Periodic extinctions of transposable elements in bacterial lineages: evidence from intragenomic variation in multiple genomes

Mol Biol Evol. 2006 Apr;23(4):723-33. doi: 10.1093/molbev/msj085. Epub 2005 Dec 22.

Abstract

Most previous work on the evolution of mobile DNA was limited by incomplete sequence information. Whole genome sequences allow us to overcome this limitation. I study the nucleotide diversity of prominent members of five insertion sequence families whose transposition activity is encoded by a single transposase gene. Eighteen among 376 completely sequenced bacterial genomes and plasmids carry between 3 and 20 copies of a given insertion sequence. I show that these copies generally show very low DNA divergence. Specifically, more than 68% of the transposase genes are identical within a genome. The average number of amino acid replacement substitutions at amino acid replacement sites is Ka = 0.013, that at silent sites is Ks = 0.1. This low intragenomic diversity stands in stark contrast to a much higher divergence of the same insertion sequences among distantly related genomes. Gene conversion among protein-coding genes is unlikely to account for this lack of diversity. The relation between transposition frequencies and silent substitution rates suggests that most insertion sequences in a typical genome are evolutionarily young and have been recently acquired. They may undergo periodic extinction in bacterial lineages. By implication, they are detrimental to their host in the long run. This is also suggested by the highly skewed and patchy distribution of insertion sequences among genomes. In sum, one can think of insertion sequences as slow-acting infectious diseases of cell lineages.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Bacteria / genetics*
  • DNA Transposable Elements / genetics*
  • Evolution, Molecular*
  • Genetic Variation*
  • Genome, Bacterial*
  • Sequence Homology, Nucleic Acid
  • Transposases / genetics

Substances

  • DNA Transposable Elements
  • Transposases