Skip to main content
SpringerLink
Log in

Impact of esterified bacteriochlorophylls on the biogenesis of chlorosomes in Chloroflexus aurantiacus

  • Regular Paper
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

A chlorosome is an antenna complex located on the cytoplasmic side of the inner membrane in green photosynthetic bacteria that contains tens of thousands of self-assembled bacteriochlorophylls (BChls). Green bacteria are known to incorporate various esterifying alcohols at the C-17 propionate position of BChls in the chlorosome. The effect of these functional substitutions on the biogenesis of the chlorosome has not yet been fully explored. In this report, we address this question by investigating various esterified bacteriochlorophyll c (BChl c) homologs in the thermophilic green non-sulfur bacterium Chloroflexus aurantiacus. Cultures were supplemented with exogenous long-chain alcohols at 52 °C (an optimal growth temperature) and 44 °C (a suboptimal growth temperature), and the morphology, optical properties and exciton transfer characteristics of chlorosomes were investigated. Our studies indicate that at 44 °C Cfl. aurantiacus synthesizes more carotenoids, incorporates more BChl c homologs with unsaturated and rigid polyisoprenoid esterifying alcohols and produces more heterogeneous BChl c homologs in chlorosomes. Substitution of phytol for stearyl alcohol of BChl c maintains similar morphology of the intact chlorosome and enhances energy transfer from the chlorosome to the membrane-bound photosynthetic apparatus. Different morphologies of the intact chlorosome versus in vitro BChl aggregates are suggested by small-angle neutron scattering. Additionally, phytol cultures and 44 °C cultures exhibit slow assembly of the chlorosome. These results suggest that the esterifying alcohol of BChl c contributes to long-range organization of BChls, and that interactions between BChls with other components are important to the assembly of the chlorosome. Possible mechanisms for how esterifying alcohols affect the biogenesis of the chlorosome are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

BChls:

Bacteriochlorophylls

Cfl. aurantiacus :

Chloroflexus aurantiacus

EIC:

Extracted ion chromatogram

GerGer alcohol:

Geranylgeraniol

LC–MS:

Liquid chromatography–mass spectrometry

LC–MS/MS:

Liquid chromatography–tandem mass spectrometry

SANS:

Small-angle neutron scattering

UHPLC:

Ultra-high-performance liquid chromatography

References

  • Bhosale P (2004) Environmental and cultural stimulants in the production of carotenoids from microorganisms. Appl Microbiol Biotechnol 63:351–361

    Article  PubMed  CAS  Google Scholar 

  • Blankenship RE, Matsuura K (2003) Antenna complexes from green photosynthetic bacteria. In: Green BR, Parson WW (eds) Anoxygenic photosynthetic bacteria. Kluwer Academic Publishers, Dordrecht, pp 195–217

    Google Scholar 

  • Chattopadhyay MK, Jagannadham MV, Vairamani M, Shivaji S (1997) Carotenoid pigments of an antarctic psychrotrophic bacterium Micrococcus roseus: temperature dependent biosynthesis, structure, and interaction with synthetic membranes. Biochem Biophys Res Commun 239:85–90

    Article  PubMed  CAS  Google Scholar 

  • Didraga C, Klugkist JA, Knoester J (2002) Optical properties of helical cylindrical molecular aggregates: the homogeneous limit. J Phys Chem B 106:11474–11486

    Article  CAS  Google Scholar 

  • Dorssen RJ, Vasmel H, Amesz J (1986) Pigment organization and energy transfer in the green photosynthetic bacterium Chloroflexus aurantiacus. II. The chlorosome. Photosynth Res 9:33–45

    Article  PubMed  Google Scholar 

  • Egawa A, Fujiwara T, Mizoguchi T, Kakitani Y, Koyama Y, Akutsu H (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

