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Chlorosome antenna complexes from green photosynthetic bacteria

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Abstract

Chlorosomes are the distinguishing light-harvesting antenna complexes that are found in green photosynthetic bacteria. They contain bacteriochlorophyll (BChl) c, d, e in natural organisms, and recently through mutation, BChl f, as their principal light-harvesting pigments. In chlorosomes, these pigments self-assemble into large supramolecular structures that are enclosed inside a lipid monolayer to form an ellipsoid. The pigment assembly is dictated mostly by pigment–pigment interactions as opposed to protein–pigment interactions. On the bottom face of the chlorosome, the CsmA protein aggregates into a paracrystalline baseplate with BChl a, and serves as the interface to the next energy acceptor in the system. The exceptional light-harvesting ability at very low light conditions of chlorosomes has made them an attractive subject of study for both basic and applied science. This review, incorporating recent advancements, considers several important aspects of chlorosomes: pigment biosynthesis, organization of pigments and proteins, spectroscopic properties, and applications to bio-hybrid and bio-inspired devices.

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References

  • Akutsu H, Egawa A, Fujiwara T (2010) Atomic structure of the bacteriochlorophyll c assembly in intact chlorosomes from Chlorobium limicola determined by solid-state NMR. Photosynth Res 104:221–231. doi:10.1007/s11120-009-9523-2

    PubMed  CAS  Google Scholar 

  • Allmaier G, Laschober C, Szymanski WW (2008) Nano ES GEMMA and PDMA, new tools for the analysis of nanobioparticles-protein complexes, lipoparticles, and viruses. J Am Soc Mass Spectrom 19:1062–1068. doi:10.1016/j.jasms.2008.05.017

    PubMed  CAS  Google Scholar 

  • Alster J, Polívka T, Arellano JB et al (2010) β-Carotene to bacteriochlorophyll c energy transfer in self-assembled aggregates mimicking chlorosomes. Chem Phys 373:90–97. doi:10.1016/j.chemphys.2010.02.006

    CAS  Google Scholar 

  • Alster J, Polívka T, Arellano JB et al (2012) Self-assembly and energy transfer in artificial light-harvesting complexes of bacteriochlorophyll c with astaxanthin. Photosynth Res 111:193–204. doi:10.1007/s11120-011-9670-0

    PubMed  CAS  Google Scholar 

  • Arellano JB, Bernt Melø T, Borrego CM et al (2007) Nanosecond laser photolysis studies of chlorosomes and artificial aggregates containing bacteriochlorophyll e: evidence for the proximity of carotenoids and bacteriochlorophyll a in chlorosomes from Chlorobium phaeobacteroides strain CL1401. Photochem Photobiol 72:669–675. doi:10.1562/0031-8655(2000)0720669NLPSOC2.0.CO2

    Google Scholar 

  • Badura A, Esper B, Ataka K et al (2006) Light-driven water splitting for (bio-)hydrogen production: photosystem 2 as the central part of a bioelectrochemical device. Photochem Photobiol 82:1385–1390. doi:10.1562/2006-07-14-RC-969

    PubMed  CAS  Google Scholar 

  • Balaban TS (2005) Tailoring porphyrins and chlorins for self-assembly in biomimetic artificial antenna systems. Acc Chem Res 38:612–623. doi:10.1021/ar040211z

    PubMed  CAS  Google Scholar 

  • Balaban TS, Holzwarth AR, Schaffner K et al (1995) CP-MAS 13C-NMR dipolar correlation spectroscopy of 13C-enriched chlorosomes and isolated bacteriochlorophyll c aggregates of Chlorobium tepidum: the self-organization of pigments is the main structural feature of chlorosomes. Biochemistry 34:15259–15266. doi:10.1021/bi00046a034

    PubMed  CAS  Google Scholar 

  • Beatty JT, Overmann J, Lince MT et al (2005) An obligately photosynthetic bacterial anaerobe from a deep-sea hydrothermal vent. Proc Natl Acad Sci USA 102:9306–9310. doi:10.1073/pnas.0503674102

    PubMed  CAS  Google Scholar 

  • Betti JA, Blankenship RE, Natarajan LV et al (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. doi:10.1016/0005-2728(82)90011-1

    CAS  Google Scholar 

  • Blankenship RE (2002) Molecular Mechanisms of Photosynthesis, 1st edn. Wiley, New York, pp 1–321

    Google Scholar 

  • Blankenship RE, Matsuura K (2003) Antenna Complexes from Green Photosynthetic Bacteria. In: Green BR, Parson WW (eds) Advances in Photosynthesis and Respiration, vol 13. Kluwer, Light Harvesting Antennas in Photosynthesis, pp 195–217

