Skip to main content
SpringerLink
Log in

Growth model of chlorosome antenna by the environment-dependent stepwise assembly of a zinc chlorophyll derivative

  • Original article
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

A zinc chlorophyll derivative possessing an oligoethylene glycol ester at the 17-propionate residue was prepared as a model of specific pigments in chlorosomes, such as bacteriochlorophylls-c, d, and e, by chemical modification of naturally occurring chlorophyll-a. The zinc chlorophyll derivative aggregated in aqueous or hexane solutions containing 1% (v/v) ethanol to give red-shifted and broadened Soret/Qy absorption bands with intense circular dichroism signals, indicating the formation of its chlorosome-like J-type self-aggregates. The atomic force microscope images of the self-aggregates prepared in aqueous or hexane solutions showed thin tube-like (ca. 3 nm diameter) or thick rod-like aggregates (> 20 nm diameter), respectively. After standing these solutions for several days, the nanotubes or nanorods further assembled to give ribbon- or bundle-like aggregates, respectively. The latter transformation (tube to ribbon) was triggered by hydrogen bonding between oligoethylene glycol esters located outside of the tubes via water or ethanol molecules. These dynamic supramolecular transformations may also be useful for revealing the growth process of bacteriochlorophyll self-aggregates in a chlorosome.

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

Reproduced with permission from the American Chemical Society

Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

AFM:

Atomic force microscope

BChl:

Bacteriochlorophyll

CD:

Circular dichroism

Chl:

Chlorophyll

HEG:

Hexaethyleneglycol monomethyl ether

HOPG:

Highly oriented pyrolytic graphite

LHA:

Light-harvesting antenna

RP-HPLC:

Reverse-phase high-performance liquid chromatography

r.t.:

Room temperature

TEM:

Transmission electron microscope

UV:

Ultraviolet

vis:

Visible

References

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

    Article  CAS  Google Scholar 

  • Bryant DA, Canniffe DP (2018) How nature designs light-harvesting antenna systems: design principles and functional realization in chlorophototrophic prokaryotes. J Phys B: At Mol Opt Phys 51:033001

    Article  Google Scholar 

  • Beatty JT, Overmann J, Lince MT, Manske AK, Lang AS, Blankenship RE, Dover CLV, Martinson TA, Plumley FG (2005) An obligately photosynthetic bacterial anaerobe from a deep-sea hydrothermal vent. Proc Natl Acad Sci USA 102:9306–9310

    Article  CAS  Google Scholar 

  • Dostál J, Pšenčík J, Zigmantas D (2016) In situ mapping of the energy flow through the entire photosynthetic apparatus. Nat Chem 8:705–710

    Article  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  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Günther LM, Jendrny M, Bloemsma EA, Tank M, Oostergetel GT, Bryant DA, Knoester J, Köhler J (2016) Structure of light-harvesting aggregates in individual chlorosomes. J Phys Chem B 120:5367–5376

    Article  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  CAS  Google Scholar 

  • Holzwarth AR, Griebenow K, Schaffner K (1992) Chlorosomes, photosynthetic antennae with novel self-organized pigment structures. J Photochem Photobiol A Chem 65:61–71

    Article  CAS  Google Scholar 

  • Huber V, Katterle M, Lysetska M, Würthner F (2005) Reversible self-organization of semisynthetic zinc chlorins into well-defined rod antennae. Angew Chem Int Ed 44:3147–3151

    Article  CAS  Google Scholar 

  • Huber V, Sengupta S, Würthner F (2008) Structure–property relationships for self-assembled zinc chlorin light-harvesting dye aggregates. Chem Eur J 14:7791–7807

    Article  CAS  Google Scholar 

  • Huh J, Saikin SK, Brookes JC, Valleau S, Fujita T, Aspuru-Guzik A (2014) Atomistic study of energy funneling in the light-harvesting complex of green sulfur bacteria. J Am Chem Soc 136:2048–2057

    Article  CAS  Google Scholar 

  • Katz JJ, Norris JR, Shipman LL, Thurnauer MC, Wasielewski MR (1978) Chlorophyll function in photosynthetic reaction center. Annu Rev Biophys Bioeng 7:393–434

    Article  CAS  Google Scholar 

  • Kemper B, Zengerling L, Spitzer D, Otter R, Bauer T, Besenius P (2018) Kinetically controlled stepwise self-assembly of AuI-metallopeptides in water. J Am Chem Soc 140:534–537

    Article  CAS  Google Scholar 

  • Li X, Buda F, de Groot HJM, Sevink GJA (2018) Contrasting modes of self-assembly and hydrogen-bonding heterogeneity in chlorosomes of Chlorobaculum tepidum. J Phys Chem C 122:14877–14888

    Article  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

    Article  CAS  Google Scholar 

  • Löhner A, Kunsel T, Röhr MIS, Jansen TLC, Sengupta S, Würthner F, Knoester J, Köhler J (2019) Spectral and structural variations of biomimetic light-harvesting nanotubes. J Phys Chem Lett 10:2715–2724

