Effects of hydrogen bonds on the redox potential and electronic structure of the bacterial primary electron donor

Anabella Ivancich, Katie Artz, JoAnn C. Williams, James Paul Allen, Tony A. Mattioli

Research output: Contribution to journalArticle

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Abstract

The primary donor, P, of photosynthetic bacterial reaction centers (RCs) is a dimer of excitonically interacting bacteriochlorophyll (BChl) molecules. The two constituents are named P(L) and P(M) to designate their close association with the L- and M-subunits, respectively, of the RC protein. A series of site-directed mutants of RCs from Rhodobacter sphaeroides has been constructed in order to model the effects of hydrogen bonding on the redox midpoint potential and electronic structure of P. The leucine residue at position M160 was genetically replaced with eight other amino acid residues capable of donating a hydrogen bond to the C9 keto carbonyl group of the P(M) BChl a molecule of P. Fourier transform (FT) (pre)resonance Raman spectroscopy with 1064 nm excitation was used to (i) determine the formation and strengths of hydrogen bonds on this latter keto carbonyl group in the reduced, neutral state (P(o)), and (ii) determine the degree of localization of the positive charge on one of the two constituent BChl molecules of P in its oxidized, radical cation state (P·+). A correlation was observed between the strength of the hydrogen bond and the increase in Po/P·+ redox midpoint potential. This correlation is less pronounced than that observed for another series of RC mutants where hydrogen bonds to the four π- conjugated carbonyl groups of P were broken or formed uniquely involving histidinyl residues [Mattioli, T. A., Lin, X., Allen, J.P. and Williams, J. C. (1995) Biochemistry 34, 6142-6152], indicating that histidinyl residues are more effective in raising the P(o)/P·+ redox midpoint potential via hydrogen bond formation than are other hydrogen bond-forming residues. In addition, an increase in positive charge localization is correlated with the strength of the hydrogen bond and with the Po/P·+ redox midpoint potential. This latter correlation was analyzed using an asymmetric bacteriochlorophyll dimer model based on Huckel-type molecular orbitals in order to obtain estimates of certain energetic parameters of the primary donor. Based on this model, the correlation is extrapolated to the case of complete localization of the positive charge on P(L) and gives a predicted value for the P/P+ redox midpoint potential similar to that experimentally determined for the Rb. sphaeroides HL(M202) heterodimer. The model yields parameters for the highest occupied molecular orbital energies of the two BChl a constituents of P which are typical for the oxidation potential of isolated BChl a in vitro, suggesting that the protein, as compared to many solvents, does not impart atypical redox properties to the BChl a constituents of P.

Original languageEnglish
Pages (from-to)11812-11820
Number of pages9
JournalBiochemistry
Volume37
Issue number34
DOIs
Publication statusPublished - Aug 25 1998

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Bacteriochlorophylls
Bacterial Structures
Oxidation-Reduction
Electronic structure
Hydrogen
Hydrogen bonds
Electrons
Molecular orbitals
Dimers
Molecules
Photosynthetic Reaction Center Complex Proteins
Rhodobacter sphaeroides
Raman Spectrum Analysis
Biochemistry
Fourier Analysis
Hydrogen Bonding
Leucine
Cations
Proteins
Raman spectroscopy

ASJC Scopus subject areas

  • Biochemistry

Cite this

Effects of hydrogen bonds on the redox potential and electronic structure of the bacterial primary electron donor. / Ivancich, Anabella; Artz, Katie; Williams, JoAnn C.; Allen, James Paul; Mattioli, Tony A.

In: Biochemistry, Vol. 37, No. 34, 25.08.1998, p. 11812-11820.

Research output: Contribution to journalArticle

Ivancich, Anabella ; Artz, Katie ; Williams, JoAnn C. ; Allen, James Paul ; Mattioli, Tony A. / Effects of hydrogen bonds on the redox potential and electronic structure of the bacterial primary electron donor. In: Biochemistry. 1998 ; Vol. 37, No. 34. pp. 11812-11820.
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N2 - The primary donor, P, of photosynthetic bacterial reaction centers (RCs) is a dimer of excitonically interacting bacteriochlorophyll (BChl) molecules. The two constituents are named P(L) and P(M) to designate their close association with the L- and M-subunits, respectively, of the RC protein. A series of site-directed mutants of RCs from Rhodobacter sphaeroides has been constructed in order to model the effects of hydrogen bonding on the redox midpoint potential and electronic structure of P. The leucine residue at position M160 was genetically replaced with eight other amino acid residues capable of donating a hydrogen bond to the C9 keto carbonyl group of the P(M) BChl a molecule of P. Fourier transform (FT) (pre)resonance Raman spectroscopy with 1064 nm excitation was used to (i) determine the formation and strengths of hydrogen bonds on this latter keto carbonyl group in the reduced, neutral state (P(o)), and (ii) determine the degree of localization of the positive charge on one of the two constituent BChl molecules of P in its oxidized, radical cation state (P·+). A correlation was observed between the strength of the hydrogen bond and the increase in Po/P·+ redox midpoint potential. This correlation is less pronounced than that observed for another series of RC mutants where hydrogen bonds to the four π- conjugated carbonyl groups of P were broken or formed uniquely involving histidinyl residues [Mattioli, T. A., Lin, X., Allen, J.P. and Williams, J. C. (1995) Biochemistry 34, 6142-6152], indicating that histidinyl residues are more effective in raising the P(o)/P·+ redox midpoint potential via hydrogen bond formation than are other hydrogen bond-forming residues. In addition, an increase in positive charge localization is correlated with the strength of the hydrogen bond and with the Po/P·+ redox midpoint potential. This latter correlation was analyzed using an asymmetric bacteriochlorophyll dimer model based on Huckel-type molecular orbitals in order to obtain estimates of certain energetic parameters of the primary donor. Based on this model, the correlation is extrapolated to the case of complete localization of the positive charge on P(L) and gives a predicted value for the P/P+ redox midpoint potential similar to that experimentally determined for the Rb. sphaeroides HL(M202) heterodimer. The model yields parameters for the highest occupied molecular orbital energies of the two BChl a constituents of P which are typical for the oxidation potential of isolated BChl a in vitro, suggesting that the protein, as compared to many solvents, does not impart atypical redox properties to the BChl a constituents of P.

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