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The Supramolecular Organization of Self-Assembling Chlorosomal Bacteriochlorophyll C, D,Ore Mimics

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The Supramolecular Organization of Self-Assembling Chlorosomal Bacteriochlorophyll C, D,Ore Mimics The supramolecular organization of self-assembling chlorosomal bacteriochlorophyll c, d,ore mimics Tobias Jochum*†, Chilla Malla Reddy†‡, Andreas Eichho¨ fer‡, Gernot Buth*, Je¸drzej Szmytkowski§¶, Heinz Kalt§¶, David Moss*, and Teodor Silviu Balaban‡¶ʈ *Institute for Synchrotron Radiation, Karlsruhe Institute of Technology, Forschungszentrum Karlsruhe, Postfach 3640, D-76021 Karlsruhe, Germany; ‡Institute for Nanotechnology, Karlsruhe Institute of Technology, Forschungszentrum Karlsruhe, Postfach 3640, D-76021 Karlsruhe, Germany; §Institute of Applied Physics, Karlsruhe Institute of Technology, Universita¨t Karlsruhe (TH), D-76131 Karslruhe, Germany; and ¶Center for Functional Nanostructures, Universita¨t Karlsruhe (TH), D-76131 Karslruhe, Germany Edited by James R. Norris, University of Chicago, Chicago, IL, and accepted by the Editorial Board July 18, 2008 (received for review March 22, 2008) Bacteriochlorophylls (BChls) c, d, and e are the main light-harvesting direct structural evidence from x-ray single crystal structures, the pigments of green photosynthetic bacteria that self-assemble into exact nature of BChl superstructures remain elusive and these nanostructures within the chlorosomes forming the most efficient have been controversially discussed in the literature (1–3, 7, antennas of photosynthetic organisms. All previous models of the 11–17). It is now generally accepted that the main feature of chlorosomal antennae, which are quite controversially discussed chlorosomes is the self-assembly of BChls and that these pig- because no single crystals could be grown so far from these or- ments are not bound by a rigid protein matrix as is the case of ganelles, involve a strong hydrogen-bonding interaction between the other, well characterized light-harvesting systems (1). Small- 31 hydroxyl group and the 131 carbonyl group. We have synthesized angle x-ray scattering (SAXS) experiments combined with trans- different self-assemblies of BChl c mimics having the same functional mission electron microscopy (TEM) and cryo-TEM both on groups as the natural counterparts, that is, a hydroxyethyl substitu- green bacterial chlorosomes from Chlorobium tepidum (11, 12) ent, a carbonyl group and a divalent metal atom ligated by a and brown bacterial chlorosomes from Chlorobium phaeovibroi- tetrapyrrole. These artificial BChl mimics have been shown by single des (7) and Chlorobium phaeobacterioides (7) have indicated a crystal x-ray diffraction to form extended stacks that are packed by lamellar structure of the BChl assemblies. The data could not be hydrophobic interactions and in the absence of hydrogen bonding. reconciled with an earlier proposed cylindrical model (13, 14) Time-resolved photoluminescence proves the ordered nature of the and this has now rekindled the discussion on the true chlorosome self-assembled stacks. FT-IR spectra show that on self-assembly the architecture. The SAXS data show sharp reflexes with Ϸ2-nm .carbonyl frequency is shifted by Ϸ30 cm؊1 to lower wavenumbers. spacings and these are assumed to represent Mg–Mg distances From the FT-IR data we can infer the proximal interactions between However, in these more recent models hydrogen bonding was the BChls in the chlorosomes consistent with a single crystal x-ray still assumed to occur between dimers (7, 12). Another very structure that shows a weak electrostatic interaction between car- recent study by solid-state NMR on 13C-labeled chlorosomes has bonyl groups and the central zinc atom. discussed all previous models and favors a parallel hydrogen- bonded dimer model as the most probable one (15, 16). Molec- chlorosome model ͉ crystal structure ͉ FT-IR ͉ light-harvesting ͉ ular mechanics calculations and exciton theory have been ap- time-resolved fluorescence plied in a very thorough theoretical investigation on the different possible geometries such as tube, lamella, or spiral-type for the reen photosynthetic bacteria appeared some three billion chlorosomal aggregates (17). Gyears ago in an anoxic atmosphere. To adapt to specific Understanding the exact architecture of the chlorosomes is illumination conditions, the green sulfur bacteria (Chlorobi- not only an important biological research goal but also this would aceae) and the phylogenetically quite distant gliding filamentous allow replication of the light-harvesting ability with fully syn- bacteria (Chloroflexaceae) have evolved a special light- thetic pigments in photovoltaic devices for biomimetic energy harvesting organelle that agglomerates bacteriochlorophylls transduction. The self-assembly algorithm programmed within (BChls) c, d,ore (Fig. 1) as the main antenna pigments (1–3). chlorosomes could be reproduced with completely artificial Because of the dense