Excitonic structure and charge separation in the heliobacterial reaction center probed by multispectral multidimensional spectroscopy

Photochemical reaction centers are the engines that drive photosynthesis. The reaction center from heliobacteria (HbRC) has been proposed to most closely resemble the common ancestor of photosynthetic reaction centers, motivating a detailed understanding of its structure-function relationship. The recent elucidation of the HbRC crystal structure motivates advanced spectroscopic studies of its excitonic structure and charge separation mechanism. We perform multispectral two-dimensional electronic spectroscopy of the HbRC and corresponding numerical simulations, resolving the electronic structure and testing and refining recent excitonic models. Through extensive examination of the kinetic data by lifetime density analysis and global target analysis, we reveal that charge separation proceeds via a single pathway in which the distinct A0 chlorophyll a pigment is the primary electron acceptor. In addition, we find strong delocalization of the initial excited state and charge separation intermediate. Our findings have general implications for the understanding of photosynthetic charge separation mechanisms, and how they might be tuned to achieve different functional goals.

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Excitonic Structure and Charge Separation in the Heliobacterial Reaction Center Probed by Multispectral Multidimensional Spectroscopy

10.26434/chemrxiv.13519169 ◽

2021 ◽

Author(s):

Yin Song ◽

Riley Sechrist ◽

Hoang Huy Nguyen ◽

William Johnson ◽

Darius Abramavičius ◽

...

Keyword(s):

Reaction Center ◽

Charge Separation ◽

Electronic Spectroscopy ◽

Spectroscopic Studies ◽

Primary Electron ◽

Reaction Centers ◽

Separation Mechanism ◽

Photosynthetic Reaction Centers ◽

Density Analysis ◽

Function Relationship

Photochemical reaction centers are the engines that drive photosynthesis. The reaction center from heliobacteria (HbRC) has been proposed to most closely resemble the common ancestor of photosynthetic reaction centers, motivating a detailed understanding of its structure-function relationship. The recent elucidation of the HbRC crystal structure motivates advanced spectroscopic studies of its excitonic structure and charge separation mechanism. We perform multispectral two-dimensional electronic spectroscopy of the HbRC and corresponding numerical simulations, resolving the electronic structure and testing and refining recent excitonic models. Through extensive examination of the kinetic data by lifetime density analysis and global target analysis, we reveal that charge separation proceeds via a single pathway in which the distinct A0 chlorophyll a pigment is the primary electron acceptor. In addition, we find strong delocalization of the initial excited state and charge separation intermediate. Our findings have general implications for the understanding of photosynthetic charge separation mechanisms, and how they might be tuned to achieve different functional goals.

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Excitonic Structure and Charge Separation in the Heliobacterial Reaction Center Probed by Multispectral Multidimensional Spectroscopy

10.26434/chemrxiv.13519169.v2 ◽

2021 ◽

Author(s):

Yin Song ◽

Riley Sechrist ◽

Hoang Huy Nguyen ◽

William Johnson ◽

Darius Abramavičius ◽

...

Keyword(s):

Reaction Center ◽

Charge Separation ◽

Electronic Spectroscopy ◽

Spectroscopic Studies ◽

Primary Electron ◽

Reaction Centers ◽

Separation Mechanism ◽

Photosynthetic Reaction Centers ◽

Density Analysis ◽

Function Relationship

Photochemical reaction centers are the engines that drive photosynthesis. The reaction center from heliobacteria (HbRC) has been proposed to most closely resemble the common ancestor of photosynthetic reaction centers, motivating a detailed understanding of its structure-function relationship. The recent elucidation of the HbRC crystal structure motivates advanced spectroscopic studies of its excitonic structure and charge separation mechanism. We perform multispectral two-dimensional electronic spectroscopy of the HbRC and corresponding numerical simulations, resolving the electronic structure and testing and refining recent excitonic models. Through extensive examination of the kinetic data by lifetime density analysis and global target analysis, we reveal that charge separation proceeds via a single pathway in which the distinct A0 chlorophyll a pigment is the primary electron acceptor. In addition, we find strong delocalization of the initial excited state and charge separation intermediate. Our findings have general implications for the understanding of photosynthetic charge separation mechanisms, and how they might be tuned to achieve different functional goals.

