A trade-off between the fitness cost of functional integrases and long-term stability of integrons

PLoS Pathog. 2012;8(11):e1003043. doi: 10.1371/journal.ppat.1003043. Epub 2012 Nov 29.

Abstract

Horizontal gene transfer (HGT) plays a major role in bacterial microevolution as evident from the rapid emergence and spread of antimicrobial drug resistance. Few studies have however addressed the population dynamics of newly imported genetic elements after HGT. Here, we show that newly acquired class-1 integrons from Salmonella enterica serovar Typhimurium and Acinetobacter baumannii, free of associated transposable elements, strongly reduce host fitness in Acinetobacter baylyi. Insertional inactivation of the integron intI1 restored fitness, demonstrating that the observed fitness costs were due to the presence of an active integrase. The biological cost of harboring class-1 integrons was rapidly reduced during serial transfers due to intI1 frameshift mutations leading to inactivated integrases. We use a mathematical model to explore the conditions where integrons with functional integrases are maintained and conclude that environmental fluctuations and episodic selection is necessary for the maintenance of functional integrases. Taken together, the presented data suggest a trade-off between the ability to capture gene cassettes and long-term stability of integrons and provide an explanation for the frequent observation of inactive integron-integrases in bacterial populations.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acinetobacter baumannii / enzymology*
  • Acinetobacter baumannii / genetics
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Base Sequence
  • Genomic Instability / physiology*
  • Integrases / genetics
  • Integrases / metabolism*
  • Integrons / physiology*
  • Molecular Sequence Data
  • Salmonella typhimurium / enzymology*
  • Salmonella typhimurium / genetics

Substances

  • Bacterial Proteins
  • Integrases

Associated data

  • GENBANK/AM991977
  • GENBANK/JX041889
  • GENBANK/JX259274

Grant support

This project was funded by the University of Tromsø and grants from the Norwegian Research Council 204263 and Tromsø Forskningsstiftelse awarded PJJ. ØS was supported by a grant from the Northern Norway Regional Health Authority. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.