Geometric and electronic structure of the Mn(IV)Fe(III) cofactor in class Ic ribonucleotide reductase: Correlation to the class ia binuclear non-heme iron enzyme

Yeonju Kwak, Wei Jiang, Laura M.K. Dassama, Kiyoung Park, Caleb B. Bell, Lei V. Liu, Shaun D. Wong, Makina Saito, Yasuhiro Kobayashi, Shinji Kitao, Makoto Seto, Yoshitaka Yoda, E. Ercan Alp, Jiyong Zhao, J. Martin Bollinger, Carsten Krebs, Edward I. Solomon

Research output: Contribution to journalArticle

22 Citations (Scopus)

Abstract

The class Ic ribonucleotide reductase (RNR) from Chlamydia trachomatis (Ct) utilizes a Mn/Fe heterobinuclear cofactor, rather than the Fe/Fe cofactor found in the β (R2) subunit of the class Ia enzymes, to react with O 2. This reaction produces a stable MnIVFeIII cofactor that initiates a radical, which transfers to the adjacent α (R1) subunit and reacts with the substrate. We have studied the Mn IVFeIII cofactor using nuclear resonance vibrational spectroscopy (NRVS) and absorption (Abs)/circular dichroism (CD)/magnetic CD (MCD)/variable temperature, variable field (VTVH) MCD spectroscopies to obtain detailed insight into its geometric/electronic structure and to correlate structure with reactivity; NRVS focuses on the FeIII, whereas MCD reflects the spin-allowed transitions mostly on the MnIV. We have evaluated 18 systematically varied structures. Comparison of the simulated NRVS spectra to the experimental data shows that the cofactor has one carboxylate bridge, with MnIV at the site proximal to Phe127. Abs/CD/MCD/VTVH MCD data exhibit 12 transitions that are assigned as d-d and oxo and OH- to metal charge-transfer (CT) transitions. Assignments are based on MCD/Abs intensity ratios, transition energies, polarizations, and derivative-shaped pseudo-A term CT transitions. Correlating these results with TD-DFT calculations defines the MnIVFeIII cofactor as having a μ-oxo, μ-hydroxo core and a terminal hydroxo ligand on the MnIV. From DFT calculations, the MnIV at site 1 is necessary to tune the redox potential to a value similar to that of the tyrosine radical in class Ia RNR, and the OH- terminal ligand on this Mn IV provides a high proton affinity that could gate radical translocation to the α (R1) subunit.

Original languageEnglish (US)
Pages (from-to)17573-17584
Number of pages12
JournalJournal of the American Chemical Society
Volume135
Issue number46
DOIs
StatePublished - Nov 20 2013

Fingerprint

Ribonucleotide Reductases
Vibrational spectroscopy
Dichroism
Electronic structure
Spectrum Analysis
Iron
Enzymes
Circular Dichroism
Discrete Fourier transforms
Charge transfer
Ligands
Protons
Chlamydia trachomatis
Magnetic Fields
Metals
Spectroscopy
Polarization
Magnetic fields
Oxidation-Reduction
Derivatives

All Science Journal Classification (ASJC) codes

  • Catalysis
  • Chemistry(all)
  • Biochemistry
  • Colloid and Surface Chemistry

