Photosynthesis Research 15:177-189 (1988) © Martinus Nijhoff Publishers, Dordrecht - Printed in the Netherlands

Regular paper

Pigment organization and energy transfer in the green photosynthetic bacterium Chloroflexus aurantiacus. III. Energy transfer in whole cells ROB J. VAN D O R S S E N & J A N A M E S Z Department of Biophysics, Huygens Laboratory of the State University, P.O. Box 9504, 2300 RA Leiden, The Netherlands Received 17 August 1987; accepted in revised form 13 October 1987

Key words: bacteriochlorophyll, Chloroflexus aurantiacus, chlorosome, energy transfer, fluorescence, green photosynthetic bacteria

Abstract. The transfer of excitation energy in intact cells of the thermophilic green photosynthetic bacterium Chloroflexus aurantiacus was studied both at low temperature and under more physiological conditions. Analysis of excitation spectra measured at 4 K indicates that the minor fraction of bacteriochlorophyll a present in the chlorosome functions as an intermediate in energy transfer between the main light-harvesting pigment BChl c and the membrane-bound B808-866 antenna complex. This supports the hypothesis that BChl a is associated with the base plate which connects the chlorosome with the membrane. The overall efficiency for energy transfer from the chlorosome to the membrane is only 15% at 4 K. High efficiencies of close to 100% are observed above 40 °C near the temperature where the cultures are grown. Cooling to 20 °C resulted in a sudden drop of the transfer efficiency which appeared to originate in the chlorosome. This decrease may be related to a lipid phase transition. Further cooling mainly affected the efficiency of transfer between the chlorosome and the membrane. This effect can only partially be explained by a decreased F6rster overlap between the chlorosomal BChl a and BChl a 808 associated with the membrane-bound antenna system. The temperature dependence of the fluorescence yield of BChl a 866 also appeared to be affected by lipid phase transitions, suggesting that this fluorescence can be used as a native probe of the physical state of the membrane.

Introduction

The antenna system of the thermophilic green filamentous bacterium Chloroflexus aurantiacus consists of two components: the B808-866 complex and the chlorosome. The chlorosomes, oblong bodies attached to the cytoplasmic membrane (Madigan and Brock 1977, Staehelin et al. 1978) contain BChl c as the major light-harvesting pigment, carotenoid and a small amount of BChl a (about 4% of the BChl c content) (Schmidt 1980, Feick et al. 1982, van Dorssen et al. 1986b). The chlorosomes serve as common

178 antennas for several reaction centers. They are eminently suited for their light-harvesting function as they contain large quantities of antenna pigments at a very high concentration. Rapid energy transfer occurs among the highly ordered BChl c chromophores (Vos et al. 1987). The B808-866 complex is situated in the membrane and contains BChl a and carotenoid. Both the chlorosome and the B808-866 complex have been isolated in a pure form (Feick et al. 1982) and the primary structures of the ~ and fl proteins of B808-866 (Wechsler et al. 1985, Zuber et al. 1987) and of the BChl c binding protein of the chlorosomes (Wechsler et al. 1984) have been determined. The earlier publications of this series (Vasmel et al. 1986, van Dorssen et al 1986b) were concerned with the spectroscopic properties of the isolated membranes and chlorosomes of C. aurantiacus. Energy transfer from BChl a 808 to BChl a 866 within the B808-866 complex was found to proceed with an efficiency of close to 100%, whereas energy transfer from BChl c to the BChl a component of the chlorosomes (BChl a 798) occurred with an efficiency of only about 55%, both at room temperature and at 4 K , as indicated by the excitation spectra of the BChl a fluorescence. Because of the favorable overlap between the emission spectrum of BChl a 798 and the absorption spectrum of BChl a 808 in the membrane it has been postulated (Betti et al. 1982, Amesz and Vasmel 1986, van Dorssen et al. 1986b) that BChl a 798 is involved in the transfer of excitations from the chlorosome to the membrane, but energy transfer from BChl a 798 to BChl a 808 has not been directly demonstrated so far. The present paper deals with measurements of energy transfer in whole cells of C. aurantiacus, both at 4 K and at more physiological temperatures. Evidence will be presented that energy transfer from BChl c to the membrane indeed occurs via BChl a 798, together with observations on efficiencies of energy transfer within the antenna system at temperatures between 10 and 50°C, the growth temperature of the bacterium.

