Mutation of the putative hydrogen-bond donor to P700 of photosystem I

Yajing Li, Marie Gabrielle Lucas, Tatyana Konovalova, Brian Abbott, Fraser MacMillan, Alexander Petrenko, Velautham Sivakumar, Ruili Wang, Gary Hastings, Feifei Gu, Johan Van Tol, Louis Claude Brunel, Russell Timkovich, Fabrice Rappaport, Kevin Edward Redding

Research output: Contribution to journalArticle

28 Citations (Scopus)

Abstract

The primary electron donor of photosystem I (PS1), called P700, is a heterodimer of chlorophyll (Chl) a and a′. The crystal structure of photosystem I reveals that the chlorophyll a′ (PA) could be hydrogen-bonded to the protein via a threonine residue, while the chlorophyll a (PB) does not have such a hydrogen bond. To investigate the influence of this hydrogen bond on P700, PsaA-Thr739 was converted to alanine to remove the H-bond to the 131-keto group of the chlorophyll a′ in Chlamydomonas reinhardtii. The PsaA-T739A mutant was capable of assembling active PS1. Furthermore the mutant PS1 contained approximately one chlorophyll a′ molecule per reaction center, indicating that P 700 was still a Chl a/a′ heterodimer in the mutant. However, the mutation induced several band shifts in the visible P700 + - P700 absorbance difference spectrum. Redox titration of P700 revealed a 60 mV decrease in the P700/P 700+ midpoint potential of the mutant, consistent with loss of a H-bond. Fourier transform infrared (FTIR) spectroscopy indicates that the ground state of P700 is somewhat modified by mutation of ThrA739 to alanine. Comparison of FTIR difference band shifts upon P700 + formation in WT and mutant PS1 suggests that the mutation modifies the charge distribution over the pigments in the P700+ state, with ∼14-18% of the positive charge on PB in WT being relocated onto PA in the mutant. 1H-electron-nuclear double resonance (ENDOR) analysis of the P700+ cation radical was also consistent with a slight redistribution of spin from the PB chlorophyll to PA, as well as some redistribution of spin within the PB chlorophyll. High-field electron paramagnetic resonance (EPR) spectroscopy at 330-GHz was used to resolve the g-tensor of P700+, but no significant differences from wild-type were observed, except for a slight decrease of anisotropy. The mutation did, however, provoke changes in the zero-field splitting parameters of the triplet state of P700 ( 3P700), as determined by EPR. Interestingly, the mutation-induced change in asymmetry of P700 did not cause an observable change in the directionality of electron transfer within PSI.

Original languageEnglish
Pages (from-to)12634-12647
Number of pages14
JournalBiochemistry
Volume43
Issue number39
DOIs
Publication statusPublished - Oct 5 2004

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Photosystem I Protein Complex
Hydrogen
Hydrogen bonds
Mutation
Electron Spin Resonance Spectroscopy
Chlorophyll
Alanine
Paramagnetic resonance
Electrons
Chlamydomonas reinhardtii
Charge distribution
Anisotropy
Fourier Analysis
Fourier Transform Infrared Spectroscopy
Threonine
Titration
Pigments
Ground state
Oxidation-Reduction
Tensors

ASJC Scopus subject areas

  • Biochemistry

Cite this

Li, Y., Lucas, M. G., Konovalova, T., Abbott, B., MacMillan, F., Petrenko, A., ... Redding, K. E. (2004). Mutation of the putative hydrogen-bond donor to P700 of photosystem I. Biochemistry, 43(39), 12634-12647. https://doi.org/10.1021/bi036329p

Mutation of the putative hydrogen-bond donor to P700 of photosystem I. / Li, Yajing; Lucas, Marie Gabrielle; Konovalova, Tatyana; Abbott, Brian; MacMillan, Fraser; Petrenko, Alexander; Sivakumar, Velautham; Wang, Ruili; Hastings, Gary; Gu, Feifei; Van Tol, Johan; Brunel, Louis Claude; Timkovich, Russell; Rappaport, Fabrice; Redding, Kevin Edward.

