Browse
Submit Data
Databases
API
Help

Dataset Information

0 Views

0 Connections

0 Citations

0 Reanalyses

0 Downloads

Omics score: 0

A dimeric chlorophyll electron acceptor differentiates type I from type II photosynthetic reaction centers.

ABSTRACT: This research addresses one of the most compelling issues in the field of photosynthesis, namely, the role of the accessory chlorophyll molecules in primary charge separation. Using a combination of empirical and computational methods, we demonstrate that the primary acceptor of photosystem (PS) I is a dimer of accessory and secondary chlorophyll molecules, Chl_2A and Chl_3A, with an asymmetric electron charge density distribution. The incorporation of highly coupled donors and acceptors in PS I allows for extensive delocalization that prolongs the lifetime of the charge-separated state, providing for high quantum efficiency. The discovery of this motif has widespread implications ranging from the evolution of naturally occurring reaction centers to the development of a new generation of highly efficient artificial photosynthetic systems.

Video abstract

SUBMITTER: Gorka M

PROVIDER: S-EPMC8267441 | biostudies-literature | 2021 Jul

REPOSITORIES: biostudies-literature

ACCESS DATA

Json Xml

Publications

A dimeric chlorophyll electron acceptor differentiates type I from type II photosynthetic reaction centers.

Gorka Michael M Charles Philip P Kalendra Vidmantas V Baldansuren Amgalanbaatar A Lakshmi K V KV Golbeck John H JH

iScience 20210611 7

This research addresses one of the most compelling issues in the field of photosynthesis, namely, the role of the accessory chlorophyll molecules in primary charge separation. Using a combination of empirical and computational methods, we demonstrate that the primary acceptor of photosystem (PS) I is a dimer of accessory and secondary chlorophyll molecules, Chl<sub>2A</sub> and Chl<sub>3A</sub>, with an asymmetric electron charge density distribution. The incorporation of highly coupled donors a ...[more]

PMID: 34278250

Similar Datasets

Energetic Diversity in the Electron-Transfer Pathways of Type I Photosynthetic Reaction Centers.

Project description:Photosynthetic reaction centers from heliobacteria (HbRC) and green sulfur bacteria (GsbRC) are homodimeric proteins and share a common ancestor with photosystem I (PSI), classified as type I reaction centers. Using the HbRC crystal structure, we calculated the redox potential (Em) values in the electron-transfer branches, solving the linear Poisson-Boltzmann equation and considering the protonation states of all titratable sites in the entire protein-pigment complex. Em(A-1) for bacteriochlorophyll g at the secondary site in HbRC (-1157 mV) is as low as Em(A-1) for chlorophyll a in PSI (-1173 mV). Em(A0/HbRC) is at the same level as Em(A0/GsbRC) and is 200 mV higher than Em(A0/PSI) due to the replacement of PsaA-Trp697/PsaB-Trp677 in PSI with PshA-Arg554 in HbRC. In contrast, Em(FX) for the Fe4S4 cluster in HbRC (-420 mV) is significantly higher than Em(FX) in GsbRC (-719 mV) and PSI (-705 mV) due to the absence of acidic residues that correspond to PscA-Asp634 in GsbRC and PsaB-Asp575 in PSI. It seems likely that type I reaction centers have evolved, adopting (bacterio)chlorophylls suitable for their light environments while maintaining electron-transfer cascades.

| S-EPMC9949227 | biostudies-literature

Electron Transfer Route between Quinones in Type-II Reaction Centers.

Project description:In photosynthetic reaction centers from purple bacteria (PbRCs) and photosystem II (PSII), the photoinduced charge separation is terminated by an electron transfer between the primary (QA) and secondary (QB) quinones. Here, we investigate the electron transfer route, calculating the superexchange coupling (HQA-QB) for electron transfer from QA to QB in the protein environment. HQA-QB is significantly larger in PbRC than in PSII. In superexchange electron tunneling, the electron transfer via unoccupied molecular orbitals of the nonheme Fe complex (QA → Fe → QB) is pronounced in PbRC, whereas the electron transfer via occupied molecular orbitals (Fe → QB followed by QA → Fe) is pronounced in PSII. The significantly large HQA-QB is caused by a water molecule that donates the H-bond to the ligand Glu-M234 in PbRC. The corresponding water molecule is absent in PSII due to the existence of D1-Tyr246. HQA-QB increases in response to the Ser-L223···QB H-bond formation caused by an extension of the H-bond network, which facilitates charge delocalization over the QB site. This explains the observed discrepancy in the QA-to-QB electron transfer between PbRC and PSII, despite their structural similarity.

| S-EPMC9707520 | biostudies-literature

Initial electron donor and acceptor in isolated Photosystem II reaction centers identified with femtosecond mid-IR spectroscopy.

