Carboxylate groups have diverse functionalities in ligands of transition metal catalysts. Here we present a conceptually different function of the carboxylates: the oxide relay. It functions by providing an intramolecular nucleophilic oxygen close to the oxo group to facilitate O-O bond formation and at a later stage a remote electrophilic center to facilitate OH- nucleophilic attack. Empirical valence bond-molecular dynamics (EVB-MD) models were generated for key bond forming steps, diffusion coefficients and binding free energies from potential of mean force estimations were calculated from molecular dynamics (MD) simulations, activation free energies of chemical steps were calculated using density functional theory (DFT). The catalyst studied is the extremely active Ru(tda)(py)(2) water oxidation catalyst. The combination of simulation methods allowed for estimation of the turnover frequencies, which were within 1 order of magnitude from the experimental results at different pH values. From the calculated reaction rates we find that at low pH the OH- anion nucleophilic attack is the rate limiting step, which changes at high pH to the O-O bond formation step. Both steps are extremely rapid, and key to the efficiency is the oxide relay functionality of a pendant carboxylate group. We cannot exclude all alternative mechanisms and suggest isotope experiments using O-18-labeled water to support or invalidate the oxide relay mechanism. The functionality was discovered for a ruthenium catalyst, but since there is nothing in the mechanism restricting it to this metal, the oxide relay functionality could open new ways to design the next-generation water oxidation catalysts with improved activity.