In: Biochemistry, Vol. 43, No. 39, 05.10.2004, p. 12634-12647.

Research output: Contribution to journalArticle

Li, Y, Lucas, MG, Konovalova, T, Abbott, B, MacMillan, F, Petrenko, A, Sivakumar, V, Wang, R, Hastings, G, Gu, F, Van Tol, J, Brunel, LC, Timkovich, R, Rappaport, F & Redding, KE 2004, 'Mutation of the putative hydrogen-bond donor to P700 of photosystem I', Biochemistry, vol. 43, no. 39, pp. 12634-12647. https://doi.org/10.1021/bi036329p
Li Y, Lucas MG, Konovalova T, Abbott B, MacMillan F, Petrenko A et al. Mutation of the putative hydrogen-bond donor to P700 of photosystem I. Biochemistry. 2004 Oct 5;43(39):12634-12647. https://doi.org/10.1021/bi036329p
Li, Yajing ; Lucas, Marie Gabrielle ; Konovalova, Tatyana ; Abbott, Brian ; MacMillan, Fraser ; Petrenko, Alexander ; Sivakumar, Velautham ; Wang, Ruili ; Hastings, Gary ; Gu, Feifei ; Van Tol, Johan ; Brunel, Louis Claude ; Timkovich, Russell ; Rappaport, Fabrice ; Redding, Kevin Edward. / Mutation of the putative hydrogen-bond donor to P700 of photosystem I. In: Biochemistry. 2004 ; Vol. 43, No. 39. pp. 12634-12647.
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abstract = "The primary electron donor of photosystem I (PS1), called P700, is a heterodimer of chlorophyll (Chl) a and a′. The crystal structure of photosystem I reveals that the chlorophyll a′ (PA) could be hydrogen-bonded to the protein via a threonine residue, while the chlorophyll a (PB) does not have such a hydrogen bond. To investigate the influence of this hydrogen bond on P700, PsaA-Thr739 was converted to alanine to remove the H-bond to the 131-keto group of the chlorophyll a′ in Chlamydomonas reinhardtii. The PsaA-T739A mutant was capable of assembling active PS1. Furthermore the mutant PS1 contained approximately one chlorophyll a′ molecule per reaction center, indicating that P 700 was still a Chl a/a′ heterodimer in the mutant. However, the mutation induced several band shifts in the visible P700 + - P700 absorbance difference spectrum. Redox titration of P700 revealed a 60 mV decrease in the P700/P 700+ midpoint potential of the mutant, consistent with loss of a H-bond. Fourier transform infrared (FTIR) spectroscopy indicates that the ground state of P700 is somewhat modified by mutation of ThrA739 to alanine. Comparison of FTIR difference band shifts upon P700 + formation in WT and mutant PS1 suggests that the mutation modifies the charge distribution over the pigments in the P700+ state, with ∼14-18{\%} of the positive charge on PB in WT being relocated onto PA in the mutant. 1H-electron-nuclear double resonance (ENDOR) analysis of the P700+ cation radical was also consistent with a slight redistribution of spin from the PB chlorophyll to PA, as well as some redistribution of spin within the PB chlorophyll. High-field electron paramagnetic resonance (EPR) spectroscopy at 330-GHz was used to resolve the g-tensor of P700+, but no significant differences from wild-type were observed, except for a slight decrease of anisotropy. The mutation did, however, provoke changes in the zero-field splitting parameters of the triplet state of P700 ( 3P700), as determined by EPR. Interestingly, the mutation-induced change in asymmetry of P700 did not cause an observable change in the directionality of electron transfer within PSI.",
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T1 - Mutation of the putative hydrogen-bond donor to P700 of photosystem I

