Ca2+-binding reduces conformational flexibility of RC-LH1 core complex from thermophile Thermochromatium tepidum

Photosynthesis Research

Volumn 111, Issue 1-2, 2012, Pages 139-147

  Jakob Grun, Selma ^a   Radeck, Jara ^a   Braun, Paula ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

Calcium binding; Light harvesting complex; Structural flexibility; Thermal stability; Thermochromatium tepidum

Indexed keywords

BACTERIOCHLOROPHYLL; CALCIUM; MANGANESE;

AMINO ACID SEQUENCE; ARTICLE; CHEMISTRY; CHROMATIACEAE; LIGHT HARVESTING SYSTEM; METABOLISM; MOLECULAR GENETICS; PHOTOSYNTHESIS; PROTEIN BINDING; PROTEIN STABILITY; SEQUENCE ALIGNMENT; SPECTROSCOPY; TEMPERATURE; TIME;

AMINO ACID SEQUENCE; BACTERIOCHLOROPHYLLS; CALCIUM; CHROMATIACEAE; LIGHT-HARVESTING PROTEIN COMPLEXES; MANGANESE; MOLECULAR SEQUENCE DATA; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS; PROTEIN BINDING; PROTEIN STABILITY; SEQUENCE ALIGNMENT; SPECTRUM ANALYSIS; TEMPERATURE; TIME FACTORS;

PROTEOBACTERIA; THERMOCHROMATIUM TEPIDUM;

EID: 84858149401     PISSN: 01668595     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11120-012-9727-8     Document Type: Article

References (49)