    Google Scholar 

  • Blankenship RE, Olson JM, Miller M (1995) Antenna complexes from green photosynthetic bacteria. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic photosynethetic bacteria. Kluwer Academic Publishers, Dordrecht, pp 399–435

    Google Scholar 

  • Bobe FW, Pfennig N, Swanson KL, Smith KM (1990) Red shift of absorption maxima in chlorobiineae through enzymic methylation of their antenna bacteriochlorophylls. Biochemistry 29:4340–4348

    PubMed  CAS  Google Scholar 

  • Boschloo G, Lindström H, Magnusson E et al (2002) Optimization of dye-sensitized solar cells prepared by compression method. J Photochem Photobiol, A 148:11–15. doi:10.1016/S1010-6030(02)00072-2

    CAS  Google Scholar 

  • Broch-due M, Ormerod JG (1978) Isolation of a BChl c mutant from Chlorobium with BChl d by cultivation at low light intensity. FEMS Microbiol Lett 3:305–308

    Google Scholar 

  • Brune DC, King GH, Infosino A et al (1987a) Antenna organization in green photosynthetic bacteria. 2. Excitation transfer in detached and membrane-bound chlorosomes from Chloroflexus aurantiacus. Biochemistry 26:8652–8658

    PubMed  CAS  Google Scholar 

  • Brune DC, Nozawa T, Blankenship RE (1987b) Antenna organization in green photosynthetic bacteria. 1. Oligomeric bacteriochlorophyll c as a model for the 740 nm absorbing bacteriochlorophyll c in Chloroflexus aurantiacus chlorosomes. Biochemistry 26:8644–8652

    PubMed  CAS  Google Scholar 

  • Bryant DA, Vassilieva EV, Frigaard N-U, Li H (2002) Selective protein extraction from Chlorobium tepidum chlorosomes using detergents. Evidence that CsmA forms multimers and binds bacteriochlorophyll a. Biochemistry 41:14403–14411

    PubMed  CAS  Google Scholar 

  • Bryant DA, Garcia Costas AM, Maresca JA et al (2007) Candidatus Chloracidobacterium thermophilum: an aerobic phototrophic Acidobacterium. Science 317:523–526. doi:10.1126/science.1143236

    PubMed  CAS  Google Scholar 

  • Bryant DA, Liu Z, Li T et al (2012) Comparative and functional genomics of anoxygenic green bacteria from the Taxa Chlorobi, Chloroflexi, and Acidobacteria. In: Burnap R, Vermaas W (eds) Functional Genomics and Evolution of Photosynthetic Systems. Springer Netherlands, Dordrecht, pp 47–102

    Google Scholar 

  • Bystrova MI, Mal’gosheva IN, Krasnovsky AA (1979) Molecular mechanism of self-assembly of aggregated bacteriochlorophyll c. Mol Biol 13:582–594

    CAS  Google Scholar 

  • Causgrove TP, Brune DC, Blankenship RE (1992) Förster energy transfer in chlorosomes of green photosynthetic bacteria. J Photochem Photobiol, B 15:171–179

    CAS  Google Scholar 

  • Chappaz-Gillot C, Marek PL, Blaive BJ et al (2012) Anisotropic organization and microscopic manipulation of self-assembling synthetic porphyrin microrods that mimic chlorosomes: bacterial light-harvesting systems. J Am Chem Soc 134:944–954. doi:10.1021/ja203838p

    PubMed  CAS  Google Scholar 

  • Chen M, Scheer H (2013) Extending the limits of natural photosynthesis and implications for technical light harvesting. J Porphyrins Phthalocyanines 17:1–15. doi:10.1142/S1088424612300108

    Google Scholar 

  • Chung S, Frank G, Zuber H, Bryant DA (1994) Genes encoding two chlorosome components from the green sulfur bacteria Chlorobium vibrioforme strain 8327D and Chlorobium tepidum. Photosynth Res 41:261–275

    CAS  Google Scholar 

  • Cohen-Bazire G, Pfennig N, Kunisawa R (1964) The fine structure of green bacteria. J Cell Biol 22:207–225

    PubMed  CAS  Google Scholar 

  • Dostál J, Mančal T, Augulis R et al (2012) Two-dimensional electronic spectroscopy reveals ultrafast energy diffusion in chlorosomes. J Am Chem Soc 134:11611–11617. doi:10.1021/ja3025627

