An international team of scientists has resolved the structure of chlorophyll in chlorosomes of green bacteria. Chlorosomes are the light harvesting antennae of these bacteria. They are elongated small pockets which can accommodate up to 250,000 chlorophyll molecules.
‘Artificial Leaves’
According to Huub de Groot, Professor of chemistry in Leiden and coordinator of the research, similar structures in the future can be useful for development of `artificial leaves': new generations of solar cells for the conversion of energy from sun light to fuels, because green bacteria can collect sunlight with a high efficiency for the conversion to chemical energy.
PNAS
The results of the research are available on the website of PNAS: http://www.pnas.org (Proceedings of the National Academy of Sciences).
The study is part of the thesis work of former group member Dr. Swapna Ganapathy
https://openaccess.leidenuniv.nl/dspace/handle/1887/13282
Nanotubes
The structure proves to be a combination of concentric nanotubes. This produces a robust and nevertheless plastic framework for the light harvesting antennae. The chlorophyll molecules form helices along which superfast energy migration to proteins in the cell membrane occurs where the chemical conversion takes place.
Evolution
The flexible structure of the chlorosomes provides freedom to vary the dimensions dependent on the intensity of light, to be able to make larger antennae for operation at low light intensity, and to organize chlorophyll in a very heterogeneous manner inside the antennae. That heterogeneity is very effective for the optimum absorption of photons at different wavelengths, the research workers discovered. This combination of a robust framework and freedom in accommodation of chlorophyll molecules has ensured that the bacteria have the possibility to adapt to low light intensity in biological evolution, for example 100 meters deep in the sea.
Last known antenna structure
For plants and algae - the other organisms which convert sunlight into chemical energy – it has been known for some time how their light-harvesting antennae worked. Chlorosomes are however very heterogeneous in their molecular composition; no chlorosome is the same. As a result, solving the structure with X-ray crystallography is no option. Biochemical and microscopic techniques produced already for dozens of years contradictory information.
Novel strategy
The research team developed a novel strategy to solve the problem with a combination of genetic techniques and two sophisticated bio-imaging methods: cryo-electronmicroscopy and solid-state NMR.
Late genes
The first what they did was to remove three genes from the bacterium which have arisen late in the evolution. The biologists in the team, research workers linked to the Pennsylvania State University in the USA, suspected that those `late' genes are responsible for the large efficiency with which the bacterium absorbs light. Chlorosomes of these mutants appeared much more uniform and have a simpler structure than those of the wild type. Moreover they proved to be less efficient. The heterogeneity is obviously one of the secrets behind the efficiency.
Precise stacking
The next step was to grow the mutant for enrichment with stable C-13 isotopes for solid state NMR. This work was performed in the Max-Planck Insitute für Bioanorganische Chemie in Germany. Already the first solid state NMR experiments made clear that a new view on the structure could be obtained. For the first time we got a clear indication that our measurements would allow us to determine the exact stacking of chlorophyll. We could determine distances between the molecules very closely and we found that the molecules piled up with their tails alternating.
Rings and tubes
To go from the microstructure to nanotubes, still another technique was used, cryo-electronmicroscopy, in Groningen. There were very distinct patterns in the images, which can only be explained with a helical arrangement of molecules. Once this was established, it was possible to combine the dimensions from the EM with the precise measurements at the molecular scale from the solid state NMR to produce a very detailed structure of the chlorosome. The result was a structure in which chlorophyll forms stacks and rings that self-assemble into concentric nanotubes. The corresponding structure of the wild the type is less uniform, and has the stacks in another direction, approximately perpendicular to the stacking in the mutant. The structural framework thus provides insight into how similar chlorosome systems can be established in different ways. This insight is important for the construction of artificial systems in a next step.
New generations solar energy collectors
The reason that chlorosomes are an attractive model for new generations solar conversion devices is that they have a simple composition and work very well, already at very low light intensity. In natural photosynthesis the quantity of sunlight is generally not the limiting factor. Green bacteria live, however, under extremely low light intensity, with sometimes only a few photons per chlorophyll molecule per day. To be able to survive on solar energy is a challenge and thanks to the PNAS research we know now much more concerning how nature has solved this problem. By the dense stacking of chlorophyll molecules there are strong links between the molecules and it is possible to combine the energy that is caught by more than the hundred thousand molecules joined together to generate sufficient flow for the conversion to chemical energy. Moreover the structure protects itself against a surplus of light. Then, disorder in the stacking appears to help: a messier structure is in this case, as it happens, better for biology. To apply the knowledge and new insights obtained from the biology in the translation to nanostructured materials for the conversion of sunlight to fuel is now the next challenge.
