Electron transfer from the A1A and A1B sites to a tethered Pt nanoparticle requires the FeS clusters for suppression of the recombination channel

Michael Gorka, Adam Perez, Carol S. Baker, Bryan Ferlez, Art Van Der Est, Donald A. Bryant, John H. Golbeck

Research output: Contribution to journalArticle

4 Citations (Scopus)

Abstract

In this work, a previously described model of electron withdrawal from the A1A/A1B sites of Photosystem I (PS I) was tested using a dihydrogen-producing PS I-NQ(CH2)15S-Pt nanoconstruct. According to this model, the rate of electron transfer from A1A/A1B to a tethered Pt nanoparticle is kinetically unfavorable relative to the rate of forward electron transfer to the FeS clusters. Dihydrogen is produced only when an external donor rapidly reduces P700+, thereby suppressing the recombination channel and allowing the electron in the FeS clusters to proceed via uphill electron transfer through the A1A/A1B quinones to the Pt nanoparticle. We tested this model by sequentially removing the FeS clusters, FB, FA, and FX, and determining the concentration of cytochrome c6 (Cyt c6) at which the backreaction was outcompeted and dihydrogen production was observed. P700-FA cores were generated in a menB insertionally inactivated strain by removing FB with HgCl2; P700-FX cores were generated in a menB psaC insertionally inactivated strain that lacks FA and FB, and P700-A1 cores were generated in a menB rubA insertionally inactivated strain that lacks FX, FA and FB. Quinone incorporation was measured using transient electron paramagnetic resonance spectroscopy and time resolved optical spectroscopy. Cyt c6 was titrated into each of these PS I preparations and the kinetics of P700+ reduction were measured. A similar experiment was carried out on PS I-NQ(CH2)15S-Pt nanoconstructs assembled from these PS I preparations. This study showed that the concentration of Cyt c6 needed to produce dihydrogen was comparable to that needed to suppress the backreaction. We conclude that the FeS clusters serve to 'park' the electron and thereby extend the duration of the charge-separated state; however, in doing so, the redox advantage of removing the electron at A1A/A1B is lost.

Original languageEnglish (US)
Pages (from-to)325-334
Number of pages10
JournalJournal of Photochemistry and Photobiology B: Biology
Volume152
DOIs
StatePublished - Nov 1 2015

Fingerprint

Photosystem I Protein Complex
Nanoparticles
Genetic Recombination
cytochromes
electron transfer
Cytochromes c6
retarding
Electrons
nanoparticles
quinones
electrons
preparation
Spectrum Analysis
spectroscopy
electron paramagnetic resonance
Quinones
Mercuric Chloride
Electron Spin Resonance Spectroscopy
kinetics
Oxidation-Reduction

All Science Journal Classification (ASJC) codes

  • Radiation
  • Radiological and Ultrasound Technology
  • Biophysics
  • Radiology Nuclear Medicine and imaging

Cite this

@article{55ebf663053047c2b54caaf6c7b20009,
title = "Electron transfer from the A1A and A1B sites to a tethered Pt nanoparticle requires the FeS clusters for suppression of the recombination channel",
abstract = "In this work, a previously described model of electron withdrawal from the A1A/A1B sites of Photosystem I (PS I) was tested using a dihydrogen-producing PS I-NQ(CH2)15S-Pt nanoconstruct. According to this model, the rate of electron transfer from A1A/A1B to a tethered Pt nanoparticle is kinetically unfavorable relative to the rate of forward electron transfer to the FeS clusters. Dihydrogen is produced only when an external donor rapidly reduces P700+, thereby suppressing the recombination channel and allowing the electron in the FeS clusters to proceed via uphill electron transfer through the A1A/A1B quinones to the Pt nanoparticle. We tested this model by sequentially removing the FeS clusters, FB, FA, and FX, and determining the concentration of cytochrome c6 (Cyt c6) at which the backreaction was outcompeted and dihydrogen production was observed. P700-FA cores were generated in a menB insertionally inactivated strain by removing FB with HgCl2; P700-FX cores were generated in a menB psaC insertionally inactivated strain that lacks FA and FB, and P700-A1 cores were generated in a menB rubA insertionally inactivated strain that lacks FX, FA and FB. Quinone incorporation was measured using transient electron paramagnetic resonance spectroscopy and time resolved optical spectroscopy. Cyt c6 was titrated into each of these PS I preparations and the kinetics of P700+ reduction were measured. A similar experiment was carried out on PS I-NQ(CH2)15S-Pt nanoconstructs assembled from these PS I preparations. This study showed that the concentration of Cyt c6 needed to produce dihydrogen was comparable to that needed to suppress the backreaction. We conclude that the FeS clusters serve to 'park' the electron and thereby extend the duration of the charge-separated state; however, in doing so, the redox advantage of removing the electron at A1A/A1B is lost.",
author = "Michael Gorka and Adam Perez and Baker, {Carol S.} and Bryan Ferlez and {Van Der Est}, Art and Bryant, {Donald A.} and Golbeck, {John H.}",
year = "2015",
month = "11",
day = "1",
doi = "10.1016/j.jphotobiol.2015.08.015",
language = "English (US)",
volume = "152",
pages = "325--334",
journal = "Journal of Photochemistry and Photobiology B: Biology",
issn = "1011-1344",
publisher = "Elsevier",

}

TY - JOUR

T1 - Electron transfer from the A1A and A1B sites to a tethered Pt nanoparticle requires the FeS clusters for suppression of the recombination channel

AU - Gorka, Michael

AU - Perez, Adam

AU - Baker, Carol S.