Materials and methods

Cells of Chloroflexus aurantiacus strain J-10-fl were grown at 52°C in medium D as described by Pierson and Castenholz (1974). Measurements between 50 and 10 °C were performed in a cuvette with an optical pathlength of 10 mm. The cells were diluted with glycerol (66% v/v) to reduce scattering and transferred directly to the cuvette. For experiments at low temperature a 2.5-mm cuvette was used. In this case, the cells were harvested by centrifugation and resuspended in 10 mM Tris, pH = 8.0. For measuring fluore-

179 scence spectra the analyzing monochromator had a half-bandwidth of 1.6 nm, while for the excitation spectra both the excitation and the analyzing monochromator were set at 3.2 nm. Prior to the measurements glycerol was added (66% v/v), again to reduce scattering and to prevent crystallization at low temperature. The apparatus to measure absorption, fluorescence emission and excitation spectra has been described by Kramer and Amesz (1982).

Results

Energy transfer at low temperature The absorption spectrum of C. aurantiacus, measured at 4 K, is shown in Fig. 1A. Qybands of BChl c and BChl a are seen at 743 nm and at 801 and 873 nm, respectively. In the blue region bands of carotenoid (515 nm) and of the Soret transitions of BChl c (461 nm) are observed. Part of the spectrum is replotted on an extended scale for a comparison with the spectrum of isolated membrane fragments (Fig. 1B) as measured by Vasmel et al. (1986). It can be seen that the shape and position of the maximum of the band of BChl a 866 in the two spectra is very similar, but below 840 nm the spectra deviate strongly and it is clear that the additional absorption must arise from the chlorosomal BChl a 798. Subtraction of the two spectra indeed yielded a band at 798nm, which accounted for 61% of the absorption at this wavelength. Comparison of the spectrum of Fig. 1A with that of isolated chlorosomes (van Dorssen et al. 1986b) showed that the maximum of the Qy band of BChl c in whole cells was somewhat red-shifted. Moreover, the band was more symmetric, resulting in a considerably higher absorption beyond 745 nm in the absorption spectrum of whole cells. After normalization at the maximum of the BChl c Qy absorption subtraction of the chlorosome spectrum from that of whole cells yielded a value of 65% for the fractional absorption by BChl a 798 at 798 nm, in good agreement with the value obtained above. An average value of 63 % was taken for further calculations (see below). These results demonstrate that for the Qyregion the spectrum of whole cells can be analyzed satisfactorily in terms of the spectra of isolated chlorosomes and membrane fragments. Upon excitation at 690 nm in the tail of the Qy band of BChl c the low temperature emission spectrum (Fig. 2) showed maxima at 755, 817 and 891 nm of BChl c, BChla 798 and BChl a 866, respectively. The positions of the latter two bands agree with those reported for the isolated chlorosomes and membranes, but the BChl c emission maximum was located at some-

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what shorter wavelength than in the isolated chlorosomes (van Dorssen et al. 1986b). It should be noted, however, that the maximum of the BChl c emission varied by as much as 6 nm for different batches of cells. Smaller variations of up to 2 nm were observed for the positions of the emission bands of BChl a 798 and BChl a 866. Figure 3 shows the low temperature excitation spectrum of the BChl a 866 emission. The most significant feature of this spectrum is the low contribution of the BChl c bands relative to those of BChl a. Comparison with the absorption spectrum indicated that BChl c transfers its excitation energy to BChl a 866 with an overall efficiency of

