Independent initiation of primary electron transfer in the two branches of the photosystem I reaction center

Marc G. Müller, Chavdar Slavov, Rajiv Luthra, Kevin Edward Redding, Alfred R. Holzwarth

Research output: Contribution to journalArticle

78 Citations (Scopus)

Abstract

Photosystem I (PSI) is a large pigment-protein complex that unites a reaction center (RC) at the core with ∼100 core antenna chlorophylls surrounding it. The RC is composed of two cofactor branches related by a pseudo-C2 symmetry axis. The ultimate electron donor, P700 (a pair of chlorophylls), and the tertiary acceptor, FX (a Fe4S 4 cluster), are both located on this axis, while each of the two branches is made up of a pair of chlorophylls (ec2 and ec3) and a phylloquinone (PhQ). Based on the observed biphasic reduction of FX, it has been suggested that both branches in PSI are competent for electron transfer (ET), but the nature and rate of the initial electron transfer steps have not been established. We report an ultrafast transient absorption study of Chlamydomonas reinhardtii mutants in which specific amino acids donating H-bonds to the 131-keto oxygen of either ec3A (PsaA-Tyr696) or ec3 B (PsaB-Tyr676) are converted to Phe, thus breaking the H-bond to a specific ec3 cofactor. We find that the rate of primary charge separation (CS) is lowered in both mutants, providing direct evidence that the primary ET event can be initiated independently in each branch. Furthermore, the data provide further support for the previously published model in which the initial CS event occurs within an ec2/ec3 pair, generating a primary ec2+ec3 - radical pair, followed by rapid reduction by P700 in the second ET step. A unique kinetic modeling approach allows estimation of the individual ET rates within the two cofactor branches.

Original languageEnglish
Pages (from-to)4123-4128
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume107
Issue number9
DOIs
Publication statusPublished - Mar 2 2010

Fingerprint

Photosystem I Protein Complex
Electrons
Chlorophyll
Vitamin K 1
Chlamydomonas reinhardtii
Oxygen
Amino Acids
Proteins

Keywords

  • Chlamydomonas
  • Electron transfer directionality
  • Femtosecond absorption
  • Photosystem I
  • Ultrafast spectroscopy

ASJC Scopus subject areas

  • General

Cite this

Independent initiation of primary electron transfer in the two branches of the photosystem I reaction center. / Müller, Marc G.; Slavov, Chavdar; Luthra, Rajiv; Redding, Kevin Edward; Holzwarth, Alfred R.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 107, No. 9, 02.03.2010, p. 4123-4128.

Research output: Contribution to journalArticle

@article{cd017e0ab60747dbbc98d03c7aa36d2b,
title = "Independent initiation of primary electron transfer in the two branches of the photosystem I reaction center",
abstract = "Photosystem I (PSI) is a large pigment-protein complex that unites a reaction center (RC) at the core with ∼100 core antenna chlorophylls surrounding it. The RC is composed of two cofactor branches related by a pseudo-C2 symmetry axis. The ultimate electron donor, P700 (a pair of chlorophylls), and the tertiary acceptor, FX (a Fe4S 4 cluster), are both located on this axis, while each of the two branches is made up of a pair of chlorophylls (ec2 and ec3) and a phylloquinone (PhQ). Based on the observed biphasic reduction of FX, it has been suggested that both branches in PSI are competent for electron transfer (ET), but the nature and rate of the initial electron transfer steps have not been established. We report an ultrafast transient absorption study of Chlamydomonas reinhardtii mutants in which specific amino acids donating H-bonds to the 131-keto oxygen of either ec3A (PsaA-Tyr696) or ec3 B (PsaB-Tyr676) are converted to Phe, thus breaking the H-bond to a specific ec3 cofactor. We find that the rate of primary charge separation (CS) is lowered in both mutants, providing direct evidence that the primary ET event can be initiated independently in each branch. Furthermore, the data provide further support for the previously published model in which the initial CS event occurs within an ec2/ec3 pair, generating a primary ec2+ec3 - radical pair, followed by rapid reduction by P700 in the second ET step. A unique kinetic modeling approach allows estimation of the individual ET rates within the two cofactor branches.",
keywords = "Chlamydomonas, Electron transfer directionality, Femtosecond absorption, Photosystem I, Ultrafast spectroscopy",
author = "M{\"u}ller, {Marc G.} and Chavdar Slavov and Rajiv Luthra and Redding, {Kevin Edward} and Holzwarth, {Alfred R.}",
year = "2010",
month = "3",
day = "2",
doi = "10.1073/pnas.0905407107",
language = "English",
volume = "107",
pages = "4123--4128",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
number = "9",

}

TY - JOUR

T1 - Independent initiation of primary electron transfer in the two branches of the photosystem I reaction center

AU - Müller, Marc G.

