Defensive Function of Transposable Elements in Bacteria

ACS Synth Biol. 2019 Sep 20;8(9):2141-2151. doi: 10.1021/acssynbio.9b00218. Epub 2019 Aug 19.

Abstract

It has been widely debated whether transposable elements have a positive or a negative effect on their host cells. This study demonstrated that transposable elements, specifically insertion sequences (ISs), can adopt a defensive role in Escherichia coli. In three different E. coli strains (S17, DH5α, and Nissle 1917), IS1 and IS10 rapidly disrupted the I-CeuI gene (encoding I-CeuI endonuclease) on the plasmid pLO11-ICeuI as early as the first generation, despite the gene-circuit being under control of an arabinose promoter. Proteomics analysis showed that the protein abundance profile of E. coli DH5α with pLO11-ICeuI in the fifth generation was nearly opposite to that of control strain (E. coli with pLO11, no I-CeuI). The DNA damage caused by the leaky expression of I-CeuI was enough to trigger a SOS response and alter lipid synthesis, ribosomal activity, RNA/DNA metabolism, central dogma and cell cycle processes in E. coli DH5α. After the ISs disrupted the expression of I-CeuI, cells fully recovered by the 31st generation had a protein abundance profile similar to that of the control strain. This study showed that ISs readily mutated a harmful gene which subsequently restored host fitness. These observations have implications for the stability of designed gene circuits in synthetic biology.

Keywords: Escherichia coli; IS1; IS10; insertion sequence; proteomics; stress; synthetic biology; transposable elements.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • DNA Transposable Elements / genetics*
  • Endodeoxyribonucleases / analysis
  • Endodeoxyribonucleases / genetics
  • Endodeoxyribonucleases / metabolism
  • Escherichia coli / genetics*
  • Escherichia coli Proteins / analysis
  • Escherichia coli Proteins / genetics
  • Escherichia coli Proteins / metabolism
  • Plasmids / genetics
  • Plasmids / metabolism
  • Proteomics
  • Synthetic Biology

Substances

  • DNA Transposable Elements
  • Escherichia coli Proteins
  • Endodeoxyribonucleases
  • endodeoxyribonuclease I-CeuI