Project description:Despite the apparent similarity between the plant Photosystem II reaction center (RC) and its purple bacterial counterpart, we show in this work that the mechanism of charge separation is very different for the two photosynthetic RCs. By using femtosecond visible-pump-mid-infrared probe spectroscopy in the region of the chlorophyll ester and keto modes, between 1,775 and 1,585 cm(-1), with 150-fs time resolution, we show that the reduction of pheophytin occurs on a 0.6- to 0.8-ps time scale, whereas P+, the precursor state for water oxidation, is formed after approximately 6 ps. We conclude therefore that in the Photosystem II RC the primary charge separation occurs between the "accessory chlorophyll" Chl(D1) and the pheophytin on the so-called active branch.

| S-EPMC1196200 | biostudies-literature

A single residue controls electron transfer gating in photosynthetic reaction centers.

Project description:Interquinone QA- → QB electron-transfer (ET) in isolated photosystem II reaction centers (PSII-RC) is protein-gated. The temperature-dependent gating frequency "k" is described by the Eyring equation till levelling off at T ≥ 240 °K. Although central to photosynthesis, the gating mechanism has not been resolved and due to experimental limitations, could not be explored in vivo. Here we mimic the temperature dependency of "k" by enlarging VD1-208, the volume of a single residue at the crossing point of the D1 and D2 PSII-RC subunits in Synechocystis 6803 whole cells. By controlling the interactions of the D1/D2 subunits, VD1-208 (or 1/T) determines the frequency of attaining an ET-active conformation. Decelerated ET, impaired photosynthesis, D1 repair rate and overall cell physiology upon increasing VD1-208 to above 130 Å3, rationalize the >99% conservation of small residues at D1-208 and its homologous motif in non-oxygenic bacteria. The experimental means and resolved mechanism are relevant for numerous transmembrane protein-gated reactions.

| S-EPMC5353731 | biostudies-literature

How photosynthetic reaction centers control oxidation power in chlorophyll pairs P680, P700, and P870.

Project description:At the heart of photosynthetic reaction centers (RCs) are pairs of chlorophyll a (Chla), P700 in photosystem I (PSI) and P680 in photosystem II (PSII) of cyanobacteria, algae, or plants, and a pair of bacteriochlorophyll a (BChla), P870 in purple bacterial RCs (PbRCs). These pairs differ greatly in their redox potentials for one-electron oxidation, E(m). For P680, E(m) is 1,100-1,200 mV, but for P700 and P870, E(m) is only 500 mV. Calculations with the linearized Poisson-Boltzmann equation reproduce these measured E(m) differences successfully. Analyzing the origin for these differences, we found as major factors in PSII the unique Mn(4)Ca cluster (relative to PSI and PbRC), the position of P680 close to the luminal edge of transmembrane alpha-helix d (relative to PSI), local variations in the cd loop (relative to PbRC), and the intrinsically higher E(m) of Chla compared with BChla (relative to PbRC).

| S-EPMC1502543 | biostudies-literature

Protein dielectric environment modulates the electron-transfer pathway in photosynthetic reaction centers.

Project description:The replacement of tyrosine by aspartic acid at position M210 in the photosynthetic reaction center of Rhodobacter sphaeroides results in the generation of a fast charge recombination pathway that is not observed in the wild-type. Apparently, the initially formed charge-separated state (cation of the special pair, P, and anion of the A-side bacteriopheophytin, H(A)) can decay rapidly via recombination through the neighboring bacteriochlorophyll (B(A)) soon after formation. The charge-separated state then relaxes over tens of picoseconds and recombination slows to the hundreds-of-picoseconds or nanosecond timescale. This dielectric relaxation results in a time-dependent blue shift of B(A)(-) absorption, which can be monitored using transient absorbance measurements. Protein dynamics also appear to modulate the electron transfer between H(A) and the next electron carrier, Q(A) (a ubiquinone). The kinetics of this reaction are complex in the mutant, requiring two kinetic terms, and the spectra associated with the two terms are distinct; a red shift of the H(A) ground-state bleaching is observed between the shorter and longer H(A)-to-Q(A) electron-transfer phases. The kinetics appears to be pH-independent, suggesting a negligible contribution of static heterogeneity originating from protonation/deprotonation in the ground state. A dynamic model based on the energy levels of the two early charge-separated states, P(+)B(A)(-) and P(+)H(A)(-), has been developed in which the energetics of these states is modulated by fast protein dielectric relaxations and this in turn alters both the kinetic complexity of the reaction and the reaction pathway.

| S-EPMC3491703 | biostudies-literature

Protein dynamics control of electron transfer in photosynthetic reaction centers from Rps. sulfoviridis.