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Fages F, Griebenow N, Griebenow K, Holzwarth AR, Schaffner K (1990) Characterization of light-harvesting pigments of Chloroflexus aurantiacus. Two new chlorophylls: oleyl (octadec-9-enyl) and cetyl (hexadecanyl) bacteriochlorophyllides c. J Chem Soc Perkin Trans I:2791–2797

    Article  Google Scholar 

  • Frigaard N-U, Bryant DA (2006) Chlorosomes: antenna organelles in photosynthetic green bacteria. In: Shively JM (ed) Complex intracellular structures in prokaryotes. Springer, Berlin, pp 79–114

    Chapter  Google Scholar 

  • Frigaard NU, Voigt GD, Bryant DA (2002) Chlorobium tepidum mutant lacking bacteriochlorophyll c made by inactivation of the bchK gene, encoding bacteriochlorophyll c synthase. J Bacteriol 184:3368–3376

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Ganapathy S, Oostergetel GT, Wawrzyniak PK, Reus M, Gomez Maqueo Chew A, Buda F, Boekema EJ, Bryant DA, Holzwarth AR, de Groot HJ (2009) Alternating syn-anti bacteriochlorophylls form concentric helical nanotubes in chlorosomes. Proc Natl Acad Sci USA 106:8525–8530

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Gomez Maqueo Chew A, Frigaard NU, Bryant DA (2007) Bacteriochlorophyllide c C-82 and C-121 methyltransferases are essential for adaptation to low light in Chlorobaculum tepidum. J Bacteriol 189:6176–6184

    Article  PubMed  Google Scholar 

  • Griebenow K, Holzwarth AR, van Mourik F, van Grondelle R (1991) Pigment organization and energy transfer in green bacteria. 2. Circular and linear dichroism spectra of protein-containing and protein-free chlorosomes isolated from Chloroflexus aurantiacus strain Ok-70-fl. Biochim Biophys Acta 1058:194–202

    Article  CAS  Google Scholar 

  • Hanada S, Pierson BK (2006) The family Chloroflexaceae The Prokaryotes, vol 7, 3rd edn. Springer, New York, pp 815–842

    Book  Google Scholar 

  • Harding RW (1974) The effect of temperature on photo-induced carotenoid biosynthesis in Neurospora crassa. Plant Physiol 54:142–147

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Hirota M, Moriyama T, Shimada K, Miller M, Olson JM, Matsuura K (1992) High degree of organization of bacteriochlorophyll c in chlorosome-like aggregates spontaneously assembled in aqueous solution. Biochim Biophys Acta 1099:271–274

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Jochum T, Reddy CM, Eichhofer A, Buth G, Szmytkowski J, Kalt H, Moss D, Balaban TS (2008) The supramolecular organization of self-assembling chlorosomal bacteriochlorophyll c, d, or e mimics. Proc Natl Acad Sci USA 105:12736–12741

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kline SR (2006) Reduction and analysis of SANS and USANS data using IGOR Pro. J Appl Crystallogr 39:895–900

    Article  CAS  Google Scholar 

  • Larsen KL, Miller M, Cox RP (1995) Incorporation of exogenons long-chain alcohols into bacteriochlorophyll c homologs by Chloroflexus aurantiacus. Arch Microbiol 163:119–123

    Article  CAS  Google Scholar 

  • Loffhagen N, Härtig C, Benndorf D, Babel W (2002) Effects of growth temperature and lipophilic carbon sources on the fatty acid composition and membrane lipid fluidity of Acinetobacter calcoaceticus 69V. Acta Biotechnol 22:235–243

    Article  Google Scholar 

  • Lopez JC, Ryan S, Blankenship RE (1996) Sequence of the bchG gene from Chloroflexus aurantiacus: relationship between chlorophyll synthase and other polyprenyltransferases. J Bacteriol 178:3369–3373

    PubMed  CAS  PubMed Central  Google Scholar 

  • Marr AG, Ingraham JL (1962) Effect of temperature on the composition of fatty acids in Escherichia coli. J Bacteriol 84:1260–1267

