Copper-cysteine interactions play an important role in Biology and herein we used the copper-substituted rubredoxin (Cu-Rd) from Desulfovibrio gigas to gain further insights into the copper-cysteine redox chemistry. EPR spectroscopy results are consistent with Cu-Rd harboring a Cu-II center in a sulfur-rich coordination, in a distorted tetrahedral structure (g(parallel to,perpendicular to) = 2.183 and 2.032 and A(parallel to,perpendicular to) = 76.4 x 10(-4) and 12 x 10(-4) cm(-1)). In Cu-Rd, two oxidation states at Cu-center (Cu-II and Cu-I) are associated with Cys oxidation-reduction, alternating in the redox cycle, as pointed by electrochemical studies that suggest internal geometry rearrangements associated with the electron transfer processes. The midpoint potential of [Cu-I(S-Cys)(2)(Cys-S-S-Cys)]/[Cu-II(S-Cys)(4)] redox couple was found to be -0.15 V vs NHE showing a large separation of cathodic and anodic peaks potential (Delta E-p = 0.575 V). Interestingly, sulfur-rich Cu-II-Rd is highly stable under argon in dark conditions, which is thermodynamically unfavorable to Cu-thiol autoreduction. The reduction of copper and concomitant oxidation of Cys can both undergo two possible pathways: oxidative as well as photochemical. Under O-2, Cu-II plays the role of the electron carrier from one Cys to O-2 followed by internal geometry rearrangement at the Cu site, which facilitates reduction at Cu-center to yield Cu-I(S-(2)(Cys-S-S-Cys). Photoinduced (irradiated at lambda(ex) = 280 nm) reduction of the Cu-II center is observed by UV-visible photolysis (above 300 nm all bands disappeared) and tryptophan fluorescence (similar to 335 nm peak enhanced) experiments. In both pathways, geometry reorganization plays an important role in copper reduction yielding an energetically compatible donoracceptor system. This model system provides unusual stability and redox chemistry rather than the universal Cu-thiol auto redox chemistry in cysteine-rich copper complexes.