RNA-Seq-based analysis of the physiologic cold shock-induced changes in Moraxella catarrhalis gene expression

PLoS One. 2013 Jul 2;8(7):e68298. doi: 10.1371/journal.pone.0068298. Print 2013.

Abstract

Background: Moraxella catarrhalis, a major nasopharyngeal pathogen of the human respiratory tract, is exposed to rapid downshifts of environmental temperature when humans breathe cold air. The prevalence of pharyngeal colonization and respiratory tract infections caused by M. catarrhalis is greatest in winter. We investigated how M. catarrhalis uses the physiologic exposure to cold air to regulate pivotal survival systems that may contribute to M. catarrhalis virulence.

Results: In this study we used the RNA-seq techniques to quantitatively catalogue the transcriptome of M. catarrhalis exposed to a 26 °C cold shock or to continuous growth at 37 °C. Validation of RNA-seq data using quantitative RT-PCR analysis demonstrated the RNA-seq results to be highly reliable. We observed that a 26 °C cold shock induces the expression of genes that in other bacteria have been related to virulence a strong induction was observed for genes involved in high affinity phosphate transport and iron acquisition, indicating that M. catarrhalis makes a better use of both phosphate and iron resources after exposure to cold shock. We detected the induction of genes involved in nitrogen metabolism, as well as several outer membrane proteins, including ompA, m35-like porin and multidrug efflux pump (acrAB) indicating that M. catarrhalis remodels its membrane components in response to downshift of temperature. Furthermore, we demonstrate that a 26 °C cold shock enhances the induction of genes encoding the type IV pili that are essential for natural transformation, and increases the genetic competence of M. catarrhalis, which may facilitate the rapid spread and acquisition of novel virulence-associated genes.

Conclusion: Cold shock at a physiologically relevant temperature of 26 °C induces in M. catarrhalis a complex of adaptive mechanisms that could convey novel pathogenic functions and may contribute to enhanced colonization and virulence.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Carbohydrate Metabolism / genetics
  • Cold Temperature*
  • Energy Metabolism / genetics
  • Gene Expression Regulation, Bacterial*
  • Humans
  • Lipid Metabolism / genetics
  • Moraxella catarrhalis / genetics*
  • Moraxella catarrhalis / pathogenicity
  • Moraxellaceae Infections / microbiology
  • Oligonucleotide Array Sequence Analysis
  • Reverse Transcriptase Polymerase Chain Reaction
  • Sequence Analysis, RNA / methods*
  • Transcriptome*
  • Virulence / genetics

Associated data

  • GEO/GSE46256

Grants and funding

This work was supported by the Swiss National Science Foundation (SNF) grants 3100A0-102246 and 3100A0-116053 (to CA). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.