Abstract
Incorporation of spirilloxanthin into carotenoidless LH2 and LH1-RC complexes from a purple sulfur bacterium Allochromatium (Alc.) minutissimum was studied. Carotenoidless cells of Alc. minutissimum were obtained using diphenylamine, a carotenoid biosynthesis inhibitor. In the course of incorporation of the carotenoid mixture, the composition of which corresponded to that of Alc. minutissimum control photosynthetic membranes, no selective incorporation of spirilloxanthin into the LH1-RC complex was detected. It is assumed that in vivo carotenoids are not incorporated into the LH2 and LH1-RC complexes from a common pool. Pure spirilloxanthin destroys both the LH2 and LH1-RC complexes. Within the concentration range of spirilloxanthin in the incorporated mixture from 27% to 52%, it was found to be incorporated into the LH2 and LH1-RC complexes with the efficiency of 13% and 33%, respectively. The possible existence of different sites of assembly for the LH2 and LH1-RC complexes is discussed, as well as of two fractions of LH2 complexes, in one of which rhodopin may be integrated, and in the other (minor) one, spirilloxanthin.
Similar content being viewed by others
References
Ashikhmin, A., Makhneva, Z., and Moskalenko, A., The LH2 complexes are assembled in the cells of purple sulfur bacterium Ectothiorhodospira haloalkaliphila with inhibition of carotenoid biosynthesis, Photosynth. Res., 2014, vol. 119, pp. 291–303.
Bolshakov, M.A., Ashikhmin, A.A., Makhneva, Z.K., and Moskalenko, A.A., Effect of illumination intensity and inhibition of carotenoid biosynthesis on assembly of peripheral light-harvesting complexes in purple sulfur bacteria Allochromatium vinosum ATCC 17899, Microbiology (Moscow), 2016, vol. 85, no. 4, pp. 420–429.
Bolshakov, M.A., Ashikhmin, A.A., Makhneva, Z.K., and Moskalenko, A.A., Peripheral light-harvesting LH2 complex can be assembled in cells of nonsulfur purple bacterium Rhodoblastus acidophilus without carotenoids, Biochemistry (Moscow), 2015, vol. 80, no. 9, pp. 1169–1177.
Carey, A.M., Hacking, K., Picken, N., Honkanen, S., Kelly, S., Niedzwiedzki, D.M., Blankenship, R.E., Shimizu, Y., Wang-Otomo, Z.Y., and Cogdell, R.J., Characterization of the LH2 spectral variants produced by the photosynthetic purple sulphur bacterium Allochromatium vinosum, Biochim. Biophys. Acta, 2014, vol. 1837, pp. 1849–1860.
Chi, S.C., Mothersole, D.J., Dilbeck, P., Niedzwiedzki, D.M., Zhang, H., Qian, P., Vasilev, C., Grayson, K.J., Jackson, P.J., Martin, E.C., Li, Y., Holten, D., and Hunter, C.N., Assembly of functional photosystem complexes in Rhodobacter sphaeroides incorporating carotenoids from the spirilloxanthin pathway, Biochim. Biophys. Acta (Bioenerg.), 2015, vol. 1847, pp. 189–201.
Cogdell, R.J., Fyfe, P.K., Barrett, S.J., Prince, S.M., Freer, A.A., Isaacs, N.W., Mcglynn, P., and Hunter, C.N. The purple bacterial photosynthetic unit, Photosynth. Res., 1996, vol. 48, pp. 55–63.
Davidson, E. and Cogdell, R.J., Reconstitution of carotenoids into the light-harvesting pigment–protein complex from the carotenoidless mutant of Rhodopseudomonas sphaeroides R26, Biochim. Biophys. Acta, 1981, vol. 635, pp. 295–303.
Gabrielsen, M., Gardiner, A.T., and Cogdell, R.J., Peripheral complexes of purple bacteria, in: The Purple Phototrophic Bacteria, 2009, vol. 28, pp. 135–153.
