Limits...
Hyperfine and nuclear quadrupole tensors of nitrogen donors in the Q(A) site of bacterial reaction centers: correlation of the histidine N(δ) tensors with hydrogen bond strength.

Taguchi AT, O'Malley PJ, Wraight CA, Dikanov SA - J Phys Chem B (2014)

Bottom Line: The hyperfine coupling constants were found to be a((14)N) = 2.3 MHz, T = 0.3 MHz for His-M219 Nδ and a((14)N) = 2.6 MHz, T = 0.3 MHz for Ala-M260 Np.Despite that His-M219 Nδ is established as the stronger of the two H-bond donors, Ala-M260 Np is found to have the larger value of a((14)N).An analysis of the available data on nuclear quadrupole tensors for imidazole nitrogens found in semiquinone-binding proteins and copper complexes reveals these systems share similar electron occupancies of the protonated nitrogen orbitals.

View Article: PubMed Central - PubMed

Affiliation: Center for Biophysics and Computational Biology, §Department of Biochemistry, and ∥Department of Veterinary Clinical Medicine, University of Illinois at Urbana-Champaign , Urbana, Illinois 61801, United States.

ABSTRACT
X- and Q-band pulsed EPR spectroscopy was applied to study the interaction of the QA site semiquinone (SQA) with nitrogens from the local protein environment in natural abundance (14)N and in (15)N uniformly labeled photosynthetic reaction centers of Rhodobacter sphaeroides. The hyperfine and nuclear quadrupole tensors for His-M219 Nδ and Ala-M260 peptide nitrogen (Np) were estimated through simultaneous simulation of the Q-band (15)N Davies ENDOR, X- and Q-band (14,15)N HYSCORE, and X-band (14)N three-pulse ESEEM spectra, with support from DFT calculations. The hyperfine coupling constants were found to be a((14)N) = 2.3 MHz, T = 0.3 MHz for His-M219 Nδ and a((14)N) = 2.6 MHz, T = 0.3 MHz for Ala-M260 Np. Despite that His-M219 Nδ is established as the stronger of the two H-bond donors, Ala-M260 Np is found to have the larger value of a((14)N). The nuclear quadrupole coupling constants were estimated as e(2)Qq/4h = 0.38 MHz, η = 0.97 and e(2)Qq/4h = 0.74 MHz, η = 0.59 for His-M219 Nδ and Ala-M260 Np, respectively. An analysis of the available data on nuclear quadrupole tensors for imidazole nitrogens found in semiquinone-binding proteins and copper complexes reveals these systems share similar electron occupancies of the protonated nitrogen orbitals. By applying the Townes-Dailey model, developed previously for copper complexes, to the semiquinones, we find the asymmetry parameter η to be a sensitive probe of the histidine Nδ-semiquinone hydrogen bond strength. This is supported by a strong correlation observed between η and the isotropic coupling constant a((14)N) and is consistent with previous computational works and our own semiquinone-histidine model calculations. The empirical relationship presented here for a((14)N) and η will provide an important structural characterization tool in future studies of semiquinone-binding proteins.

Show MeSH
Correlation between a(14N) and ηfor the semiquinone Nδ data in Table 3: (1) QARb. sphaeroides; (2) QARp. viridis; (3)QA PSII; (4) QBRb. sphaeroides; (5) QD NarGHI. The linear fit to the Nδ data (dashed line) is described by a(14N) = 3.23η – 0.74 (MHz).
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4126732&req=5

fig10: Correlation between a(14N) and ηfor the semiquinone Nδ data in Table 3: (1) QARb. sphaeroides; (2) QARp. viridis; (3)QA PSII; (4) QBRb. sphaeroides; (5) QD NarGHI. The linear fit to the Nδ data (dashed line) is described by a(14N) = 3.23η – 0.74 (MHz).

Mentions: The isotropic hyperfine constant a(14N) for the histidine Nδ nitrogensfrom Table 3 is plotted as a function of ηin Figure 10. A remarkably good linear correlationis observedfor all quinone sites considered. A larger hyperfine coupling (indicativeof a stronger hydrogen bond) is found to correlate with a larger valueof η. Because His-M219 Nδ of SQA (Rb. sphaeroides) has the largestvalue of a(14N), the other semiquinonesare likely engaged in weaker hydrogen bonding with the histidine.Therefore, the nqi tensors for the other semiquinone data in Table 3 can be assigned as having Qmax oriented perpendicular to the imidazole plane, in accordancewith the calculations of Fritscher described above.32 This nqi tensor orientation is consistent with that determinedpreviously for the copper diene-substituted imidazole model compoundsand copper proteins (plotted alongside the semiquinone data in Figure 9).17


Hyperfine and nuclear quadrupole tensors of nitrogen donors in the Q(A) site of bacterial reaction centers: correlation of the histidine N(δ) tensors with hydrogen bond strength.

