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Solution structures of the core light-harvesting alpha and beta polypeptides from Rhodospirillum rubrum: implications for the pigment-protein and protein-protein interactions.

Wang ZY, Gokan K, Kobayashi M, Nozawa T
J Mol Biol 347 465-77 (2005)
Cited: 23 times
EuropePMC logo PMID: 15740753

Abstract

We have determined the solution structures of the core light-harvesting (LH1) alpha and beta-polypeptides from wild-type purple photosynthetic bacterium Rhodospirillum rubrum using multidimensional NMR spectroscopy. The two polypeptides form stable alpha helices in organic solution. The structure of alpha-polypeptide consists of a long helix of 32 amino acid residues over the central transmembrane domain and a short helical segment at the N terminus that is followed by a three-residue loop. Pigment-coordinating histidine residue (His29) in the alpha-polypeptide is located near the middle of the central helix. The structure of beta-polypeptide shows a single helix of 32 amino acid residues in the membrane-spanning region with the pigment-coordinating histidine residue (His38) at a position close to the C-terminal end of the helix. Strong hydrogen bonds have been identified for the backbone amide protons over the central helical regions, indicating a rigid property of the two polypeptides. The overall structures of the R.rubrum LH1 alpha and beta-polypeptides are different from those previously reported for the LH1 beta-polypeptide of Rhodobacter sphaeroides, but are very similar to the structures of the corresponding LH2 alpha and beta-polypeptides determined by X-ray crystallography. A model constructed for the structural subunit (B820) of LH1 complex using the solution structures reveals several important features on the interactions between the LH1 alpha and beta-polypeptides. The significance of the N-terminal regions of the two polypeptides for stabilizing both B820 and LH1 complexes, as clarified by many experiments, may be attributed to the interactions between the short N-terminal helix (Trp2-Gln6) of alpha-polypeptide and a GxxxG motif in the beta-polypeptide.

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  1. Strategies for dealing with conformational sampling in structural calculations of flexible or kinked transmembrane peptides. Rainey JK, Fliegel L, Sykes BD. Biochem Cell Biol 84 918-929 (2006)

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  2. Possible pathway for ubiquinone shuttling in Rhodospirillum rubrum revealed by molecular dynamics simulation. Aird A, Wrachtrup J, Schulten K, Tietz C. Biophys J 92 23-33 (2007)
  3. Backbone structure of a small helical integral membrane protein: A unique structural characterization. Page RC, Lee S, Moore JD, Opella SJ, Cross TA. Protein Sci 18 134-146 (2009)
  4. Solution structure of a human minimembrane protein Ost4, a subunit of the oligosaccharyltransferase complex. Gayen S, Kang C. Biochem Biophys Res Commun 409 572-576 (2011)
  5. Characterization of the photosynthetic apparatus and proteome of Roseobacter denitrificans. Tang K, Zong R, Zhang F, Xiao N, Jiao N. Curr Microbiol 60 124-133 (2010)
  6. Versatile design of biohybrid light-harvesting architectures to tune location, density, and spectral coverage of attached synthetic chromophores for enhanced energy capture. Harris MA, Jiang J, Niedzwiedzki DM, Jiao J, Taniguchi M, Kirmaier C, Loach PA, Bocian DF, Lindsey JS, Holten D, Parkes-Loach PS. Photosynth Res 121 35-48 (2014)
  7. Ca(2+)-binding reduces conformational flexibility of RC-LH1 core complex from thermophile Thermochromatium tepidum. Jakob-Grun S, Radeck J, Braun P. Photosynth Res 111 139-147 (2012)
  8. The PufX protein of Rhodobacter capsulatus affects the properties of bacteriochlorophyll a and carotenoid pigments of light-harvesting complex 1. Aklujkar M, Beatty JT. Arch Biochem Biophys 443 21-32 (2005)
  9. Identification of chromatophore membrane protein complexes formed under different nitrogen availability conditions in Rhodospirillum rubrum. Selao TT, Branca R, Chae PS, Lehtiö J, Gellman SH, Rasmussen SG, Nordlund S, Norén A. J Proteome Res 10 2703-2714 (2011)
  10. Specific Ca2+-binding motif in the LH1 complex from photosynthetic bacterium Thermochromatium tepidum as revealed by optical spectroscopy and structural modeling. Ma F, Kimura Y, Yu LJ, Wang P, Ai XC, Wang ZY, Zhang JP. FEBS J 276 1739-1749 (2009)
  11. Energy Transfer Dynamics in an RC-LH1-PufX Tubular Photosynthetic Membrane. Hsin J, Strümpfer J, Sener M, Qian P, Hunter CN, Schulten K. New J Phys 12 (2010)
  12. Structure of the dimeric RC-LH1-PufX complex from Rhodobaca bogoriensis investigated by electron microscopy. Semchonok DA, Chauvin JP, Frese RN, Jungas C, Boekema EJ. Philos Trans R Soc Lond B Biol Sci 367 3412-3419 (2012)
  13. Overexpression and characterization of the Rhodobacter sphaeroides PufX membrane protein in Escherichia coli. Onodera S, Suzuki H, Shimada Y, Kobayashi M, Nozawa T, Wang ZY. Photochem Photobiol 83 139-144 (2007)
  14. Puf operon sequences and inferred structures of light-harvesting complexes of three closely related Chromatiaceae exhibiting different absorption characteristics. Rücker O, Köhler A, Behammer B, Sichau K, Overmann J. Arch Microbiol 194 123-134 (2012)
  15. Cryo-EM structure of the Rhodospirillum rubrum RC-LH1 complex at 2.5 Å. Qian P, Croll TI, Swainsbury DJK, Castro-Hartmann P, Moriarty NW, Sader K, Hunter CN. Biochem J 478 3253-3263 (2021)
  16. Isotopic labeling of proteins by utilizing photosynthetic bacteria. Suzuki H, Shimada Y, Kobayashi M, Kudo M, Nozawa T, Wang ZY. Anal Biochem 347 324-326 (2005)
  17. All-atom structures and calcium binding sites of the bacterial photosynthetic LH1-RC core complex from Thermochromatium tepidum. Khrenova MG, Nemukhin AV, Grigorenko BL, Wang P, Zhang JP. J Mol Model 20 2287 (2014)
  18. Bridging Carotenoid-to-Bacteriochlorophyll Energy Transfer of Purple Bacteria LH2 With Temperature Variations: Insights From Conformational Changes. Mao R, Wang X, Gao J. Front Chem 9 764107 (2021)
  19. Thermodynamics of the beta(2) association in light-harvesting complex I of Rhodospirillum rubrum. Implication of peptide identity in dimer stability. Seguin J, Mayer C, Robert B, Arluison V. FEBS J 275 1240-1247 (2008)


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