Transcription, translation, and the evolution of specialists and generalists

Shaobin Zhong, Stephen P Miller, Daniel E. Dykhuizen, Antony M Dean

Research output: Contribution to journalArticlepeer-review

15 Scopus citations

Abstract

We used DNA microarrays to measure transcription and iTRAQ 2D liquid chromatography-mass spectrometry/mass spectrometry (a mass-tag labeling proteomic technique) to measure protein expression in 14 strains of Escherichia coli adapted for hundreds of generations to growth-limiting concentrations of either lactulose, methylgalactoside, or a 72:28 mixture of the two. The two ancestors, TD2 and TD10, differ only in their lac operons and have similar transcription and protein expression profiles. Changes in transcription and protein expression are observed at 30-250 genes depending on the evolved strain. Lactulose specialists carry duplications of the lac operon and show increased transcription and translation at lac. Methylgalactoside specialists are galS - and so constitutively transcribe and translate mgl, which encodes a transporter of methylgalactoside. However, there are two strains that carry lac duplications, are galS -, and show increased transcription and translation at both operons. One is a generalist, the other a lactulose specialist. The generalist fails to sweep to fixation because its lac +, galS + competitor expresses the csg adhesin and sticks to the chemostat wall, thereby preventing complete washout. Transcription and translation are sometimes decoupled. Lactulose-adapted strains show increased protein expression at fru, a fructose transporter, without evidence of increased transcription. This suggests that fructose, produced by the action of β-galactosidase on lactulose, may leach from cells before being recouped. Reduced expression, at "late" flagella genes and the constitutive gat operon, is an adaptation to starvation. A comparison with two other long-term evolution experiments suggests that certain aspects of adaptation are predictable, some are characteristic of an experimental system, whereas others seem erratic.

Original languageEnglish (US)
Pages (from-to)2661-2678
Number of pages18
JournalMolecular biology and evolution
Volume26
Issue number12
DOIs
StatePublished - Dec 2009

Keywords

  • Chemostats
  • E. coli
  • Evolution
  • Generalists
  • Lac
  • Protonomics
  • Specialists

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