Structural and energetic insights into Mn-to-Fe substitution in the oxygen-evolving complex

Area of Science:

• Biochemistry
• Photosynthesis research
• Computational chemistry

Background:

• Manganese (Mn) is crucial for water splitting in photosystem II (PSII).
• Iron (Fe) is abundant but not utilized in the natural water oxidation catalyst.
• Understanding this elemental preference is key to artificial photosynthesis.

Purpose of the Study:

• Investigate why manganese, not iron, is used in the photosystem II water oxidation catalyst.
• Explore the electronic and structural differences between Mn and Fe in the catalytic cluster.

Main Methods:

• Employed a quantum mechanical/molecular mechanical (QM/MM) approach.
• Modeled the Fe4CaO5 cluster within the PSII protein environment.
• Assumed equivalence between Mn(III/IV) and Fe(II/III) oxidation states.

Main Results:

• Fe substitution led to protonation of μ-oxo bridges by Arg357 and D1-His337.
• The Fe4CaO5 cluster lacked the S2 conformation variability seen in Mn4CaO5.
• An absent low-barrier H-bond in the Fe4CaO5 cluster hinders ligand water deprotonation.

Conclusions:

• The inability of the Fe4CaO5 cluster to deprotonate ligand water highlights the necessity of manganese for natural water splitting.
• Structural and electronic differences explain manganese's unique role in photosynthesis.