Abstract
In previous work (Zurdo J, Fernández-Cabrera C and Ramírez JM (1993) Biochem J 290: 531–537), it had been shown that selective extraction of the carotenoid from the light-harvesting protein 2 (LH2) of Rhodobacter capsulatus induced the dissociation of 800-nm absorbing bacteriochlorophyll (Bchl), a 10-nm red shift of 854-nm Bchl, and a decrease of the stability of the protein in detergent solution. In the present study, the Fourier transform Raman and near-infrared circular dichroism spectra of native and carotenoid-depleted LH2 membrane preparations were compared. It was found that while the coupled carbonyls of 854-nm Bchl remained specifically H-bonded to the peptides after carotenoid extraction, the optical activity of the near-infrared electronic transition was significantly altered. Given the excitonic origin of such optical activity, our data suggest that carotenoid extraction elicits a rearrengement of the chromophore cluster and of the associated polypeptide subunits. This implies a significant role of the carotenoid in maintaining the native quaternary structure of the protein, which would be consistent with the observed dissociation of 800-nm Bchl and the loss of solubilized LH2 stability that result from carotenoid removal. There is no evidence for a similar role of the carotenoid in the LH1 protein.
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Abbreviations
- Bchl:
-
bacteriochlorophyll
- FT:
-
Fourier transform
- CD:
-
circular dichroism
- LH1 and LH2:
-
the bacterial light-harvesting proteins 1 and 2
References
Brunisholz RA and Zuber H (1992) Structure, function and organization of antenna polypeptides and antenna complexes from the three families of Rhodospirillaneae. J Photochem Photobiol B Biol 15: 113–140
Callahan PM and Cotton TM (1987) Assignment of bacteriochlorophyll a ligation state from absorption and resonance Raman data. J Am Chem Soc 109: 7001–7007
Clayton RK and Clayton BJ (1981) B850 pigment-protein complex of Rhodopseudomonas sphaeroides: Extinction coefficients, circular dichroism and the reversible binding of bacteriochlorophyll. Proc Natl Acad Sci USA 78: 5583–5587
Cogdell RJ and Scheer H (1985) Circular dichroism of light-harvesting complexes from purple photosynthetic bacteria. Photochem Photobiol 42: 669–678
Fowler GJS, Sockalingum GD, Robert B and Hunter CN (1994) Blue shifts in bacteriochlorophyll absorbance correlate with changed hydrogen bonding patterns in light-harvesting 2 mutants of Rhodobacter sphaeroides with alterations at α-Tyr-44 and α-Tyr-45. Biochem J 299: 695–700
Germeroth L, Lottspeich F, Robert B and Michel H (1993) Unexpected similarities of the B800–850 light-harvesting complex from Rhodospirillum molischianum to the B870 light-harvesting complexes from other purple photosynthetic bacteria. Biochemistry 32: 5615–5621
Giménez-Gallego G, DelValle Tascón S and Ramírez JM (1978) Photooxidase system of Rhodospirillum rubrum II. Its role in the regulation of cyclic photophosphorylation. Z Pflanzenphysiol 87: 25–36
Lang HP and Hunter CN (1994) The relationship between carotenoid biosynthesis and the assembly of the light-harvesting LH2 complex in Rhodobacter sphaeroides. Biochem J 298: 197–205
Lozano RM, Manzano I, Gómez R and Ramírez JM (1989) Changes in the native carotenoid of bacterial pigment-protein complexes. Biochim Biophys Acta 976: 196–202
Lozano RM, Fernández-Cabrera C and Ramírez JM (1990) The contribution of the carotenoid to the visible circular dichroism of the light-harvesting antenna in Rhodospirillum rubrum. Biochem J 270: 469–472
Mäntele W, Sawatzki J, Doi M, Gad'on N and Drews G (1991) Bacteriochlorophyll-protein interaction in the light-harvesting complex B800–850 from Rhodobacter sulfidophilus: A Fouriertransform Raman spectroscopic investigation. Biochim Biophys Acta 1057: 367–372
Mattioli TA, Hoffmann A, Lutz M and Schrader B (1990) Spectroscopie Raman par transformée de Fourier de la bactériochlorophylle a en prérésonance sur la transition Q y . C R Acad Sci, Ser 3 310: 441–446
Mattioli TA, Hoffmann A, Robert B, Schrader B and Lutz M (1991) Primary donor structure and interactions in bacterial reaction centers from near-infrared Fourier transform resonance Raman spectroscopy. Biochemistry 30: 4648–4654
McDermott G, Prince SM, Freer AA, Hawthornwaite-Lawless AM, Papiz MZ, Cogdell RJ and Isaacs NW (1995) Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria. Nature 374: 517–521
Olsen JD and Hunter CN (1995) Protein structure modelling of the bacterial light-harvesting complex. Photochem Photobiol 60: 521–535
Robert B and Lutz M (1985) Structures of antenna complexes of several Rhodospirillales from their resonance Raman spectra. Biochim Biophys Acta 807: 10–23
Scolnik PA, Walker MA and Marrs BL (1980a) Biosynthesis of carotenoids derived from neurosporene in Rhodopseudomonas capsulata. J Biol Chem 255: 2427–2432
Scolnik PA, Zannoni D and Marrs BL (1980b) Spectral and functional comparisons between the carotenoids of the two antenna complexes of Rhodopseudomonas capsulata. Biochim Biophys Acta 593: 230–240
Sturgis JN, Jirsakova V, Reiss-Husson F, Cogdell RJ and Robert B (1995) Structure and properties of the bacteriochlorophyll binding site in peripheral light-harvesting complexes of purple bacteria. Biochemistry 34: 517–523
Tinoco I (1963) The exciton contribution to the optical rotation of polymers. Radiation Res 20: 133–139
VanGrondelle R (1985) Excitation energy transfer, trapping and annihilation in photosynthetic systems. Biochim Biophys Acta 811: 147–195
Visschers RW, VanGrondelle R and Robert B (1993) Resonance Raman spectroscopy of the B820 subunit of the core antenna from Rhodospirillum rubrum G9. Biochim Biophys Acta 1183: 369–373
Zuber H (1986) Structure of light-harvesting antenna complexes of photosynthetic bacteria, cyanobacteria and red algae. Trends Biochem Sci 11: 414–419
Zurdo J, Lozano RM, Fernández-Cabrera C and Ramírez JM (1991) Dimeric carotenoid interaction in the light-harvesting antenna of purple phototrophic bacteria. Biochem J 274: 881–884
Zurdo J, Fernández-Cabrera C and Ramírez JM (1993) A structural role of the carotenoid in the light-harvesting II protein of Rhodobacter capsulatus. Biochem J 290: 531–537
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In memoriam of Daniel I. Arnon.
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Zurdo, J., Centeno, M.A., Odriozola, J.A. et al. The structural role of the carotenoid in the bacterial light-harvesting protein 2 (LH2) of Rhodonbacter capsulatus. A Fourier transform Raman spectroscopy and circular dichroism study. Photosynth Res 46, 363–369 (1995). https://doi.org/10.1007/BF00020452
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DOI: https://doi.org/10.1007/BF00020452