Gall, A., Henry, S., Takaichi, S., Bruno, R., and Cogdell, R.J., Preferential incorporation of colored-carotenoids occurs in the LH2 complexes from non-sulphur purple bacteria under carotenoid-limiting conditions, Photosynth. Res., 2005, vol. 86, pp. 25–35.
Hoff, A.J. and Deisenhofer, J., Photophysics of photosynthesis. Structure and spectroscopy of reaction centers of purple bacteria, Physics Rep., 1997, vol. 287, pp. l–247.
Hunter, C.N., Tucker, J.D., and Niederman, R.A., The assembly and organisation of photosynthetic membranes in Rhodobacter sphaeroides, Photochem. Photobiol. Sci., 2005, vol. 4, pp. 1023–1027.
Koepke, J., Hu, X., Munke, C., Schulten, K., and Michel, H., The crystal structure of the light harvesting complex II (B800-850) from Rhodospirillum molischianum, Structure, 1996, vol. 4, pp. 581–597.
Kondrat’eva, E.N., Fotosinteziruyushchie bakterii i baketrial’nyi fotosintez (Photosynthesizing Bacteria and Bacterial Photosynthesis), Moscow: Mos. Gos. Univ., 1972.
Lang, H.P. and Hunter, C.N., The relationship between carotenoid biosynthesis and the assembly of the light-harvesting LH2 complex in Rhodobacter sphaeroides, Biochem. J., 1994, vol. 298, pp. 197–205.
Lang, H.P., Cogdell, R.G., Takaichi, S., and Hunter, C.N., Complete DNA sequence, specific Tn5 insertion map, and gene assignment of the carotenoid biosynthesis pathway of Rhodobacter sphaeroides, J. Bacteriol., 1995, vol. 177, pp. 2064–2073.
Leszek, F., Akahane, J., and Koyama, Y., Carotenoidinduced cooperative formation of bacterial photosynthetic LH1 complex, Biochemistry, 2004, vol. 43, pp. 487–496.
Löhner, A., Carey, A.M., Hacking, K., Picken, N., Kelly, S., Cogdell, R., and Köhler, J., The origin of the split B800 absorption peak in the LH2 complexes from Allochromatium vinosum, Photosynth. Res., 2015, vol. 123, pp. 23–31.
Makhneva, Z., Bolshakov, M., and Moskalenko, A., Heterogeneity of carotenoid content and composition in LH2 of the purple sulphur bacterium Allochromatium minutissimum grown under carotenoid-biosynthesis inhibition, Photosynth. Res., 2008, vol. 98, pp. 633–641.
Makhneva, Z.K., Bolshakov, M.A., Ashikhmin, A.A., Erokhin, Y.E., and Moskalenko, A.A., Influence of blue light on the structure stability of antenna complexes from Allochromatium minutissimum with different content of carotenoids, Biochemistry (Moscow) Suppl. Ser. A: Membrane Cell Biol., 2009, vol. 3, no. 2
McDermott, G., Prince, S., Freer, A., Hawthornthwaite-Lawless, A., Papiz, M., Cogdell, R.G., and Isaacs, N., Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria, Nature, 1995, vol. 374, pp. 517–521.
Moskalenko, A.A. and Karapetyan, N.V., Structural role of carotenoids in photosynthetic membranes, Z. Naturforsch., 1996, vol. 51, pp. 763–771.
Moskalenko, A.A., Mahold, O., and Erokhin, Yu.E., Localization of the polypeptides of pigment-protein complexes of Chromatium minutissimum, Doklady, 1983, vol. 270, no. 1, pp. 251–253.
Moskalenko, A.A., Makhneva, Z.K., Fiedor, L., and Scheer, H. Effects of carotenoid inhibition on the photosynthetic RC–LH1 complex in purple sulphur bacterium Thiorhodospira sibirica, Photosynth. Res., 2005, vol. 86, pp. 71–80.
Nakagawa, K., Suzuki, S., Fujii, R., Gardiner, A.T., Cogdell, R.G., Nango, M., and Hashimoto, H., Probing the effect of the binding site on the electrostatic behavior of a series of carotenoids reconstituted into the light-harvesting 1 complex from purple photosynthetic bacterium Rhodospirillum rubrum detected by Stark spectroscopy, J. Phys. Chem. B., 2008, vol. 112, pp. 9467–9475.
