RNA helicase-regulated processing of the Synechocystis rimO-crhR operon results in differential cistron expression and accumulation of two sRNAs

J Biol Chem. 2020 May 8;295(19):6372-6386. doi: 10.1074/jbc.RA120.013148. Epub 2020 Mar 24.

Abstract

The arrangement of functionally-related genes in operons is a fundamental element of how genetic information is organized in prokaryotes. This organization ensures coordinated gene expression by co-transcription. Often, however, alternative genetic responses to specific stress conditions demand the discoordination of operon expression. During cold temperature stress, accumulation of the gene encoding the sole Asp-Glu-Ala-Asp (DEAD)-box RNA helicase in Synechocystis sp. PCC 6803, crhR (slr0083), increases 15-fold. Here, we show that crhR is expressed from a dicistronic operon with the methylthiotransferase rimO/miaB (slr0082) gene, followed by rapid processing of the operon transcript into two monocistronic mRNAs. This cleavage event is required for and results in destabilization of the rimO transcript. Results from secondary structure modeling and analysis of RNase E cleavage of the rimO-crhR transcript in vitro suggested that CrhR plays a role in enhancing the rate of the processing in an auto-regulatory manner. Moreover, two putative small RNAs are generated from additional processing, degradation, or both of the rimO transcript. These results suggest a role for the bacterial RNA helicase CrhR in RNase E-dependent mRNA processing in Synechocystis and expand the known range of organisms possessing small RNAs derived from processing of mRNA transcripts.

Keywords: RNA helicase; RNA processing; Synechocystis CrhR RNA helicase; cold-stress response; cyanobacteria; differential operon cistron expression; post-transcriptional regulation; rimO–crhR dicistronic RNA; small noncoding regulatory RNA; stress response.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 5' Untranslated Regions / genetics
  • Base Sequence
  • Gene Expression Regulation, Bacterial
  • Operon / genetics*
  • RNA Helicases / metabolism*
  • RNA, Untranslated / metabolism*
  • Synechocystis / enzymology*
  • Synechocystis / genetics*

Substances

  • 5' Untranslated Regions
  • RNA, Untranslated
  • RNA Helicases