1. 13C=O-labeled phospholipids: hydrogen bonding to carbonyl groups Biochemistry 27 8239 8249 3233207 10.1021/bi00421a038 1:CAS:528: DyaL1cXls1KjsL0%3D
2. Braun P, Fiedor L (2009) Design and assembly of functional light harvesting complexes. In: Hunter NC, Daldal F, Thurnauer M C, Beatty T (eds) The purple photosynthetic bacteria. Advances in photosynthesis and respiration, Govindjee (ed), Springer, Dordrecht, pp 913-940
3. P Braun E Goldberg C Negron M von Jan F Xu V Nanda R Koder D Noy 2011 Design principles for chlorophyll binding sites in helical proteins Proteins 79 463 476 21117078 10.1002/prot.22895 1:CAS:528:DC%2BC3MXitVCitr0%3D
4. Braun P, Vegh AP, von Jan M, Strohmann B, Hunter CN, Robert B, Scheer H (2003) Identification of intramembrane hydrogen bonding between 13(1) keto group of bacteriochlorophyll and serine residue alpha27 in the LH2 light-harvesting complex. Biochim Biophys Acta 1607:19-26 (Pubitemid 37214828)
5. M Byler HM Farrel Jr 1989 Infrared spectroscopic evidence for calcium ion interaction with carboxylate groups of casein J Dairy Sci 72 1719 1723 10.3168/jds.S0022-0302(89)79287-0 1:CAS:528:DyaL1MXltFeru78%3D
6. C Cambillau JM Claverie 2000 Structural and genomic correlates of hyperthermostability J Biol Chem 275 32383 32386 10940293 10.1074/jbc.C000497200 1:CAS:528:DC%2BD3cXnslOisLc%3D
7. Conzen JP (2006) Multivariate calibration: a practical guide for developing methods in the quantitative analytical chemistry. 2nd English edn. Bruker Optics, Ettlingen
8. A Dezi F Francia A Mallardi G Colafemmina G Palazzo G Venturosi 2007 Stabilization of charge separation and cardiolipin confinement in antenna-reaction centre complexes purified from Rhodobacter sphaeroides Biochim Biophys Acta 1767 1041 1056 17588528 10.1016/j.bbabio.2007.05.006 1:CAS:528:DC%2BD2sXot1yktb0%3D (Pubitemid 47101787)
9. I Fathir M Ashikaga K Tanaka T Katano T Nirasawa M Kobayashi Z-Y Wang T Nozawa 1998 Biochemical and spectral characterization of the core light harvesting complex 1 (LH1) from the thermophile purple sulphur bacterium Chromatium tepidum Photosynth Res 58 193 202 10.1023/A:1006146713751 1:CAS:528:DyaK1MXhtFCku70%3D (Pubitemid 29054122)
10. I Fathir T Mori T Nogi M Kobayashi T Miki K Nozawa 2001 Structure of the H subunit of the photosynthetic reaction centre from the thermophile purple sulphur bacterium Thermochromatium tepidum. Implications for the specific binding of the lipid molecule to the membrane protein complex Eur J Biochem 268 2652 2657 11322886 10.1046/j.1432-1327.2001.02158.x 1:CAS:528: DC%2BD3MXjsVyhtrc%3D (Pubitemid 32853004)
11. GJ Fowler GD Sockalingum B Robert, et al. 1994 Blue shifts in bacteriochlorophyll absorbance correlate with changed hydrogen bonding patterns in light-harvesting 2 mutants of Rhodobacter sphaeroides with alterations at alpha-Tyr-44 and alpha-Tyr-45 Biochem J 299 695 700 8192657 1:CAS:528: DyaK2cXivFCnsr0%3D (Pubitemid 24138536)
12. D Garcia P Parot A Vermeglio MT Madigan 1986 The light-harvesting complexes of a thermophile purple sulphur photosynthetic bacterium Chromatium tepidum Biochim Biophys Acta 850 390 395 10.1016/0005-2728(86)90195-7 1:CAS:528:DyaL28XkslKhs7w%3D
13. J Glaeser J Overmann 1999 Selective enrichment and characterization of Roseospirillum parvum, gen. nov and sp. 197 nov., a new purple nonsulfur bacterium with unusual light absorption properties Arch Microbiol 171 405 416 10369896 10.1007/s002030050727 1:CAS:528:DyaK1MXktVChsb0%3D (Pubitemid 29262408)
14. DS Gregory ACR Martin JC Cheetham AR Rees 1993 The prediction and characterization of metal binding sites in proteins Protein Eng 6 29 35 8433968 10.1093/protein/6.1.29 1:CAS:528:DyaK3sXhvVKisL4%3D (Pubitemid 23048937)
15. AS Holt EE Jacobs 1955 Infra-red absorption spectra of chlorophylls and derivatives Plant Physiol 30 553 559 16654824 10.1104/pp.30.6.553 1:CAS:528:DyaG28XksFektA%3D%3D
16. B Honig A Nicholls 1995 Classical electrostatics in biology and chemistry Science 268 1144 1149 7761829 10.1126/science.7761829 1:CAS:528: DyaK2MXlvVyqsrY%3D
