From the environment to the host: re-wiring of the transcriptome of Pseudomonas aeruginosa from 22°C to 37°C

PLoS One. 2014 Feb 24;9(2):e89941. doi: 10.1371/journal.pone.0089941. eCollection 2014.

Abstract

Pseudomonas aeruginosa is a highly versatile opportunistic pathogen capable of colonizing multiple ecological niches. This bacterium is responsible for a wide range of both acute and chronic infections in a variety of hosts. The success of this microorganism relies on its ability to adapt to environmental changes and re-program its regulatory and metabolic networks. The study of P. aeruginosa adaptation to temperature is crucial to understanding the pathogenesis upon infection of its mammalian host. We examined the effects of growth temperature on the transcriptome of the P. aeruginosa PAO1. Microarray analysis of PAO1 grown in Lysogeny broth at mid-exponential phase at 22°C and 37°C revealed that temperature changes are responsible for the differential transcriptional regulation of 6.4% of the genome. Major alterations were observed in bacterial metabolism, replication, and nutrient acquisition. Quorum-sensing and exoproteins secreted by type I, II, and III secretion systems, involved in the adaptation of P. aeruginosa to the mammalian host during infection, were up-regulated at 37°C compared to 22°C. Genes encoding arginine degradation enzymes were highly up-regulated at 22°C, together with the genes involved in the synthesis of pyoverdine. However, genes involved in pyochelin biosynthesis were up-regulated at 37°C. We observed that the changes in expression of P. aeruginosa siderophores correlated to an overall increase in Fe²⁺ extracellular concentration at 37°C and a peak in Fe³⁺ extracellular concentration at 22°C. This suggests a distinct change in iron acquisition strategies when the bacterium switches from the external environment to the host. Our work identifies global changes in bacterial metabolism and nutrient acquisition induced by growth at different temperatures. Overall, this study identifies factors that are regulated in genome-wide adaptation processes and discusses how this life-threatening pathogen responds to temperature.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptation, Physiological / genetics
  • Adaptation, Physiological / physiology*
  • Gene Expression Regulation, Bacterial / genetics
  • Gene Expression Regulation, Bacterial / physiology*
  • Host-Pathogen Interactions
  • Microarray Analysis
  • Pseudomonas aeruginosa / genetics
  • Pseudomonas aeruginosa / metabolism*
  • Reverse Transcriptase Polymerase Chain Reaction
  • Temperature*
  • Transcriptome / genetics*

Grants and funding

This work was supported by a grant from the Cystic Fibrosis Foundation to J.B.G. (GOLDBE10G0). F.H.D. was supported by a postdoctoral fellowship from the Cystic Fibrosis Foundation (DAMRON10F0). S.A. was supported by Ministerio de Economia y Competitividad and Instituto de Salud Carlos III (SAF2008-03967 and REIPI RD06/0008). The authors also gratefully acknowledge the financial support of the European Union projects MICROME (KBBE, #222886), and INFECT (Health, 305340) to V.M.d.S. P.B. was supported by the Helmholtz Centre for Infection Research, Germany (project: Systems Biology of Pseudomonas, number 1100187). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.