Escherichia coli Hsp31 is a homodimeric member of the ThiI/DJ-1/PfpI superfamily that combines molecular chaperone and aminopeptidase activities. Although it was originally identified on the basis of its induction by heat shock, little is known about the regulation of hchA, the structural gene encoding Hsp31. Here, we show that hchA is transcribed from dual promoters recognized by the sigmaD (sigma70) and sigmaS (sigma38) subunits of RNA polymerase (E). In exponentially growing cells, the nucleoid-binding protein H-NS downregulates Hsp31 synthesis, and hchA thermal induction primarily relies on the relief of H-NS-mediated silencing of EsigmaD-dependent transcription. This uncommon alternative to the use of a heat-shock sigma factor guarantees that Hsp31 concentration remains high throughout the length of the high temperature exposure phase. Entry into stationary phase leads to enhanced hchA transcription from its EsigmaS-dependent promoter. Consistent with a role of Hsp31 in the management of starvation, hchA null mutants exhibit a decrease ability to survive in deep stationary phase relative to hchA+ cells. Based on hchA heat-inducibility and membership in the sigmaS general stress regulon, we propose that Hsp31 performs a protective function under a wide range of stress conditions.