Spectroscopic methods combined with density functional calculations are used to develop a detailed bonding description of the mu(4)-sulfide bridged tetranuclear Cu-Z cluster in N2O reductase. The ground state of Cu-Z has the 1Cu(II)/3Cu(I) configuration. The single electron hole dominantly resides on one Cu atom (Cu-I) and partially delocalizes onto a second Cu atom (Cu-II) via a Cu-I-S-Cu-II sigma/sigma superexchange pathway which is manifested by a Cu-II --> Cu-I intervalence transfer transition in absorption. The observed excited-state spectral features of Cu-Z are dominated by the S --> Cu-I charge-transfer transitions and Cu-I based d-d transitions. The intensity pattern of individual S --> Cu-I charge-transfer transitions reflects different bonding interactions of the sulfur valence orbitals with the four Cu's in the Cu-Z cluster, which are consistent with the individual Cu-S force constants obtained from a normal coordinate analysis of the Cu-Z resonance Raman frequencies and profiles. The Cu-I d orbital splitting pattern correlates with its distorted T-shaped ligand field geometry and accounts for the observed low g(II) value of Cu-Z in EPR. The dominantly localized electronic structure description of the Cu-Z site results from interactions of Cull with the two additional Cu's of the cluster (Cu-III/Cu-IV), where the Cu-Cu electrostatic interactions lead to hole localization with no metal-metal bonding. The substrate binding edge of Cu-Z has a dominantly oxidized Cu-I and a dominantly reduced Cu-IV. The electronic structure description of Cu-Z provides a strategy to overcome the reaction barrier of N2O reduction at this Cu-I/Cu-IV edge by simultaneous two-electron transfer to N2O in a bridged binding mode. One electron can be donated directly from Cu-IV and the other from Cull through the Cu-II-S-Cu-I sigma/sigma superexchange pathway. A frontier orbital scheme provides molecular insight into the catalytic mechanism of N2O reduction by the Cu-Z cluster.