Mutation-Induced Changes in the Protein Environment and Site Energies in the (M)L214G Mutant of the Rhodobacter sphaeroides Bacterial Reaction Center

Abstract

This work focuses on the low-temperature (5 K) photochemical (transient) hole-burned (HB) spectra within the P870 absorption band, and their theoretical analysis, for the (M)L214G mutant of the photosynthetic Rhodobacter sphaeroides bacterial reaction center (bRC). To provide insight into system-bath interactions of the bacteriochlorophyll a (BChl a) special pair, i.e., P870, in the mutated bRC, the optical line shape function for the P870 band is calculated numerically. On the basis of the modeling studies, we demonstrate that (M)L214G mutation leads to a heterogeneous population of bRCs with modified (increased) total electron-phonon coupling strength of the special pair BChl a and larger inhomogeneous broadening. Specifically, we show that after mutation in the (M)L214G bRC a large fraction (∼50%) of the bacteriopheophytin (HA) chromophores shifts red and the 800 nm absorption band broadens, while the remaining fraction of HA cofactors retains nearly the same site energy as HA in the wild-type bRC. Modeling using these two subpopulations allowed for fits of the absorption and nonresonant (transient) HB spectra of the mutant bRC in the charge neutral, oxidized, and charge-separated states using the Frenkel exciton Hamiltonian, providing new insight into the mutant's complex electronic structure. Although the average (M)L214G mutant quantum efficiency of P(+)QA(-) state formation seems to be altered in comparison with the wild-type bRC, the average electron transfer time (measured via resonant transient HB spectra within the P870 band) was not affected. Thus, mutation in the vicinity of the electron acceptor (HA) does not tune the charge separation dynamics. Finally, quenching of the (M)L214G mutant excited states by P(+) is addressed by persistent HB spectra burned within the B band in chemically oxidized samples.

Explaining Spectral Asymmetries and Excitonic Characters of the Core Pigment Pairs in the Bacterial Reaction Center Using a Screened Range-Separated Hybrid Functional

“…There have been several computational studies targeting BRC systems ,,, including studies focusing on the Q y spectra , of the core pigments as the BChl monomer and BChl dimers. − However, open questions regarding these bands remain. For example, a proper characterization of the blue-shifted P state is required to investigate its role in capturing the excitation energy as hypothesized by earlier studies. , The actual spectral splitting in the P bands is difficult to resolve since the blue-shifted state is a dark state that eludes spectral studies. − Other spectral trends related to the BChl pair and the BPhe pair are also challenging full understanding, where the B A state is blue-shifted over that of B B , whereas a red-shift is indicated for the H A state over the H B one. − …”

Impact of Single-Point Mutations on the Excitonic Structure and Dynamics in a Fenna–Matthews–Olson Complex

“…It was also shown that (M)­L214G mutation in the WT bacterial reaction center (bRC) modified the total electron–phonon coupling strength of the special pair BChl a and significantly increased inhomogeneous broadening . A presence of different subpopulations was also observed in the (M)­L214G mutant, where after mutation a large fraction (∼50%) of the H A chromophores shifted red (with the significantly broadened absorption band), while the remaining fraction of H A cofactors remained nearly the same site energy as H A in WT bRC . The latter, however, did not affect the electron transfer time in the (M)­L214G mutant, which was similar to that observed in the WT bRC (∼1 ps), though the quantum efficiency of P + Q A – state formation in the mutant has been altered.…”

“…For example, it was demonstrated that a small alteration in the local structure of the Escherichia coli cyclic AMP receptor protein (CRP), via amino acid substitution, dramatically changes overall protein dynamics, which plays an important role in modulating the allosteric behavior of CRP . It was also shown that (M)­L214G mutation in the WT bacterial reaction center (bRC) modified the total electron–phonon coupling strength of the special pair BChl a and significantly increased inhomogeneous broadening . A presence of different subpopulations was also observed in the (M)­L214G mutant, where after mutation a large fraction (∼50%) of the H A chromophores shifted red (with the significantly broadened absorption band), while the remaining fraction of H A cofactors remained nearly the same site energy as H A in WT bRC .…”

Excited state distribution function for probing Herzberg–Teller vibronic coupling using linear optical response theory: Application to glassy pheophytin a

“…The spectral density in Equations (), and () can have any physically plausible form that suits the conditions of the experiment or the model at hand and certainly is not limited to Equation (). For example, besides the spectral density of the Brownian oscillator model shown in Equation (), the spectral density of Fleming, 39 Mayer, 23,40 Toutounji, 17 or the spectral density proposed by Jankowiak, 20–22 Renger, 24,25 or Rätsep 26 in photosynthetic complexes may undoubtedly be employed, depending on the conditions and the parameters of the problem at hand. A vitally important relationship (widely used in the Brownian oscillator model) that embodies the molecular motion of the surrounding environment in the electronic transition dipole moment time correlation functions is of which the Fourier transform renders the linear absorption line shape function.…”

“…For example, the bath spectral density may be employed to evaluate temporal average values (e.g., time correlation functions) with the aid of the fluctuation‐dissipation theorem 17–19 . Utilizing the spectral density in evaluating the transition dipole moment correlation function will allow encompassing many cases and conditions to probe dynamical effects using the appropriate experimental or theoretical spectral density 17–27 . While the bath spectral density approach has been a popular tool to study the aforementioned correlation functions, and therefore the electronic excited state dynamics when coupled to lattice vibrations (phonons), this article will introduce a novel method that is capable of probing the excited vibronic state and the consequential spectral dynamics.…”