Mimicking the properties of the oxygen-evolving complex in purple bacterial reaction centers

One of the most critical events in the development of the earth, ~ 3 billion years ago, was the emergence of organisms that were capable of water oxidation and thus had an essentially unlimited source of electrons by using water as a reductant. Following from this picture of the development of the earth is the idea that primitive anaerobic phototrophs evolved into cyanobacteria, algae and plants. The protein complexes that perform the primary conversion of light, namely the bacterial reaction center and photosystem II, are then evolutionary related despite their different cellular functions.

The bacterial reaction center from Rhodobacter sphaeroides is composed of three protein subunits, the L (yellow), M (blue), and H (green) and 9 cofactors (red). The protein is an integral membrane proteins with L and M subunits having 5 transmembrane helices and the H subunit having one. The cofactors are composed of bacteriochlorophylls, bacteriopheophytins, quinones, and a non-heme iron atom. The cofactors are arranged into two branches with only one, the A branch shown on the right, being active. The protein strongly influences the properties of the cofactors, in particular the primary electron donor, the bacteriochlorophyll dimer are the top of the figure.

The bacterial reaction center and photosystem II, possess a common structural motif of a central core with two-fold symmetry formed by subunits each containing five transmembrane helices and two branches of cofactors. The shared structural and functional features provide a basis for experiments in the bacterial reaction center that are designed to investigate three key attributes required for water oxidation by photosystem II.

Critical for the ability of photosystem II to oxidize water is that it is the strongest naturally occurring oxidant. The bacterial reaction center can be converted into a very strong oxidant by the introduction of hydrogen bonds to the bacteriochlorophyll dimer as shown by the shift of the redox curves to increasing potentials as mutations are added. For the Y_M mutant, all four mutations are present and the reaction centers are very strong oxidants.

The water oxidation process is a four electron transfer process that also requires the transfer of protons. Photosystem II makes use of a amino acid radical, tyrosyl Y_Z, to couple the proton and electron transfer. The Y_M mutant is highly oxidizing and also able to oxidize tyrosines as evidenced by the light-induced changes in their optical spectra.

Details concerning the evolution of the different photosystems are unknown. However, the Y_M mutant has properties of a possible evolutionary intermediate photosystem, namely the ability to oxidize specific tyrosines. Thus, evolution may have proceeded by the photosystems of primitive photosynthetic bacteria becoming highly oxidizing and then gaining the ability to oxidize manganese.

In photosystem II, the four electron equivalents are collected in the manganese cluster, whose molecular arrangement remains unknown. We are now investigating the ability of the highly oxidizing reaction centers to oxidize manganese. Based upon the changes of the optical spectra, manganese can rapidly be oxidized by the highly oxidizing reaction centers. Work is underway to create a new cofactor, a bound manganese cluster that functions as an electron donor mimicking the cluster in photosystem II.

Relevant Publications
X. Lin, H. A. Murchison, V. Nargaragan, W. W. Parson, J. P. Allen, and J. C. Williams (1994) "Specific alteration of the oxidation potential of the electron donor in reaction centers from Rhodobacter sphaeroides" Proc. Natl. Acad. Sci. USA 91, 10265-10269. (PDF)

T. A. Mattioli, X. Lin, J. P. Allen, and J. C. Williams (1995) "Correlation between multiple hydrogen bonding and alteration of the oxidation potential of the bacteriochlorophyll dimer of reaction centers from Rhodobacter sphaeroides" Biochemistry, 34, 6142-6152.

J. Rautter, F. Lendzian, C. Schulz, A. Fetsch, M. Kuhn, X. Lin, J. C. Williams, J. P. Allen, and W. Lubitz (1995) "ENDOR-Studies of the primary donor cation radical in mutant reaction centers of Rhodobacter sphaeroides with altered hydrogen-bond interactions" Biochemistry 34, 8130-8143.

J. P. Allen and J. C. Williams (1998) “Photosynthetic reaction centers” FEBS Letters, 438, 5-9.

L. Kalman, R. LoBrutto, J. P. Allen, and J. C. Williams (1999) “Modified reaction centres oxidize tyrosine in reactions that mirror photosystem II” Nature 402, 696-699. (PDF)

A. J. Narváez, L. Kálmán, R. LoBrutto, J. P. Allen, and J. C. Williams (2002) “Influence of the protein environment on the properties of a tyrosyl radical in reaction centers from Rhodobacter sphaeroides” Biochemistry, in press.

Frank Müh, Friedhelm Lendzian, Mason Roy, JoAnn C. Williams, James P. Allen and Wolfgang Lubitz (2002) “Pigment-protein interactions in bacterial reaction centers and their influence on oxidation potential and spin density distribution of the primary donor” J. Phys. Chem. B.,106, 3226-3236.

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