Antenna organization in green photosynthetic bacteria. 1. Oligomeric bacteriochlorophyll c as a model for the 740 nm absorbing bacteriochlorophyll c in Chloroflexus aurantiacus chlorosomes

Abstract

Bacteriochlorophyll (BChl) c was extracted from Chloroflexus aurantiacus and purified by reverse-phase high-pressure liquid chromatography. This pigment consists of a complex mixture of homologues, the major component of which is 4-ethyl-5-methylbacteriochlorophyll c stearyl ester. Unlike previously characterized BChls c, the pigment from C. aurantiacus is a racemic mixture of diastereoisomers with different configurations at the 2a chiral center. Diluting a concentrated methylene chloride solution of BChl c with hexane produces an oligomer with absorption maxima at 740-742 and at 460-462 nm. Both the absorption spectrum and the fluorescence emission spectrum (maximum at 750 nm) of this oligomer closely match those of BChl c in chlorosomes. Further support for this model comes from the ability of alcohols, which disrupt BChl c oligomers by ligating the central Mg atom, to convert BChl c in chlorosomes to a monomeric form when added in low concentrations. The lifetime of fluorescence from the 740 nm absorbing BChl c oligomer is about 80 ps. Although exciton quenching might be unusually fast in the in vitro BChl c oligomer because of its large size and/or the presence of minor impurities, this result suggests that energy transfer from the BChl c antenna in chlorosomes must be very fast if it is to be efficient.

Structural differences in chlorosomes from Chloroflexus aurantiacus grown under different conditions support the BChl c‐binding function of the 5.7 kDa polypeptide

“…We observed that the CD intensity of low-light chlorosomes only doubled upon treatment with proteinase K compared to a fivefold increase in the high-light chlorosomes. There is some evidence that BChl c in the chlorosome is organized as oligomers [8,9], which may be bound to protein in order to maintain parallel transition moments between clusters of BChl c [2.5,26]. There are several reports that BChl c aggregates in hexane [27,28], in aqueous suspension, or after LDS treatment [4], and after proteolytic treatment [4,18] exhibited higher rotational strength than BChl c in chlorosomes of ChlorojZexus auruntiucus.…”

Complete Assignment of1H NMR Spectra and Structural Analysis of Intact BacteriochlorophyllcDimer in Solution

“…Purified BChl c forms oligomers in hexane with the Q y absorption peak at ∼740 nm, about 70 nm red-shifted from that of its monomeric form as observed in methanol, and the absorption spectra closely resemble that of BChl c in chlorosomes. 16,17 In addition to the 740 nm oligomer, there are at least two other aggregates formed in CH 2 Cl 2 , CHCl 3 , and CCl 4 (or benzene) with absorption maxima at 680 and 710 nm for R-type BChl c. 8,18,19 The 710 nm species is reported to exhibit unusual spectroscopic properties, in particular an intense fluorescence emission. 8,20 A large number of studies have been made to elucidate the structure of the 740 nm aggregate in relation with the organization of BChl c in chlorosomes.…”

“…16,17 In addition to the 740 nm oligomer, there are at least two other aggregates formed in CH 2 Cl 2 , CHCl 3 , and CCl 4 (or benzene) with absorption maxima at 680 and 710 nm for R-type BChl c. 8,18,19 The 710 nm species is reported to exhibit unusual spectroscopic properties, in particular an intense fluorescence emission. 8,20 A large number of studies have been made to elucidate the structure of the 740 nm aggregate in relation with the organization of BChl c in chlorosomes. [8][9][10][11]16,17,[21][22][23] Descriptions of the large aggregation structure have converged into two basic models 3 in which the BChl c molecules are arranged in antiparallel or parallel chains.…”

Structural and Functional Roles of Carotenoids in Chlorosomes

“…In vitro assembly studies in aqueous buffers have also suggested that hydrophobic carotenoids may augment self-assembly of BChls into aggregates by enhancing interaction between the hydrophobic tails of esterifying alcohols within lamellae (18,19). Furthermore, carotenoids can be extracted from chlorosomes isolated from several species by nonpolar solvents, such as hexane (9,20). Structural characterization of hexane-treated chlorosomes from Chlorobium phaeovibrioides (containing BChl e as the main pigment) demonstrated that carotenoids are located within lamellae and increase the apparent spacing between adjacent lamellar layers (9).…”