Coupling of collective motions of the protein matrix to vibrations of the non-heme iron in bacterial photosynthetic reaction centers

• Published in: Biochimica et biophysica acta 2010-10, Vol.1797 (10), p.1696-1704
• Main Authors: Orzechowska, A., Lipińska, M., Fiedor, J., Chumakov, A., Zając, M., Ślęzak, T., Matlak, K., Strzałka, K., Korecki, J., Fiedor, L., Burda, K.
• Format: Article
• Language: English
• Subjects: Bacteria - chemistry; Bacteria - metabolism; Bacterial Proteins - chemistry; Bacterial Proteins - metabolism; Collective motions; Density of vibrational states; Electron Transport; Iron - chemistry; Iron - metabolism; Kinetics; Models, Chemical; Mössbauer spectroscopy; Non-heme iron vibrations; Nuclear inelastic scattering; Photosynthetic Reaction Center Complex Proteins - chemistry; Photosynthetic Reaction Center Complex Proteins - metabolism; Protons; Quinones - chemistry; Quinones - metabolism; Rhodobacter sphaeroides - chemistry; Rhodobacter sphaeroides - metabolism; Rhodospirillum rubrum - chemistry; Rhodospirillum rubrum - metabolism; Spectroscopy, Mossbauer; Temperature; Vibration
• ISSN: 0005-2728; 0006-3002; 1879-2650
• DOI: 10.1016/j.bbabio.2010.06.012

Non-heme iron is a conservative component of type II photosynthetic reaction centers of unknown function. We found that in the reaction center from Rba. sphaeroides it exists in two forms, high and low spin ferrous states, whereas in Rsp. rubrum mostly in a low spin state, in line with our earlier finding of its low spin state in the algal photosystem II reaction center (Burda et al., 2003). The temperature dependence of the non-heme iron displacement studied by Mössbauer spectroscopy shows that the surrounding of the high spin iron is more flexible (Debye temperature ~ 165 K) than that of the low spin atom (~ 207 K). Nuclear inelastic scattering measurements of the collective motions in the Rba. sphaeroides reaction center show that the density of vibrational states, originating from non-heme iron, has well-separated modes between lower (4–17 meV) and higher (17–25 meV) energies while in the one from Rsp. rubrum its distribution is more uniform with only little contribution of low energy (~ 6 meV) vibrations. It is the first experimental evidence that the fluctuations of the protein matrix in type II reaction center are correlated to the spin state of non-heme iron. We propose a simple mechanism in which the spin state of non-heme iron directly determines the strength of coupling between the two quinone acceptors (Q A and Q B) and fast collective motions of protein matrix that play a crucial role in activation and regulation of the electron and proton transfer between these two quinones. We suggest that hydrogen bond network on the acceptor side of reaction center is responsible for stabilization of non-heme iron in different spin states.