The protein regulator ArgR and the sRNA derived from the 3'-UTR region of its gene, ArgX, both regulate the arginine deiminase pathway in Lactococcus lactis

PLoS One. 2019 Jun 20;14(6):e0218508. doi: 10.1371/journal.pone.0218508. eCollection 2019.

Abstract

Small regulatory RNAs (sRNAs) and their enormous potential and versatility have provided us with an astounding insight in the complexity of bacterial transcriptomes. sRNAs have been shown to be involved in a variety of cellular processes that range from stress to general metabolism. Here we report that the gene encoding the transcriptional regulator ArgR is immediately followed by the gene of the small regulatory RNA ArgX. The latter is transcribed from its own promoter. The production of ArgX is induced by increasing arginine concentrations and repressed by CcpA. Previously, ArgR was shown to act as a transcriptional repressor of the catabolic arginine deiminase pathway (arc operon) by binding in the promoter region of arcA. Here we demonstrate that ArgX downregulates arc mRNA levels. Furthermore, ArgX putatively blocks the translation of one of the genes in the operon, arcC1, a process that would redirect an intermediate in arginine degradation, carbamoyl phosphate, towards pyrimidine synthesis. Our findings exemplify, for the first time, the combinatorial power of a transcription factor and a small regulatory RNA derived from the 3'-UTR region. The regulators ArgR and ArgX share a common target, but act on transcription and on RNA level, respectively.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 3' Untranslated Regions
  • Arginine / metabolism
  • Bacterial Proteins / genetics*
  • Bacterial Proteins / metabolism
  • Gene Expression Regulation, Bacterial*
  • Hydrolases / genetics
  • Hydrolases / metabolism
  • Lactococcus lactis / genetics*
  • Lactococcus lactis / metabolism
  • Operon
  • Promoter Regions, Genetic
  • RNA, Small Interfering / genetics*
  • RNA, Small Interfering / metabolism
  • Repressor Proteins / genetics*
  • Repressor Proteins / metabolism

Substances

  • 3' Untranslated Regions
  • ArgR protein, Bacteria
  • Bacterial Proteins
  • RNA, Small Interfering
  • Repressor Proteins
  • Arginine
  • Hydrolases
  • arginine deiminase

Grants and funding

Our study was partly funded by the Top Institute for Food and Nutrition (TiFN). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.