Single-sided hydrogen bonding to the quinone cofactor in photosystem I probed by selective 13C-labelled naphthoquinones and transient EPR

I. Karyagina, John H. Golbeck, N. Srinivasan, Dietmar Stehlik, H. Zimmermann

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Abstract

Hydrogen bonding between the protein and one or both of the two 1,4-quinone carbonyl groups of a benzo- or naphtho-quinone constitutes a significant protein-cofactor interaction in photosynthetic reaction centers. The redistribution of charge and spin density due to a particular H-bonding scheme leaves the largest hyperfine couplings (hfc) at the highest density positions, i.e., the nuclei of the carbonyl groups directly involved in H-bonding. The spin density changes at the ring carbon positions are accessed experimentally via electron paramagnetic resonance-determined hfc tensor elements of selective 13C isotope labels in one of the two carbonyl groups. Complete hfc tensor data are presented for each of the 13C positions in the functional charge-separated state in reaction centers of photosystem I (PS I) isolated from cyanobacteria. A highly asymmetric H-bonding scheme for the A 1 quinone binding site due to a single dominant H-bond to one carbonyl group is confirmed. A comparison to other well-studied quinone binding sites of other protein-cofactor systems with more complex H-bonding schemes reveals the uniqueness of the PS I site. The single-sided A1 quinone site provides an ideal test case for the various sets of density functional theory (DFT) calculations that are currently available. While the overall agreement between experimental and calculated data is quite satisfactory, a significant discrepancy is found for the high-spin-density 13C position associated with the H-bonded carbonyl. The dominant hfc component (and spin density) is underestimated in the DFT calculations, not only for the high-asymmetry case in PS I, but also for other quinone binding sites with less asymmetry that result from more complex H-bonding schemes. The consequences and potential relevance of this finding for biological function are discussed.

Original languageEnglish (US)
Pages (from-to)287-310
Number of pages24
JournalApplied Magnetic Resonance
Volume30
Issue number3-4
DOIs
StatePublished - Jan 1 2006

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quinones
hydrogen
proteins
asymmetry
tensors
density functional theory
uniqueness
leaves
electron paramagnetic resonance
isotopes
nuclei
carbon
rings
interactions

All Science Journal Classification (ASJC) codes

  • Atomic and Molecular Physics, and Optics

Cite this

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title = "Single-sided hydrogen bonding to the quinone cofactor in photosystem I probed by selective 13C-labelled naphthoquinones and transient EPR",
abstract = "Hydrogen bonding between the protein and one or both of the two 1,4-quinone carbonyl groups of a benzo- or naphtho-quinone constitutes a significant protein-cofactor interaction in photosynthetic reaction centers. The redistribution of charge and spin density due to a particular H-bonding scheme leaves the largest hyperfine couplings (hfc) at the highest density positions, i.e., the nuclei of the carbonyl groups directly involved in H-bonding. The spin density changes at the ring carbon positions are accessed experimentally via electron paramagnetic resonance-determined hfc tensor elements of selective 13C isotope labels in one of the two carbonyl groups. Complete hfc tensor data are presented for each of the 13C positions in the functional charge-separated state in reaction centers of photosystem I (PS I) isolated from cyanobacteria. A highly asymmetric H-bonding scheme for the A 1 quinone binding site due to a single dominant H-bond to one carbonyl group is confirmed. A comparison to other well-studied quinone binding sites of other protein-cofactor systems with more complex H-bonding schemes reveals the uniqueness of the PS I site. The single-sided A1 quinone site provides an ideal test case for the various sets of density functional theory (DFT) calculations that are currently available. While the overall agreement between experimental and calculated data is quite satisfactory, a significant discrepancy is found for the high-spin-density 13C position associated with the H-bonded carbonyl. The dominant hfc component (and spin density) is underestimated in the DFT calculations, not only for the high-asymmetry case in PS I, but also for other quinone binding sites with less asymmetry that result from more complex H-bonding schemes. The consequences and potential relevance of this finding for biological function are discussed.",
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Single-sided hydrogen bonding to the quinone cofactor in photosystem I probed by selective 13C-labelled naphthoquinones and transient EPR. / Karyagina, I.; Golbeck, John H.; Srinivasan, N.; Stehlik, Dietmar; Zimmermann, H.

In: Applied Magnetic Resonance, Vol. 30, No. 3-4, 01.01.2006, p. 287-310.

Research output: Contribution to journalArticle

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T1 - Single-sided hydrogen bonding to the quinone cofactor in photosystem I probed by selective 13C-labelled naphthoquinones and transient EPR

AU - Karyagina, I.

AU - Golbeck, John H.

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AU - Stehlik, Dietmar

AU - Zimmermann, H.

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AB - Hydrogen bonding between the protein and one or both of the two 1,4-quinone carbonyl groups of a benzo- or naphtho-quinone constitutes a significant protein-cofactor interaction in photosynthetic reaction centers. The redistribution of charge and spin density due to a particular H-bonding scheme leaves the largest hyperfine couplings (hfc) at the highest density positions, i.e., the nuclei of the carbonyl groups directly involved in H-bonding. The spin density changes at the ring carbon positions are accessed experimentally via electron paramagnetic resonance-determined hfc tensor elements of selective 13C isotope labels in one of the two carbonyl groups. Complete hfc tensor data are presented for each of the 13C positions in the functional charge-separated state in reaction centers of photosystem I (PS I) isolated from cyanobacteria. A highly asymmetric H-bonding scheme for the A 1 quinone binding site due to a single dominant H-bond to one carbonyl group is confirmed. A comparison to other well-studied quinone binding sites of other protein-cofactor systems with more complex H-bonding schemes reveals the uniqueness of the PS I site. The single-sided A1 quinone site provides an ideal test case for the various sets of density functional theory (DFT) calculations that are currently available. While the overall agreement between experimental and calculated data is quite satisfactory, a significant discrepancy is found for the high-spin-density 13C position associated with the H-bonded carbonyl. The dominant hfc component (and spin density) is underestimated in the DFT calculations, not only for the high-asymmetry case in PS I, but also for other quinone binding sites with less asymmetry that result from more complex H-bonding schemes. The consequences and potential relevance of this finding for biological function are discussed.

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