Many intracellular bacteria, including Legionella pneumophila, rely on Type IV secretion system (T4SS) to translocate a repertoire of effector proteins into host cells for their survival and growth. T4CP is a hexameric ATPase that links translocating substrates to the transenvelope secretion conduit. Yet, how a large number of effector proteins are selectively recruited and processed by T4CPs remains enigmatic. DotL, the T4CP of L. pneumophila, contains an ATPase domain and a unique C-terminal extension whose function is unknown. Unlike T4CPs recruiting plasmid DNA for translocation, DotL appeared to function by forming a multi-protein complex together with four other proteins. Herein, we found that the C-terminal extension of DotL interacts with DotN, IcmS, IcmW and a newly identified subunit LvgA, and show that this pentameric assembly binds Legionella effector proteins. We determined the crystal structure of this assembly, and built an architecture of the T4CP holocomplex by combining a homology model of the N-terminal ATPase domain of DotL. The holocomplex is a hexamer of a bipartite structure composed of a membrane-proximal ATPase domain and a membrane-distal substrate-recognition assembly. The presented information represents the architecture and functional dissection of the multi-protein T4CP complexes in pathogenic bacteria, and provides important insights into their substrate recruitment and processing.