    PubMed  Google Scholar 

  • Egawa A, Fujiwara T, Mizoguchi T et al (2007) Structure of the light-harvesting bacteriochlorophyll c assembly in chlorosomes from Chlorobium limicola determined by solid-state NMR. Proc Natl Acad Sci USA 104:790–795. doi:10.1073/pnas.0605911104

    PubMed  CAS  Google Scholar 

  • Ellerby LM, Nishida CR, Nishida F et al (1992) Encapsulation of proteins in transparent porous silicate glasses prepared by the sol–gel method. Science 255:1113–1115

    PubMed  CAS  Google Scholar 

  • Escalante M, Maury P (2007) Directed assembly of functional light harvesting antenna complexes onto chemically patterned surfaces. Nanotechnology 19:025101. doi:10.1088/0957-4484/19/02/025101

    PubMed  Google Scholar 

  • Feick RG, Fuller RC (1984) Topography of the photosynthetic apparatus of Chloroflexus aurantiacus. Biochemistry 23:3693–3700. doi:10.1021/bi00311a019

    CAS  Google Scholar 

  • Frese R, Oberheide U, Van Stokkum I et al (1997) The organization of bacteriochlorophyll c in chlorosomes from Chloroflexus aurantiacus and the structural role of carotenoids and protein—An absorption, linear dichroism, circular dichroism and Stark spectroscopy study. Photosynth Res 54:115–126

    CAS  Google Scholar 

  • Frigaard N-U, Bryant DA (2006) Chlorosomes: antenna organelles in photosynthetic green bacteria. Microbiol Monogr 2:80–114. doi:10.1007/7171

    Google Scholar 

  • Frigaard N-U, Takaichi S, Hirota M et al (1997) Quinones in chlorosomes of green sulfur bacteria and their role in the redox-dependent fluorescence studied in chlorosome-like bacteriochlorophyll c aggregates. Arch Microbiol 167:343–349. doi:10.1007/s002030050453

    CAS  Google Scholar 

  • Frigaard N-U, Li H, Milks KJ, Bryant DA (2004) Nine mutants of Chlorobium tepidum each unable to synthesize a different chlorosome protein still assemble functional chlorosomes. J Bacteriol 186:646–653. doi:10.1128/JB.186.3.646

    PubMed  CAS  Google Scholar 

  • Frigaard N-U, Li H, Martinsson P et al (2005) Isolation and characterization of carotenosomes from a bacteriochlorophyll c-less mutant of Chlorobium tepidum. Photosynth Res 86:101–111. doi:10.1007/s11120-005-1331-8

    PubMed  CAS  Google Scholar 

  • Frolov L, Wilner O, Carmeli C, Carmeli I (2008) Fabrication of oriented multilayers of photosystem I proteins on solid surfaces by auto-metallization. Adv Mater 20:263–266. doi:10.1002/adma.200701474

    CAS  Google Scholar 

  • Fujita T, Brookes JC, Saikin SK, Aspuru-Guzik A (2012) Memory-assisted exciton diffusion in the chlorosome light-harvesting antenna of green sulfur bacteria. J Phys Chem Lett 3:2357–2361. doi:10.1021/jz3008326

    CAS  Google Scholar 

  • Ganapathy S, Oostergetel GT, Wawrzyniak PK et al (2009) Alternating syn-anti bacteriochlorophylls form concentric helical nanotubes in chlorosomes. Proc Natl Acad Sci USA 106:8525–8530. doi:10.1073/pnas.0903534106

    PubMed  CAS  Google Scholar 

  • Ganapathy S, Oostergetel GT, Reus M et al (2012) Structural variability in wild-type and bchQ bchR mutant chlorosomes of the green sulfur bacterium Chlorobaculum tepidum. Biochemistry 51:4488–4498. doi:10.1021/bi201817x

    PubMed  CAS  Google Scholar 

  • Garab G, Van Amerongen H (2009) Linear dichroism and circular dichroism in photosynthesis research. Photosynth Res 101:135–146. doi:10.1007/s11120-009-9424-4

    PubMed  CAS  Google Scholar 

  • Garcia Costas AM, Tsukatani Y, Romberger SP et al (2011) Ultrastructural analysis and identification of envelope proteins of “Candidatus Chloracidobacterium thermophilum” chlorosomes. J Bacteriol 193:6701–6711. doi:10.1128/JB.06124-11

    PubMed  Google Scholar 

  • Garcia Costas AM, Tsukatani Y, Rijpstra WIC et al (2012) Identification of the bacteriochlorophylls, carotenoids, quinones, lipids, and hopanoids of “Candidatus Chloracidobacterium thermophilum”. J Bacteriol 194:1158–1168. doi:10.1128/JB.06421-11

