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Journal of bacteriology
04 19, 2022;204 (4): e0059221.

The Role and Targets of the RNA-Binding Protein ProQ in the Gram-Negative Bacterial Pathogen Pasteurella multocida.

Emily L Gulliver, Brandon M Sy, Julia L Wong, Deanna S Deveson Lucas, David R Powell, Marina Harper, Jai J Tree, John D Boyce
Author Information
  1. Emily L Gulliver: Department of Microbiology, Infection Program, Monash Biomedicine Discovery Institute, Monash University, Clayton, Victoria, Australia.
  2. Brandon M Sy: School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, New South Wales, Australia.
  3. Julia L Wong: School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, New South Wales, Australia.
  4. Deanna S Deveson Lucas: Department of Microbiology, Infection Program, Monash Biomedicine Discovery Institute, Monash University, Clayton, Victoria, Australia.
  5. David R Powell: Monash Bioinformatics Platform, Monash Universitygrid.1002.3, Clayton, Victoria, Australia.
  6. Marina Harper: Department of Microbiology, Infection Program, Monash Biomedicine Discovery Institute, Monash University, Clayton, Victoria, Australia.
  7. Jai J Tree: School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, New South Wales, Australia. ORCID
  8. John D Boyce: Department of Microbiology, Infection Program, Monash Biomedicine Discovery Institute, Monash University, Clayton, Victoria, Australia. ORCID
PMID: 35323048 DOI: 10.1128/jb.00592-21

Abstract

The Gram-negative pathogen Pasteurella multocida is the causative agent of many important animal diseases. While a number of P. multocida virulence factors have been identified, very little is known about how gene expression and protein production is regulated in this organism. One mechanism by which bacteria regulate transcript abundance and protein production is riboregulation, which involves the interaction of a small RNA (sRNA) with a target mRNA to alter transcript stability and/or translational efficiency. This interaction often requires stabilization by an RNA-binding protein such as ProQ or Hfq. In Escherichia coli and a small number of other species, ProQ has been shown to play a critical role in stabilizing sRNA-mRNA interactions and preferentially binds to the 3' stem-loop regions of the mRNA transcripts, characteristic of intrinsic transcriptional terminators. The aim of this study was to determine the role of ProQ in regulating P. multocida transcript abundance and identify the RNA targets to which it binds. We assessed differentially expressed transcripts in a mutant and identified sites of direct ProQ-RNA interaction using UV-cross-linking and analysis of cDNA (CRAC). These analyses demonstrated that ProQ binds to, and stabilizes, ProQ-dependent sRNAs and transfer RNAs in P. multocida via adenosine-enriched, highly structured sequences. The binding of ProQ to two RNA molecules was characterized, and these analyses showed that ProQ bound within the coding sequence of the transcript PmVP161_1121, encoding an uncharacterized protein, and within the 3' region of the putative sRNA Prrc13. Regulation in P. multocida involving the RNA-binding protein Hfq is required for hyaluronic acid capsule production and virulence. This study further expands our understanding of riboregulation by examining the role of a second RNA-binding protein, ProQ, in transcript regulation and abundance in P. multocida.

Keywords

Pasteurella multocida ProQ RNA-binding proteins sRNA

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MeSH Term

Escherichia coli
Escherichia coli Proteins
Gene Expression Regulation, Bacterial
Host Factor 1 Protein
Pasteurella multocida
RNA, Bacterial
RNA, Messenger
RNA, Small Untranslated
RNA-Binding Proteins

Chemicals

Escherichia coli Proteins
Host Factor 1 Protein
ProQ protein, E coli
RNA, Bacterial
RNA, Messenger
RNA, Small Untranslated
RNA-Binding Proteins
Journal Article Research Support, Non-U.S. Gov't

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