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Access to Primary Charge Separation Mechanism in Photosynthetic Reaction Centers: Anisotropic Excitation Spectra of Electric Field Modulated Fluorescence Yields

ENERGYO ◽

10.1515/energyo.0089.00010 ◽

2018 ◽

Author(s):

U. Eberl ◽

A. Ogrodnik ◽

M. E. Michel-Beyerle

Keyword(s):

Electric Field ◽

Charge Separation ◽

Reaction Centers ◽

Separation Mechanism ◽

Photosynthetic Reaction Centers ◽

Primary Charge Separation ◽

Excitation Spectra ◽

Modulated Fluorescence

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Primary processes in the bacterial reaction center probed by two-dimensional electronic spectroscopy

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1721927115 ◽

2018 ◽

Vol 115 (14) ◽

pp. 3563-3568 ◽

Cited By ~ 20

Author(s):

Andrew Niedringhaus ◽

Veronica R. Policht ◽

Riley Sechrist ◽

Arkaprabha Konar ◽

Philip D. Laible ◽

...

Keyword(s):

Excited State ◽

Reaction Center ◽

Charge Separation ◽

Purple Bacteria ◽

Electronic Spectroscopy ◽

Reaction Centers ◽

Purple Bacterium ◽

Absorption Bands ◽

Sequential Reaction ◽

Special Pair

In the initial steps of photosynthesis, reaction centers convert solar energy to stable charge-separated states with near-unity quantum efficiency. The reaction center from purple bacteria remains an important model system for probing the structure–function relationship and understanding mechanisms of photosynthetic charge separation. Here we perform 2D electronic spectroscopy (2DES) on bacterial reaction centers (BRCs) from two mutants of the purple bacterium Rhodobacter capsulatus, spanning the Qy absorption bands of the BRC. We analyze the 2DES data using a multiexcitation global-fitting approach that employs a common set of basis spectra for all excitation frequencies, incorporating inputs from the linear absorption spectrum and the BRC structure. We extract the exciton energies, resolving the previously hidden upper exciton state of the special pair. We show that the time-dependent 2DES data are well-represented by a two-step sequential reaction scheme in which charge separation proceeds from the excited state of the special pair (P*) to P+HA− via the intermediate P+BA−. When inhomogeneous broadening and Stark shifts of the B* band are taken into account we can adequately describe the 2DES data without the need to introduce a second charge-separation pathway originating from the excited state of the monomeric bacteriochlorophyll BA*.

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Acquirement of water-splitting ability and alteration of the charge-separation mechanism in photosynthetic reaction centers

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.2000895117 ◽

2020 ◽

Vol 117 (28) ◽

pp. 16373-16382 ◽

Cited By ~ 5

Author(s):

Hiroyuki Tamura ◽

Keisuke Saito ◽

Hiroshi Ishikita

Keyword(s):

Excitation Energy ◽

Water Splitting ◽

Charge Separation ◽

Purple Bacteria ◽

D1 Protein ◽

Reaction Centers ◽

Electronic Coupling ◽

Separation Mechanism ◽

Photosynthetic Reaction Centers ◽

Charged Residues

In photosynthetic reaction centers from purple bacteria (PbRC) and the water-oxidizing enzyme, photosystem II (PSII), charge separation occurs along one of the two symmetrical electron-transfer branches. Here we report the microscopic origin of the unidirectional charge separation, fully considering electron–hole interaction, electronic coupling of the pigments, and electrostatic interaction with the polarizable entire protein environments. The electronic coupling between the pair of bacteriochlorophylls is large in PbRC, forming a delocalized excited state with the lowest excitation energy (i.e., the special pair). The charge-separated state in the active branch is stabilized by uncharged polar residues in the transmembrane region and charged residues on the cytochromec2binding surface. In contrast, the accessory chlorophyll in the D1 protein (ChlD1) has the lowest excitation energy in PSII. The charge-separated state involves ChlD1•+and is stabilized predominantly by charged residues near the Mn4CaO5cluster and the proceeding proton-transfer pathway. It seems likely that the acquirement of water-splitting ability makes ChlD1the initial electron donor in PSII.

