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How manganese is delivered to photosystems

Biogenesis centers identified for the first time

Munich, 02/07/2012

Manganese is indispensable for photosynthesis. The metal is an essential component of photosynthetic reaction centers, as it is required for the conversion of light into chemical energy and for synthesis of the molecular oxygen in the atmosphere. However, how manganese ions reach their sites of action in photosynthetic cells has been unclear. Now a research team at LMU’s BioCenter, led by Professor Jörg Nickelsen, has identified a protein that acts as a shuttle for manganese and delivers the ion to the photosystems. The findings add a further facet to our understanding of the intricate process of photosystem assembly. Indeed, in the longer term, they could facilitate the design of artificial photosystems for the production of environmentally friendly fuels such as hydrogen. The researchers were also able to demonstrate the existence of dedicated assembly centers for the first time. These so-called “biogenesis centers” are specialized membrane regions where various parts of the photosystems are put together before their final assembly elsewhere in the cell. Transfer of manganese to the reaction centers also occurs in such regions. (Plant Cell, 7.2.2012)

Plants, algae and various types of bacteria are capable of carrying out photosynthesis, i.e. they can convert sunlight into chemical energy and carbohydrates. Life as we know it on Earth would not be possible without photosynthesis, as it is also responsible for the synthesis of the oxygen on which all aerobic organisms depend. The solar radiation that powers photosynthesis is captured by biochemical complexes called photosystems – molecular machines that reside in special membrane systems named thylakoids, and are made up of several different proteins in addition to the chlorophyll molecules that absorb sunlight. One of these multiprotein complexes – photosystem II – also contains four atoms of the metal manganese. Manganese is an essential trace element for all organisms, but in higher plants and other photosynthetic life-forms it catalyzes one of the most remarkable biochemical reactions known – the splitting of water with the release of molecular oxygen. This reaction is the source of the oxygen in Earth’s atmosphere. The oxygen-evolving photosystem II is constructed in assembly-line fashion in a specific sequence of steps. Assembly involves the action of accessory factors which are not present in the final structure. This is why it was unclear at what point in the process the manganese is incorporated into photosystem II. In the new study, the LMU team used the cyanobacterium Synechocystis as a model, and found that an accessory protein termed PratA plays a crucial role in manganese transfer. They were able to show that PratA binds to the metal and acts as a shuttle to transport it to photosystem II.

Interestingly, the transfer of manganese does not occur in the thylakoid membrane itself. Instead the operation takes place in specialized membrane regions that connect the thylakoids in the interior of the cell with the plasma membrane that forms its outer boundary. “The existence of such so-called biogenesis centers has been suggested in recent years, and we have now confirmed their presence for the first time,” says Nickelsen. In these biogenesis centers, early steps in the construction of photosystem II take place. The resulting precursor complexes are then transported to the thylakoid membrane for final assembly. Furthermore, according to Nickelsen, “Initial experiments on Arabidopsis thaliana (thale cress) indicate that the mechanism of manganese transport has been conserved during evolution and proceeds in a similar fashion in both cyanobacteria and higher plants.”

Efficient uptake of manganese into photosystem II is crucial for the water-splitting reaction, in which a pair of water molecules is converted into a single molecule of oxygen, four electrons and four protons. In principle, protons and electrons can be combined to form hydrogen. Indeed, in the long term, a better understanding of the water-splitting reaction could expedite the design of synthetic photosystems as chemical reactors for the production of clean fuels like hydrogen. In light of the ever increasing demand for energy, the development of sustainable systems for the generation of environmentally friendly fuels is one of the most important challenges we face. (göd/PH)

Initial Steps in Photosystem II de novo Assembly and Preloading with Manganese Take Place in Biogenesis Centers in Synechocytis
A. Stengel, I.L. Gügel, D. Hilger, B. Rengstl, H. Jung, J. Nickelsen
The Plant Cell, online 7.2.2012

Professor Jörg Nickelsen
Biozentrum LMU München
Phone: +49 (0) 89 2180 74773
Fax: +49 (0) 89 2180 9974773

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