Revealing the Involvement of Extended Hydrogen Bond Networks in the Cooperative Function between Distant Sites in Bacterial Reaction Centers

Julia Tandori,Laura Baciou,Emil Alexov,Péter Maróti,Marianne Schiffer,Deborah K Hanson,Pierre Sebban

doi:10.1074/jbc.c100537200

Julia Tandori, Laura Baciou + Show 5 more

Open Access

https://doi.org/10.1074/jbc.c100537200

Copy DOI

Abstract

In reaction center proteins of photosynthetic bacteria, the amplitude of proton uptake induced by the one-electron reduction of either of the two quinone electron acceptors (Q(A) and Q(B)) is an intrinsic observable of the electrostatic interactions associated with the redox function of the complex. We report here that, in Rhodobacter capsulatus, complete restoration of proton uptake (upon formation of Q(A)(-) and Q(B)(-)) to the level found in the wild type is observed in a mutant reaction center in which a tyrosine substitution in the Q(A) environment (Ala(M274) --> Tyr) is coupled with mutations of acidic residues near Q(B) (Glu(L212) --> Ala/Asp(L213) --> Ala) that initially cancel the proton uptake above pH 8. This result demonstrates that proton uptake occurs by strong cooperation between structural motifs, such as hydrogen-bonded networks, that span the 18 A distance between the two quinone acceptors.

Highlights

Revealing the Involvement of Extended Hydrogen Bond Networks in the Cooperative Function between Distant Sites in Bacterial Reaction Centers*
In reaction center proteins of photosynthetic bacteria, the amplitude of proton uptake induced by the oneelectron reduction of either of the two quinone electron acceptors (QA and QB) is an intrinsic observable of the electrostatic interactions associated with the redox function of the complex
In Rhodobacter capsulatus, complete restoration of proton uptake to the level found in the wild type is observed in a mutant reaction center in which a tyrosine substitution in the QA environment (AlaM247 3 Tyr) is coupled with mutations of acidic residues near QB (GluL212 3 Ala/AspL213 3 Ala) that initially cancel the proton uptake above pH 8

Summary

Accelerated Publication

THE JOURNAL OF BIOLOGICAL CHEMISTRY Vol 276, No 49, Issue of December 7, pp. 45513–45515, 2001. In Rhodobacter capsulatus, complete restoration of proton uptake (upon formation of QA؊ and QB؊) to the level found in the wild type is observed in a mutant reaction center in which a tyrosine substitution in the QA environment (AlaM247 3 Tyr) is coupled with mutations of acidic residues near QB (GluL212 3 Ala/AspL213 3 Ala) that initially cancel the proton uptake above pH 8. This result demonstrates that proton uptake occurs by strong cooperation between structural motifs, such as hydrogenbonded networks, that span the 18 Å distance between the two quinone acceptors. We suggest that strong interactions involving extended hydrogen-bonded networks between QA and QB (18 Å) are directly involved in the proton uptake by the protein

MATERIALS AND METHODS

Proton Uptake by Extended Hϩ Bond Networks in Proteins

RESULTS AND DISCUSSION