AU - Li, Yajing

AU - Lucas, Marie Gabrielle

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AU - Abbott, Brian

AU - MacMillan, Fraser

AU - Petrenko, Alexander

AU - Sivakumar, Velautham

AU - Wang, Ruili

AU - Hastings, Gary

AU - Gu, Feifei

AU - Van Tol, Johan

AU - Brunel, Louis Claude

AU - Timkovich, Russell

AU - Rappaport, Fabrice

AU - Redding, Kevin Edward

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N2 - The primary electron donor of photosystem I (PS1), called P700, is a heterodimer of chlorophyll (Chl) a and a′. The crystal structure of photosystem I reveals that the chlorophyll a′ (PA) could be hydrogen-bonded to the protein via a threonine residue, while the chlorophyll a (PB) does not have such a hydrogen bond. To investigate the influence of this hydrogen bond on P700, PsaA-Thr739 was converted to alanine to remove the H-bond to the 131-keto group of the chlorophyll a′ in Chlamydomonas reinhardtii. The PsaA-T739A mutant was capable of assembling active PS1. Furthermore the mutant PS1 contained approximately one chlorophyll a′ molecule per reaction center, indicating that P 700 was still a Chl a/a′ heterodimer in the mutant. However, the mutation induced several band shifts in the visible P700 + - P700 absorbance difference spectrum. Redox titration of P700 revealed a 60 mV decrease in the P700/P 700+ midpoint potential of the mutant, consistent with loss of a H-bond. Fourier transform infrared (FTIR) spectroscopy indicates that the ground state of P700 is somewhat modified by mutation of ThrA739 to alanine. Comparison of FTIR difference band shifts upon P700 + formation in WT and mutant PS1 suggests that the mutation modifies the charge distribution over the pigments in the P700+ state, with ∼14-18% of the positive charge on PB in WT being relocated onto PA in the mutant. 1H-electron-nuclear double resonance (ENDOR) analysis of the P700+ cation radical was also consistent with a slight redistribution of spin from the PB chlorophyll to PA, as well as some redistribution of spin within the PB chlorophyll. High-field electron paramagnetic resonance (EPR) spectroscopy at 330-GHz was used to resolve the g-tensor of P700+, but no significant differences from wild-type were observed, except for a slight decrease of anisotropy. The mutation did, however, provoke changes in the zero-field splitting parameters of the triplet state of P700 ( 3P700), as determined by EPR. Interestingly, the mutation-induced change in asymmetry of P700 did not cause an observable change in the directionality of electron transfer within PSI.

AB - The primary electron donor of photosystem I (PS1), called P700, is a heterodimer of chlorophyll (Chl) a and a′. The crystal structure of photosystem I reveals that the chlorophyll a′ (PA) could be hydrogen-bonded to the protein via a threonine residue, while the chlorophyll a (PB) does not have such a hydrogen bond. To investigate the influence of this hydrogen bond on P700, PsaA-Thr739 was converted to alanine to remove the H-bond to the 131-keto group of the chlorophyll a′ in Chlamydomonas reinhardtii. The PsaA-T739A mutant was capable of assembling active PS1. Furthermore the mutant PS1 contained approximately one chlorophyll a′ molecule per reaction center, indicating that P 700 was still a Chl a/a′ heterodimer in the mutant. However, the mutation induced several band shifts in the visible P700 + - P700 absorbance difference spectrum. Redox titration of P700 revealed a 60 mV decrease in the P700/P 700+ midpoint potential of the mutant, consistent with loss of a H-bond. Fourier transform infrared (FTIR) spectroscopy indicates that the ground state of P700 is somewhat modified by mutation of ThrA739 to alanine. Comparison of FTIR difference band shifts upon P700 + formation in WT and mutant PS1 suggests that the mutation modifies the charge distribution over the pigments in the P700+ state, with ∼14-18% of the positive charge on PB in WT being relocated onto PA in the mutant. 1H-electron-nuclear double resonance (ENDOR) analysis of the P700+ cation radical was also consistent with a slight redistribution of spin from the PB chlorophyll to PA, as well as some redistribution of spin within the PB chlorophyll. High-field electron paramagnetic resonance (EPR) spectroscopy at 330-GHz was used to resolve the g-tensor of P700+, but no significant differences from wild-type were observed, except for a slight decrease of anisotropy. The mutation did, however, provoke changes in the zero-field splitting parameters of the triplet state of P700 ( 3P700), as determined by EPR. Interestingly, the mutation-induced change in asymmetry of P700 did not cause an observable change in the directionality of electron transfer within PSI.

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