Mn(II) Binding and Subsequent Oxidation by the Multicopper Oxidase MnxG Investigated by Electron Paramagnetic Resonance Spectroscopy

Lizhi Tao, Troy A. Stich, Cristina N. Butterfield, Christine A. Romano, Thomas G. Spiro, Bradley Tebo, William H. Casey, R. David Britt

Research output: Contribution to journalArticle

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Abstract

The dynamics of manganese solid formation (as MnOx) by the multicopper oxidase (MCO)-containing Mnx protein complex were examined by electron paramagnetic resonance (EPR) spectroscopy. Continuous-wave (CW) EPR spectra of samples of Mnx, prepared in atmosphere and then reacted with Mn(II) for times ranging from 7 to 600 s, indicate rapid oxidation of the substrate manganese (with two-phase pseudo-first-order kinetics modeled using rate coefficients of: k1obs = 0.205 ± 0.001 s-1 and k2obs = 0.019 ± 0.001 s-1). This process occurs on approximately the same time scale as in vitro solid MnOx formation when there is a large excess of Mn(II). We also found CW and pulse EPR spectroscopic evidence for at least three classes of Mn(II)-containing species in the reaction mixtures: (i) aqueous Mn(II), (ii) a specifically bound mononuclear Mn(II) ion coordinated to the Mnx complex by one nitrogenous ligand, and (iii) a weakly exchange-coupled dimeric Mn(II) species. These findings provide new insights into the molecular mechanism of manganese mineralization.

Original languageEnglish (US)
Pages (from-to)10563-10575
Number of pages13
JournalJournal of the American Chemical Society
Volume137
Issue number33
DOIs
StatePublished - Aug 5 2015
Externally publishedYes

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Electron Spin Resonance Spectroscopy
Manganese
Paramagnetic resonance
Spectrum Analysis
Oxidoreductases
Spectroscopy
Oxidation
Atmosphere
Ligands
Ions
Proteins
Kinetics
Substrates

ASJC Scopus subject areas

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

Cite this

Mn(II) Binding and Subsequent Oxidation by the Multicopper Oxidase MnxG Investigated by Electron Paramagnetic Resonance Spectroscopy. / Tao, Lizhi; Stich, Troy A.; Butterfield, Cristina N.; Romano, Christine A.; Spiro, Thomas G.; Tebo, Bradley; Casey, William H.; Britt, R. David.

In: Journal of the American Chemical Society, Vol. 137, No. 33, 05.08.2015, p. 10563-10575.

Research output: Contribution to journalArticle

Tao, Lizhi ; Stich, Troy A. ; Butterfield, Cristina N. ; Romano, Christine A. ; Spiro, Thomas G. ; Tebo, Bradley ; Casey, William H. ; Britt, R. David. / Mn(II) Binding and Subsequent Oxidation by the Multicopper Oxidase MnxG Investigated by Electron Paramagnetic Resonance Spectroscopy. In: Journal of the American Chemical Society. 2015 ; Vol. 137, No. 33. pp. 10563-10575.
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abstract = "The dynamics of manganese solid formation (as MnOx) by the multicopper oxidase (MCO)-containing Mnx protein complex were examined by electron paramagnetic resonance (EPR) spectroscopy. Continuous-wave (CW) EPR spectra of samples of Mnx, prepared in atmosphere and then reacted with Mn(II) for times ranging from 7 to 600 s, indicate rapid oxidation of the substrate manganese (with two-phase pseudo-first-order kinetics modeled using rate coefficients of: k1obs = 0.205 ± 0.001 s-1 and k2obs = 0.019 ± 0.001 s-1). This process occurs on approximately the same time scale as in vitro solid MnOx formation when there is a large excess of Mn(II). We also found CW and pulse EPR spectroscopic evidence for at least three classes of Mn(II)-containing species in the reaction mixtures: (i) aqueous Mn(II), (ii) a specifically bound mononuclear Mn(II) ion coordinated to the Mnx complex by one nitrogenous ligand, and (iii) a weakly exchange-coupled dimeric Mn(II) species. These findings provide new insights into the molecular mechanism of manganese mineralization.",
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AU - Romano, Christine A.

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AU - Casey, William H.

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N2 - The dynamics of manganese solid formation (as MnOx) by the multicopper oxidase (MCO)-containing Mnx protein complex were examined by electron paramagnetic resonance (EPR) spectroscopy. Continuous-wave (CW) EPR spectra of samples of Mnx, prepared in atmosphere and then reacted with Mn(II) for times ranging from 7 to 600 s, indicate rapid oxidation of the substrate manganese (with two-phase pseudo-first-order kinetics modeled using rate coefficients of: k1obs = 0.205 ± 0.001 s-1 and k2obs = 0.019 ± 0.001 s-1). This process occurs on approximately the same time scale as in vitro solid MnOx formation when there is a large excess of Mn(II). We also found CW and pulse EPR spectroscopic evidence for at least three classes of Mn(II)-containing species in the reaction mixtures: (i) aqueous Mn(II), (ii) a specifically bound mononuclear Mn(II) ion coordinated to the Mnx complex by one nitrogenous ligand, and (iii) a weakly exchange-coupled dimeric Mn(II) species. These findings provide new insights into the molecular mechanism of manganese mineralization.

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