    PubMed  Google Scholar 

  • Gerola PD, Olson JM (1986) A new bacteriochlorophyll a-protein complex associated with chlorosomes of green sulfur bacteria. Biochim Biophys Acta 848:69–76

    PubMed  CAS  Google Scholar 

  • Gloe A, Pfennig N, Brockmann H Jr, Trowitzsch W (1975) A new bacteriochlorophyll from brown-colored chlorobiaceae. Arch Microbiol 102:103–109

    PubMed  CAS  Google Scholar 

  • Gomez Maqueo Chew A, Frigaard N-U, Bryant DA (2007) Bacteriochlorophyllide c C-8(2) and C-12(1) methyltransferases are essential for adaptation to low light in Chlorobaculum tepidum. J Bacteriol 189:6176–6184. doi:10.1128/JB.00519-07

    PubMed  Google Scholar 

  • Harada J, Mizoguchi T, Tsukatani Y et al (2012) A seventh bacterial chlorophyll driving a large light-harvesting antenna. Sci Rep 2:671. doi:10.1038/srep00671

    PubMed  Google Scholar 

  • Harada J, Mizoguchi T, Satoh S et al (2013) Specific gene bciD for C7-methyl oxidation in bacteriochlorophyll e biosynthesis of brown-colored green sulfur bacteria. PLoS ONE 8:e60026. doi:10.1371/journal.pone.0060026

    PubMed  CAS  Google Scholar 

  • Hnilova M, Karaca BT, Park J et al (2012) Fabrication of hierarchical hybrid structures using bio-enabled layer-by-layer self-assembly. Biotechnol Bioeng 109:1120–1130. doi:10.1002/bit.24405

    PubMed  CAS  Google Scholar 

  • Hogan CJ Jr, Kettleson EM, Ramaswami B et al (2006) Charge reduced electrospray size spectrometry of mega-and gigadalton complexes: whole viruses and virus fragments. Anal Chem 78:844–852

    PubMed  CAS  Google Scholar 

  • Hohmann-Marriott MF, Blankenship RE (2007) Hypothesis on chlorosome biogenesis in green photosynthetic bacteria. FEBS Lett 581:800–803. doi:10.1016/j.febslet.2007.01.078

    PubMed  CAS  Google Scholar 

  • Holzwarth AR, 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

    CAS  Google Scholar 

  • Holzwarth AR, Griebenow K, Schaffner K (1990) A photosynthetic antenna system which contains a protein-free chromophore aggregate. Zeitschrift für Naturforschung C 45c:203–206

    Google Scholar 

  • Huang RY-C, Wen J, Blankenship RE, Gross ML (2012) Hydrogen-deuterium exchange mass spectrometry reveals the interaction of Fenna–Matthews–Olson protein and chlorosome CsmA protein. Biochemistry 51:187–193. doi:10.1021/bi201620y

    PubMed  CAS  Google Scholar 

  • Huijser A, Marek PL, Savenije TJ et al (2007) Photosensitization of TiO2 and SnO2 by artificial self-assembling mimics of the natural chlorosomal bacteriochlorophylls. J Phys Chem C 111:11726–11733

    CAS  Google Scholar 

  • Huster MS, Smith KM (1990) Biosynthetic studies of substituent homologation in bacteriochlorophylls c and d. Biochemistry 29:4348–4355

    PubMed  CAS  Google Scholar 

  • Imhoff JF (2003) Phylogenetic taxonomy of the family Chlorobiaceae on the basis of 16S rRNA and fmo (Fenna–Matthews–Olson protein) gene sequences. Int J Syst Evol Microbiol 53:941–951. doi:10.1099/ijs.0.02403-0

    PubMed  CAS  Google Scholar 

  • Kopnov F, Cohen-Ofri I, Noy D (2011) Electron transport between photosystem II and photosystem I encapsulated in sol–gel glasses. Angew Chem Int Ed Engl 50:12347–12350. doi:10.1002/anie.201106293

    PubMed  CAS  Google Scholar 

  • Krasnovsky AA, Bystrova MI (1980) Self-assembly of chlorophyll aggregated structures. Biosystems 12:181–194. doi:10.1016/0303-2647(80)90016-7

    PubMed  CAS  Google Scholar 

  • Li H (2006) Organization and function of chlorosome proteins in the green sulfur bacterium Chlorobium tepidum. The Pennsylvania State University, University Park

    Google Scholar 

  • Li H, Bryant DA (2009) Envelope proteins of the CsmB/CsmF and CsmC/CsmD motif families influence the size, shape, and composition of chlorosomes in Chlorobaculum tepidum. J Bacteriol 191:7109–7120. doi:10.1128/JB.00707-09