Project description:In the cycle of photosynthetic reaction centers, the initially oxidized special pair of bacteriochlorophyll molecules is subsequently reduced by an electron transferred over a chain of four hemes of the complex. Here, we examine the kinetics of electron transfer between the proximal heme c-559 of the chain and the oxidized special pair in the reaction center from Rps. sulfoviridis in the range of temperatures from 294 to 40 K. The experimental data were obtained for three redox states of the reaction center, in which one, two, or three nearest hemes of the chain are reduced prior to special pair oxidation. The experimental kinetic data are analyzed in terms of a Sumi-Marcus-type model developed in our previous paper,1 in which similar measurements were reported on the reaction centers from Rps. viridis. The model allows us to establish a connection between the observed nonexponential electron-transfer kinetics and the local structural relaxation dynamics of the reaction center protein on the microsecond time scale. The activation energy for relaxation dynamics of the protein medium has been found to be around 0.1 eV for all three redox states, which is in contrast to a value around 0.4-0.6 eV in Rps. viridis.1 The possible nature of the difference between the reaction centers from Rps. viridis and Rps. sulfoviridis, which are believed to be very similar, is discussed. The role of the protein glass transition at low temperatures and that of internal water molecules in the process are analyzed.

| S-EPMC2855845 | biostudies-literature

Structural, dynamic, and energetic aspects of long-range electron transfer in photosynthetic reaction centers.

Project description:Intramolecular electron transfer within proteins plays an essential role in biological energy transduction. Electron donor and acceptor cofactors are bound in the protein matrix at specific locations, and protein-cofactor interactions as well as protein conformational changes can markedly influence the electron transfer rates. To assess these effects, we have investigated charge recombination from the primary quinone acceptor to the special pair bacteriochlorophyll dimer in wild-type reaction centers of Rhodobacter sphaeroides and four mutants with widely modified free energy gaps. After light-induced charge separation, the recombination kinetics were measured in the light- and dark-adapted forms of the protein from 10 to 300 K. The data were analyzed by using the spin-boson model, which allowed us to self-consistently determine the electronic coupling energy, the distribution of energy gaps, the spectral density of phonons, and the reorganization energy. The analysis revealed slow changes of the energy gap after charge separation. Interesting correlations of the control parameters governing electron transfer were found and related to structural and dynamic properties of the protein.

| S-EPMC314149 | biostudies-literature

Hopping Maps for Photosynthetic Reaction Centers().

Project description:Photosynthetic reaction centers (PRCs) employ multiple-step tunneling (hopping) to separate electrons and holes that ultimately drive the chemistry required for metabolism. We recently developed hopping maps that can be used to interpret the rates and energetics of electron/hole hopping in three-site (donor-intermediate-acceptor) tunneling reactions, including those in PRCs. Here we analyze several key ET reactions in PRCs, including forward ET in the L-branch, and hopping that could involve thermodynamically uphill intermediates in the M-branch, which is ET-inactive in vivo. We also explore charge recombination reactions, which could involve hopping. Our hopping maps support the view that electron flow in PRCs involves strong electronic coupling between cofactors and reorganization energies that are among the lowest in biology (? 0.4 eV).

| S-EPMC3530024 | biostudies-literature

High throughput engineering to revitalize a vestigial electron transfer pathway in bacterial photosynthetic reaction centers.

Project description:Photosynthetic reaction centers convert light energy into chemical energy in a series of transmembrane electron transfer reactions, each with near 100% yield. The structures of reaction centers reveal two symmetry-related branches of cofactors (denoted A and B) that are functionally asymmetric; purple bacterial reaction centers use the A pathway exclusively. Previously, site-specific mutagenesis has yielded reaction centers capable of transmembrane charge separation solely via the B branch cofactors, but the best overall electron transfer yields are still low. In an attempt to better realize the architectural and energetic factors that underlie the directionality and yields of electron transfer, sites within the protein-cofactor complex were targeted in a directed molecular evolution strategy that implements streamlined mutagenesis and high throughput spectroscopic screening. The polycistronic approach enables efficient construction and expression of a large number of variants of a heteroligomeric complex that has two intimately regulated subunits with high sequence similarity, common features of many prokaryotic and eukaryotic transmembrane protein assemblies. The strategy has succeeded in the discovery of several mutant reaction centers with increased efficiency of the B pathway; they carry multiple substitutions that have not been explored or linked using traditional approaches. This work expands our understanding of the structure-function relationships that dictate the efficiency of biological energy-conversion reactions, concepts that will aid the design of bio-inspired assemblies capable of both efficient charge separation and charge stabilization.

| S-EPMC3318735 | biostudies-literature

OmicsDI is part of the ELIXIR infrastructure

OmicsDI is an Elixir interoperability service. Learn more ›

Tweets

OmicsDI Databases

PRIDE
PeptideAtlas
MassIVE
JPOST Repository
Physiome Model Repository

EGA
EVA
ENA
LINCS
PAXDB
Cell Collective

MetaboLights
Metabolomics Workbench
MetabolomeExpress
GNPS
BioModels
FAIRDOMHub

ArrayExpress
dbGaP
ExpressionAtlas
GEO
NODE

Information

Databases
Help
API
Contact us
Code on GitHub
Terms of use
Submit Data