Escherichia coli ClpA, an Hsp100/Clp chaperone and an integral component of the ATP-dependent ClpAP protease, participates in the dissolution and degradation of regulatory proteins and protein aggregates. ClpA consists of three functional domains: an N-terminal domain and two ATPase domains, D1 and D2. The N-domain is attached to D1 by a mobile linker and is made up of two tightly bound, identically folded alpha-helical bundles related by a pseudo 2-fold symmetry. Between the halves of the pseudo-dimer is a large flexible acidic loop that becomes better ordered upon binding of the small adaptor protein, ClpS. We have identified a number of structural features in the N-domain, including a Zn(++) binding motif, several interfaces for binding to ClpS, and a prominent hydrophobic surface area that binds peptides in different configurations. These structural motifs may contribute to binding of protein or peptide substrates with weak affinity and broad specificity. Kinetic studies comparing wild-type ClpA to a mutant ClpA with its N-domain deleted show that the N-domains contribute to the binding of a non-specific protein substrate but not of a folded substrate with the specific SsrA recognition tag. A functional model is proposed in which the N-domains in ClpA function as tentacles to weakly hold on to proteins thereby enhancing local substrate concentration.