AU - Slavov, Chavdar

AU - Luthra, Rajiv

AU - Redding, Kevin Edward

AU - Holzwarth, Alfred R.

PY - 2010/3/2

Y1 - 2010/3/2

N2 - Photosystem I (PSI) is a large pigment-protein complex that unites a reaction center (RC) at the core with ∼100 core antenna chlorophylls surrounding it. The RC is composed of two cofactor branches related by a pseudo-C2 symmetry axis. The ultimate electron donor, P700 (a pair of chlorophylls), and the tertiary acceptor, FX (a Fe4S 4 cluster), are both located on this axis, while each of the two branches is made up of a pair of chlorophylls (ec2 and ec3) and a phylloquinone (PhQ). Based on the observed biphasic reduction of FX, it has been suggested that both branches in PSI are competent for electron transfer (ET), but the nature and rate of the initial electron transfer steps have not been established. We report an ultrafast transient absorption study of Chlamydomonas reinhardtii mutants in which specific amino acids donating H-bonds to the 131-keto oxygen of either ec3A (PsaA-Tyr696) or ec3 B (PsaB-Tyr676) are converted to Phe, thus breaking the H-bond to a specific ec3 cofactor. We find that the rate of primary charge separation (CS) is lowered in both mutants, providing direct evidence that the primary ET event can be initiated independently in each branch. Furthermore, the data provide further support for the previously published model in which the initial CS event occurs within an ec2/ec3 pair, generating a primary ec2+ec3 - radical pair, followed by rapid reduction by P700 in the second ET step. A unique kinetic modeling approach allows estimation of the individual ET rates within the two cofactor branches.

AB - Photosystem I (PSI) is a large pigment-protein complex that unites a reaction center (RC) at the core with ∼100 core antenna chlorophylls surrounding it. The RC is composed of two cofactor branches related by a pseudo-C2 symmetry axis. The ultimate electron donor, P700 (a pair of chlorophylls), and the tertiary acceptor, FX (a Fe4S 4 cluster), are both located on this axis, while each of the two branches is made up of a pair of chlorophylls (ec2 and ec3) and a phylloquinone (PhQ). Based on the observed biphasic reduction of FX, it has been suggested that both branches in PSI are competent for electron transfer (ET), but the nature and rate of the initial electron transfer steps have not been established. We report an ultrafast transient absorption study of Chlamydomonas reinhardtii mutants in which specific amino acids donating H-bonds to the 131-keto oxygen of either ec3A (PsaA-Tyr696) or ec3 B (PsaB-Tyr676) are converted to Phe, thus breaking the H-bond to a specific ec3 cofactor. We find that the rate of primary charge separation (CS) is lowered in both mutants, providing direct evidence that the primary ET event can be initiated independently in each branch. Furthermore, the data provide further support for the previously published model in which the initial CS event occurs within an ec2/ec3 pair, generating a primary ec2+ec3 - radical pair, followed by rapid reduction by P700 in the second ET step. A unique kinetic modeling approach allows estimation of the individual ET rates within the two cofactor branches.

KW - Chlamydomonas

KW - Electron transfer directionality

KW - Femtosecond absorption

KW - Photosystem I

KW - Ultrafast spectroscopy

UR - http://www.scopus.com/inward/record.url?scp=77749233753&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=77749233753&partnerID=8YFLogxK

U2 - 10.1073/pnas.0905407107

DO - 10.1073/pnas.0905407107

M3 - Article

C2 - 20142514

AN - SCOPUS:77749233753

VL - 107

SP - 4123

EP - 4128

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 9

ER -