packing of green BChls, as revealed by pigments (18–22), that lends hope that it can be used in early electron microscopy studies (4–6), these organelles that are solid-state devices such as hybrid solar cells (23, 24). This would attached to the inner side of the cytoplastic membrane were enable efficient light capturing and operation also under low- called ‘‘chlorosomes’’ to reflect their ‘‘green sac’’ nature. Some light illumination conditions. Such an optimal photon manage- brown bacterial species also have well developed chlorosomes ment is not possible with the present, state-of-the-art solar cells. (7). An aerobic phototroph having chlorosomes and belonging to Our synthetic BChl c, d,ore mimics (Fig. 1) have the advantages the phylum Acidobacteria was discovered recently in hot springs (8). By scavenging photons at great depths, chlorosomal express- ing bacteria thrive where other forms of life cannot rely on Author contributions: T.S.B. designed research; T.J., C.M.R., A.E., J.S., D.M., and T.S.B. performed research; G.B., H.K., and D.M. contributed new reagents/analytic tools; T.J., A.E., photosynthesis. In the Black Sea, for example, a Chlorobium J.S., D.M., and T.S.B. analyzed data; T.S.B. wrote the paper; G.B. built the Small Crystal species that contains BChl e was identified as much as 100 m Diffractometry (SCD) beamline at the ANKA Synchrotron; and H.K. supervised the time- under the water surface (9). Astonishingly, a BChl c-containing resolved fluorescence measurements and built the set-up. microbe has recently been found at a depth of 2,390 m, close to The authors declare no conflict of interest. a volcanic vent in the Pacific Ocean, showing that chlorosomes This article is a PNAS Direct Submission. J.R.N. is a guest editor invited by the Editorial Board. enable photosynthesis with near-infrared wavelengths even in Data deposition: The atomic coordinates have been deposited in the Cambridge Crystal- the absence of solar radiation (10). lographic Data Center (ID code CCDC-677194). Very recent high-resolution images confirm that chlorosomes †T.J. and C.M.R. contributed equally to this work. are flattened cigar-shaped nanostructures with dimensions of ʈTo whom correspondence should be addressed. E-mail: [email protected]. Ϸ20 ϫ 50 ϫ 200 nm (7, 11). Their size varies depending on the This article contains supporting information online at www.pnas.org/cgi/content/full/ organism and illumination conditions of the habitat. Despite 0802719105/DCSupplemental. more than three decades of research efforts, in the absence of © 2008 by The National Academy of Sciences of the USA 12736–12741 ͉ PNAS ͉ September 2, 2008 ͉ vol. 105 ͉ no. 35 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0802719105 Downloaded by guest on September 29, 2021 OH OH 7 H C H3C * R 3 * 3 3 8 H3C R N N (H C) C C(CH3)3 3 3 N N 10 R20 Mg* 20 Zn* N N 18 (H C) C N N C(CH ) 12 3 3 3 3 H3C R ** 17 13 13 O O H3C COO 1-Zn c 7 20 BChl : R = R = CH3 d 7 20 BChl : R = CH3; R = H e 7 20 BChl : R = CHO; R = CH3 OH OH H C H3C * 3 * 3 5 Fig. 1. Naturally occurring BChls and their synthetic 8 12 (H C) C C(CH ) porphyrinic mimics. In BChls R and R can be differ- (H C) C C(CH3)3 3 3 N N 3 3 3 3 N N ent homologous groups such as methyl, ethyl, n- Zn* Zn* propyl, or isobutyl. Farnesol is depicted as the long- (H C) C N N N N C(CH ) BIOPHYSICS (H3C)3C C(CH3)3 3 3 3 3 chain alcohol esterifying the 17-propionic acid but also other fatty alcohols such as stearol, cetol, phytol, 15 17 geranyl-geraniol, etc., can be encountered in various bacteria. Metal-centered asterisks denote stereo- 2-Zn H C O O 3 H3C 3-Zn centers formed on ligation. The atom numbering of porphyrins deliberately follows that of BChls. 1 that they are readily available without the need of culturing The 3 -carbon atom of the hydroxyethyl group is a stereocenter CHEMISTRY bacteria and are chemically more stable. (asterisks in Fig. 1) that generates two enantiomorphic porphyrins. In the present study we have examined the Fourier transform We have used the racemic mixture because the separated enanti- infrared (FT-IR) spectra of self-assemblies from synthetic BChl omers self-assemble less readily (21). It thus appears that the models possessing a hydroxyethyl group in the northern half of heterochiral self-assembly is thermodynamically favored compared the porphyrin molecule and an acetyl recognition group in the with a homochiral mechanism. This explains why in the chloro- southern half. To investigate the importance of hydrogen bond- somes both 31-epimers of BChls are encountered, which was a ing and metal ligation, additional compounds lacking either a long-standing question because, in natural systems, enantiopure hydroxyl group (4-Zn–6-Zn, 4-Mg, and 5-Mg) or the metal atom compounds are usually the outcome of enzymatic biosyntheses. (1-FB–3-FB) were also studied (Fig. 2). Zinc as the central metal The BChl mimics 1-Zn–6-Zn self-assemble in nonpolar sol- atom leads to more stable assemblies than magnesium.
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