    PubMed  CAS  Google Scholar 

  • Li H, Frigaard N-U, Bryant DA (2006) Molecular contacts for chlorosome envelope proteins revealed by cross-linking studies with chlorosomes from Chlorobium tepidum. Biochemistry 45:9095–9103. doi:10.1021/bi060776y

    PubMed  CAS  Google Scholar 

  • Li H, Frigaard N-U, Bryant DA (2013) [2Fe-2S] proteins in chlorosomes: CsmI and CsmJ participate in light-dependent control of energy transfer in chlorosomes of Chlorobaculum tepidum. Biochemistry. doi:10.1021/bi301454g

    Google Scholar 

  • Linnanto JM, Korppi-Tommola JEI (2004) Semiempirical PM5 molecular orbital study on chlorophylls and bacteriochlorophylls: comparison of semiempirical, ab initio, and density functional results. J Comput Chem 25:123–138. doi:10.1002/jcc.10344

    PubMed  CAS  Google Scholar 

  • Linnanto JM, Korppi-Tommola JEI (2008) Investigation on chlorosomal antenna geometries: tube, lamella and spiral-type self-aggregates. Photosynth Res 96:227–245. doi:10.1007/s11120-008-9304-3

    PubMed  CAS  Google Scholar 

  • Liu Z, Bryant DA (2011) Identification of a gene essential for the first committed step in the biosynthesis of bacteriochlorophyll c. J Biol Chem 286:22393–22402. doi:10.1074/jbc.M111.249433

    PubMed  CAS  Google Scholar 

  • Luo T-JM, Soong R, Lan E et al (2005) Photo-induced proton gradients and ATP biosynthesis produced by vesicles encapsulated in a silica matrix. Nat Mater 4:220–224. doi:10.1038/nmat1322

    PubMed  CAS  Google Scholar 

  • Manske AK, Glaeser J, Kuypers MMM (2005) Physiology and phylogeny of green sulfur bacteria forming a monospecific phototrophic assemblage at a depth of 100 M. Appl Environ Microbiol 71:8049–8060. doi:10.1128/AEM.71.12.8049

    PubMed  CAS  Google Scholar 

  • Maresca JA, Gomez Maqueo Chew A et al (2004) The bchU Gene of Chlorobium tepidum encodes the C-20 methyltransferase in bacteriochlorophyll c biosynthesis. J Bacteriol 186:2558–2566. doi:10.1128/JB.186.9.2558

    PubMed  CAS  Google Scholar 

  • Marschall E, Jogler M, Hessge U, Overmann J (2010) Large-scale distribution and activity patterns of an extremely low-light-adapted population of green sulfur bacteria in the Black Sea. Environ Microbiol 12:1348–1362. doi:10.1111/j.1462-2920.2010.02178.x

    PubMed  CAS  Google Scholar 

  • Martinez-Planells A, Arellano JB, Borrego CM et al (2002) Determination of the topography and biometry of chlorosomes by atomic force microscopy. Photosynth Res 71:83–90. doi:10.1023/A:1014955614757

    PubMed  CAS  Google Scholar 

  • Martiskainen J, Linnanto JM, Aumanen V et al (2012) Excitation energy transfer in isolated chlorosomes from Chlorobaculum tepidum and Prosthecochloris aestuarii. Photochem Photobiol 88:675–683. doi:10.1111/j.1751-1097.2012.01098.x

    PubMed  CAS  Google Scholar 

  • Mass O, Pandithavidana DR, Ptaszek M et al (2011) De novo synthesis and properties of analogues of the self-assembling chlorosomal bacteriochlorophylls. New J Chem 35:2671. doi:10.1039/c1nj20611g

    CAS  Google Scholar 

  • Mimuro M, Nozawa T, Tamai N et al (1989) Excitation energy flow in chlorosome antennas of green photosynthetic bacteria. J Phys Chem 93:7503–7509. doi:10.1021/j100358a047

    CAS  Google Scholar 

  • Modesto-Lopez LB, Thimsen EJ, Collins AM et al (2010) Electrospray-assisted characterization and deposition of chlorosomes to fabricate a biomimetic light-harvesting device. Energy Environ Sci 3:216. doi:10.1039/b914758f

    CAS  Google Scholar 

  • Montaño GA, Bowen BP, LaBelle JT et al (2003a) Characterization of Chlorobium tepidum chlorosomes: a calculation of bacteriochlorophyll c per chlorosome and oligomer modeling. Biophys J 85:2560–2565. doi:10.1016/S0006-3495(03)74678-5

