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ProQ has recently emerged as a major post-transcriptional regulator in bacteria through directly binding to diverse mRNAs and small non-coding RNAs (sRNAs). However, the impact of ProQ in many pathogenic bacteria remains poorly understood. In this study, we investigated the role of ProQ in enterohaemorrhagic Escherichia coli (EHEC), a non-invasive intestinal pathogen. We found that deletion of proQ significantly enhanced cell adherence ability of EHEC and led to upregulation of the locus of enterocyte effacement (LEE) pathogenicity island. This effect was accompanied by reduced expression of genes encoding known LEE regulators, including protein factors (ihfA and hns) and sRNAs (GlmY and GlmZ), resulting from decreased stability of their transcripts in the absence of proQ. Additionally, proQ positively regulated bacterial motility by stabilizing fliC mRNA. We further demonstrated that ProQ directly binds to ihfA, hns, glmY/glmZ and fliC transcripts at secondary structures located near their 3’ ends. Beyond virulence regulation, ProQ also contributed to antibiotic persistence of EHEC and its survival under host-associated stress conditions. Collectively, our findings highlight ProQ as a key gene regulator in EHEC, providing new insights into how this pathogen modulates its virulence at the post-transcriptional level.