Differential charge polarization of axial histidines in bacterial reaction centers balances the asymmetry of the special pair.
In photosynthesis, light energy is transformed into chemical energy that sustains most forms of life on earth. Solid-state NMR spectroscopy in conjunction with density functional theory modeling can resolve electronic structure down to the atomic level in large membrane proteins. In this work, we have used this technique to address the mechanisms underlying the photochemical reactivity of the special pair in the bacterial reaction center. For charge separation, the electrostatics is important, as the Coulomb barrier must be overcome. On the basis of (15)N NMR data, we resolve a subtle charge-balancing mechanism in the ground state by an axial histidine that is connected to the central Mg(2+) on one side and hydrogen-bonded on the other side. Formation of the hydrogen bond between BChl-a-His and H(2)O leads to a difference in electron density relative to the separate BChl-a-His and H(2)O fragments, with excess positive charge on the imidazole ring. This can lower the kinetic barrier for accommodating the different length scales of electron and proton transfer for separation of spin and charge in a bidirectional proton-coupled electron-transfer mechanism.
Alia
A
A
SSNMR, Leiden Institute of Chemistry, Gorlaeus Laboratoria, Einsteinweg 55, P.O. Box 9502, 2300 RA Leiden, The Netherlands.
Wawrzyniak
Piotr K
PK
Janssen
Geertje J
GJ
Buda
Francesco
F
Matysik
Jörg
J
de Groot
Huub J M
HJ
D001426:Bacterial Proteins / Q000737:chemistry* / Q000378:metabolism*; D006639:Histidine / Q000737:chemistry* / Q000378:metabolism; D009682:Magnetic Resonance Spectroscopy; D045322:Photosynthetic Reaction Center Complex Proteins / Q000737:chemistry* / Q000378:metabolism*; D011789:Quantum Theory; D012242:Rhodobacter sphaeroides
D001426:Bacterial Proteins; D045322:Photosynthetic Reaction Center Complex Proteins; D006639:Histidine