    PubMed  CAS  PubMed Central  Google Scholar 

  • Mizoguchi T, Yoshitomi T, Harada J, Tamiaki H (2011) Temperature- and time-dependent changes in the structure and composition of glycolipids during the growth of the green sulfur photosynthetic bacterium Chlorobaculum tepidum. Biochemistry 50:4504–4512

    Article  PubMed  CAS  Google Scholar 

  • Nelson DL, Cox MM (2012) Lehninger principles of biochemistry, 6th edn. W.H. Freeman, New York

    Google Scholar 

  • O’Dell WB, Beatty KJ, Tang JK, Blankenship RE, Urban VS, O’Neill H (2012) Sol–gel entrapped light harvesting antennae: immobilization and stabilization of chlorosomes for energy harvesting. J Mater Chem 22:22582–22591

    Article  Google Scholar 

  • Oelze J, Golecki JR (1995) Membranes and chlorosomes of green bacteria: structure, composition and development. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic photosynthetic bacteria. Kluwar Academic, Dordrecht, pp 259–278

    Google Scholar 

  • Olson JM (1998) Chlorophyll organization and function in green photosynthetic bacteria. Photochem Photobiol 67:61–75

    Article  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

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Psencik J, Collins AM, Liljeroos L, Torkkeli M, Laurinmaki P, Ansink HM, Ikonen TP, Serimaa RE, Blankenship RE, Tuma R, Butcher SJ (2009) Structure of chlorosomes from the green filamentous bacterium Chloroflexus aurantiacus. J Bacteriol 191:6701–6708

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Psencik J, Torkkeli M, Zupcanova A, Vacha F, Serimaa RE, Tuma R (2010) The lamellar spacing in self-assembling bacteriochlorophyll aggregates is proportional to the length of the esterifying alcohol. Photosynth Res 104:211–219

    Article  PubMed  CAS  Google Scholar 

  • Schmidt K, Maarzahl M, Mayer F (1980) Development and pigmentation of chlorosomes in Chloroflexus aurantiacus strain Ok-70-fl. Arch Microbiol 127:87–97

    Article  CAS  Google Scholar 

  • Smith KM, Craig GW, Kehres LA, Pfennig N (1983) Reversed-phase high-performance liquid chromatography and structural assignments of the bacteriochlorophylls c. J Chromatogr A 281:209–223

    Article  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

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Sorensen 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

    Article  PubMed  CAS  Google Scholar 

  • Stanier RY, Smith JHC (1960) The chlorophylls of green bacteria. Biochim Biophys Acta 41:478–484

    Article  PubMed  CAS  Google Scholar 

  • Tang KH, Blankenship RE (2010) Both forward and reverse TCA cycles operate in green sulfur bacteria. J Biol Chem 285:35848–35854

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Tang KH, Blankenship RE (2012) Neutron and light scattering studies of light-harvesting photosynthetic antenna complexes. Photosynth Res 111:205–217

    Article  PubMed  CAS  Google Scholar 

  • Tang KH, Wen J, Li X, Blankenship RE (2009) Role of the AcsF protein in Chloroflexus aurantiacus. J Bacteriol 191:3580–3587

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Tang KH, Urban VS, Wen J, Xin Y, Blankenship RE (2010) SANS investigation of the photosynthetic machinery of Chloroflexus aurantiacus. Biophys J 99:2398–2407

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Tang KH, Barry K, Chertkov O, Dalin E, Han CS, Hauser LJ, Honchak BM, Karbach LE, Land ML, Lapidus A, Larimer FW, Mikhailova N, Pitluck S, Pierson BK, Blankenship RE (2011a) Complete genome sequence of the filamentous anoxygenic phototrophic bacterium Chloroflexus aurantiacus. BMC Genom 12:334

    Article  CAS  Google Scholar 

  • Tang KH, Zhu L, Urban VS, Collins AM, Biswas P, Blankenship RE (2011b) Temperature and ionic strength effects on the chlorosome light-harvesting antenna complex. Langmuir 27:4816–4828

