Weak temperature dependence of P + H A − recombination in mutant Rhodobacter sphaeroides reaction centers

Abstract

In contrast with findings on the wild-type Rhodobacter sphaeroides reaction center, biexponential P+HA− → PHA charge recombination is shown to be weakly dependent on temperature between 78 and 298 K in three variants with single amino acids exchanged in the vicinity of primary electron acceptors. These mutated reaction centers have diverse overall kinetics of charge recombination, spanning an average lifetime from ~2 to ~20 ns. Despite these differences a protein relaxation model applied previously to wild-type reaction centers was successfully used to relate the observed kinetics to the temporal evolution of the free energy level of the state P+HA− relative to P+BA−. We conclude that the observed variety in the kinetics of charge recombination, together with their weak temperature dependence, is caused by a combination of factors that are each affected to a different extent by the point mutations in a particular mutant complex. These are as follows: (1) the initial free energy gap between the states P+BA− and P+HA−, (2) the intrinsic rate of P+BA− → PBA charge recombination, and (3) the rate of protein relaxation in response to the appearance of the charge separated states. In the case of a mutant which displays rapid P+HA− recombination (ELL), most of this recombination occurs in an unrelaxed protein in which P+BA− and P+HA− are almost isoenergetic. In contrast, in a mutant in which P+HA− recombination is relatively slow (GML), most of the recombination occurs in a relaxed protein in which P+HA− is much lower in energy than P+HA−. The weak temperature dependence in the ELL reaction center and a YLH mutant was modeled in two ways: (1) by assuming that the initial P+BA− and P+HA− states in an unrelaxed protein are isoenergetic, whereas the final free energy gap between these states following the protein relaxation is large (~250 meV or more), independent of temperature and (2) by assuming that the initial and final free energy gaps between P+BA− and P+HA− are moderate and temperature dependent. In the case of the GML mutant, it was concluded that the free energy gap between P+BA− and P+HA− is large at all times.Electronic supplementary materialThe online version of this article (doi:10.1007/s11120-016-0239-9) contains supplementary material, which is available to authorized users.

Inverted-region electron transfer as a mechanism for enhancing photosynthetic solar energy conversion efficiency

“…ET reactions in the purple bacterial photosynthetic RCs (PBRCs) have been by far the most widely studied (28), and it is primarily in connection with this system that the idea of invertedregion ET is considered (15,16). However, in PBRCs the primary radical pair recombination reaction (so-called P + H L − recombination), at least for the native or wild-type (WT) system, is known not to occur in the inverted region (29)(30)(31)(32). In fact, the unproductive P + H L − recombination reaction in WT PBRCs is nearly activationless (33).…”

“…In fact, the unproductive P + H L − recombination reaction in WT PBRCs is nearly activationless (33). In PBRCs it appears to be the case that mechanisms related to protein relaxations in response to ET are (more) important in maximizing photosynthetic efficiency (29)(30)(31)(32).…”

Synthetically tuneable biomimetic artificial photosynthetic reaction centres that closely resemble the natural system in purple bacteria

“…1) are comparable. In the natural system, charge separation to the first state stable for times longer than its production time is to species P + H L – , that takes 4–7 ps to appear, 62 secondary charge separation then occurs 62 in 200–250 ps ahead of primary charge recombination (0.6 to 10 ns), 62 and then secondary charge recombination takes 100 ms. 94 The corresponding times for the biomimetic compounds are 20–40 ps, 250–500 ps, 0.3–2 ns, and 5–90 μs, respectively. All are within an order of magnitude of the natural system except for the secondary charge recombination times, which are 3–4 orders of magnitude shorter.…”

“…In the natural system, through-space interactions mediated dynamically by intervening matter are critical. 48,49,58–62,94 Such effects are difficult to control in artificial systems and so are replaced with through-bond coupling mechanisms in rigid molecules, 78,84,95–103 and a critical design criteria is therefore to establish similar couplings using this device-robust mechanism. A great advantage of the chemical routes presented to biomimetic solar-energy harvesting is that it can readily be modified to make broadband or narrowband absorbers, for example, for use in solar cells or phototherapy, respectively, 40,96,98,104 for upconversion units with unprecedented efficiency, 105–107 and as tailor-made components for determining mechanism and improving solar cell functions.…”

High-pressure tuning of primary photochemistry in bacterial photosynthesis: membrane-bound versus detergent-isolated reaction centers

“…This type of membrane-embedded Rba. sphaeroides RC, both wild-type and altered through mutation, has been used previously to study multiple aspects of photochemical charge separation and charge recombination (e.g., see (Beekman 1995;Beekman 1996;Vos 1994a;Vos 1994b;Brederode 1997;Brederode 1999;Gibasiewicz 2011;Gibasiewicz 2013;Gibasiewicz 2016)). The second type of sample comprised YM210W RCs purified from such membranes using detergent.…”