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. 1999 Sep;153(1):5–12. doi: 10.1093/genetics/153.1.5

Mutational adaptation of Escherichia coli to glucose limitation involves distinct evolutionary pathways in aerobic and oxygen-limited environments.

K Manch 1, L Notley-McRobb 1, T Ferenci 1
PMCID: PMC1460742  PMID: 10471695

Abstract

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 O(2) 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 O(2) 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 O(2)-limited conditions with wild-type or Mgl(-) bacteria.

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Selected References

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  1. Begley G. S., Warner K. A., Arents J. C., Postma P. W., Jacobson G. R. Isolation and characterization of a mutation that alters the substrate specificity of the Escherichia coli glucose permease. J Bacteriol. 1996 Feb;178(3):940–942. doi: 10.1128/jb.178.3.940-942.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Buhr A., Daniels G. A., Erni B. The glucose transporter of Escherichia coli. Mutants with impaired translocation activity that retain phosphorylation activity. J Biol Chem. 1992 Feb 25;267(6):3847–3851. [PubMed] [Google Scholar]
  3. Buhr A., Erni B. Membrane topology of the glucose transporter of Escherichia coli. J Biol Chem. 1993 Jun 5;268(16):11599–11603. [PubMed] [Google Scholar]
  4. Cole H. A., Wimpenny J. W., Hughes D. E. The ATP pool in Escherichia coli. I. Measurement of the pool using modified luciferase assay. Biochim Biophys Acta. 1967;143(3):445–453. doi: 10.1016/0005-2728(67)90050-3. [DOI] [PubMed] [Google Scholar]
  5. Curtis S. J., Epstein W. Phosphorylation of D-glucose in Escherichia coli mutants defective in glucosephosphotransferase, mannosephosphotransferase, and glucokinase. J Bacteriol. 1975 Jun;122(3):1189–1199. doi: 10.1128/jb.122.3.1189-1199.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dean A. M. Selection and neutrality in lactose operons of Escherichia coli. Genetics. 1989 Nov;123(3):441–454. doi: 10.1093/genetics/123.3.441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Death A., Ferenci T. Between feast and famine: endogenous inducer synthesis in the adaptation of Escherichia coli to growth with limiting carbohydrates. J Bacteriol. 1994 Aug;176(16):5101–5107. doi: 10.1128/jb.176.16.5101-5107.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Death A., Ferenci T. The importance of the binding-protein-dependent Mgl system to the transport of glucose in Escherichia coli growing on low sugar concentrations. Res Microbiol. 1993 Sep;144(7):529–537. doi: 10.1016/0923-2508(93)90002-j. [DOI] [PubMed] [Google Scholar]
  9. Death A., Notley L., Ferenci T. Derepression of LamB protein facilitates outer membrane permeation of carbohydrates into Escherichia coli under conditions of nutrient stress. J Bacteriol. 1993 Mar;175(5):1475–1483. doi: 10.1128/jb.175.5.1475-1483.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dykhuizen D. E. Chemostats used for studying natural selection and adaptive evolution. Methods Enzymol. 1993;224:613–631. doi: 10.1016/0076-6879(93)24046-w. [DOI] [PubMed] [Google Scholar]
  11. Dykhuizen D. E., Hartl D. L. Selection in chemostats. Microbiol Rev. 1983 Jun;47(2):150–168. doi: 10.1128/mr.47.2.150-168.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Ferenci T. Adaptation to life at micromolar nutrient levels: the regulation of Escherichia coli glucose transport by endoinduction and cAMP. FEMS Microbiol Rev. 1996 Jul;18(4):301–317. doi: 10.1111/j.1574-6976.1996.tb00246.x. [DOI] [PubMed] [Google Scholar]
