Deep sequencing analysis of small noncoding RNA and mRNA targets of the global post-transcriptional regulator, Hfq

PLoS Genet. 2008 Aug 22;4(8):e1000163. doi: 10.1371/journal.pgen.1000163.

Abstract

Recent advances in high-throughput pyrosequencing (HTPS) technology now allow a thorough analysis of RNA bound to cellular proteins, and, therefore, of post-transcriptional regulons. We used HTPS to discover the Salmonella RNAs that are targeted by the common bacterial Sm-like protein, Hfq. Initial transcriptomic analysis revealed that Hfq controls the expression of almost a fifth of all Salmonella genes, including several horizontally acquired pathogenicity islands (SPI-1, -2, -4, -5), two sigma factor regulons, and the flagellar gene cascade. Subsequent HTPS analysis of 350,000 cDNAs, derived from RNA co-immunoprecipitation (coIP) with epitope-tagged Hfq or control coIP, identified 727 mRNAs that are Hfq-bound in vivo. The cDNA analysis discovered new, small noncoding RNAs (sRNAs) and more than doubled the number of sRNAs known to be expressed in Salmonella to 64; about half of these are associated with Hfq. Our analysis explained aspects of the pleiotropic effects of Hfq loss-of-function. Specifically, we found that the mRNAs of hilD (master regulator of the SPI-1 invasion genes) and flhDC (flagellar master regulator) were bound by Hfq. We predicted that defective SPI-1 secretion and flagellar phenotypes of the hfq mutant would be rescued by overexpression of HilD and FlhDC, and we proved this to be correct. The combination of epitope-tagging and HTPS of immunoprecipitated RNA detected the expression of many intergenic chromosomal regions of Salmonella. Our approach overcomes the limited availability of high-density microarrays that have impeded expression-based sRNA discovery in microorganisms. We present a generic strategy that is ideal for the systems-level analysis of the post-transcriptional regulons of RNA-binding proteins and for sRNA discovery in a wide range of bacteria.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Flagella / metabolism
  • Gene Expression Profiling
  • Gene Expression Regulation, Bacterial
  • Host Factor 1 Protein / genetics
  • Host Factor 1 Protein / metabolism*
  • Molecular Sequence Data
  • RNA Processing, Post-Transcriptional*
  • RNA, Bacterial / genetics
  • RNA, Bacterial / metabolism
  • RNA, Messenger / genetics*
  • RNA, Messenger / metabolism
  • RNA, Untranslated / genetics*
  • RNA, Untranslated / metabolism
  • Regulon
  • Salmonella typhimurium / genetics*
  • Salmonella typhimurium / growth & development
  • Salmonella typhimurium / metabolism
  • Sequence Analysis, DNA / methods*
  • Virulence

Substances

  • Host Factor 1 Protein
  • RNA, Bacterial
  • RNA, Messenger
  • RNA, Untranslated

Associated data

  • GEO/GSE10149