17. Invernizzi G, Papaleo E, Grandori R, De Gioia L, Lotti M (2009) Relevance of metal ions for lipase stability: structural rearrangements induced in the Burkholderia glumae lipase by calcium depletion. J Struct Biol. doi: 10.1016/j.jsb.2009.07.021
18. K Ishikawa H Nakamura K Morikawa S Kanaya 1993 Stabilization of Escherichia coli ribonuclease HI by cavity-filling mutations within a hydrophobic core Biochemistry 32 6171 6178 8390295 10.1021/bi00075a009 1:CAS:528:DyaK3sXks1Knu7w%3D (Pubitemid 23196872)
19. Ishimura M, Honda S, Uedaira H, Odahara T, Miyake J (1995) Thermal denaturation of photosynthetic membrane proteins from Rhodobacter sphaeroides. Thermochim Acta 266:355-364
20. MR Jones 2007 Lipids in photosynthetic reaction centres: structural roles and functional holes Prog Lipid Res 46 56 87 16963124 10.1016/j.plipres.2006. 06.001 1:CAS:528:DC%2BD28Xht1CnsLfK
21. y transition of the core complex in thermophile purple sulphur bacterium Thermochromatium tepidum. J Biol Chem 283:13867-13873
22. Y Kimura L-J Yu Y Hirano H Suzuki Z-Y Wang 2009 Calcium ions are required for the enhanced thermal stability of the light-harvesting-reaction centre core complex from thermophile purple sulphur bacterium Thermochromatium tepidum J Biol Chem 284 93 99 18977753 10.1074/jbc.M806840200 1:CAS:528:DC%2BD1cXhsFCjtLnK
23. Y Kimura Y Inada L-J Yu Z-Y Wang T Ohno 2011 A spectroscopic variant of the light-harvesting 1 core complex from the thermophile purple sulphur bacterium Thermochromatium tepidum Biochemistry 50 3638 3648 21462972 10.1021/bi200278u 1:CAS:528:DC%2BC3MXkvVantbY%3D
24. LG Kwa A Garcia-Martinez AP Vegh B Strohmann B Robert P Braun 2004 H-bonding in a model bacteriochlorophyll binding site drives assembly of light harvesting complex J Biol Chem 279 15067 15075 14742420 10.1074/jbc.M312429200 1:CAS:528:DC%2BD2cXivVKgsr8%3D (Pubitemid 38618900)
25. LG Kwa D Wegmann B Brügger F Wieland G Wanner P Braun 2008 Mutation of a single residue, glutamate β10, alters protein-lipid interactions of light harvesting complex II Mol Microbiol 67 63 77 18034796 1:CAS:528: DC%2BD1cXitVGjsbc%3D (Pubitemid 350231135)
26. Lafrance C-P, Blochet J-E, Pezolet M (1997) N- Acylphosphatidylethanolamines: effect of the N-Acyl chain length on its orientation. Biophys J 72:2559-2568 (Pubitemid 27227591)
27. AH Lewis RN McElhaney W Pohle HH Mantsch 1994 Components of the carbonyl stretching band in the infrared spectra of hydrated 1,2-diacylglycerolipid bilayers. a re-evaluation Biophys J 67 2367 2375 7696476 10.1016/S0006-3495(94) 80723-4 1:CAS:528:DyaK2MXisVajuro%3D (Pubitemid 24369660)
28. ZX Liang J Tsigos T Lee V Bouriotis KA Resing NG Ahn JP Klinmann 2004 Evidence for increased local flexibility in psychrophilic alcohol dehydrogenase relative to its thermophile homologue Biochemistry 43 14676 14683 15544338 10.1021/bi049004x 1:CAS:528:DC%2BD2cXptVyrur0%3D (Pubitemid 39524942)
29. 2+-binding motif in the LH1 complex from photosynthetic bacterium Thermochromatium tepidum as revealed by optical spectroscopy and structural modeling FEBS J 276 1739 1749 19226412 10.1111/j.1742-4658.2009.06905.x 1:CAS:528:DC%2BD1MXjsFWgtLo%3D
30. MT Madigan 1984 A novel photosynthetic purple bacterium isolated from a Yellowstone hot spring Science 225 313 315 17749561 10.1126/science.225.4659.313 1:STN:280:DC%2BC3cvitlCksg%3D%3D
31. D Marsh LI Horvath 1998 Structure, dynamics and composition of the lipid-protein interface. Perspectives from spin-labelling Biochim Biophys Acta 1376 267 296 9804973 1:CAS:528:DyaK1cXntVyitrg%3D (Pubitemid 28517881)
32. G McDermott SM Prince AA Freer A Hawthornthwaite-Lawless MZ Papiz R Cogdell 1995 Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria Nature 374 517 521 10.1038/374517a0 1:CAS:528:DyaK2MXkvVKqsb8%3D
33. M Nara M Tanokura 2008 Infrared spectroscopic study of the metal coordination structures of calcium-binding proteins Biochim Biophys Res Commun 369 225 239 10.1016/j.bbrc.2007.11.188 1:CAS:528:DC%2BD1cXjs12rs7Y%3D
34. T Nogi I Fathir M Kobayashi T Nozawa K Miki 2000 Crystal structures of photosynthetic reaction centre and high-potential iron-sulfur protein from Thermochromatium tepidum; thermostability and electron transfer Proc Natl Acad Sci USA 97 13561 13566 11095707 10.1073/pnas.240224997 1:CAS:528: DC%2BD3cXoslygtbk%3D