    PubMed  Google Scholar 

  • Montaño GA, Wu H-M, Lin S et al (2003b) Isolation and characterization of the B798 light-harvesting baseplate from the chlorosomes of Chloroflexus aurantiacus. Biochemistry 42:10246–10251. doi:10.1021/bi034350k

    PubMed  Google Scholar 

  • Niedzwiedzki DM, Blankenship RE (2010) Singlet and triplet excited state properties of natural chlorophylls and bacteriochlorophylls. Photosynth Res 106:227–238. doi:10.1007/s11120-010-9598-9

    PubMed  CAS  Google Scholar 

  • Novoderezhkin V, Taisova A, Fetisova ZG (2001) Unit building block of the oligomeric chlorosomal antenna of the green photosynthetic bacterium Chloroflexus aurantiacus: modeling of nonlinear optical spectra. Chem Phys Lett 335:234–240

    CAS  Google Scholar 

  • O’Dell WB, Beatty KJ, Tang K-H et al (2012) Sol–gel entrapped light harvesting antennas: immobilization and stabilization of chlorosomes for energy harvesting. J Mater Chem 22:22582. doi:10.1039/c2jm34357f

    Google Scholar 

  • O’Regan B, Grätzel M (1991) A low-cost, high-efficiency solar cell based on dye-sensitized colloidal TiO2 films. Nature 353:737–740

    Google Scholar 

  • Oostergetel GT, Reus M, Gomez Maqueo Chew A et al (2007) Long-range organization of bacteriochlorophyll in chlorosomes of Chlorobium tepidum investigated by cryo-electron microscopy. FEBS Lett 581:5435–5439. doi:10.1016/j.febslet.2007.10.045

    PubMed  CAS  Google Scholar 

  • Oostergetel GT, Van Amerongen H, Boekema EJ (2010) The chlorosome: a prototype for efficient light harvesting in photosynthesis. Photosynth Res 104:245–255. doi:10.1007/s11120-010-9533-0

    PubMed  CAS  Google Scholar 

  • Orf GS, Tank M, Vogl K et al (2013) Spectroscopic insights into the decreased efficiency of chlorosomes containing bacteriochlorophyll f. Biochim Biophys Acta 1827:493–501. doi:10.1016/j.bbabio.2013.01.006

    PubMed  CAS  Google Scholar 

  • Pandit A, De Groot HJM (2011) Solid-state NMR applied to photosynthetic light-harvesting complexes. Photosynth Res. doi:10.1007/s11120-011-9674-9

    PubMed  Google Scholar 

  • Pedersen MØ, Borch J, Højrup P et al (2006) The light-harvesting antenna of Chlorobium tepidum: interactions between the FMO protein and the major chlorosome protein CsmA studied by surface plasmon resonance. Photosynth Res 89:63–69. doi:10.1007/s11120-006-9081-9

    PubMed  Google Scholar 

  • Pedersen MØ, Pham L, Steensgaard DB, Miller M (2008a) A reconstituted light-harvesting complex from the green sulfur bacterium Chlorobium tepidum containing CsmA and bacteriochlorophyll a. Biochemistry 47:1435–1441. doi:10.1021/bi701616r

    PubMed  CAS  Google Scholar 

  • Pedersen MØ, Underhaug J, Dittmer J et al (2008b) The three-dimensional structure of CsmA: a small antenna protein from the green sulfur bacterium Chlorobium tepidum. FEBS Lett 582:2869–2874. doi:10.1016/j.febslet.2008.07.020

    PubMed  CAS  Google Scholar 

  • Pedersen MØ, Linnanto JM, Frigaard N-U et al (2010) A model of the protein-pigment baseplate complex in chlorosomes of photosynthetic green bacteria. Photosynth Res 104:233–243. doi:10.1007/s11120-009-9519-y

    PubMed  CAS  Google Scholar 

  • Prokhorenko VI, Steensgaard DB, Holzwarth AR (2000) Exciton dynamics in the chlorosomal antennae of the green bacteria Chloroflexus aurantiacus and Chlorobium tepidum. Biophys J 79:2105–2120. doi:10.1016/S0006-3495(00)76458-7

    PubMed  CAS  Google Scholar 

  • Prokhorenko VI, Steensgaard DB, Holzwarth AR (2003) Exciton theory for supramolecular chlorosomal aggregates: 1. Aggregate size dependence of the linear spectra. Biophys J 85:3173–3186. doi:10.1016/S0006-3495(03)74735-3

    PubMed  CAS  Google Scholar 

  • Pšenčík J, Ma Y-Z, Arellano JB et al (2002) Excitation energy transfer in chlorosomes of Chlorobium phaeobacteroides strain CL1401: the role of carotenoids. Photosynth Res 71:5–18. doi:10.1023/A:1014943312031

