A novel CsrA titration mechanism regulates fimbrial gene expression in Salmonella typhimurium

A hierarchical control of fimbrial gene expression limits laboratory grown cultures of Salmonella enterica serovar typhimurium (S. typhimurium) to the production of type I fimbriae encoded by the fimAICDHF operon. Here we show that an unlikely culprit, namely the 5'-untranslated region (5'-UTR) of a messenger (m)RNA, coordinated the regulation. Binding of CsrA to the 5'-UTR of the pefACDEF transcript was required for expression of plasmid-encoded fimbriae. The 5'-UTR of the fimAICDHF transcript cooperated with two small untranslated RNAs, termed CsrB and CsrC, in antagonizing the activity of the RNA binding protein CsrA. Through this post-transcriptional mechanism, the 5'-UTR of the fimAICDHF transcript prevented production of PefA, the major structural subunit of plasmid-encoded fimbriae. This regulatory mechanism limits the costly expression of plasmid-encoded fimbriae to host environments in a mouse model. Collectively, our data suggest that the 5'-UTR of an mRNA coordinates a hierarchical control of fimbrial gene expression in S. typhimurium.