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Novel multipulse saturation spectroscopy for quantum yield determination of charge separation in modified photosynthetic reaction centers

Chemical Physics Letters ◽

10.1016/s0009-2614(99)00461-3 ◽

1999 ◽

Vol 306 (5-6) ◽

pp. 239-248 ◽

Cited By ~ 1

Author(s):

P. Müller ◽

G. Hartwich ◽

A. Ogrodnik ◽

M.E. Michel-Beyerle

Keyword(s):

Quantum Yield ◽

Charge Separation ◽

Reaction Centers ◽

Photosynthetic Reaction Centers ◽

Saturation Spectroscopy ◽

Yield Determination

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Theory for spectral hole burning of the primary electron donor state of photosynthetic reaction centers

Biochimica et Biophysica Acta (BBA) - Bioenergetics ◽

10.1016/0005-2728(88)90166-1 ◽

1988 ◽

Vol 932 ◽

pp. 287-305 ◽

Cited By ~ 84

Author(s):

J.M. Hayes ◽

J.K. Gillie ◽

D. Tang ◽

G.J. Small

Keyword(s):

Electron Donor ◽

Primary Electron ◽

Reaction Centers ◽

Hole Burning ◽

Spectral Hole Burning ◽

Photosynthetic Reaction Centers ◽

Primary Electron Donor ◽

Spectral Hole ◽

Donor State

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De Novo Protein Design of Photochemical Reaction Centers

10.21203/rs.3.rs-932621/v1 ◽

2021 ◽

Author(s):

Nathan Ennist ◽

Zhenyu Zhao ◽

Steven Stayrook ◽

Bohdana Discher ◽

P Leslie 'Les' Dutton ◽

...

Keyword(s):

Reaction Center ◽

Charge Separation ◽

Rational Design ◽

De Novo ◽

Metal Cluster ◽

Protein Structures ◽

Essential Elements ◽

Reaction Centers ◽

Transient Absorption Spectroscopy

Abstract Natural photosynthetic protein complexes capture sunlight to power the energetic catalysis that supports life on Earth. Yet these natural protein structures carry an evolutionary legacy of complexity and fragility that encumbers protein reengineering efforts and obfuscates the underlying design rules for light-driven charge separation. De novo development of a simplified photosynthetic reaction center protein can clarify practical engineering principles needed to build new enzymes for efficient solar-to-fuel energy conversion. Here we report the rational design, X-ray crystal structure, and electron transfer activity of a multi-cofactor protein that incorporates essential elements of photosynthetic reaction centers. This highly stable, modular artificial protein framework can be reconstituted in vitro with interchangeable redox centers for nanometer-scale photochemical charge separation. Transient absorption spectroscopy demonstrates Photosystem II-like tyrosine and metal cluster oxidation, and we measure charge separation lifetimes exceeding 100 ms, ideal for light-activated catalysis. This de novo-designed reaction center builds upon engineering guidelines established for charge separation in earlier synthetic photochemical triads and modified natural proteins, and it shows how synthetic biology may lead to a new generation of genetically encoded, light-powered catalysts for solar fuel production.

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Access to Primary Charge Separation Mechanism in Photosynthetic Reaction Centers: Anisotropic Excitation Spectra of Electric Field Modulated Fluorescence Yields

Zeitschrift für Naturforschung A ◽

10.1515/zna-1990-0601 ◽

1990 ◽

Vol 45 (6) ◽

pp. 763-770 ◽

Cited By ~ 5

Author(s):

U. Eberl

Keyword(s):

Electron Transfer ◽

Electric Field ◽

Radical Pair ◽

Primary Electron ◽

Reaction Centers ◽

Separation Mechanism ◽

Primary Charge Separation ◽

Excitation Spectra ◽

Primary Radical ◽

Primary Radical Pair

AbstractTwo-step sequential and unistep, superexchange primary electron transfer form primary radical pair states which differ in the direction and magnitude of their dipole moments as revealed in the X-ray structure analysis. The direction can be measured by the excitation anisotropy of electric field induced changes of the fluorescence yield. This method determines angles between the dipole of the primary radical pair and photoselected transition moments (in absorption and emission) of cofactors in the reaction centers. Transitions particularly favourable for discrimination between the two models of primary electron transfer are discussed.

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