Probing M-branch electron transfer and cofactor environment in the bacterial photosynthetic reaction center by addition of a hydrogen bond to the M-side bacteriopheophytin

Christine Kirmaier, Agnes Cua, Chunyan He, Dewey Holten, David F. Bocian

    Research output: Contribution to journalArticle

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    Abstract

    Subpicosecond time-resolved absorption and steady-state resonance Raman (RR) studies are reported for Rhodobacter capsulatus reaction centers (RCs) that incorporate an Asp in place of Val M131 near the ring V keto group of the M-side bacteriopheophytin (BPhM). The L-side C2-symmetry analogue of residue M131 is Glu L104, which is known to form a hydrogen bond to the ring V keto group of BPhL in the wild-type RC. The effects of the V(M 131)D mutation were probed in the triple mutant V(M131)D/G(M201)D/L(M212)H, which also incorporates an Asp at M201 near the L-side bacteriochlorophyll (BChlL) as well as the "beta" mutation L(M212)H that results in replacement of the native BPhL with a BChl molecule (denoted β). The primary photochemistry in the triple mutant (denoted V(M131)D-DH) is similar to that reported previously for the G(M201)D/L(M212)H double mutant (denoted DH). Upon excitation, P* decays with a time constant of 15 ps via a combination of electron transfer to the L side (70%), decay to the ground state (15%), and electron transfer to the M side to form P+BPhM- (15%). The bleaching of the QX ground-state absorption band of BPhM observed upon formation of P+BPhM- is red shifted 1-2 nm from ∼527 nm in the DH RC to ∼529 nm in the V(M131)D-DH mutant, and the BPhM anion band is shifted 20 nm from 645 to 665 nm. RR experiments reveal that the ring V keto vibration of BPhM at 1705 cm-1 in the wild-type RC downshifts to 1697 cm-1 in the V(M131)D mutant. Collectively, these results indicate that the Asp introduced at M131 forms a hydrogen bond to the ring V keto group of BPhM in both ground (neutral) and anionic states of this cofactor, and further demonstrate that M-side electron transfer to form P+BPhM- occurs in both mutants. Comparison of the effects engendered by the addition of the hydrogen to BPhM with those found previously upon removal of the Glu L104 hydrogen bond to BPhL give insights into specific and global effects of the protein on the properties of these symmetry-related cofactors.

    Original languageEnglish (US)
    Pages (from-to)495-503
    Number of pages9
    JournalJournal of Physical Chemistry B
    Volume106
    Issue number2
    DOIs
    StatePublished - Jan 17 2002

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    Photosynthetic Reaction Center Complex Proteins
    Hydrogen bonds
    electron transfer
    hydrogen bonds
    Ground state
    Electrons
    Bacteriochlorophylls
    Photochemical reactions
    rings
    mutations
    Bleaching
    Vibrations (mechanical)
    Anions
    Absorption spectra
    Hydrogen
    Negative ions
    Proteins
    Molecules
    ground state
    symmetry

    ASJC Scopus subject areas

    • Physical and Theoretical Chemistry
    • Surfaces, Coatings and Films
    • Materials Chemistry

    Cite this

    Probing M-branch electron transfer and cofactor environment in the bacterial photosynthetic reaction center by addition of a hydrogen bond to the M-side bacteriopheophytin. / Kirmaier, Christine; Cua, Agnes; He, Chunyan; Holten, Dewey; Bocian, David F.

    In: Journal of Physical Chemistry B, Vol. 106, No. 2, 17.01.2002, p. 495-503.

    Research output: Contribution to journalArticle

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    abstract = "Subpicosecond time-resolved absorption and steady-state resonance Raman (RR) studies are reported for Rhodobacter capsulatus reaction centers (RCs) that incorporate an Asp in place of Val M131 near the ring V keto group of the M-side bacteriopheophytin (BPhM). The L-side C2-symmetry analogue of residue M131 is Glu L104, which is known to form a hydrogen bond to the ring V keto group of BPhL in the wild-type RC. The effects of the V(M 131)D mutation were probed in the triple mutant V(M131)D/G(M201)D/L(M212)H, which also incorporates an Asp at M201 near the L-side bacteriochlorophyll (BChlL) as well as the {"}beta{"} mutation L(M212)H that results in replacement of the native BPhL with a BChl molecule (denoted β). The primary photochemistry in the triple mutant (denoted V(M131)D-DH) is similar to that reported previously for the G(M201)D/L(M212)H double mutant (denoted DH). Upon excitation, P* decays with a time constant of 15 ps via a combination of electron transfer to the L side (70{\%}), decay to the ground state (15{\%}), and electron transfer to the M side to form P+BPhM- (15{\%}). The bleaching of the QX ground-state absorption band of BPhM observed upon formation of P+BPhM- is red shifted 1-2 nm from ∼527 nm in the DH RC to ∼529 nm in the V(M131)D-DH mutant, and the BPhM anion band is shifted 20 nm from 645 to 665 nm. RR experiments reveal that the ring V keto vibration of BPhM at 1705 cm-1 in the wild-type RC downshifts to 1697 cm-1 in the V(M131)D mutant. Collectively, these results indicate that the Asp introduced at M131 forms a hydrogen bond to the ring V keto group of BPhM in both ground (neutral) and anionic states of this cofactor, and further demonstrate that M-side electron transfer to form P+BPhM- occurs in both mutants. Comparison of the effects engendered by the addition of the hydrogen to BPhM with those found previously upon removal of the Glu L104 hydrogen bond to BPhL give insights into specific and global effects of the protein on the properties of these symmetry-related cofactors.",
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    T1 - Probing M-branch electron transfer and cofactor environment in the bacterial photosynthetic reaction center by addition of a hydrogen bond to the M-side bacteriopheophytin

