Electron and proton transfer in bacterial reaction centers

The reaction center (RC) protein of photosynthetic bacteria performs the primary photochemistry by coupling light-induced electron transfer to vectorial proton transfer across the membrane [1]. It plays a central role in photosynthetic energy conversion by facilitating the light-induced double reduction and protonation of a bound quinone molecule, QB. The first electron transfer to QB does not involve direct protonation of the quinone molecule; however, the nearby amino acid residues change their protonation state in response to the change in the electrostatic field associated with the formation of QB-. The second electron transfer is coupled with direct protonation of the quinone leading to formation of quinol, QBH2. The quinol dissociates from the protein and releases its protons on the periplasmic side of the membrane, resulting in the formation of a proton gradient that drives ATP synthesis. The vacant QB site of the protein becomes occupied by a free quinone molecule from the membrane pool, resetting the photocycle for an additional turnover.

The lecture will focus on the kinetic analysis of the photocycle of isolated RC protein driven either by single saturating flashes [7] or by continuous illumination of high intensity [8]. Depending on the conditions, the rate limiting steps of the photocycle could be the first or second electron transfer/proton uptake, the exchange rates of the quinone/quinol at the cytoplasmic site or the cyctochrome at the periplasmic site of the RC or the light intensity [8]. Wide variety of mutations [2,4,5,10] leading to surprising changes in the electron and proton transfer [2,3,6,9] characteristics of the bacterial RC will be discussed. We will argue that significant part of the observed effects can be attributed to changes in the electrostatic environment caused by mutation [2,4,5]. It will be demonstrated that the electrostatic potential near QB- is finely tuned to allow efficient electron and proton transfer to QB [2,7,10].

1. P. Maróti: Flash-induced proton transfer in photosynthetic bacteria (minireview). Photosynthesis Research 37, 1-17 (1993)
2. P. Maróti, D. K. Hanson, L. Baciou, M. Schiffer and P. Sebban: Proton conduction within the reaction centers of Rhodobacter capsulatus: The electrostatic role of the protein. Proc. Natl. Acad. Sci. USA, 91, 5617-5621 (1994).
3. L. Kálmán and P. Maróti: Stabilization of reduced primary quinone by proton uptake in reaction centers of Rhodobacter sphaeroides. Biochemistry, 33, 9237-9244 (1994).
4. P. Sebban, P. Maróti, M. Schiffer and D.K. Hanson: Electrostatic dominoes: Long distance propagation of mutational effects in photosynthetic reaction centers of Rhodobacter capsulatus. Biochemistry, 34, 8390-8397 (1995).
5. P. Maróti, D.K. Hanson, M. Schiffer and P. Sebban: Long-range electrostatic interaction in the bacterial photosynthetic reaction centre. Nature - Structural Biology 2 (12), 1057-1059, (1995).
6. L. Kálmán, T. Gajda, P. Sebban and P. Maróti: pH-metric study of reaction centers from photosynthetic bacteria in micellular solutions: protonatable groups equilibrate with the aqueous bulk phase. Biochemistry 36 (15) 4489-4496 (1997).
7. P. Maróti and C.A. Wraight: Kinetics of H+-ion binding by the P+QA- state of the bacterial photosynthetic reaction centers: Rate limitation within the protein. Biophysical Journal 73, 367-381 (1997)
8. Sz. Osváth and P. Maróti: Coupling of cytochrome and quinone turnovers in photocycle of reaction center from photosynthetic bacteria Rhodobacter sphaeroides. Biophysical Journal 73, 972-982 (1997).
9. L. Kálmán and P. Maróti: Conformation-activated protonation in reaction centers of the photosynthetic bacterium Rhodobacter sphaeroides. Biochemistry 36, 15269-15276 (1997).
10. J. Miksovska, L. Kálmán, M. Schiffer, P. Maróti, P. Sebban and D. K. Hanson: In bacterial reaction centers rapid delivery of the second proton to QB can be achieved in the absence of L212 Glu. Biochemistry 36, 12216-12226 (1997).