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. 1996 May;143(1):15–26. doi: 10.1093/genetics/143.1.15

Long-Term Experimental Evolution in Escherichia Coli. IV. Targets of Selection and the Specificity of Adaptation

M Travisano 1, R E Lenski 1
PMCID: PMC1207249  PMID: 8722758

Abstract

This study investigates the physiological manifestation of adaptive evolutionary change in 12 replicate populations of Escherichia coli that were propagated for 2000 generations in a glucose-limited environment. Representative genotypes from each population were assayed for fitness relative to their common ancestor in the experimental glucose environment and in 11 novel single-nutrient environments. After 2000 generations, the 12 derived genotypes had diverged into at least six distinct phenotypic classes. The nutrients were classified into four groups based upon their uptake physiology. All 12 derived genotypes improved in fitness by similar amounts in the glucose environment, and this pattern of parallel fitness gains was also seen in those novel environments where the limiting nutrient shared uptake mechanisms with glucose. Fitness showed little or no consistent improvement, but much greater genetic variation, in novel environments where the limiting nutrient differed from glucose in its uptake mechanisms. This pattern of fitness variation in the novel nutrient environments suggests that the independently derived genotypes adapted to the glucose environment by similar, but not identical, changes in the physiological mechanisms for moving glucose across both the inner and outer membranes.