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The absorbance at 743 nm was 0.40 (4 K). The inset shows the calculated transfer efficiency in the region around 740 nm (dashed line). only 15%. The height o f the band at 8 0 3 n m is also relatively low. Since energy transfer f r o m BChl a 808 to BChl a 866 is k n o w n to proceed with high efficiency (Vasmel et al. 1986), the reduced height at 803 n m m a y be a s s u m e d to reflect a reduced transfer efficiency between BChl a 798 and BChl a 808 o f the B 8 0 8 - 8 6 6 complex. F r o m the relative absorption by BChl a 798, this transfer efficiency was calculated to be 31%. The excitation spectrum o f the BChl a 798 fluorescence (Fig. 4) w a s similar to that o f

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isolated chlorosomes (van Dorssen et al. 1986b), and from the relative heights of the bands near 741 and 800 nm a similar efficiency of 49% for energy transfer from BChl c to BChl a 798 was calculated. The somewhat blue-shifted position of the band near 800 nm as compared to that in the excitation spectrum of Fig. 3 reflects the absence of a contribution by BChl a 808. The above data support the hypothesis that BChl a 798 functions as an intermediate in energy transfer from the chlorosome to the membrane. At low temperature the efficiency of energy transfer from BChl c to BChl a 798 is about 50%, from BChl a 798 to BChl a 808 (and hence to BChl a 866) it is 31%0, and together these efficiencies result in an overall efficiency for energy transfer from BChl c to BChl a 866 of only 15%, as was actually observed. The efficiencies mentioned above were derived by comparing the amplitudes in the maxima of the corresponding bands. The inset of Fig. 3 shows the transfer efficiency from BChl c to BChl a 866, calculated across the BChl c band. The value was constant at wavelengths below 745 nm and then dropped sharply on the long-wavelength side of the BChl c band to a value of only half of that observed between 700 and 745 nm. Similar observations were made for the calculated efficiencies across the BChl c bands in the excitation spectra of the BChl a 798 and BChl c fluorescence (not shown). These results indicate the presence of a long-wave absorbing form of BChl c in the chlorosomes which has a low yield of fluorescence and does not or only with low efficiency transfer its excitation energy to BChl a 798.

183

Fluorescence properties at "physiologial'" temperatures Figure 5 shows fluorescence spectra of C. aurantiacus at 10 and 52°C. Maxima were observed at 755, 805 and 882 nm at 52°C, but the intensity of the long-wavelength emission was strongly dependent on the temperature. Decreasing the temperature from 52 to 10°C gave an approximately threefold increase in the emission at 882nm, whereas the amplitudes of the emission bands at shorter wavelengths were little changed. In the spectra of Fig. 5 a small increase can be observd at 755 as well as at 805 nm, but with some other samples a small decrease occurred at 755 nm upon cooling. At room temperature (20 °C) the intensity of the exciting light was sufficient to bring the cells into a condition of maximum fluorescence within a few hundred ms. The ratio between the maximum and the initial fluorescence intensity (Fmax/F0) was 2.5 for the BChl a 866 fluorescence. No induction occurred in the fluorescence of BChl c and BChl a 798. This shows that in contrast to green sulfur bacteria (Clayton 1965) "back transfer" of energy to the chlorosome does not take place, presumably because of the larger energy difference in C. aurantiacus. No induction of the BChl a 866 fluorescence was observed at 50 °C. A comparison of the integrated emissions of samples of C. aurantiacus and Rhodospirillum rubrum chromatophores (Van Grondelle 1985, Den Hollander 1983) (excitation 860 nm) gave an absolute yield of fluorescence (Fmax) of 2-3% for BChl a 866 at 20 °C. The yield of BChl c fluorescence in whole cells at 20 °C was 0.5%, i.e. about 8 I

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184 times higher than in isolated chlorosomes (Vos et al., 1987). This indicates that strong quenching processes occur in the isolated chlorosomes. Such a strong quenching was also observed in chlorosomes of Chlorobium limicola, where it could partially be relieved by the addition of dithionite (van Dorssen et al. 1986a). Excitation spectra for the BChl a 866 emission are shown in Fig. 6, together with the corresponding absorption spectra. At 52 °C the excitation spectrum followed the absorption spectrum fairly closely, indicating that the I

