Structure and self-assembly of antennae pigments in green photosynthetic
bacteria
Roman Tuma
Chlorosomes are large light harvesting complexes found in sulphur (Chlorobiaceae) and
filamentous (Chloroflexaceae) green photosynthetic bacteria. Because of the high light
harvesting efficiency of chlorosomes, species of green bacteria are capable of surviving under
extremely low-light conditions, e.g. in depths of lakes and oceans. Hence, the chlorosome is
considered a good model for developing highly efficient artificial light harvesting systems
and other sensitive photonic devices.
A typical chlorosome is an ellipsoidal body (200 nm x 50 nm) which is attached to the inner
leaflet of bacterial plasma membrane and contains on the order of 105 bacteriochlorophyll
molecules (the major chlorosomal pigment), plus additional minor pigments
(bacteriochlorophyll a, carotenoids and quinones) and several protein species. However,
bacteriochlorophyll molecules are self-assembled into tightly packed, curved lamellar stacks
(Fig. 1) without the support of structural proteins. The resulting dense packing assures strong
excitonic coupling between pigments which, in turn, is the basis for fast energy transfer
within the chlorosome.
Figure 1: (A) A schematic cross-section through the chlorosome showing the internal lamellar structure. (BC) The two-plausible arrangements (parallel in B and anti-parallel in C) of bacteriochlorophyll molecules
(green) within the lamellar stacks. (D) Partitioning of carotenoids (red) within the hydrophobic phase of the
lamellae. Lamellar spacing, c ~2.1 nm, for Chlorobium tepidum chlorosomes.
We use a combination of solution X-ray scattering, cryo-electron microscopy and optical
spectroscopy to gain insight into chlorosome structure and self-assembly of chlorosomal
pigments. The results demonstrated that carotenoids are essential for bacteriochlorophyll
assembly. They partition into the hydrophobic phase created by the aliphatic chains of
esterifying alcohols (e.g. farnesols) within the lamellae and augment the self-assembly
process (Fig 1D). Consequently, lamellar spacing increases with the length of farnesol chains
and the amount of carotenoids. Our recent results indicate that the short-range order of
pigments can be reversibly restored in vitro. However, the long-range lamellar order that is
often seen in intact chlorosomes is irreversibly lost upon disassembly in vitro and thus has to
result from a template-assisted assembly. The results provide basis for engineering pigment
systems suitable for directed self-assembly on surfaces and within prefabricated
nanostructures.
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Publications
Ikonen, T.P., Li, H., Psencik, J., Laurinmäki, P., Butcher, S.J., Frigaard, N.-U., Serimaa, R.E.,
Bryant, D.A. & Tuma, R. (2007) X-ray scattering and electron cryomicroscopy study on
the effect of carotenoid biosynthesis to the structure of Chlorobium tepidum
chlorosomes. Biophys. J. 93, 620-28.
Arellano, J.B., Torkkeli, M., Tuma, R., Laurinmäki, P., Melø, T.B., Ikonen, T.P., Butcher,
S.J., Serimaa, R.E. & Psencık, J. (2008) Hexanol-induced order-disorder transitions in
lamellar self-assembling aggregates of bacteriochlorophyll c in Chlorobium Tepidum
chlorosomes. Langmuir 24, 2035-41.
Funding
This work was funded by Academy of Finland and the national agencies of the participating
countries.
Acknowledgements
This is an ongoing collaboration between several groups: Profs. Sarah Butcher and Ritva
Serimaa at the University of Helsinki, Finland, Dr. Jakub Psencik at Charles University,
Prague, Czech Republic, and Dr. Juan Arellano at CSIC, Salamanca, Spain. The work on role
of carotenoids in chlorosome biogenesis was done in collaboration with Prof. Donald Bryant
at Penn State University, University Park, USA.
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