Abstract
The absorption and circular dichroism spectra of the chlorosomes isolated from green photosynthetic Chloroflexus aurantiacus bacteria grown under different illumination were studied. It was found that the spectra shift to a red side and become narrower and larger in amplitude as this illumination decreases. A theoretical modeling of data obtained was carried out using a theory of excitons. It was concluded that the number of bacteriochlorophyll c molecules in the linear chains (that form a basis of the elementary blocks of chlorosomes) increases as the intensity of light, under which bacteria are grown, decreases. It was suggested that this phenomenon increases the efficiency of capturing weak light fluxes and, thus, increases the chances of bacterial survival in conditions of sunlight deficiency.
REFERENCES
Oelze, J. and Golecki, J., Membranes and chlorosomes of green bacteria: structure, composition and development, in Anoxygenic Photosynthetic Bacteria, Blankenship, R.E., Madigan, M.T., and Bauer, C.E., Eds., Amsterdam: Kluwer Acad., 1995, pp. 259–278.
Frigaard, N.-U. and Bryant, D., Chlorosomes: antenna organelles in green photosynthetic bacteria, Microbiology Monographs, vol. 2: Complex intracellular structures in prokaryotes., Shively, J.M., Ed., Berlin: Springer-Verlag, 2006, pp. 79–114.
Krasnovsky, A. and Bystrova, M., Self-assembly of chlorophyll aggregated structures, BioSystems, 1980, vol. 12, no. 3, pp. 181–194.
Smith, K., Kehres, L., and Fajer, J., Aggregation of bacteriochlorophylls c, d or e. Models for the antenna chlorophylls of green and brown photosynthetic bacteria, J. Am. Chem. Soc., 1983, vol. 105, no. 5, pp. 1387–1389.
Fetisova, Z.G. and Fok, M.V., Means of optimizing conversion of light energy in the primary stages of photosynthesis. I. The need for optimizing the structure of a photosynthetic unit and calculation of its efficiency, Mol. Biol., 1984, vol. 18, no. 6, pp. 1354–1359.
Staehelin, L., Golecki, J., Fuller, R., and Drews, G., Visualization of the supramolecular architecture of chlorosomes (Chlorobium type vesicles) in freeze-fractured cells of Chloroflexus aurantiacus, Arch. Microbiol., 1978, vol. 119, no. 3, pp. 269–277.
Sprague, S., Staehelin, L., DiBartolomeis, M., and Fuller, R., Isolation and development of chlorosomes in the green bacterium Chloroflexus aurantiacus, J. Bacteriol., 1981, vol. 147, no. 3, pp. 1021–1031.
Saga, Y. and Tamiaki, H., Transmission electron microscopic study on supramolecular nanostructures of bacteriochlorophyll self-aggregates in chlorosomes of green photosynthetic bacteria, J. Biosci. Bioeng., 2006, vol. 102, no. 2, pp. 18–23.
Egawa, A., Fujiwara, T., Mizoguchi, T., Kakitani, Y., Koyama, Y., and Akutsu, H., Structure of the light-harvesting bacteriochlorophyll c assembly in chlorosomes from Chlorobium limicola determined by solid-state NMR, Proc. Natl. Acad. Sci. U. S. A., 2007, vol. 104, no. 3, pp. 790–795.
Ganapathy, S., Oostergetel, G., Wawrzyniak, P., Reus, M., Gomez Maqueo Chew, A., Buda, F., Boekema, E., Bryant, D., Holzwarth, A., and de Groot, H., Alternating syn-anti bacteriochlorophylls form concentric helical nanotubes in chlorosomes, Proc. Natl. Acad. Sci. U. S. A., 2009, vol. 106, no. 21, pp. 8525–8530.
Günther, L., Jendrny, M., Bloemsma, E., Tank, M., Oostergetel, G., Bryant, D., Knoester, J., and Köhler, J., Structure of light-harvesting aggregates in individual chlorosomes, J. Phys. Chem. B, 2016, vol. 120, no. 24, pp. 5367−5376.
Pšenčik, J., Ikonen, T., Laurinmäki, P., Merckel, M., Butcher, S., Serimaa, R., and Tuma, R., Lamellar organization of pigments in chlorosomes, the light harvesting system of green bacteria, Biophys. J., 2004, vol. 87, no. 2, pp. 1165–1172.
Pšenčik, J., Torkkeli, M., Zupčanová, A., Vácha, F., Serimaa, R., and Tuma, R., The lamellar spacing in self-assembling bacteriochlorophyll aggregates is proportional to the length of the esterifying alcohol, Photosynth. Res., 2010, vol. 104, no. 2, pp. 211–219.
Van Dorssen, R.J., Vasmel, H., and Amesz, J., Pigment organization and energy transfer in the green photosynthetic bacterium Chloroflexus aurantiacus. II. The chlorosome, Photosynth. Res., 1986, vol. 9, no. 1, pp. 33–45.
Novoderezhkin, V., Taisova, A., Fetisova, Z., Blankenship, R., Savikhin, S., Buck, D., and Struve, W., Energy transfers in the B808-866 antenna from the green bacterium Chloroflexus aurantiacus, Biophys. J., 1998, vol. 74, no. 4, pp. 2069–2075.
