FAM, Amesz J (1990) Purification and properties of an antenna-reaction center complex from heliobacteria. Biochim Biophys Acta 1015:223–230CrossRefGoogle Scholar
  97. van der Est A, Hager-Braun C, Leibl W, Hauska G, Stehlik D (1998) Transient electron paramagnetic resonance spectroscopy on green-sulfur bacteria and heliobacteria at two microwave frequencies. Biochim Biophys Acta 1409:87–98PubMedCrossRefGoogle Scholar
  98. van Dorssen RJ, Vasmel H, Amesz J (1985) Antenna organization and energy transfer in membranes of Heliobacterium chlorum. Biochim Biophys Acta 809:199–203CrossRefGoogle Scholar
  99. Vassiliev IR, Jung YS, Mamedov MD, Semenov AY, Golbeck JH (1997) Near-IR absorbance changes and electrogenic reactions in the microsecond-to-second time domain in photosystem I. Biophys J 72:301–315PubMedGoogle Scholar
  100. Vermaas WFJ (1994) Evolution of heliobacteria: implications for photosynthetic reaction center complexes. Photosynth Res 41:285–294PubMedCrossRefGoogle Scholar
  101. Vos MH, Klaassen HE, van Gorkom HJ (1989) Electron transport in Heliobacterium chlorum whole cells studied by electroluminescence and absorbance difference spectroscopy. Biochim Biophys Acta 973:163–169Google Scholar
  102. Woese CR, Debrunner-Vossbrinck BA, Oyaizu H, Stackebrandt E, Ludwig W (1985) Gram-positive bacteria: possible photosynthetic ancestry. Science 229:762–765PubMedCrossRefGoogle Scholar
  103. Xiong J, Inoue K, Bauer CE (1998) Tracking molecular evolution of photosynthesis by characterization of a major photosynthesis gene cluster from Heliobacillus mobilis. Proc Natl Acad Sci USA 95:14851–14856PubMedCrossRefGoogle Scholar
  104. Zouni A, Witt HT, Kern J, Fromme P, Krauß N, Saenger W, Orth P (2001) Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature 409:739–743PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  1. 1.Department of Biochemistry and Molecular BiologyThe Pennsylvania State UniversityUniversity ParkUSA
  2. 2.Department of ChemistryThe Pennsylvania State UniversityUniversity ParkUSA

Personalised recommendations