    Article  PubMed  CAS  Google Scholar 

  • Tang JK, Saikin SK, Pingali SV, Enriquez MM, Huh J, Frank HA, Urban VS, Aspuru-Guzik A (2013a) Temperature and carbon assimilation regulate the chlorosome biogenesis in green sulfur bacteria. Biophys J 105:1346–1356

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Tang JK, Xu Y, Muhlmann GM, Zare F, Khin Y, Tam SW (2013b) Temperature shift effect on the Chlorobaculum tepidum chlorosomes. Photosynth Res 115:23–41

    Article  PubMed  CAS  Google Scholar 

  • van Rossum BJ, Steensgaard DB, Mulder FM, Boender GJ, Schaffner K, Holzwarth AR, deGroot HJ (2001) A refined model of the chlorosomal antennae of the green bacterium Chlorobium tepidum from proton chemical shift constraints obtained with high-field 2-D and 3-D MAS NMR dipolar correlation spectroscopy. Biochemistry 40:1587–1595

    Article  PubMed  Google Scholar 

  • Wang ZY, Umetsu M, Yoza K, Kobayashi M, Imai M, Matsushita Y, Niimura N, Nozawa T (1997) A small-angle neutron scattering study on the small aggregates of bacteriochlorophylls in solutions. Biochim Biophys Acta 1320:73–82

    Article  CAS  Google Scholar 

  • Worcester DL, Michalski TJ, Katz JJ (1986) Small-angle neutron scattering studies of chlorophyll micelles: models for bacterial antenna chlorophyll. Proc Natl Acad Sci USA 83:3791–3795

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Worcester DL, Michalski TJ, Tyson RL, Bowman MK, Katz JJ (1989) Structure, red-shifted absorption and electron-transport properties of specific aggregates of chlorophylls. Physica B 156:502–504

    Article  Google Scholar 

  • Zupcanova A, Arellano JB, Bina D, Kopecky J, Psencik J, Vacha F (2008) The length of esterifying alcohol affects the aggregation properties of chlorosomal bacteriochlorophylls. Photochem Photobiol 84:1187–1194

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

JKT thanks PARC Scientific Exchange Program for supporting SANS measurements and Dr. Sai Venkatesh Pingali at Bio-SANS CG-3 for assisting SANS measurement and discussing SANS data. Bio-SANS CG-3 is a resource of the Center for Structural Molecular Biology at ORNL supported by the U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research Project ERKP291. ADH and DMF acknowledge support from NSF Plant Genome Research Program grant IOS-1238812. Work in the laboratory of HAF was supported by grants from the National Science Foundation (MCB-1243565) and the University of Connecticut Research Foundation. JKT is supported by start-up funds.

Author information

Authors and Affiliations

  1. Department of Chemistry and Biochemistry, Clark University, Worcester, MA, 01610, USA

    Yaya Wang & Joseph Kuo-Hsiang Tang

  2. Departments of Plant Biology and Horticultural Science, and The Microbial and Plant Genomics Institute, University of Minnesota, Twin Cities, MN, 55455, USA

    Dana M. Freund & Adrian D. Hegeman

  3. Department of Chemistry, University of Connecticut, Storrs, CT, 06269, USA

    Nikki M. Magdaong & Harry A. Frank

  4. Center for Structural Molecular Biology, Biology and Soft Matter Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA

    Volker S. Urban

Authors
  1. Yaya Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dana M. Freund
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nikki M. Magdaong
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Volker S. Urban
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Harry A. Frank
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Adrian D. Hegeman
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Joseph Kuo-Hsiang Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Joseph Kuo-Hsiang Tang.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, Y., Freund, D.M., Magdaong, N.M. et al. Impact of esterified bacteriochlorophylls on the biogenesis of chlorosomes in Chloroflexus aurantiacus . Photosynth Res 122, 69–86 (2014). https://doi.org/10.1007/s11120-014-0017-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-014-0017-5

Keywords

Search

Navigation