35. SK Papageorgiou EP Kouvelos EP Favvas AA Sapalidis GE Romanos FK Katsaros 2010 Metal-carboxylate interactions in metal-alginate complexes studied with FTIR spectroscopy Carbohydr Res 345 469 473 20044077 10.1016/j.carres.2009.12. 010 1:CAS:528:DC%2BC3cXhtlGitbs%3D
36. HP Permentier S Neerken J Overmann J Amesz 2001 A bacteriochlorophyll a antenna complex from purple bacteria absorbing at 963 nm Biochemistry 40 5573 5578 11331023 10.1021/bi0024308 1:CAS:528:DC%2BD3MXis1OjurY%3D (Pubitemid 32458260)
37. AW Roszak TD Howard J Southall AT Gardiner CJ Law NW Isaacs RJ Cogdell 2003 Crystal structure of the RC-LH1 core complex from Rhodopseudomonas palustris Science 302 1969 1972 14671305 10.1126/science.1088892 1:CAS:528:DC%2BD3sXps1amsL8%3D (Pubitemid 37523505)
38. S Scheuring JN Sturgis 2009 Atomic force microscopy of the bacterial photosynthetic apparatus: plain pictures of an elaborate machinery Photosynth Res 102 197 211 19266309 10.1007/s11120-009-9413-7 1:CAS:528:DC%2BD1MXhsVWht77L
39. MK Sener JD Olsen CN Hunter K Schulten 2007 Atomic-level structural and functional model of a bacterial photosynthetic membrane vesicle Proc Natl Acad Sci USA 104 15723 15728 17895378 10.1073/pnas.0706861104 1:CAS:528: DC%2BD2sXhtFGns7%2FP (Pubitemid 350035367)
40. KS Siddiqui R Cavicchioli 2006 Cold-adapted enzymes Annu Rev Biochem 75 403 433 16756497 10.1146/annurev.biochem.75.103004.142723 1:CAS:528: DC%2BD28XosVKhs7s%3D (Pubitemid 44118038)
41. MV Silber G Gabriel B Strohmann A Garcia-Martin B Robert P Braun 2008 Fine tuning of the spectral properties of LH2 by single amino acid residues Photosynth Res 96 145 151 18365764 10.1007/s11120-008-9294-1 1:CAS:528:DC%2BD1cXksVKks74%3D
42. J Sturgis B Robert E Goormaghtigh 1998 Transmembrane helix stability: the effect of helix-helix interactions studied by Fourier transform infrared spectroscopy Biophys J 74 988 994 9533710 10.1016/S0006-3495(98)74022-6 1:CAS:528:DyaK1cXhs1Krsr8%3D (Pubitemid 28345292)
43. JN Sturgis JD Tucker JD Olsen CN Hunter RA Niederman 2009 Atomic force microscopy studies of native photosynthetic membranes Biochemistry 48 3679 3698 19265434 10.1021/bi900045x 1:CAS:528:DC%2BD1MXkvVSkurc%3D
44. H Suzuki Y Hirano Y Kimura S Takaichi Kobayashi MK Miki Z-Y Wang 2007 Purification, characterization and crystallization of the core complex from thermophile purple sulphur bacterium Thermochromatium tepidum Biochim Biophys Acta 1767 1057 1063 17658456 10.1016/j.bbabio.2007.06.002 1:CAS:528: DC%2BD2sXot1yktbo%3D (Pubitemid 47101789)
45. C Tuschak JT Beatty J Overmann 2004 Photosynthesis genes and LH1 proteins of Roseospirillum parvum 930I, a purple non-sulphur bacterium with unusual spectral properties Photosynth Res 81 181 199 10.1023/B:PRES.0000035046.91126.bd 1:CAS:528:DC%2BD2cXls1Ols7s%3D (Pubitemid 39040103)
46. Vigano C, Smeyers M, Raussens V, Scheirlinck F, Ruysschaert JM, Goormaghtigh E (2003) Hydrogen-deuterium exchange in membrane proteins monitored by IR spectroscopy: a new tool to resolve protein structure and dynamics. Wiley InterScience. doi: 10.1002/bip.20035
47. ZY Wang K Gokan M Kobayashi T Nozawa 2005 Solution structures of the core light-harvesting a and b polypeptides from Rhodospirillum rubrum: implications for the pigment-protein and protein-protein interactions J Mol Biol 347 465 477 15740753 10.1016/j.jmb.2005.01.017 1:CAS:528:DC%2BD2MXhvVGitb0%3D (Pubitemid 40312471)
48. AJ Watson AV Hughs PK Fyfe MC Wakeham K Holden-Dye P Heathcote MR Jones 2005 On the role of basic residues in adapting the reaction centre-LH1 complex for growth at elevated temperatures in purple bacteria Photosynth Res 86 10 81 10.1007/s11120-005-4047-x (Pubitemid 41361263)
49. L-J Yu S Kato Z-J Wang 2010 Examination of the putative Ca2 + -binding site in the light-harvesting complex 1 of thermophile purple sulphur bacterium Thermochromatium tepidum Photosynth Res 106 215 220 20886371 10.1007/s11120-010-9596-y 1:CAS:528:DC%2BC3cXhsF2gsrzP