Mechanism of a novel metal-free carbonic anhydrase

Phys Chem Chem Phys. 2024 Nov 4. doi: 10.1039/d4cp03099k. Online ahead of print.

Abstract

The recently discovered metal-free carbonic anhydrase (CA) enzyme may significantly impact the global carbon dioxide (CO2) cycle, as it can irreversibly perform the CO2 hydration reaction. In this study, we investigated several key aspects of metal-free CA, including the identification of the catalytic site, the determination of the CO2 binding site, and the mechanism of catalysis. This is achieved through classical molecular dynamics (MD) simulations, quantum chemical density functional theory (DFT), and hybrid quantum mechanics/molecular mechanics (QM/MM) calculations. Our study indicates that the experimental structure based on X-ray crystallography, which shows the 'bicarbonate (HCO3-) product' trapped in the hydrophilic region of metal-free CA, might not accurately depict the actual enzyme-substrate interaction. Instead, the simulation reveals that CO2 prefers the hydrophobic zone, which serves as the primary catalytic site. It also highlights the strategic role of a gatekeeper residue (Phe504), which assists in regulating the transportation of CO2 by tilting its aromatic plane. Additionally, the hybrid QM/MM calculations establish that CO2 hydration is catalyzed within the hydrophobic zone by a deprotonated tyrosine with the help of an organized water chain.