Chlorosome

A Chlorosome is a photosynthetic antenna complex found in green sulfur bacteria (GSB) and some green filamentous anoxygenic phototrophs (FAP) (Chloroflexaceae, Oscillochloridaceae). They differ from other antenna complexes by their large size and lack of protein matrix supporting the photosynthetic pigments. Green sulfur bacteria are a group of organisms that generally live in extremely low-light environments, such as at depths of 100 metres in the Black Sea. The ability to capture light energy and rapidly deliver it to where it needs to go is essential to these bacteria, some of which see only a few photons of light per chlorophyll per day. To achieve this, the bacteria contain chlorosome structures, which contain up to 250,000 chlorophyll molecules. Chlorosomes are ellipsoidal bodies, in GSB their length varies from 100 to 200 nm, width of 50-100 nm and height of 15 - 30 nm,^[1] in FAP the chlorosomes are somewhat smaller.

Structure

Inside the GSB cell, the chlorosomes are thought to be attached to the reaction centers in the cell membrane via FMO-proteins and a chlorosome baseplate composed of csmA proteins. Chlorosomes from FAP lack the FMO complex. The composition of the chlorosomes is mostly bacteriochlorophyll with small amounts of carotenoids and quinones surrounded by a galactolipid monolayer with ten different proteins attached to it.

Organization of the light harvesting pigments

Bacteriochlorophyll and carotenoids are two molecules responsible for harvesting light energy. Current models of the organization of bacteriochlorophyll and carotenoids (the main constituents) inside the chlorosomes have put them in a lamellar organization, where the long farnesol tails of the bacteriochlorophyll intermix with carotenoids and each other, forming a structure resembling a lipid multilayer.^[2]

Recently, another study has determined the organization of the bacteriochlorophyll molecules in green sulfur bacteria.^[3] Because they have been so difficult to study, the chlorosomes in green sulfur bacteria are the last class of light-harvesting complexes to be characterized structurally by scientists. Each individual chlorosome has a unique organization and this variability in composition had prevented scientists from using X-ray crystallography to characterize the internal structure. To get around this problem, the team used a combination of different experimental approaches. Genetic techniques to create a mutant bacterium with a more regular internal structure, cryo-electron microscopy to identify the larger distance constraints for the chlorosome, solid-state nuclear magnetic resonance (NMR) spectroscopy to determine the structure of the chlorosome's component chlorophyll molecules, and modeling to bring together all of the pieces and create a final picture of the chlorosome.

To create the mutant, three genes were inactivated that green sulfur bacteria acquired late in their evolution. In this way it was possible to go backward in evolutionary time to an intermediate state with much less variable and better ordered chlorosome organelles than the wild-type. The chlorosomes were isolated from the mutant and the wild-type forms of the bacteria. Cryo-electron microscopy was used to take pictures of the chlorosomes. The images reveal that the chlorophyll molecules inside chlorosomes have a nanotube shape. The team then used MAS NMR spectroscopy to resolve the microscopic arrangement of chlorophyll inside the chlorosome. With distance constraints and DFT ring current analyses the organization was found to consist of unique syn-anti monomer stacking. The combination of NMR, cryo-electron microscopy and modeling enabled the scientists to determine that the chlorophyll molecules in green sulfur bacteria are arranged in helices. In the mutant bacteria, the chlorophyll molecules are positioned at a nearly 90-degree angle in relation to the long axis of the nanotubes, whereas the angle is less steep in the wild-type organism. The structural framework can accommodate disorder to improve the biological light harvesting function, which implies that a less ordered structure has a better performance.

An alternative energy source

The interactions that lead to the assembly of the chlorophylls in chlorosomes are rather simple and the results may one day be used to build artificial photosynthetic systems that convert solar energy to electricity or biofuel.

List of bacterial species containing chlorosomes

• Chlorobiaceae
  • Chlorobium limicola
  • Chlorobium phaeobacteroides
  • Chlorobium phaeovibrioides
  • Chlorobium vibrioforme
  • Chlorobium tepidum
  • Pelodictyon lutoleum
  • Prostecochloris aestuarii
• Chloroflexaceae
  • Chloroflexus aurantiacus
  • Chloroflexus aggregans
  • Chloronema giganteum
• Oscillochloridaceae
  • Oscillochloris trichoides
• Acidobacteriaceae
  • Chloracidobacterium thermophilum^[4]

Notes

1. ↑ A Martinez-Planells et al.: Determination of the topography and biometry of chlorosomes by atomic force microscopy, Photosynthesis Research 71, 2002, p. 83-90
2. ↑ J. Pšenčík et al.: Lamellar Organization of Pigments in Chlorosomes, the Light Harvesting Complexes of Green Photosynthetic Bacteria, Biophys J. 87(2), 2004, p. 1165–1172.
3. ↑ Swapna Ganapathy, Gert T. Oostergetel, Piotr K. Wawrzyniak, Michael Reus, Aline Gomez Maqueo Chew, Francesco Buda, Egbert J. Boekema, Donald A. Bryant, Alfred R. Holzwarth, and Huub J. M. de Groot: Alternating syn-anti bacteriochlorophylls form concentric helical nanotubes in chlorosomes, Proc. Natl. Acad. Sci. USA 106, 2009, p. 8525-8530. doi:10.1073/pnas.0903534106
4. ↑ Bryant, Donald A.; Costas, AM; Maresca, JA; Chew, AG; Klatt, CG; Bateson, MM; Tallon, LJ; Hostetler, J; et al. (2007-07-27), "Candidatus Chloracidobacterium thermophilum: An Aerobic Phototrophic Acidobacterium", Science, 317 (5837): 523–526, doi:10.1126/science.1143236, PMID 17656724  CS1 maint: Explicit use of et al. (link)