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185 efficiency of energy transfer from BChl c and BChl a 798 to BChl a 866 approached a value of 100°/0 at this temperature. Upon lowering the temperature to 10°C the efficiency of energy transfer from BChl c to the B808-866 complex dropped to 65%. No change was observed in the relative height of the band near 800 nm. This suggests that the effect is due to a lowered efficiency of energy transfer from BChl c to BChl a 798 in the chlorosome. Warming to 52 °C restored this efficiency to its original value. Fig. 7 shows the calculated transfer efficiency from BChl c to BChl a 866 as a function of temperature. Above 42 °C a constant value of 100% is observed. Over the region of 40 to 20 °C a sudden decrease occurs and upon further cooling the efficiency versus temperature curve flattens out. The shape of this curve seems to suggest that the observed decrease of the efficiency is related to a lipid phase transition. The reversibility of this process provides additional evidence for this notion. Figure 8 shows the intensity of the BChl a 866 emission excited at 860 nm as a function of temperature. The intensity of the emission increased monotonously with decreasing temperature, but small plateaus (arrows) are observed at 37 and 28 °C, suggesting the occurrence of lipid phase transitions at these temperatures. These results indicate that BChl a may function as a native probe of the physical state of the photosynthetic membrane, as was earlier observed for chlorophyll a in green plants and algae (Murata and Fork 1975). I

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Discussion

The antenna system of green bacteria differs markedly from that of photosynthetic purple bacteria as the main light-harvesting system is located in an extra-membraneous structure, the chlorosome. The minor fraction of BChl a in the chlorosome, BChl a 798, may play an important role in the transfer of energy to the membrane. It has been suggested that this pigment is associated with a small chlorosome protein located in the base plate, i.e. the attachment site of the chlorosome to the membrane (Feick and Fuller 1984). Energy transfer from BChl c to BChl a 798 in the chlorosome and from BChl a 808 to BChl a 866 in the membrane had already been demonstrated in isolated systems (van Dorssen et al. 1986b, Vasmel et al. 1986). The results obtained with whole cells, presented in this paper, provide direct evidence that energy transfer between the chlorosome and the membrane indeed occurs from BChl a 798 to BChl a 808. Our results provide an estimate for the maximal distance between BChl a 798 and BChl a 808. For isolated chlorosomes a lifetime of excited BChl a 798 has been measured of 165 _+ 25 ps (Brune and Blankenship 1987). On basis of this value, and from the orientations of the transition dipoles of BChl a 798 and BChl a 808 with respect to the normal of the membrane plane (van Dorssen et al. 1986b, Vasmel et al. 1986), the distance parameter f~o in the well-known F6rster equation can be calculated to be