Cite this

Kwak, Yeonju ; Jiang, Wei ; Dassama, Laura M.K. ; Park, Kiyoung ; Bell, Caleb B. ; Liu, Lei V. ; Wong, Shaun D. ; Saito, Makina ; Kobayashi, Yasuhiro ; Kitao, Shinji ; Seto, Makoto ; Yoda, Yoshitaka ; Alp, E. Ercan ; Zhao, Jiyong ; Bollinger, J. Martin ; Krebs, Carsten ; Solomon, Edward I. / Geometric and electronic structure of the Mn(IV)Fe(III) cofactor in class Ic ribonucleotide reductase : Correlation to the class ia binuclear non-heme iron enzyme. In: Journal of the American Chemical Society. 2013 ; Vol. 135, No. 46. pp. 17573-17584.
@article{29a2077bea61467c9560107d888b18bc,
title = "Geometric and electronic structure of the Mn(IV)Fe(III) cofactor in class Ic ribonucleotide reductase: Correlation to the class ia binuclear non-heme iron enzyme",
abstract = "The class Ic ribonucleotide reductase (RNR) from Chlamydia trachomatis (Ct) utilizes a Mn/Fe heterobinuclear cofactor, rather than the Fe/Fe cofactor found in the β (R2) subunit of the class Ia enzymes, to react with O 2. This reaction produces a stable MnIVFeIII cofactor that initiates a radical, which transfers to the adjacent α (R1) subunit and reacts with the substrate. We have studied the Mn IVFeIII cofactor using nuclear resonance vibrational spectroscopy (NRVS) and absorption (Abs)/circular dichroism (CD)/magnetic CD (MCD)/variable temperature, variable field (VTVH) MCD spectroscopies to obtain detailed insight into its geometric/electronic structure and to correlate structure with reactivity; NRVS focuses on the FeIII, whereas MCD reflects the spin-allowed transitions mostly on the MnIV. We have evaluated 18 systematically varied structures. Comparison of the simulated NRVS spectra to the experimental data shows that the cofactor has one carboxylate bridge, with MnIV at the site proximal to Phe127. Abs/CD/MCD/VTVH MCD data exhibit 12 transitions that are assigned as d-d and oxo and OH- to metal charge-transfer (CT) transitions. Assignments are based on MCD/Abs intensity ratios, transition energies, polarizations, and derivative-shaped pseudo-A term CT transitions. Correlating these results with TD-DFT calculations defines the MnIVFeIII cofactor as having a μ-oxo, μ-hydroxo core and a terminal hydroxo ligand on the MnIV. From DFT calculations, the MnIV at site 1 is necessary to tune the redox potential to a value similar to that of the tyrosine radical in class Ia RNR, and the OH- terminal ligand on this Mn IV provides a high proton affinity that could gate radical translocation to the α (R1) subunit.",
author = "Yeonju Kwak and Wei Jiang and Dassama, {Laura M.K.} and Kiyoung Park and Bell, {Caleb B.} and Liu, {Lei V.} and Wong, {Shaun D.} and Makina Saito and Yasuhiro Kobayashi and Shinji Kitao and Makoto Seto and Yoshitaka Yoda and Alp, {E. Ercan} and Jiyong Zhao and Bollinger, {J. Martin} and Carsten Krebs and Solomon, {Edward I.}",
year = "2013",
month = "11",
day = "20",
doi = "10.1021/ja409510d",
language = "English (US)",
volume = "135",
pages = "17573--17584",
journal = "Journal of the American Chemical Society",
issn = "0002-7863",
publisher = "American Chemical Society",
number = "46",

}

Kwak, Y, Jiang, W, Dassama, LMK, Park, K, Bell, CB, Liu, LV, Wong, SD, Saito, M, Kobayashi, Y, Kitao, S, Seto, M, Yoda, Y, Alp, EE, Zhao, J, Bollinger, JM, Krebs, C & Solomon, EI 2013, 'Geometric and electronic structure of the Mn(IV)Fe(III) cofactor in class Ic ribonucleotide reductase: Correlation to the class ia binuclear non-heme iron enzyme', Journal of the American Chemical Society, vol. 135, no. 46, pp. 17573-17584. https://doi.org/10.1021/ja409510d

Geometric and electronic structure of the Mn(IV)Fe(III) cofactor in class Ic ribonucleotide reductase : Correlation to the class ia binuclear non-heme iron enzyme. / Kwak, Yeonju; Jiang, Wei; Dassama, Laura M.K.; Park, Kiyoung; Bell, Caleb B.; Liu, Lei V.; Wong, Shaun D.; Saito, Makina; Kobayashi, Yasuhiro; Kitao, Shinji; Seto, Makoto; Yoda, Yoshitaka; Alp, E. Ercan; Zhao, Jiyong; Bollinger, J. Martin; Krebs, Carsten; Solomon, Edward I.

In: Journal of the American Chemical Society, Vol. 135, No. 46, 20.11.2013, p. 17573-17584.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Geometric and electronic structure of the Mn(IV)Fe(III) cofactor in class Ic ribonucleotide reductase

T2 - Correlation to the class ia binuclear non-heme iron enzyme

AU - Kwak, Yeonju

AU - Jiang, Wei

AU - Dassama, Laura M.K.

AU - Park, Kiyoung

AU - Bell, Caleb B.

AU - Liu, Lei V.

AU - Wong, Shaun D.

