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The Antenna Reaction Center Complex of Heliobacteria: Composition, Energy Conversion and Electron Transfer1

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The Antenna Reaction Center Complex of Heliobacteria: Composition, Energy Conversion and Electron Transfer1 View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Biochimica et Biophysica Acta 1507 (2001) 278^290 www.bba-direct.com Review The antenna reaction center complex of heliobacteria: composition, energy conversion and electron transfer1 Sieglinde Neerken *, Jan Amesz Department of Biophysics, Huygens Laboratory, Leiden University, P.O. Box 9504, 2300 RA Leiden, The Netherlands Received 11 December 2000; received in revised form 26 April 2001; accepted 18 June 2001 Abstract A survey is given of various aspects of the photosynthetic processes in heliobacteria. The review mainly refers to results obtained since 1995, which had not been covered earlier. It first discusses the antenna organization and pigmentation. The pigments of heliobacteria include some unusual species: bacteriochlorophyll (BChl) g, the main pigment, 81 hydroxy chlorophyll a, which acts as primary electron acceptor, and 4,4P-diaponeurosporene, a carotenoid with 30 carbon atoms. Energy conversion within the antenna is very fast: at room temperature thermal equilibrium among the approx. 35 BChls g of the antenna is largely completed within a few ps. This is then followed by primary charge separation, involving a dimer of BChl g (P798) as donor, but recent evidence indicates that excitation of the acceptor pigment 81 hydroxy chlorophyll a gives rise to an alternative primary reaction not involving excited P798. The final section of the review concerns secondary electron transfer, an area that is relatively poorly known in heliobacteria. ß 2001 Elsevier Science B.V. All rights reserved. Keywords: Heliobacterium; Electron transfer; Energy transfer; Bacteriochlorophyll g 1. Introduction green sulfur bacteria, were already described in the 19th century. The discovery of the heliobacteria The heliobacteria were discovered in 1984 by Gest presents us with a splendid example of a scienti¢c and Favinger [1]. Their isolation, together with that accomplishment made as a result not of planned re- of the green ¢lamentous bacteria in 1974 [2], doubled search, but of a keen observation. This was described the number of known groups of anoxygenic photo- by Gest some years ago [3]: an accidental error in the synthetic bacteria. The other two, the purple and the preparation of an enrichment medium used in a mi- crobiology class at Indiana University produced a culture with an unusual brownish-green color. The culture was not discarded, as many of us would do, Abbreviations: A0, primary electron acceptor; ARC, antenna reaction center; BChl, bacteriochlorophyll; Chl, chlorophyll; but examined and found to contain a new species of HPLC, high performance liquid chromatography; MK, menaqui- photosynthetic bacteria. The newly isolated species none; P798, primary electron donor; RC, reaction center was called Heliobacterium (Hbt.) chlorum and found * Corresponding author. Fax: +31-71-527-5819. to belong to an entirely new group of photosynthetic E-mail address: [email protected] (S. Neerken). 1 Dedicated with fond memories and thanks to my mentor and bacteria with unusual pigmentation, and with a new friend, Jan Amesz, who died on 29 January 2001 shortly after the and hitherto unknown pigment, bacteriochlorophyll completion of this review. g [4]. 0005-2728 / 01 / $ ^ see front matter ß 2001 Elsevier Science B.V. All rights reserved. PII: S0005-2728(01)00207-9 BBABIO 45081 15-10-01 S. Neerken, J. Amesz / Biochimica et Biophysica Acta 1507 (2001) 278^290 279 Fig. 1. Taxonomic relationship of some species of heliobacteria. The lengths of the connecting lines are proportional to the number of substitutions in 16S rRNA gene sequence analyses. Adapted from [28]. Fig. 2. Elution pattern obtained by normal phase HPLC of an extract from Hbt. chlorum [46]. Note the di¡erent scales for the two parts of the ¢gure. Peak 1 is the carotenoid recently identi- The heliobacteria are the only photosynthetic or- ¢ed as 4,4P-diaponeurosporene [35], peak 5 BChl g. Peak 4 is ganisms that can be classi¢ed under the Gram-pos- the 132 epimer, BChl gP, which in dimeric form may constitute itive bacteria [5,6], in the so-called low GC group. the primary electron donor, P798 [34]. The polar pigment of They are taxonomically closer to the cyanobacteria peak 6 is 81 hydroxy Chl a, the primary electron acceptor. than to the other groups of anoxygenic photosyn- thetic bacteria [5,7,8]. Their evolutionary position same activity for primary photochemistry as have has been discussed repeatedly [5,7^18]. Perhaps a isolated membranes or intact cells [32,33]. These hundred strains and species of heliobacteria have complexes, called antenna reaction center (ARC) now been isolated [17,19^28], belonging to four gen- complexes [33], contain a total of about 35 BChl g era, which appear to be closely related [20,21,27,29] molecules [33,34], two molecules of a pigment that (see Fig. 1). Most have been found in soil samples, was identi¢ed as 81 hydroxy chlorophyll (Chl) a and usually from rice ¢elds [1,21,22,24^26], but other carotenoid. On the basis of its absorption spectrum strains have been isolated from hot springs and mobility in HPLC (Fig. 2) the carotenoid was [23,26,28,30] or from the banks of soda lakes ¢rst thought to be neurosporene [15,31], but more [20,27]. Most seem to produce endospores [19,23,25]. recently it was shown to be 4,4P-diaponeurosporene, This review will focus on results obtained during the last 5 or 6 years; earlier work has been reviewed [15,24,31] and will be discussed mainly as a basis for more recent experiments. 2. Antenna structure and pigments The pigment system of heliobacteria is simple: it consists of a single pigment^protein complex that is embedded in the cytoplasmic membrane and con- tains both the reaction center (RC) and BChls that have an antenna function. Invaginations of this membrane or extramembranous organelles to accom- modate additional antenna pigments have not been observed, and it has been shown that one can obtain Fig. 3. Absorption spectra of membrane fragments from Hba. and purify detergent solubilized protein complexes mobilis at 6 K (solid line) and at room temperature (dotted that have the same pigment composition and the line). The spectra are not to scale (adapted from [41]). BBABIO 45081 15-10-01 280 S. Neerken, J. Amesz / Biochimica et Biophysica Acta 1507 (2001) 278^290 with 30 instead of 40 carbon atoms [35]. This pig- ment has never been observed in other groups of photosynthetic organisms, but it has been found in some non-photosynthetic ones [36]. Takaichi et al. [35] suggested that heliobacteria may be unable to produce C20 precursors (see below). The pigment composition of heliobacteria is re- £ected in their absorption spectrum, as illustrated for Heliobacillus (Hba.) mobilis in Fig. 3. The band at 791 nm at room temperature is due to Qy absorp- tion by BChl g; the Qx band is located at 577 nm, whereas the band at 670 nm is due to 81 hydroxy Chl a, which we shall henceforth call Chl a 670. At room temperature, the Qy band of BChl g shows no struc- ture, but at liquid nitrogen temperature or lower, Fig. 4. Absorption spectrum of BChl g in diethyl ether (adapted three bands can be discerned, at 779, 794 and 809 from [115]). nm. The precise location of these bands may vary somewhat. They were ¢rst observed by van Dorssen et al. [37] in Hbt. chlorum and were supposed to complex) without peripheral antenna. The size of this re£ect the presence of three spectral pools of BChl `core antenna' apparently cannot be varied in re- g: BChl g 778, BChl g 793 and BChl g 808. Although sponse to external conditions. In this respect the he- the ARC complex is probably an exciton-coupled liobacteria would resemble those purple bacteria that system (see next section), the bands may in ¢rst ap- have only an LH1 antenna like Rhodospirillum ru- proximation be assigned to speci¢c BChl g mole- brum and Blastochloris (formerly Rhodopseudomonas cules. For the sake of convenience we shall therefore [42]) viridis. These bacteria too have a constant or use the above mentioned designations throughout almost constant number of about 30 BChls per re- this paper. The three pools are not re£ected in reso- action center [43]. It is somewhat surprising that the nance Raman spectra, which show a remarkably ho- heliobacteria have such a small and invariable anten- mogeneous population of pentacoordinated BChl g na, since most are supposed to live in mud or soil [38]. The primary electron donor, P798, is a dimer of [31], where little light would be available. However, BChl g, presumably of its 132 epimer (BChl gP) [34]. one should keep in mind that the actual growth con- The amount of BChl gP was found to be one per ditions of the heliobacteria are not well known. They approx. 17 BChls g, giving a BChl g to reaction can grow in the dark by anaerobic fermentation of center ratio of approx. 35 [34]. P798 shows bleaching lactate [44], which would be a commonly available upon photooxidation at 798 nm at room temperature substrate in rice soils. and at 793 nm at cryogenic temperature [15,31]. The BChl g is a `new' pigment, not earlier found in di¡erential extinction coe¤cient for P798 oxidation nature. Its electronic structure, and hence its absorp- has been determined in two di¡erent experiments and tion spectrum (Fig. 4), resembles those of BChls a appears to be higher than that of any primary elec- and b, but the esterifying alcohol of BChl g is farne- tron donor determined to date. Values of 180 mM31 sol (C15) instead of phytol (C20) of BChls a and b cm31 [39] and 225^240 mM31 cm31 [40] have been [6,34,35].
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