Taguchi AT, O'Malley PJ, Wraight CA, Dikanov SA - J Phys Chem B (2014)

Correlation between a(14N) and ηfor the semiquinone Nδ data in Table 3: (1) QARb. sphaeroides; (2) QARp. viridis; (3)QA PSII; (4) QBRb. sphaeroides; (5) QD NarGHI. The linear fit to the Nδ data (dashed line) is described by a(14N) = 3.23η – 0.74 (MHz).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4126732&req=5

fig10: Correlation between a(14N) and ηfor the semiquinone Nδ data in Table 3: (1) QARb. sphaeroides; (2) QARp. viridis; (3)QA PSII; (4) QBRb. sphaeroides; (5) QD NarGHI. The linear fit to the Nδ data (dashed line) is described by a(14N) = 3.23η – 0.74 (MHz).
Mentions: The isotropic hyperfine constant a(14N) for the histidine Nδ nitrogensfrom Table 3 is plotted as a function of ηin Figure 10. A remarkably good linear correlationis observedfor all quinone sites considered. A larger hyperfine coupling (indicativeof a stronger hydrogen bond) is found to correlate with a larger valueof η. Because His-M219 Nδ of SQA (Rb. sphaeroides) has the largestvalue of a(14N), the other semiquinonesare likely engaged in weaker hydrogen bonding with the histidine.Therefore, the nqi tensors for the other semiquinone data in Table 3 can be assigned as having Qmax oriented perpendicular to the imidazole plane, in accordancewith the calculations of Fritscher described above.32 This nqi tensor orientation is consistent with that determinedpreviously for the copper diene-substituted imidazole model compoundsand copper proteins (plotted alongside the semiquinone data in Figure 9).17

Bottom Line: The hyperfine coupling constants were found to be a((14)N) = 2.3 MHz, T = 0.3 MHz for His-M219 Nδ and a((14)N) = 2.6 MHz, T = 0.3 MHz for Ala-M260 Np.Despite that His-M219 Nδ is established as the stronger of the two H-bond donors, Ala-M260 Np is found to have the larger value of a((14)N).An analysis of the available data on nuclear quadrupole tensors for imidazole nitrogens found in semiquinone-binding proteins and copper complexes reveals these systems share similar electron occupancies of the protonated nitrogen orbitals.

View Article: PubMed Central - PubMed

Affiliation: Center for Biophysics and Computational Biology, §Department of Biochemistry, and ∥Department of Veterinary Clinical Medicine, University of Illinois at Urbana-Champaign , Urbana, Illinois 61801, United States.

ABSTRACT
X- and Q-band pulsed EPR spectroscopy was applied to study the interaction of the QA site semiquinone (SQA) with nitrogens from the local protein environment in natural abundance (14)N and in (15)N uniformly labeled photosynthetic reaction centers of Rhodobacter sphaeroides. The hyperfine and nuclear quadrupole tensors for His-M219 Nδ and Ala-M260 peptide nitrogen (Np) were estimated through simultaneous simulation of the Q-band (15)N Davies ENDOR, X- and Q-band (14,15)N HYSCORE, and X-band (14)N three-pulse ESEEM spectra, with support from DFT calculations. The hyperfine coupling constants were found to be a((14)N) = 2.3 MHz, T = 0.3 MHz for His-M219 Nδ and a((14)N) = 2.6 MHz, T = 0.3 MHz for Ala-M260 Np. Despite that His-M219 Nδ is established as the stronger of the two H-bond donors, Ala-M260 Np is found to have the larger value of a((14)N). The nuclear quadrupole coupling constants were estimated as e(2)Qq/4h = 0.38 MHz, η = 0.97 and e(2)Qq/4h = 0.74 MHz, η = 0.59 for His-M219 Nδ and Ala-M260 Np, respectively. An analysis of the available data on nuclear quadrupole tensors for imidazole nitrogens found in semiquinone-binding proteins and copper complexes reveals these systems share similar electron occupancies of the protonated nitrogen orbitals. By applying the Townes-Dailey model, developed previously for copper complexes, to the semiquinones, we find the asymmetry parameter η to be a sensitive probe of the histidine Nδ-semiquinone hydrogen bond strength. This is supported by a strong correlation observed between η and the isotropic coupling constant a((14)N) and is consistent with previous computational works and our own semiquinone-histidine model calculations. The empirical relationship presented here for a((14)N) and η will provide an important structural characterization tool in future studies of semiquinone-binding proteins.

Show MeSH