Vibrational analysis on the revised potential energy curve of the low-barrier hydrogen bond in photoactive yellow protein

Yusuke Kanematsu,Hironari Kamikubo,Mikio Kataoka,Masanori Tachikawa

doi:10.1016/j.csbj.2015.10.003

Abstract

Photoactive yellow protein (PYP) has a characteristic hydrogen bond (H bond) between p-coumaric acid chromophore and Glu46, whose OH bond length has been observed to be 1.21Å by the neutron diffraction technique [Proc. Natl. Acad. Sci. 106, 440–4]. Although it has been expected that such a drastic elongation of the OH bond could be caused by the quantum effect of the hydrogen nucleus, previous theoretical computations including the nuclear quantum effect have so far underestimated the bond length by more than 0.07Å. To elucidate the origin of the difference, we performed a vibrational analysis of the H bond on potential energy curve with O…O distance of 2.47Å on the equilibrium structure, and that with O…O distance of 2.56Å on the experimental crystal structure. While the vibrationally averaged OH bond length for equilibrium structure was underestimated, the corresponding value for crystal structure was in reasonable agreement with the corresponding experimental values. The elongation of the O…O distance by the quantum mechanical or thermal fluctuation would be indispensable for the formation of a low-barrier hydrogen bond in PYP.

Highlights

Photoactive yellow protein (PYP) is a water-soluble photosensor protein found in halophilic photosynthetic bacteria
They have assigned a hydrogen bond between Glu46 and pcoumaric acid chromophore of PYP with significantly long O-H bond of 1.21 Å as low-barrier hydrogen bond (LBHB), which had never been directly observed in proteins until
The corresponding energy levels and the vibrationally averaged OH bond lengths are shown in Experimental

Summary

Introduction

Photoactive yellow protein (PYP) is a water-soluble photosensor protein found in halophilic photosynthetic bacteria. It has been found that Arg located near the chromophore was deprotonated (neutral), whereas it had been believed to be protonated to act as counterion for the negative chromophore according to X-ray crystallography[3] and electronic structure calculation [4] It was, claimed by Saito and Ishikita that Arg should be protonated and the H-bond between pCA and Glu was not LBHB but a normal H-bond according to the potential energy profile analysis with the conventional QM/MM calculation, and the comparison between the experimental chemical shifts in solution [5] and their computational values under the previously mentioned condition [6,7]. Kanematsu et al / Computational and Structural Biotechnology Journal 14 (2016) 16–19

Computational detail

The vibrational analysis on the equilibrium structure

The vibrational analysis on the crystal structure

Conclusion