Abstract
Chemical oxidation of the chlorosomes from Chloroflexus aurantiacus and Chlorobium tepidum green bacteria produces bacteriochlorophyll radicals, which are characterized by an anomalously narrow EPR signal compared to in vitro monomeric BChl c .+ [Van Noort PI, Zhu Y, LoBrutto R and Blankenship RE (1997) Biophys J 72: 316–325]. We have performed oxidant concentration and temperature-dependent X-band EPR measurements in order to elucidate the line narrowing mechanism. The linewidth decreases as the oxidant concentration is increased only for Chloroflexus indicating that for this system Heisenberg spin exchange is at least partially responsible for the EPR spectra narrowing. For both species the linewidth is decreasing on increasing the temperature. This indicates that temperature-activated electron transfer is the main narrowing mechanism for BChl radicals in chlorosomes. The extent of the electron transfer process among different BChl molecules has been evaluated and a comparison between the two species representative of the two green bacteria families has been made. In parallel, high frequency EPR experiments have been performed on the oxidized chlorosomes of Chloroflexus and Chlorobium at 110 and 330 GHz in the full temperature range investigated at X-band. The g-tensor components obtained from the simulation of the 330 GHz EPR spectrum from Chlorobium show the same anisotropy as those of monomeric Chl a .+ [Bratt PJ, Poluektov OG, Thurnauer MC, Krzystek J, Brunel LC, Schrier J, Hsiao YW, Zerner M and Angerhofer A (2000) J Phys Chem B 104: 6973–6977]. The spectrum of Chloroflexus has a nearly axial g-tensor with reduced anisotropy compared to Chlorobium and monomeric Chl a in vitro. g-tensor values and temperature dependence of the linewidth have been discussed in terms of the differences in the local structure of the chlorosomes of the two families.
Similar content being viewed by others
References
Aasa R and Vänngård T (1975) EPR signal intensity and powder shapes: a reexamination. J Magn Res 19: 308–315
Arellano JB, Psencik J, Borrego CM, Ma YZ, Guyoneaud R, Garcia Gil J and Gillbro T (2000) Effect of carotenoid biosynthesis inhibition on the chlorosome organization in Chlorobium phaeobacteroides strain CL1401. Photochem Photobiol 71: 715–723
Bowman MK, Michalski TJ, Tyson RL, Worcester DL and Katz JJ (1988) Electron spin resonance of charge carriers in chlorophyll a/water micelles. Proc Natl Acad Sci USA 85: 1498–1502
Bratt PJ, Rohrer M, Krzystek J, Evans MCW, Brunel LC and Angerhofer A (1997) Submillimeter high-field EPR studies of the primary donor in plant Photosystem I P700. J Phys Chem B 101: 9686–9689
Bratt PJ, Ringus E, Hassan A, Van Tol H, Maniero AL, Brunel LC, Rohrer M, Bubenzer Hange C, Scheer H and Angerhofer A (1999) EPR on biological samples beyond the limits of superconducting magnets-the primary donor cation of purple bacterial photosynthesis. J Phys Chem B 103: 10973–10977
Bratt PJ, Poluektov OG, Thurnauer MC, Krzystek J, Brunel LC, Schrier J, Hsiao YW, Zerner M and Angerhofer A (2000) The gfactor anisotropy of plant chlorophyll a ·+. J Phys Chem B 104: 6973–6977
Carbonera D, Bordignon E, Giacometti G, Agostini G, Vianelli A and Vannini C (2001) Fluorescence and absorption detected magnetic resonance of chlorosomes from green bacteria Chlorobium tepidum and Chloroflexus aurantiacus. A comparative study. J Phys Chem B 105: 246–255
Crystall B, Booth PY, Klug DR, Barber J and Porter G (1989) Resolution of a long lived fluorescence component from D1/D2/cytochrome b-559 reaction centers. FEBS Lett 249: 75–78
Dikshit SN, Weber S and Norris JR (1998) Exploring photosynthetic antenna with electron paramagnetic resonance. In: Ziessow D et al. (eds) Magnetic resonance and related phenomena. Proceedings of the Joint 29th Ampere-13th ISMAR International Conference, Vol 1, p 165. Technische Universität Berlin, Berlin
Fetisova Z, Freiberg A, Mauring K, Novoderezhkin V, Taisova A and Timpmann K (1996) Excitation energy transfer in chlorosomes of green bacteria: theoretical and experimental studies. Biophys J 71: 995–1010
Francke C and Amesz J (1997) Isolation and pigment composition of the antenna system of four species of green sulfur bacteria. Photosynth Res 52: 137–146
Frese R, Oberheide U, van Stokkum I, van Grondelle R, Foidl M, Oelze J and van Amerongen H (1997) The organization of bacteriochlorophyll c in chlorosomes from Chloroflexus aurantiacus and the structural role of carotenoids and protein. Photosynth Res 54: 115–126
Frigaard NU, Matsuura K, Hirota M, Miller M and Cox RP (1998) Studies of the location and function of isoprenoid quinones in chlorosomes from green sulfur bacteria. Photosynth Res 58: 81–90
Gerola PD and Olson JM (1986) A new bacteriochlorophyll a-protein complex associated with chlorosomes of green sulfur bacteria. Biochim Biophys Acta 848: 69–76
Gingras G and Picorel R (1990) Supramolecular arrangement of Rhodospirillum rubrum B880 holochrome as studied by radiation inactivation and electron paramagnetic resonance. Proc Natl Acad Sci USA 87: 3405–3409
