Aminoacyl tRNA synthetases, components of the translation apparatus, have alternative functions outside of translation. The structural and mechanistic basis of these alternative functions is of great interest. As an example, reverse transcription of the HIV genome is primed by a human lysine-specific tRNA (tRNA(LYs3)) that is packaged (into the virion) by the HIV Gag protein with lysyl-tRNA synthetase (LysRS). Not understood is the structural basis for simultaneous packaging of tRNALYs3, LysRS, and Gag. Here, ab initio computational methods, together with our recent high-resolution 3-D structure of human LysRS, produced an energy-minimized model where Gag, tRNA(LYs), and LysRS form a ternary complex. Interestingly, the model requires normally homodimeric LysRS to dissociate into a monomer that bridges between Gag and tRNALYs3. Earlier experiments of others and new experiments presented here, which tested an engineered dissociated form of LysRS, were consistent with the ab initio "bridging monomer" model. The results support an emerging theme that alterative functions of tRNA synthetases may come, in part, from protein surfaces exposed by dynamic equilibria.