187 4.2 < ~ < 5.2nm. P~0 is defined (Knox 1975) as the distance between a pair of donor and acceptor molecules at which energy transfer is equally fast as the combined rates of other de-excitation processes of the donor; in this case the distance is measured along the normal to the membrane. Since it seems likely that BChl a fluorescence is more strongly quenched in isolated chlorosomes than in intact cells (see also Brune and Blankenship, 1987), R0 may be higher than the value given above. This means that BChl a 798 can still be located at a considerable distance from the membrane, if BChl a 808, in analogy to the assumed position of BChl a 800 in purple bacteria (Zuber et al. 1987) is situated on the cytoplasmic side. At 4 K the overlap integral between BChl a 798 and BChl a 808 is only 35% smaller than at room temperature, due to the large width of the BChl a 808 absorption band ( ~ 30 nm). It thus appears that the efficiency of energy transfer from BChl a 798 to BChl a 808 decreases more strongly than can be explained by the decrease in overlap alone. At 52 °C, the temperature at which the bacteria were grown, energy transfer from the chlorosome to the membrane was found to proceed with a high efficiency, approaching 100%. However, cooling to temperatures below 40 °C caused a fairly sudden drop in this efficiency and at room temperature the transfer efficiency had decreased already by about 40%. The effect appears to be due mainly to a drop in the energy transfer between BChl c and BChl a 798, while the transfer from BChl a 798 to the membrane still seemed to proceed in an efficient manner. Upon lowering the temperature to 4 K the transfer efficiency from BChl c to BChl a 798 remains more or less constant. The shape of the efficiency versus temperature curve in the region 10-50 °C (Fig. 7) may suggest the involvement of lipid phase transitions. The same may apply to the observed yield changes in the BChl a 866 fluorescence in this temperature range (Fig. 8), which effect may e.g. be related to changes in electron transfer rates. Evidence for a phase transition in membranes of C. aurantiacus has been obtained by Oelze and Fuller (1983) by means of microcalorimetry. In model systems containing only a single lipid species the transition from the solid to the liquid crystalline state occurs over a small temperature range (AT ~_ 1 °C), but in natural bilayers a broader temperature range of 10-30 °C is observed (Overath et al. 1976). Lowering the temperature below the transition temperature not only causes the disappearance of the rapid lateral diffusion of the lipid molecules, but also a decrease in their spacing and an increase in the thickness of the bilayer. The observed drop in the transfer efficiency between BChl c and BChl a 798 from close to 100% at 52 °C to approximately 65% at 10 °C cannot be explained by a decrease in the overlap integral. However, it could result from

188 an increase in the spacing between both c h r o m o p h o r e s related to a lipid phase transition, I f this were the sole explanation a m u c h stronger increase o f the yield o f the BChl c fluorescence should be observed. This indicates an increase in the rate o f the non-radiative de-excitation o f BChl c resulting in a more effective competition o f this process with energy transfer to BChl a 798. The analysis is further complicated by the presence o f a BChl c fraction which at 4 K has a low fluorescence yield and a low transfer efficiency, and which seems to manifest itself at higher temperatures, as indicated by the d r o p in efficiency in the excitation spectrum at 760-780 n m (Fig. 6).

Acknowledgements We would like to t h a n k A . H . M . de Wit for culturing the bacteria. The investigation was supported by the Netherlands F o u n d a t i o n s for Chemical Research (SON) and for Biophysics, financed by the Netherlands Organization for the A d v a n c e m e n t o f Pure Research (ZWO).

References Amesz J and Vasmel H (1986) Fluorescence properties of photosynthetic bacteria. In: Govindjee, Amesz J and Fork DC, eds. Light Emission by Plants and Bacteria, pp423~49, New York: Academic Press Betti JA, Blankenship RE, Natarajan LV, Dickinson LC and Fuller RC (1982) Antenna organization and evidence for the function of a new antenna pigment species in the green photosynthetic bacterium Chloroflexus aurantiacus. Biochim Biophys Acta 680:194-201 Brune DC and Blankenship RE (1987) Light absorption and fluorescence of BChl c in chlorosomes from Chloroflexus aurantiacus and in an in vitro model. In: Biggins J, ed. Progress in Photosynthesis, Vol. I, pp. 419422. Dordrecht: Martinus Nijhoff Clayton RK (1965) Characteristics of fluorescence and delayed light from green photosynthetic bacteria and algae. J Gen Microbiol 48:633-646 Den Hollander WTF, Bakker JGC and van Grondelle R (1983) Trapping, loss and annihilation of excitations in a photosynthetic system. Biochim Biophys Acta 725:492-507 Feick RG and Fuller RC (1984) Topography of the photosynthetic apparatus of Chloroflexus aurantiacus. Biochemistry 23:3693-3700 Feick RG, Fitzpatrick M and Fuller RC (I 982) Isolation and characterization of cytoplasmic membranes and chlorosomes from the green bacterium Chloroflexus aurantiacus. J Bacteriol 150:905-915 Knox RS (1975) Excitation energy transfer and migration. In: Govindjee, ed. Bioenergetics of Photosynthesis, pp. 183 221. New York: Academic Press. Kramer HJM and Amesz J (1982) Anisotropy of the emission and absorption bands o f spinach chloroplasts by fluorescence polarization and polarized excitation spectra at low temperature. Biochim Biophys Acta 682:201-207 Madigan M T and Brock TD (1977) "Chlorobium-type" vesicles of photosynthetically grown

