Mutational Adaptation of Escherichia coli to Glucose Limitation Involves Distinct Evolutionary Pathways in Aerobic and Oxygen-Limited Environments

Corresponding author: Thomas Ferenci, Department of Microbiology G08, University of Sydney, Sydney, NSW 2006, Australia., t.ferenci{at}microbio.usyd.edu.au (E-mail)

Communicating editor: R. MAURER

Mutational adaptations leading to improved glucose transport were followed with Escherichia coli K-12 growing in glucose-limited continuous cultures. When populations were oxygen limited as well as glucose limited, all bacteria within 280 generations contained mutations in a single codon of the ptsG gene. V12F and V12G replacements in the enzyme IIBC^Glc component of the glucose phosphotransferase system were responsible for improved transport. In stark contrast, ptsG mutations were uncommon in fully aerobic glucose-limited cultures, in which polygenic mutations in mgl, mlc, and malT (regulating an alternate high-affinity Mgl/LamB uptake pathway) spread through the adapted population. Hence the same organism adapted to the same selection (glucose limitation) by different evolutionary pathways depending on a secondary environmental factor. The clonal diversity in the adapted populations was also significantly different. The PtsG V12F substitution under O₂ limitation contributed to a universal "winner clone" whereas polygenic, multiallelic changes led to considerable polymorphism in aerobic cultures. Why the difference in adaptive outcomes? E. coli physiology prevented scavenging by the LamB/Mgl system under O₂ limitation; hence, ptsG mutations provided the only adaptive pathway. But ptsG mutations in aerobic cultures are overtaken by mgl, mlc, and malT adaptations with better glucose-scavenging ability. Indeed, when an mglA::Tn10 mutant with an inactivated Mgl/LamB pathway was introduced into two independent aerobic chemostats, adaptation of the Mgl^- strain involved the identical ptsG mutation found under O₂-limited conditions with wild-type or Mgl^- bacteria.

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