Uphill electron transfer in the tetraheme cytochrome subunit of the Rhodopseudomonas viridis photosynthetic reaction center: Evidence from site- directed mutagenesis
Biochemistry, ISSN: 0006-2960, Vol: 39, Issue: 13, Page: 3592-3602
2000
- 40Citations
- 36Captures
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Metrics Details
- Citations40
- Citation Indexes40
- 40
- CrossRef31
- Captures36
- Readers36
- 36
Article Description
The cytochrome (cyt) subunit of the photosynthetic reaction center from Rhodopseudomonas viridis contains four heme groups in a linear arrangement in the spatial order heme1, heme2, heme4, and heme3. Heme3 is the direct electron donor to the photooxidized primary electron donor (special pair, P). This heme has the highest redox potential (E(m)) among the hemes in the cyt subunit. The E(m) of heme3 has been specifically lowered by site-directed mutagenesis in which the Arg residue at the position of 264 of the cyt was replaced by Lys. The mutation decreases the E(m) of heme3 from +380 to +270 mV, i.e., below that of heme2 (+320 mV). In addition, a blue shift of the α- band was found to accompany the mutation. The assignment of the lowered E(m) and the shifted α-band to heme3 was confirmed by spectroscopic measurements on RC crystals. The structure of the mutant RC has been determined by X-ray crystallography. No remarkable differences were found in the structure apart from the mutated residue itself. The velocity of the electron transfer (ET) from the tetraheme cyt to P was measured under several redox conditions by following the rereduction of P at 1283 nm after a laser flash. Heme3 donates an electron to P with t(1/2) = 105 ns, i.e., faster than in the wild-type reaction center (t(1/2) = 190 ns), as expected from the larger driving force. The main feature is that a phase with t(1/2) ≃ 2 μs dominates when heme3 is oxidized but heme2 is reduced. We conclude that the ET from heme2 to heme3 has a t(1/2) of ~2 μs, i.e., the same as in the WT, despite the fact that the reaction is endergonic by 50 meV instead of exergonic by 60 meV. We propose that the reaction kinetics is limited by the very uphill ET from heme2 to heme4, the ΔG°of which is about the same (+230 meV) in both cases. The interpretation is further supported by measurements of the activation energy (216 meV in the wild-type, 236 meV in the mutant) and by approximate calculations of ET rates. Altogether these results demonstrate that the ET from heme2 to heme3 is stepwise, starting with a first very endergonic step from heme2 to heme4.
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