    AU - Kirmaier, Christine

    AU - Cua, Agnes

    AU - He, Chunyan

    AU - Holten, Dewey

    AU - Bocian, David F.

    PY - 2002/1/17

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    N2 - Subpicosecond time-resolved absorption and steady-state resonance Raman (RR) studies are reported for Rhodobacter capsulatus reaction centers (RCs) that incorporate an Asp in place of Val M131 near the ring V keto group of the M-side bacteriopheophytin (BPhM). The L-side C2-symmetry analogue of residue M131 is Glu L104, which is known to form a hydrogen bond to the ring V keto group of BPhL in the wild-type RC. The effects of the V(M 131)D mutation were probed in the triple mutant V(M131)D/G(M201)D/L(M212)H, which also incorporates an Asp at M201 near the L-side bacteriochlorophyll (BChlL) as well as the "beta" mutation L(M212)H that results in replacement of the native BPhL with a BChl molecule (denoted β). The primary photochemistry in the triple mutant (denoted V(M131)D-DH) is similar to that reported previously for the G(M201)D/L(M212)H double mutant (denoted DH). Upon excitation, P* decays with a time constant of 15 ps via a combination of electron transfer to the L side (70%), decay to the ground state (15%), and electron transfer to the M side to form P+BPhM- (15%). The bleaching of the QX ground-state absorption band of BPhM observed upon formation of P+BPhM- is red shifted 1-2 nm from ∼527 nm in the DH RC to ∼529 nm in the V(M131)D-DH mutant, and the BPhM anion band is shifted 20 nm from 645 to 665 nm. RR experiments reveal that the ring V keto vibration of BPhM at 1705 cm-1 in the wild-type RC downshifts to 1697 cm-1 in the V(M131)D mutant. Collectively, these results indicate that the Asp introduced at M131 forms a hydrogen bond to the ring V keto group of BPhM in both ground (neutral) and anionic states of this cofactor, and further demonstrate that M-side electron transfer to form P+BPhM- occurs in both mutants. Comparison of the effects engendered by the addition of the hydrogen to BPhM with those found previously upon removal of the Glu L104 hydrogen bond to BPhL give insights into specific and global effects of the protein on the properties of these symmetry-related cofactors.

    AB - Subpicosecond time-resolved absorption and steady-state resonance Raman (RR) studies are reported for Rhodobacter capsulatus reaction centers (RCs) that incorporate an Asp in place of Val M131 near the ring V keto group of the M-side bacteriopheophytin (BPhM). The L-side C2-symmetry analogue of residue M131 is Glu L104, which is known to form a hydrogen bond to the ring V keto group of BPhL in the wild-type RC. The effects of the V(M 131)D mutation were probed in the triple mutant V(M131)D/G(M201)D/L(M212)H, which also incorporates an Asp at M201 near the L-side bacteriochlorophyll (BChlL) as well as the "beta" mutation L(M212)H that results in replacement of the native BPhL with a BChl molecule (denoted β). The primary photochemistry in the triple mutant (denoted V(M131)D-DH) is similar to that reported previously for the G(M201)D/L(M212)H double mutant (denoted DH). Upon excitation, P* decays with a time constant of 15 ps via a combination of electron transfer to the L side (70%), decay to the ground state (15%), and electron transfer to the M side to form P+BPhM- (15%). The bleaching of the QX ground-state absorption band of BPhM observed upon formation of P+BPhM- is red shifted 1-2 nm from ∼527 nm in the DH RC to ∼529 nm in the V(M131)D-DH mutant, and the BPhM anion band is shifted 20 nm from 645 to 665 nm. RR experiments reveal that the ring V keto vibration of BPhM at 1705 cm-1 in the wild-type RC downshifts to 1697 cm-1 in the V(M131)D mutant. Collectively, these results indicate that the Asp introduced at M131 forms a hydrogen bond to the ring V keto group of BPhM in both ground (neutral) and anionic states of this cofactor, and further demonstrate that M-side electron transfer to form P+BPhM- occurs in both mutants. Comparison of the effects engendered by the addition of the hydrogen to BPhM with those found previously upon removal of the Glu L104 hydrogen bond to BPhL give insights into specific and global effects of the protein on the properties of these symmetry-related cofactors.

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