    PubMed  Google Scholar 

  • Pšenčík J, Ma Y-Z, Arellano JB et al (2003) Excitation energy transfer dynamics and excited-state structure in chlorosomes of Chlorobium phaeobacteroides. Biophys J 84:1161–1179. doi:10.1016/S0006-3495(03)74931-5

    PubMed  Google Scholar 

  • Pšenčík J, Ikonen TP, Laurinmäki PA et al (2004) Lamellar organization of pigments in chlorosomes, the light harvesting complexes of green photosynthetic bacteria. Biophys J 87:1165–1172. doi:10.1529/biophysj.104.040956

    PubMed  Google Scholar 

  • Pšenčík J, Arellano JB, Ikonen TP et al (2006) Internal structure of chlorosomes from brown-colored chlorobium species and the role of carotenoids in their assembly. Biophys J 91:1433–1440. doi:10.1529/biophysj.106.084228

    PubMed  Google Scholar 

  • Pšenčík J, Collins AM, Liljeroos L et al (2009) Structure of chlorosomes from the green filamentous bacterium Chloroflexus aurantiacus. J Bacteriol 191:6701–6708. doi:10.1128/JB.00690-09

    PubMed  Google Scholar 

  • Saga Y, Shibata Y, Itoh S, Tamiaki H (2007) Direct counting of submicrometer-sized photosynthetic apparatus dispersed in medium at cryogenic temperature by confocal laser fluorescence microscopy: estimation of the number of bacteriochlorophyll c in single light-harvesting antenna complexes chlorosomes of green photosynthetic bacteria. J Phys Chem B 111:12605–12609. doi:10.1021/jp071559p

    PubMed  CAS  Google Scholar 

  • Sakuragi Y, Frigaard N-U, Shimada K, 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

    PubMed  CAS  Google Scholar 

  • Savikhin S, Blankenship RE, Struve WS (1996) Ultrafast energy transfer in chlorosomes from the green photosynthetic bacterium Chloroflexus aurantiacus. J Phys Chem 100:3320–3322

    PubMed  CAS  Google Scholar 

  • Schmidt K (1978) Biosynthesis of carotenoids. In: Clayton R, Sistrom W (eds) The photosynthetic bacteria. Plenum Press, New York, pp 729–750

    Google Scholar 

  • Senge M, Smith NW, Smith KM (1993) Structure and conformation of photosynthetic pigments and related compounds. 5′. Structural investigation of nickel(II) bacteriopetroporphyrins related to the bacteriochlorophylls c and d: evidence for localized conformational distortion in the c-series. Inorg Chem 32:1259–1265

    CAS  Google Scholar 

  • Shah VB, Orf GS, Reisch S et al (2012) Characterization and deposition of various light-harvesting antenna complexes by electrospray atomization. Anal Bioanal Chem 404:2329–2338. doi:10.1007/s00216-012-6368-x

    PubMed  CAS  Google Scholar 

  • Smith KM, Kehres LA, Fajer J (1983) Aggregation of the bacteriochlorophylls c, d, and e. Models for the antenna chlorophylls of green and brown photosynthetic bacteria. J Am Chem Soc 105:1387–1389. doi:10.1021/ja00343a062

    CAS  Google Scholar 

  • Somsen OJ, Van Grondelle R, Van Amerongen H (1996) Spectral broadening of interacting pigments: polarized absorption by photosynthetic proteins. Biophys J 71:1934–1951. doi:10.1016/S0006-3495(96)79392-X

    PubMed  CAS  Google Scholar 

  • Sørensen PG, Cox RP, Miller M (2008) Chlorosome lipids from Chlorobium tepidum: characterization and quantification of polar lipids and wax esters. Photosynth Res 95:191–196. doi:10.1007/s11120-007-9242-5

    PubMed  Google Scholar 

  • Springer JW, Faries KM, Diers JR et al (2012) Effects of substituents on synthetic analogs of chlorophylls. Part 3: the distinctive impact of auxochromes at the 7- versus 3-positions. Photochem Photobiol 88:651–674. doi:10.1111/j.1751-1097.2012.01083.x

    PubMed  CAS  Google Scholar 

  • Staehelin LA, Golecki JR, Fuller RC, Drews G (1978) Visualization of the supramolecular architecture of chlorosomes (chlorobium type vesicles) in freeze-fractured cells of Chloroflexus aurantiacus. Arch Microbiol 119:269–277. doi:10.1007/BF00405406