AU - Ferlez, Bryan

AU - Van Der Est, Art

AU - Bryant, Donald A.

AU - Golbeck, John H.

PY - 2015/11/1

Y1 - 2015/11/1

N2 - In this work, a previously described model of electron withdrawal from the A1A/A1B sites of Photosystem I (PS I) was tested using a dihydrogen-producing PS I-NQ(CH2)15S-Pt nanoconstruct. According to this model, the rate of electron transfer from A1A/A1B to a tethered Pt nanoparticle is kinetically unfavorable relative to the rate of forward electron transfer to the FeS clusters. Dihydrogen is produced only when an external donor rapidly reduces P700+, thereby suppressing the recombination channel and allowing the electron in the FeS clusters to proceed via uphill electron transfer through the A1A/A1B quinones to the Pt nanoparticle. We tested this model by sequentially removing the FeS clusters, FB, FA, and FX, and determining the concentration of cytochrome c6 (Cyt c6) at which the backreaction was outcompeted and dihydrogen production was observed. P700-FA cores were generated in a menB insertionally inactivated strain by removing FB with HgCl2; P700-FX cores were generated in a menB psaC insertionally inactivated strain that lacks FA and FB, and P700-A1 cores were generated in a menB rubA insertionally inactivated strain that lacks FX, FA and FB. Quinone incorporation was measured using transient electron paramagnetic resonance spectroscopy and time resolved optical spectroscopy. Cyt c6 was titrated into each of these PS I preparations and the kinetics of P700+ reduction were measured. A similar experiment was carried out on PS I-NQ(CH2)15S-Pt nanoconstructs assembled from these PS I preparations. This study showed that the concentration of Cyt c6 needed to produce dihydrogen was comparable to that needed to suppress the backreaction. We conclude that the FeS clusters serve to 'park' the electron and thereby extend the duration of the charge-separated state; however, in doing so, the redox advantage of removing the electron at A1A/A1B is lost.

AB - In this work, a previously described model of electron withdrawal from the A1A/A1B sites of Photosystem I (PS I) was tested using a dihydrogen-producing PS I-NQ(CH2)15S-Pt nanoconstruct. According to this model, the rate of electron transfer from A1A/A1B to a tethered Pt nanoparticle is kinetically unfavorable relative to the rate of forward electron transfer to the FeS clusters. Dihydrogen is produced only when an external donor rapidly reduces P700+, thereby suppressing the recombination channel and allowing the electron in the FeS clusters to proceed via uphill electron transfer through the A1A/A1B quinones to the Pt nanoparticle. We tested this model by sequentially removing the FeS clusters, FB, FA, and FX, and determining the concentration of cytochrome c6 (Cyt c6) at which the backreaction was outcompeted and dihydrogen production was observed. P700-FA cores were generated in a menB insertionally inactivated strain by removing FB with HgCl2; P700-FX cores were generated in a menB psaC insertionally inactivated strain that lacks FA and FB, and P700-A1 cores were generated in a menB rubA insertionally inactivated strain that lacks FX, FA and FB. Quinone incorporation was measured using transient electron paramagnetic resonance spectroscopy and time resolved optical spectroscopy. Cyt c6 was titrated into each of these PS I preparations and the kinetics of P700+ reduction were measured. A similar experiment was carried out on PS I-NQ(CH2)15S-Pt nanoconstructs assembled from these PS I preparations. This study showed that the concentration of Cyt c6 needed to produce dihydrogen was comparable to that needed to suppress the backreaction. We conclude that the FeS clusters serve to 'park' the electron and thereby extend the duration of the charge-separated state; however, in doing so, the redox advantage of removing the electron at A1A/A1B is lost.

UR - http://www.scopus.com/inward/record.url?scp=84947708660&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84947708660&partnerID=8YFLogxK

U2 - 10.1016/j.jphotobiol.2015.08.015

DO - 10.1016/j.jphotobiol.2015.08.015

M3 - Article

C2 - 26541876

AN - SCOPUS:84947708660

VL - 152

SP - 325

EP - 334

JO - Journal of Photochemistry and Photobiology B: Biology

JF - Journal of Photochemistry and Photobiology B: Biology

SN - 1011-1344

ER -