189 Chloroflexus aurantiacus observed using negative staining techniques. J Gen Microbiol 102: 279~285 Murata N and Fork DC (1975) Temperature dependence of chlorophyll a fluorescence in relation to the physical phase of membrane lipids in algae and higher plants. Plant Physiol 56:791 796 Oelze J and Fuller RC (1983) Temperature dependence of growth and membrane-bound activities of Chloroflexus aurantiacus energy metabolism. J Bacteriol 155:90-96 Overath P, Thilo L and Tr/iuble H (1976) Lipid phase transitions and membrane function. Trends Biochem Sci 1:186-189 Pierson BK and Castenholz RW (1974) A phototrophic gliding filamentous bacterium of hot springs. Chloroflexus aurantiacus, gen. and sp. nov.. Arch Mikrobiol 100:5-24 Schmidt K (1980) A comparative study on the composition of chlorosomes and cytoplasmic membranes from Chloroflexus aurantiacus strain OK-70-fl and Chlorobium limocola f. thiosulphatophilum strain 6230. Arch Microbiol 124:21-31 Staehelin LA, Golecki JR, Fuller RC and Drews G (1978) Visualization of the supermolecular architecture of chlorosomes (chlorobium type vesicles) in freeze-fractured cells of Chloroflexus aurantiacus. Arch Microbiol 119; 269-277 Van Dorssen ILl, Gerola PD, Olson JM and Amesz J (1986a) Optical and structural properties of chlorosomes of the photosynthetic green sulfur bacterium Chlorobium limicola. Biochim Biophys Acta 848:77-82 Van Dorssen ILl, Vasmel H and Amesz J (1986b) Pigment organization and energy transfer in the green photosynthetic bacterium Chloroflexus aurantiacus. II. The chlorosome. Photosynth Res 9:33-45 Van Grondelle R (1985) Excitation energy transfer, trapping and annihilation in photosynthetic systems. Biochim Biophys Acta 811:147-195 Vasmel H, van Dorssen RJ, de Vos GJ and Amesz J (1986) Pigment organization and energy transfer in the green photosynthetic bacterium Chloroflexus aurantiacus. I. The cytoplasmic membrane. Photosynth Res 7:281-294 Vos M, Nuijs AM, van Grondelle R, van Dorssen RJ, Gerola PD and Amesz J (1987) Excitation transfer in chlorosomes of green photosynthetic bacteria. Biochim Biophys Acta 891:27~285 Wechsler T, Suter F, Fuller RC and Zuber (1984) The complete amino acid sequence of the bacteriochlorophyll c binding polypeptide from chlorosomes of the green photosynthetic bacterium Chloroflexus aurantiacus. FEBS Lett 181:173-178 Wechsler T, Brunisholz R, Suter F, Fuller RC and Zuber H (1985) The complete amino acid sequence of a bacteriochlorophyll a binding polypeptide isolated from the cytoplasmic membrane of the green photosynthetic bacterium Chloroflexus aurantiacus. FEBS Lett 191: 34~38 Zuber H, Brunisholz R and Sidler W (1987) Structure and function of light-harvesting pigment-protein complexes. In: Amesz J, ed. Photosynthesis, pp233-271. Amsterdam: Elsevier.

Pigment organization and energy transfer in the green photosynthetic bacterium Chloroflexus aurantiacus. III. Energy transfer in whole cells.

The transfer of excitation energy in intact cells of the thermophilic green photosynthetic bacterium Chloroflexus aurantiacus was studied both at low ...
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