Linnanto, J. and Korppi-Tommola, J., Exciton description of chlorosome to baseplate excitation energy transfer in filamentous anoxygenic phototrophs and green sulfur bacteria, J. Phys. Chem. B, 2013, vol. 117, no. 38, pp. 11144−11161.
Pierson, B. and Castenholz, R., Studies of pigments and growth in Chloroflexus aurantiacus, a phototrophic filamentous bacterium, Arch. Microbiol., 1974, vol. 100, no. 1, pp. 283−305.
Schmidt, K., Maarzahl, M., and Mayer, F., Development and pigmentation of chlorosomes in Chloroflexus aurantiacus Ok-70-fl, Arch. Microbiol., 1980, vol. 127, no. 2, pp. 87−97.
Taisova, A., Keppen, O., Lukashev, E., Arutyunyan, A., and Fetisova, Z., Study of the chlorosomal antenna of the green mesophilic filamentous bacterium Oscillochloris trichoides, Photosynth. Res., 2002, vol. 74, no. 1, pp. 73−85.
Davydov, A.S., Teoriya molekulyarnykh eksitonov (Theory of Molecular Excitons), Moscow: Nauka, 1968.
Fetisova, Z., Freiberg, A., Mauring, K., Novoderezhkin, V., Taisova, A., and Timpmann, K., Excitation energy transfer in chlorosomes of green bacteria: theoretical and experimental studies, Biophys. J., 1996, vol. 71, no. 2, pp. 995−1010.
Mauring, K., Novoderezhkin, V., Taisova, A., and Fetisova, Z., Exciton levels structure of antenna bacteriochlorophyll c aggregates in the green bacterium Chloroflexus aurantiacus as probed by 1.8-293 K fluorescence spectroscopy, FEBS Lett., 1999, vol. 456, no. 2, pp. 239−242.
Gülen, D., Significance of the excitonic intensity borrowing in the J-/H-aggregates of bacteriochlorophylls/chlorophylls, Photosynth. Res., 2006, vol. 87, no. 2, pp. 205–214.
Oostergetel, G., van Amerongen, H., and Boekema, E., The chlorosome: a prototype for efficient light harvesting in photosynthesis, Photosynth. Res., 2010, vol. 104, no. 2, pp. 245−255.
Scholes, G.D., Fleming, G.R., Alexandra Olaya-Castro, A., and van Grondelle, R., Lessons from nature about solar light harvesting, Nat. Chem., 2011, vol. 3, no. 10, pp. 763−774.
Golecki, J. and Oelze, J., Quantitative relationship between bactenochlorophyll content, cytoplasmic membrane structure and chlorosome size in Chloroflexus aurantiacus, Arch. Microbiol., 1987, vol. 148, no. 3, pp. 236−241.
Furumaki, S., Vácha, F., Habuchi, S., Tsukatani, Y., Bryant, D., and Vacha, M., Absorption linear dichroism measured directly on a single light-harvesting system: the role of disorder in chlorosomes of green photosynthetic bacteria, J. Am. Chem. Soc., 2011, vol. 133, no. 17, pp. 6703−6710.
Linnanto, J. and Korppi-Tommola, J., Investigation on chlorosomal antenna geometries: tube, lamella and spiral-type self-aggregates, Photosynth. Res., 2008, vol. 96, no. 3, pp. 227–245.
Prokhorenko, V.I., Steensgaard, D.B., and Holzwarth, A.R., Exciton dynamics in the chlorosomal antennae of the green bacteria Chloroflexus aurantiacus and Chlorobium tepidum, Biophys. J., 2000, vol. 79, no. 4, pp. 2105–2120.
Furumaki, S., Yabiku, Y., Habuchi, S., Tsukatani, Y., Bryant, D., and Vacha, M., Circular dichroism measured on single chlorosomal light-harvesting complexes of green photosynthetic bacteria, J. Phys. Chem. Lett., 2012, vol. 3, no. 23, pp. 3545−3549.
Jendrny, M., Aartsma, T., and Kӧhler, J., Insights into the excitonic states of individual chlorosomes from Chlorobaculum tepidum, Biophys. J., 2014, vol. 106, no. 9, pp. 1921−1927.
Hartigan, N., Tharia, H., Sweeney, F., Lawless, A., and Papiz, M., The 7.5-Å electron density and spectroscopic properties of a novel low-light B800 LH2 from Rhodopseudomonas palustris, Biophys. J., 2002, vol. 82, no. 2, pp. 963−977.
ACKNOWLEDGMENTS
We are grateful to A.M. Arutyunyan for the assistance in measuring CD spectra.
Funding
This work was supported by the state task “Photobiophysics of Solar Energy Conversion in Living Systems” (no. AAAA-A17-117120540070-0).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
CONFLICT OF INTEREST
The authors declare that they have no conflicts of interest.
This article does not contain any studies involving animals and human participants.
Additional information
Translated by A. Barkhash
About this article
Cite this article
Yakovlev, A.G., Taisova, A.S. & Fetisova, Z.G. Adaptation of Green Photosynthetic Bacteria to Different Illumination According to Spectroscopy Data on Chlorosomes. Moscow Univ. Biol.Sci. Bull. 78, 53–58 (2023). https://doi.org/10.3103/S0096392523020116
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.3103/S0096392523020116