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Selected References

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  1. Büchel D. E., Gronenborn B., Müller-Hill B. Sequence of the lactose permease gene. Nature. 1980 Feb 7;283(5747):541–545. doi: 10.1038/283541a0. [DOI] [PubMed] [Google Scholar]
  2. Chauvin F., Brand L., Roseman S. Sugar transport by the bacterial phosphotransferase system. Characterization of the Escherichia coli enzyme I monomer/dimer equilibrium by fluorescence anisotropy. J Biol Chem. 1994 Aug 12;269(32):20263–20269. [PubMed] [Google Scholar]
  3. Chauvin F., Brand L., Roseman S. Sugar transport by the bacterial phosphotransferase system. Characterization of the Escherichia coli enzyme I monomer/dimer transition kinetics by fluorescence anisotropy. J Biol Chem. 1994 Aug 12;269(32):20270–20274. [PubMed] [Google Scholar]
  4. Cowan S. W., Schirmer T., Rummel G., Steiert M., Ghosh R., Pauptit R. A., Jansonius J. N., Rosenbusch J. P. Crystal structures explain functional properties of two E. coli porins. Nature. 1992 Aug 27;358(6389):727–733. doi: 10.1038/358727a0. [DOI] [PubMed] [Google Scholar]
  5. Davis T., Yamada M., Elgort M., Saier M. H., Jr Nucleotide sequence of the mannitol (mtl) operon in Escherichia coli. Mol Microbiol. 1988 May;2(3):405–412. doi: 10.1111/j.1365-2958.1988.tb00045.x. [DOI] [PubMed] [Google Scholar]
  6. De Reuse H., Danchin A. Positive regulation of the pts operon of Escherichia coli: genetic evidence for a signal transduction mechanism. J Bacteriol. 1991 Jan;173(2):727–733. doi: 10.1128/jb.173.2.727-733.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. De Reuse H., Danchin A. The ptsH, ptsI, and crr genes of the Escherichia coli phosphoenolpyruvate-dependent phosphotransferase system: a complex operon with several modes of transcription. J Bacteriol. 1988 Sep;170(9):3827–3837. doi: 10.1128/jb.170.9.3827-3837.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Drake J. W. A constant rate of spontaneous mutation in DNA-based microbes. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7160–7164. doi: 10.1073/pnas.88.16.7160. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Erni B., Zanolari B., Kocher H. P. The mannose permease of Escherichia coli consists of three different proteins. Amino acid sequence and function in sugar transport, sugar phosphorylation, and penetration of phage lambda DNA. J Biol Chem. 1987 Apr 15;262(11):5238–5247. [PubMed] [Google Scholar]
  10. Ferenci T., Schwentorat M., Ullrich S., Vilmart J. Lambda receptor in the outer membrane of Escherichia coli as a binding protein for maltodextrins and starch polysaccharides. J Bacteriol. 1980 May;142(2):521–526. doi: 10.1128/jb.142.2.521-526.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Figge R. M., Ramseier T. M., Saier M. H., Jr The mannitol repressor (MtlR) of Escherichia coli. J Bacteriol. 1994 Feb;176(3):840–847. doi: 10.1128/jb.176.3.840-847.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gould S. J., Lewontin R. C. The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proc R Soc Lond B Biol Sci. 1979 Sep 21;205(1161):581–598. doi: 10.1098/rspb.1979.0086. [DOI] [PubMed] [Google Scholar]
  13. Jahreis K., Postma P. W., Lengeler J. W. Nucleotide sequence of the ilvH-fruR gene region of Escherichia coli K12 and Salmonella typhimurium LT2. Mol Gen Genet. 1991 Apr;226(1-2):332–336. doi: 10.1007/BF00273623. [DOI] [PubMed] [Google Scholar]
  14. Kalnins A., Otto K., Rüther U., Müller-Hill B. Sequence of the lacZ gene of Escherichia coli. EMBO J. 1983;2(4):593–597. doi: 10.1002/j.1460-2075.1983.tb01468.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Klein W., Boos W. Induction of the lambda receptor is essential for effective uptake of trehalose in Escherichia coli. J Bacteriol. 1993 Mar;175(6):1682–1686. doi: 10.1128/jb.175.6.1682-1686.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kornberg H. L. Fructose transport by Escherichia coli. Philos Trans R Soc Lond B Biol Sci. 1990 Jan 30;326(1236):505–513. doi: 10.1098/rstb.1990.0028. [DOI] [PubMed] [Google Scholar]
  17. Kukuruzinska M. A., Harrington W. F., Roseman S. Sugar transport by the bacterial phosphotransferase system. Studies on the molecular weight and association of enzyme I. J Biol Chem. 1982 Dec 10;257(23):14470–14476. [PubMed] [Google Scholar]
  18. Lee C. A., Saier M. H., Jr Mannitol-specific enzyme II of the bacterial phosphotransferase system. III. The nucleotide sequence of the permease gene. J Biol Chem. 1983 Sep 10;258(17):10761–10767. [PubMed] [Google Scholar]
  19. Lenski R. E., Souza V., Duong L. P., Phan Q. G., Nguyen T. N., Bertrand K. P. Epistatic effects of promoter and repressor functions of the Tn10 tetracycline-resistance operon of the fitness of Escherichia coli. Mol Ecol. 1994 Apr;3(2):127–135. doi: 10.1111/j.1365-294x.1994.tb00113.x. [DOI] [PubMed] [Google Scholar]
  20. Lenski R. E., Travisano M. Dynamics of adaptation and diversification: a 10,000-generation experiment with bacterial populations. Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):6808–6814. doi: 10.1073/pnas.91.15.6808. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. LiCalsi C., Crocenzi T. S., Freire E., Roseman S. Sugar transport by the bacterial phosphotransferase system. Structural and thermodynamic domains of enzyme I of Salmonella typhimurium. J Biol Chem. 1991 Oct 15;266(29):19519–19527. [PubMed] [Google Scholar]