Hassan AK, Pardi LA, Krzystek J, Sienkiewicz A, Goy P, Rohrer M and Brunel LC (2000) Ultrawide band multifrequency high-field EMR technique: a methodology for increasing spectroscopic information. J Magn Res 142: 300–312
Hildebrandt P, Tamiaki H, Holzwarth AR and Schaffner K (1994) Resonance Raman spectroscopic study of metallochlorin aggregates. Implications for the supramolecular structure in chlorosomal Bchl c antennae of green bacteria. J Phys Chem 98: 2192–2197
Holzwarth AR and Schaffner K (1994) On the structure of bacteriochlorophyll molecular aggregates in the chlorosomes of green bacteria. A molecular modelling study. Photosynth Res 41: 225–233
Kispert LD, Joseph J, McGraw J, Robinson T and Drobner R (1987) EPR study of arene radical cation salt crystals. Synth Metals 19: 67–72
Konovalova TA, Krzystek J, Bratt PJ, van Tol J, Brunel LC and Kispert LD (1999) 95–670 GHz EPR studies of canthaxanthin radical cation stabilized on a silica-alumina surface. J Phys Chem B 103: 5782–5786
Kubo R and Tomita K (1954) A general theory of magnetic resonance absorption. J Phys Soc Jpn 9: 888–919
Lakshmi KV, Reifler MJ, Brudvig GW, Poluektov OG, Wagner AM and Thurnauer MC (2000) High-field EPR study of carotenoid and chlorophyll cation radicals in Photosystem II. J Phys Chem B 104: 10445–10448
Malik KA (1996) A modified medium and method for the cultivation of Chloroflexus. J Microbiol Meth 27: 147–150
Mizoguchi T, Sakamoto S, Koyama Y, Ogura K and Inagaki F (1998) The structure of the aggregate form of bacteriochlorophyll c showing the Q(y) absorption above 740 nm as determined by the ring-current effects on H-1 and C-13 nuclei and by H-1-H-1 intermolecular NOE correlations. Photochem Photobiol 67: 239–248
Norris JR, Uphaus RA, Crespi HL and Katz JJ (1971) Electron spin resonance of chlorophyll and the origin of signal I in photosynthesis. Proc Natl Acad Sci USA 68: 625–628
Nozawa T, Noguchi T and Tasumi M (1990) Resonance Raman studies on the structure of bacteriochlorophyll c in chlorosomes from Chloroflexus aurantiacus. J Biochem 108: 737–740
Olson JM (1998) Chlorophyll organization and function in green photosynthetic bacteria. Photochem Photobiol 67: 61–75
Prokhorenko VI, Steensgaard DB and Holzwarth AR (2000) Exciton dynamics in the chlorosomal antennae of the green bacteria Chloroflexus aurantiacus and Chlorobium tepidum. Biophysical J 79: 2105–2120
Sakuragi Y, Frigaard NU, Shimada K and Matsuura K (1999) Association of bacteriochlorophyll a with the CsmA protein in chlorosomes of the photosynthetic green filamentous bacterium Chloroflexus aurantiacus. Biochim Biophys Acta 1413: 172–180
Savikhin S, van Noort PI, Zhu Y, Lin S, Blankenship RE and Struve W (1995) Ultrafast energy transfer in light-harvesting chlorosomes from the green sulfur bacterium Chlorobium tepidum. Chem Phys 194: 245–258
Steensgaard DB, Wackerbarth H, Hildebrandt P and Holzwarth AR (2000) Diastereoselective control of bacteriochlorophyll e aggregation. 31-S-BChl e is essential for the formation of chlorosome-like aggregates. J Phys Chem B 104: 10379–10386
Tang J, Dikshit SN and Norris JR (1995) Electron spin resonance line shapes for one-and two-dimensional random walk processes. J Chem Phys 103: 2873–2881
van Noort PI, Zhu Y, LoBrutto R and Blankenship RE (1997) Redox effects on the excited-state lifetime in chlorosomes and bacteriochlorophyll c oligomers. Biophys J 72: 316–325
van Rossum BJ, Steensgaard DB, Mulder FM, Boender GJ, Schaffner K, Holzwarth AR and de Groot HJM (2001) A refined model of the chlorosomal antennae of the green bacterium Chlorobium tepidum from proton chemical shift constraints obtained with high-field 2-D and 3-D MAS NMR dipolar correlation spectroscopy. Biochemistry 40: 1587–1595
Wahlund TM, Woese CR, Castenholz RW and Madigan MT (1991) A thermophilic green sulfur bacterium from New Zealand hot springs, Chlorobium tepidum sp. nov. Arch Microbiol 156: 81–90
Weber S, Fuchs M, Möbius K, Dikshit SN and Norris JR (1998) Using high-field and time-resolved EPR to probe structure and function of purple bacterial antenna complexes. In: Ziessow D et al. (eds) Magnetic resonance and related phenomena. Proceeding of the Joint 29th Ampere-13th ISMAR International Conference, Vol 2, p 875. Technische Universität Berlin, Berlin
Wu H-M, Rätsep M, Young CS, Jankowiak R, Blankenship RE and Small GJ (2000) High-pressure and Stark hole-burning studies of chlorosomes antennas from Chlorobium tepidum. Biophys J 79: 1561–1572
Yang SI, Lammi RK, Seth J, Riggs JA, Arai T, Kim DH, Bocian DF, Holten D and Lindsey JS (1998) Excited-state energy transfer and ground-state hole electron hopping in p-phenylene-linked porphyrin dimers. J Phys Chem B 102: 9426–9436
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Di Valentin, M., Malorni, D., Maniero, A.L. et al. Structural investigation of oxidized chlorosomes from green bacteria using multifrequency electron paramagnetic resonance up to 330 GHz. Photosynthesis Research 71, 33–44 (2002). https://doi.org/10.1023/A:1014999429778
Issue Date:
DOI: https://doi.org/10.1023/A:1014999429778