AU - Saito, Makina

AU - Kobayashi, Yasuhiro

AU - Kitao, Shinji

AU - Seto, Makoto

AU - Yoda, Yoshitaka

AU - Alp, E. Ercan

AU - Zhao, Jiyong

AU - Bollinger, J. Martin

AU - Krebs, Carsten

AU - Solomon, Edward I.

PY - 2013/11/20

Y1 - 2013/11/20

N2 - The class Ic ribonucleotide reductase (RNR) from Chlamydia trachomatis (Ct) utilizes a Mn/Fe heterobinuclear cofactor, rather than the Fe/Fe cofactor found in the β (R2) subunit of the class Ia enzymes, to react with O 2. This reaction produces a stable MnIVFeIII cofactor that initiates a radical, which transfers to the adjacent α (R1) subunit and reacts with the substrate. We have studied the Mn IVFeIII cofactor using nuclear resonance vibrational spectroscopy (NRVS) and absorption (Abs)/circular dichroism (CD)/magnetic CD (MCD)/variable temperature, variable field (VTVH) MCD spectroscopies to obtain detailed insight into its geometric/electronic structure and to correlate structure with reactivity; NRVS focuses on the FeIII, whereas MCD reflects the spin-allowed transitions mostly on the MnIV. We have evaluated 18 systematically varied structures. Comparison of the simulated NRVS spectra to the experimental data shows that the cofactor has one carboxylate bridge, with MnIV at the site proximal to Phe127. Abs/CD/MCD/VTVH MCD data exhibit 12 transitions that are assigned as d-d and oxo and OH- to metal charge-transfer (CT) transitions. Assignments are based on MCD/Abs intensity ratios, transition energies, polarizations, and derivative-shaped pseudo-A term CT transitions. Correlating these results with TD-DFT calculations defines the MnIVFeIII cofactor as having a μ-oxo, μ-hydroxo core and a terminal hydroxo ligand on the MnIV. From DFT calculations, the MnIV at site 1 is necessary to tune the redox potential to a value similar to that of the tyrosine radical in class Ia RNR, and the OH- terminal ligand on this Mn IV provides a high proton affinity that could gate radical translocation to the α (R1) subunit.

AB - The class Ic ribonucleotide reductase (RNR) from Chlamydia trachomatis (Ct) utilizes a Mn/Fe heterobinuclear cofactor, rather than the Fe/Fe cofactor found in the β (R2) subunit of the class Ia enzymes, to react with O 2. This reaction produces a stable MnIVFeIII cofactor that initiates a radical, which transfers to the adjacent α (R1) subunit and reacts with the substrate. We have studied the Mn IVFeIII cofactor using nuclear resonance vibrational spectroscopy (NRVS) and absorption (Abs)/circular dichroism (CD)/magnetic CD (MCD)/variable temperature, variable field (VTVH) MCD spectroscopies to obtain detailed insight into its geometric/electronic structure and to correlate structure with reactivity; NRVS focuses on the FeIII, whereas MCD reflects the spin-allowed transitions mostly on the MnIV. We have evaluated 18 systematically varied structures. Comparison of the simulated NRVS spectra to the experimental data shows that the cofactor has one carboxylate bridge, with MnIV at the site proximal to Phe127. Abs/CD/MCD/VTVH MCD data exhibit 12 transitions that are assigned as d-d and oxo and OH- to metal charge-transfer (CT) transitions. Assignments are based on MCD/Abs intensity ratios, transition energies, polarizations, and derivative-shaped pseudo-A term CT transitions. Correlating these results with TD-DFT calculations defines the MnIVFeIII cofactor as having a μ-oxo, μ-hydroxo core and a terminal hydroxo ligand on the MnIV. From DFT calculations, the MnIV at site 1 is necessary to tune the redox potential to a value similar to that of the tyrosine radical in class Ia RNR, and the OH- terminal ligand on this Mn IV provides a high proton affinity that could gate radical translocation to the α (R1) subunit.

UR - http://www.scopus.com/inward/record.url?scp=84888347732&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84888347732&partnerID=8YFLogxK

U2 - 10.1021/ja409510d

DO - 10.1021/ja409510d

M3 - Article

C2 - 24131208

AN - SCOPUS:84888347732

VL - 135

SP - 17573

EP - 17584

JO - Journal of the American Chemical Society

JF - Journal of the American Chemical Society

SN - 0002-7863

IS - 46

ER -