  22. Liljeström P. L., Liljeström P. Nucleotide sequence of the melA gene, coding for alpha-galactosidase in Escherichia coli K-12. Nucleic Acids Res. 1987 Mar 11;15(5):2213–2220. doi: 10.1093/nar/15.5.2213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Maddox J. Is molecular biology yet a science? Nature. 1992 Jan 16;355(6357):201–201. doi: 10.1038/355201a0. [DOI] [PubMed] [Google Scholar]
  24. Miles J. S., Guest J. R. Nucleotide sequence and transcriptional start point of the phosphomannose isomerase gene (manA) of Escherichia coli. Gene. 1984 Dec;32(1-2):41–48. doi: 10.1016/0378-1119(84)90030-1. [DOI] [PubMed] [Google Scholar]
  25. Mueller L. D. Evolution of competitive ability in Drosophila by density-dependent natural selection. Proc Natl Acad Sci U S A. 1988 Jun;85(12):4383–4386. doi: 10.1073/pnas.85.12.4383. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Muramatsu S., Mizuno T. Nucleotide sequence of the region encompassing the glpKF operon and its upstream region containing a bent DNA sequence of Escherichia coli. Nucleic Acids Res. 1989 Jun 12;17(11):4378–4378. [PMC free article] [PubMed] [Google Scholar]
  27. Orchard L. M., Kornberg H. L. Sequence similarities between the gene specifying 1-phosphofructokinase (fruK), genes specifying other kinases in Escherichia coli K12, and lacC of Staphylococcus aureus. Proc Biol Sci. 1990 Nov 22;242(1304):87–90. doi: 10.1098/rspb.1990.0108. [DOI] [PubMed] [Google Scholar]
  28. Peri K. G., Goldie H., Waygood E. B. Cloning and characterization of the N-acetylglucosamine operon of Escherichia coli. Biochem Cell Biol. 1990 Jan;68(1):123–137. doi: 10.1139/o90-017. [DOI] [PubMed] [Google Scholar]
  29. Plumbridge J., Kolb A. CAP and Nag repressor binding to the regulatory regions of the nagE-B and manX genes of Escherichia coli. J Mol Biol. 1991 Feb 20;217(4):661–679. doi: 10.1016/0022-2836(91)90524-a. [DOI] [PubMed] [Google Scholar]
  30. Postma P. W., Lengeler J. W., Jacobson G. R. Phosphoenolpyruvate:carbohydrate phosphotransferase systems of bacteria. Microbiol Rev. 1993 Sep;57(3):543–594. doi: 10.1128/mr.57.3.543-594.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Prior T. I., Kornberg H. L. Nucleotide sequence of fruA, the gene specifying enzyme IIfru of the phosphoenolpyruvate-dependent sugar phosphotransferase system in Escherichia coli K12. J Gen Microbiol. 1988 Oct;134(10):2757–2768. doi: 10.1099/00221287-134-10-2757. [DOI] [PubMed] [Google Scholar]
  32. Saier M. H., Jr Protein phosphorylation and allosteric control of inducer exclusion and catabolite repression by the bacterial phosphoenolpyruvate: sugar phosphotransferase system. Microbiol Rev. 1989 Mar;53(1):109–120. doi: 10.1128/mr.53.1.109-120.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Saier M. H., Jr, Simoni R. D., Roseman S. The physiological behavior of enzyme I and heat-stable protein mutants of a bacterial phosphotransferase system. J Biol Chem. 1970 Nov 10;245(21):5870–5873. [PubMed] [Google Scholar]
  34. Schindler H., Rosenbusch J. P. Matrix protein from Escherichia coli outer membranes forms voltage-controlled channels in lipid bilayers. Proc Natl Acad Sci U S A. 1978 Aug;75(8):3751–3755. doi: 10.1073/pnas.75.8.3751. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Travisano M., Mongold J. A., Bennett A. F., Lenski R. E. Experimental tests of the roles of adaptation, chance, and history in evolution. Science. 1995 Jan 6;267(5194):87–90. doi: 10.1126/science.7809610. [DOI] [PubMed] [Google Scholar]
  36. Webster C., Gardner L., Busby S. The Escherichia coli melR gene encodes a DNA-binding protein with affinity for specific sequences located in the melibiose-operon regulatory region. Gene. 1989 Nov 30;83(2):207–213. doi: 10.1016/0378-1119(89)90106-6. [DOI] [PubMed] [Google Scholar]
  37. Weissenborn D. L., Wittekindt N., Larson T. J. Structure and regulation of the glpFK operon encoding glycerol diffusion facilitator and glycerol kinase of Escherichia coli K-12. J Biol Chem. 1992 Mar 25;267(9):6122–6131. [PubMed] [Google Scholar]
  38. Yamada M., Saier M. H., Jr Glucitol-specific enzymes of the phosphotransferase system in Escherichia coli. Nucleotide sequence of the gut operon. J Biol Chem. 1987 Apr 25;262(12):5455–5463. [PubMed] [Google Scholar]
  39. Yamada M., Saier M. H., Jr Positive and negative regulators for glucitol (gut) operon expression in Escherichia coli. J Mol Biol. 1988 Oct 5;203(3):569–583. doi: 10.1016/0022-2836(88)90193-3. [DOI] [PubMed] [Google Scholar]
  40. Yazyu H., Shiota-Niiya S., Shimamoto T., Kanazawa H., Futai M., Tsuchiya T. Nucleotide sequence of the melB gene and characteristics of deduced amino acid sequence of the melibiose carrier in Escherichia coli. J Biol Chem. 1984 Apr 10;259(7):4320–4326. [PubMed] [Google Scholar]
  41. Ye S. Z., Larson T. J. Structures of the promoter and operator of the glpD gene encoding aerobic sn-glycerol-3-phosphate dehydrogenase of Escherichia coli K-12. J Bacteriol. 1988 Sep;170(9):4209–4215. doi: 10.1128/jb.170.9.4209-4215.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]

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