  13. Ferenci T. Regulation by nutrient limitation. Curr Opin Microbiol. 1999 Apr;2(2):208–213. doi: 10.1016/S1369-5274(99)80036-8. [DOI] [PubMed] [Google Scholar]
  14. Hansen S. R., Hubbell S. P. Single-nutrient microbial competition: qualitative agreement between experimental and theoretically forecast outcomes. Science. 1980 Mar 28;207(4438):1491–1493. doi: 10.1126/science.6767274. [DOI] [PubMed] [Google Scholar]
  15. Helling R. B., Vargas C. N., Adams J. Evolution of Escherichia coli during growth in a constant environment. Genetics. 1987 Jul;116(3):349–358. doi: 10.1093/genetics/116.3.349. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lanz R., Erni B. The glucose transporter of the Escherichia coli phosphotransferase system. Mutant analysis of the invariant arginines, histidines, and domain linker. J Biol Chem. 1998 May 15;273(20):12239–12243. doi: 10.1074/jbc.273.20.12239. [DOI] [PubMed] [Google Scholar]
  17. Larson T. J., Ludtke D. N., Bell R. M. sn-Glycerol-3-phosphate auxotrophy of plsB strains of Escherichia coli: evidence that a second mutation, plsX, is required. J Bacteriol. 1984 Nov;160(2):711–717. doi: 10.1128/jb.160.2.711-717.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lengeler J. W. Carbohydrate transport in bacteria under environmental conditions, a black box? Antonie Van Leeuwenhoek. 1993;63(3-4):275–288. doi: 10.1007/BF00871223. [DOI] [PubMed] [Google Scholar]
  19. Mat-Jan F., Williams C. R., Clark D. P. Mutations permitting the anaerobic growth of Escherichia coli on trehalose. FEMS Microbiol Lett. 1991 Mar 1;62(2-3):149–152. doi: 10.1016/0378-1097(91)90149-5. [DOI] [PubMed] [Google Scholar]
  20. Miller J. H. Spontaneous mutators in bacteria: insights into pathways of mutagenesis and repair. Annu Rev Microbiol. 1996;50:625–643. doi: 10.1146/annurev.micro.50.1.625. [DOI] [PubMed] [Google Scholar]
  21. Muir M., Williams L., Ferenci T. Influence of transport energization on the growth yield of Escherichia coli. J Bacteriol. 1985 Sep;163(3):1237–1242. doi: 10.1128/jb.163.3.1237-1242.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Notley-McRobb L., Ferenci T. The generation of multiple co-existing mal-regulatory mutations through polygenic evolution in glucose-limited populations of Escherichia coli. Environ Microbiol. 1999 Feb;1(1):45–52. doi: 10.1046/j.1462-2920.1999.00003.x. [DOI] [PubMed] [Google Scholar]
  23. Notley L., Ferenci T. Differential expression of mal genes under cAMP and endogenous inducer control in nutrient-stressed Escherichia coli. Mol Microbiol. 1995 Apr;16(1):121–129. doi: 10.1111/j.1365-2958.1995.tb02397.x. [DOI] [PubMed] [Google Scholar]
  24. Rosenzweig R. F., Sharp R. R., Treves D. S., Adams J. Microbial evolution in a simple unstructured environment: genetic differentiation in Escherichia coli. Genetics. 1994 Aug;137(4):903–917. doi: 10.1093/genetics/137.4.903. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Ruijter G. J., van Meurs G., Verwey M. A., Postma P. W., van Dam K. Analysis of mutations that uncouple transport from phosphorylation in enzyme IIGlc of the Escherichia coli phosphoenolpyruvate-dependent phosphotransferase system. J Bacteriol. 1992 May;174(9):2843–2850. doi: 10.1128/jb.174.9.2843-2850.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Senn H., Lendenmann U., Snozzi M., Hamer G., Egli T. The growth of Escherichia coli in glucose-limited chemostat cultures: a re-examination of the kinetics. Biochim Biophys Acta. 1994 Dec 15;1201(3):424–436. doi: 10.1016/0304-4165(94)90072-8. [DOI] [PubMed] [Google Scholar]

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