Niederman, R.A., Structure, function and formation of bacterial intracytoplasmic membranes, complex intracellular structures in prokaryotes, in: Microbiology Monographs, Shively, J.M., Ed., Berlin: Springer, 2006, vol. 2, pp. 193–227.
Niedzwiedzki, D.M., Bina, D., Picken, N., Honkanen, S., Blankenship, R.E., Holten, D., and Cogdell, R.J., Spectroscopic studies of two spectral variants of light-harvesting complex 2 (LH2) from the photosynthetic purple sulfur bacterium Allochromatium vinosum, Biochim. Biophys. Acta, 2012, vol. 1817, pp. 1576–1587.
Noguchi, T., Hayashi, H., and Tasumi, M., Factors controlling the efficiency of energy transfer from carotenoids to bacteriochlorophyll in purple photosynthetic bacteria, Biochim. Biophys. Acta, 1990, vol. 1017, pp. 280–290.
Papagiannakis, E., Das, S.K., Gall, A., van Stokkum, I.H.M., Robert, B., van Grondelle, R., Frank, H.A., and Kennis, J.T.M., Light harvesting by carotenoids incorporated into the B850 light-harvesting complex from Rhodobacter sphaeroides R-26.1: Excitedstate relaxation, ultrafast triplet formation and energy transfer to bacteriochlorophyll, J. Phys. Chem. B, 2003, vol. 107, pp. 5642–5649.
Prince, S.M., Howard, T.D., Myles, D.A., Wilkinson, C., Papiz, M.Z., Freer, A.A., Cogdell, R.J., and Isaacs, N.W., Detergent structure in crystals of the integral membrane light-harvesting complex LH2 from Rhodopseudomonas acidophila strain 10050, J. Mol. Biol., 2003, vol. 326, pp. 307–315.
Schwerzmann, R.U. and Bachofen, R., carotenoid profiles in pigment-protein complexes of Rhodospirillum rubrum, Plant Cell Phisiol., 1989, vol. 30, pp. 497–504.
Takaichi, S., Distribution and biosynthesis of carotenoids, in The Purple Phototrophic Bacteria, Daldal, F., Thurnauer, M.C., Beatty, J.T., and Hunter, C.N., Eds., New York: Springer, 2009, pp. 97–117.
Telfer, A., Pascal, A., and Gall, A., Carotenoids in photosynthesis, in: Carotenoids. Natural Functions, Britton, G., Liaaen-Jensen, S., and Pfanger, H., Eds., Birkhauser Verlag, 2008, pp. 265–308.
Toropygina, O.A., Makhneva, Z.K., and Moskalenko, A.A., Reconstitution of carotenoids into the light-harvesting complex B800–850 of Chromatium minutissimum, Biochemistry (Moscow), 2003, vol. 68, no. 8, pp. 901–911.
Yeliseev, A.A., Eraso, J.M., and Kaplan, S., Differential carotenoid composition of the B875 and B800–850 photosynthetic antenna complexes in Rhodobacter sphaeroides 2.4.1: involvement of spheroidene and spheroidenone in adaptation to changes in light intensity and oxygen availability, J. Bacteriol., 1996, vol. 178, pp. 5877–5883.
Author information
Authors and Affiliations
Corresponding author
Additional information
Original Russian Text © M.A. Bol’shakov, A.A. Ashikhmin, Z.K. Makhneva, A.A. Moskalenko, 2017, published in Mikrobiologiya, 2017, Vol. 86, No. 5, pp. 538–550.
Rights and permissions
About this article
Cite this article
Bol’shakov, M.A., Ashikhmin, A.A., Makhneva, Z.K. et al. Spirilloxanthin incorporation into the LH2 and LH1-RC pigment-protein complexes from a purple sulfur bacterium Allochromatium minutissimum . Microbiology 86, 549–559 (2017). https://doi.org/10.1134/S0026261717050058
Received:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S0026261717050058