    Google Scholar 

  • Staehelin LA, Golecki JR, Drews G (1980) Supramolecular organization of chlorosomes (chlorobium vesicles) and of their membrane attachment sites in Chlorobium limicola. Biochim Biophys Acta 589:30–45

    PubMed  CAS  Google Scholar 

  • Struck A, Cmiel E, Katheder I et al (1992) Bacteriochlorophylls modified at position C-3: long range intramolecular interaction with position C-132. Biochim Biophys Acta 1101:321–328

    CAS  Google Scholar 

  • Suzuki JY, Bollivar DW, Bauer CE (1997) Genetic analysis of chlorophyll biosynthesis. Ann Rev Genet 31:61–89

    PubMed  CAS  Google Scholar 

  • Tamiaki H, Komada J, Kunieda M et al (2011) In vitro synthesis and characterization of bacteriochlorophyll-f and its absence in bacteriochlorophyll-e producing organisms. Photosynth Res 107:133–138. doi:10.1007/s11120-010-9603-3

    PubMed  CAS  Google Scholar 

  • Tanaka A, Ito H, Tanaka R et al (1998) Chlorophyll a oxygenase (CAO) is involved in chlorophyll b formation from chlorophyll a. Proc Natl Acad Sci USA 95:12719–12723

    PubMed  CAS  Google Scholar 

  • Tang K-H, Barry K, Chertkov O et al (2011) Complete genome sequence of the filamentous anoxygenic phototrophic bacterium Chloroflexus aurantiacus. BMC Genomics 12:334. doi:10.1186/1471-2164-12-334

    PubMed  CAS  Google Scholar 

  • Theroux SJ, Redlinger TE, Fuller RC, Robinson SJ (1990) Gene encoding the 5.7-kilodalton chlorosome protein of Chloroflexus aurantiacus: regulated message levels and a predicted carboxy-terminal protein extension. J Bacteriol 172:4497–4504

    PubMed  CAS  Google Scholar 

  • Vassilieva EV, Antonkine ML, Zybailov BL et al (2001) Electron transfer may occur in the chlorosome envelope: the CsmI and CsmJ proteins of chlorosomes are 2Fe-2S ferredoxins. Biochemistry 40:464–473

    PubMed  CAS  Google Scholar 

  • Vassilieva EV, Ormerod JG, Bryant DA (2002) Biosynthesis of chlorosome proteins is not inhibited in acetylene-treated cultures of Chlorobium vibrioforme. Photosynth Res 71:69–81. doi:10.1023/A:1014903630687

    PubMed  CAS  Google Scholar 

  • Vogl K, Tank M, Orf GS et al (2012) Bacteriochlorophyll f: properties of chlorosomes containing the “forbidden chlorophyll”. Frontiers Microbiol 3:1–12. doi:10.3389/fmicb.2012.00298

    Google Scholar 

  • Wang J, Brune DC, Blankenship RE (1990) Effects of oxidants and reductants on the efficiency of excitation transfer in green photosynthetic bacteria. Biochim Biophys Acta 1015:457–463

    PubMed  CAS  Google Scholar 

  • Wen J, Tsukatani Y, Cui W et al (2011) Structural model and spectroscopic characteristics of the FMO antenna protein from the aerobic chlorophototroph, Candidatus Chloracidobacterium thermophilum. Biochim Biophys Acta 1807:157–164. doi:10.1016/j.bbabio.2010.09.008

    PubMed  CAS  Google Scholar 

  • Xiong J, Fischer WM, Inoue K et al (2000) Molecular evidence for the early evolution of photosynthesis. Science 289:1724–1730. doi:10.1126/science.289.5485.1724

    PubMed  CAS  Google Scholar 

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Acknowledgments

The authors thank the following for helpful discussions: Dr. Dariusz M. Niedzweidzki (Washington University in St. Louis), Dr. Jakub Pšenčík (Charles University), Dr. Donald A. Bryant (The Pennsylvania State University), Dr. Sándor Á. Kovács (Washington University in St. Louis), Dr. Cynthia Lo (Washington University in St. Louis), and Mr. Vivek Shah (Washington University in St. Louis). This work has been supported by the Photosynthetic Antenna Research Center, an Energy Frontier Research Center funded by the U.S. Department of Energy, Office of Science, Office of Basic Energy Sciences under award DE-SC0001035. Research described on the FMO protein has been supported by DOE grant DE-FG02-10ER15902 to R.E.B.

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The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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Orf, G.S., Blankenship, R.E. Chlorosome antenna complexes from green photosynthetic bacteria. Photosynth Res 116, 315–331 (2013). https://doi.org/10.1007/s11120-013-9869-3

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