    Article  Google Scholar 

  • Matsubara S, Tamiaki H (2019) Phototriggered dynamic and biomimetic growth of chlorosomal self-aggregates. J Am Chem Soc 141:1207–1211

    Article  CAS  Google Scholar 

  • Matsubara S, Tamiaki H (2020) Photoactivated supramolecular assembly using “caged chlorophylls” for the generation of nanotubular self-aggregates having controllable lengths. ACS Appl Nano Mater 3:1841–1847

    Article  CAS  Google Scholar 

  • Miyatake T, Tamiaki H (2005) Self-aggregates of bacteriochlorophylls-c, d and e in a light-harvesting antenna system of green photosynthetic bacteria: Effect of stereochemistry at the chiral 3-(1-hydroxyethyl) group on the supramolecular arrangement of chlorophyllous pigments. J Photochem Photobiol C: Photochem Rev 6:89–107

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Oostergetel GT, Reus M, Chew AGM, Bryant DA, Boekema EJ, Holzwarth AR (2007) Long-range organization of bacteriochlorophyll in chlorosomes of Chlorobium tepidum investigated by cryo-electron microscopy. FEBS Lett 581:5435–5439

    Article  CAS  Google Scholar 

  • Orf GS, Blankenship RE (2013) Chlorosome antenna complexes from green photosynthetic bacteria. Photosynth Res 116:315–331

    Article  CAS  Google Scholar 

  • Pšenčík J, Ikonen TP, Laurinmäki P, Merckel MC, Butcher SJ, Serimaa RE, Tuma R (2004) Lamellar organization of pigments in chlorosomes, the light harvesting complexes of green photosynthetic bacteria. Biophys J 87:1165–1172

    Article  Google Scholar 

  • Pšenčík J, Butcher SJ, Tuma R (2014) Chlorosomes: structure, function and assembly. In: Hohmann-Marriott MF (ed) The structural basis of biological energy generation. Springer, Dordrecht, pp 77–109

    Chapter  Google Scholar 

  • Saga Y, Tamiaki H (2006) Transmission electron microscopic study on supramolecular nanostructures of bacteriochlorophyll self-aggregates in chlorosomes of green photosynthetic bacteria. J Biosci Bioeng 102:118–123

    Article  CAS  Google Scholar 

  • Saga Y, Shibata Y, Tamiaki H (2010) Spectral properties of single light-harvesting complexes in bacterial photosynthesis. J Photochem Photobiol C: Photochem Rev 11:15–24

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Sengupta S, Würthner F (2013) Chlorophyll J-aggregates: from bioinspired dye stacks to nanotubes, liquid crystals, and biosupramolecular electronics. Acc Chem Res 46:2498–2512

    Article  CAS  Google Scholar 

  • Shoji S, Hashishin T, Tamiaki H (2012) Construction of chlorosomal rod self-aggregates in the solid state on any substrates from synthetic chlorophyll derivatives possessing an oligomethylene chain at the 17-propionate residue. Chem Eur J 18:13331–13341

    Article  CAS  Google Scholar 

  • Shoji S, Ogawa T, Hashishin T, Ogasawara S, Watanabe H, Usami H, Tamiaki H (2016) Nanotubes of biomimetic supramolecules constructed by synthetic metal chlorophyll derivatives. Nano Lett 16:3650–3654

    Article  CAS  Google Scholar 

  • Tamiaki H (1996) Supramolecular structure in extramembraneous antennae of green photosynthetic bacteria. Coord Chem Rev 148:183–197

    Article  CAS  Google Scholar 

  • Tamiaki H, Yagai S, Miyatake T (1998) Synthetic zinc tetrapyrroles complexing with pyridine as a single axial ligand. Bioorg Med Chem 6:2171–2178

    Article  CAS  Google Scholar 

  • Zhang K, Yeung MCL, Leung SYL, Yam VWW (2018) Energy landscape in supramolecular coassembly of platinum(II) complexes and polymers: morphological diversity, transformation, and dilution stability of nanostructures. J Am Chem Soc 140:9594–9605

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by Japan Society for the Promotion of Science (JSPS) KAKENHI Grant Numbers 18J21058, 20J30005, and JP17H06436 in Scientific Research on Innovative Areas “Innovation for Light-Energy Conversion (I4LEC)”.

Author information

Authors and Affiliations

  1. Graduate School of Life Sciences, Ritsumeikan University, Kusatsu, Shiga, 525-8577, Japan

    Shogo Matsubara & Hitoshi Tamiaki

Authors
  1. Shogo Matsubara
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hitoshi Tamiaki
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hitoshi Tamiaki.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file 1 (DOCX 8342 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Matsubara, S., Tamiaki, H. Growth model of chlorosome antenna by the environment-dependent stepwise assembly of a zinc chlorophyll derivative. Photosynth Res 145, 129–134 (2020). https://doi.org/10.1007/s11120-020-00766-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-020-00766-3

Keywords

Search

Navigation