Role of a Water Network around the Mn4CaO5 Cluster in Photosynthetic Water Oxidation: A Fourier Transform Infrared Spectroscopy and Quantum Mechanics/Molecular Mechanics Calculation Study.

Abstract:

:Photosynthetic water oxidation takes place at the Mn4CaO5 cluster in photosystem II. Around the Mn4CaO5 cluster, a hydrogen bond network is formed by several water molecules, including four water ligands. To clarify the role of this water network in the mechanism of water oxidation, we investigated the effects of the removal of Ca(2+) and substitution with metal ions on the vibrations of water molecules coupled to the Mn4CaO5 cluster by means of Fourier transform infrared (FTIR) difference spectroscopy and quantum mechanics/molecular mechanics (QM/MM) calculations. The OH stretching vibrations of nine water molecules forming a network between D1-D61 and YZ were calculated using the QM/MM method. On the the calculated normal modes, a broad positive feature at 3200-2500 cm(-1) in an S2-minus-S1 FTIR spectrum was attributed to the vibrations of strongly hydrogen-bonded OH bonds of water involving the vibrations of water ligands to a Mn ion and the in-phase coupled vibration of a water network connected to YZ, while bands in the 3700-3500 cm(-1) region were assigned to the coupled vibrations of weakly hydrogen-bonded OH bonds of water. All the water bands were lost upon Ca(2+) depletion and Ba(2+) substitution, which inhibit the S2 → S3 transition, indicating that a solid water network was broken by these treatments. By contrast, Sr(2+) substitution slightly altered the water bands around 3600 cm(-1), reflecting minor modification in water interactions, consistent with the retention of water oxidation activity with a decreased efficiency. These results suggest that the water network around the Mn4CaO5 cluster plays an essential role in the water oxidation mechanism particularly in a concerted process of proton transfer and water insertion during the S2 → S3 transition.

journal_name

Biochemistry

journal_title

Biochemistry

authors

Nakamura S,Ota K,Shibuya Y,Noguchi T

doi

10.1021/acs.biochem.5b01120

subject

Has Abstract

pub_date

2016-01-26 00:00:00

pages

597-607

issue

3

eissn

0006-2960

issn

1520-4995

journal_volume

55

pub_type

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