Crossref journal-article
American Society for Microbiology
Journal of Bacteriology (235)
Abstract

ABSTRACTTwelve populations ofEscherichia coliB all lostd-ribose catabolic function during 2,000 generations of evolution in glucose minimal medium. We sought to identify the population genetic processes and molecular genetic events that caused these rapid and parallel losses. Seven independent Rbs−mutants were isolated, and their competitive fitnesses were measured relative to that of their Rbs+progenitor. These Rbs−mutants were all about 1 to 2% more fit than the progenitor. A fluctuation test revealed an unusually high rate, about 5 × 10−5per cell generation, of mutation from Rbs+to Rbs−, which contributed to rapid fixation. At the molecular level, the loss of ribose catabolic function involved the deletion of part or all of the ribose operon (rbsgenes). The physical extent of the deletion varied between mutants, but each deletion was associated with an IS150element located immediately upstream of therbsoperon. The deletions apparently involved transposition into various locations within therbsoperon; recombination between the new IS150copy and the one upstream of therbsoperon then led to the deletion of the intervening sequence. To confirm that the beneficial fitness effect was caused by deletion of therbsoperon (and not some undetected mutation elsewhere), we used P1 transduction to restore the functionalrbsoperon to two Rbs−mutants, and we constructed another Rbs−strain by gene replacement with a deletion not involving IS150. All three of these new constructs confirmed that Rbs−mutants have a competitive advantage relative to their Rbs+counterparts in glucose minimal medium. The rapid and parallel evolutionary losses of ribose catabolic function thus involved both (i) an unusually high mutation rate, such that Rbs−mutants appeared repeatedly in all populations, and (ii) a selective advantage in glucose minimal medium that drove these mutants to fixation.

Bibliography

Cooper, V. S., Schneider, D., Blot, M., & Lenski, R. E. (2001). Mechanisms Causing Rapid and Parallel Losses of Ribose Catabolism in Evolving Populations ofEscherichia coliB. Journal of Bacteriology, 183(9), 2834–2841.

Authors 4
  1. Vaughn S. Cooper (first)
  2. Dominique Schneider (additional)
  3. Michel Blot (additional)
  4. Richard E. Lenski (additional)
References 39 Referenced 239
  1. 10.1128/jb.150.2.762-769.1982
  2. 10.1093/nar/25.17.3389
  3. Atwood K. C. Schneider L. K. Ryan F. J. Periodic selection in Escherichia coli.Proc. Natl. Acad. Sci. USA371951146155 (10.1073/pnas.37.3.146) / Proc. Natl. Acad. Sci. USA / Periodic selection in Escherichia coli by Atwood K. C. (1951)
  4. 10.1126/science.277.5331.1453
  5. Blot M. Transposable elements and adaptation of host bacteria.Genetica931994512 (10.1007/BF01435235) / Genetica / Transposable elements and adaptation of host bacteria by Blot M. (1994)
  6. Boyle J. S. Lew A. M. An inexpensive alternative to glassmilk for DNA purification.Trends Genet.1119958 (10.1016/S0168-9525(00)88977-5) / Trends Genet. / An inexpensive alternative to glassmilk for DNA purification by Boyle J. S. (1995)
  7. Chao L. Vargas C. Spear B. B. Cox E. C. Transposable elements as mutator genes in evolution.Nature3031983633635 (10.1038/303633a0) / Nature / Transposable elements as mutator genes in evolution by Chao L. (1983)
  8. Cooper V. S. Lenski R. E. The population genetics of ecological specialization in evolving Escherichia coli populations.Nature4072000736739 (10.1038/35037572) / Nature / The population genetics of ecological specialization in evolving Escherichia coli populations by Cooper V. S. (2000)
  9. Cunningham C. W. Jeng K. Husti J. Badgett M. Molineux I. J. Hillis D. M. Bull J. J. Parallel molecular evolution of deletions and nonsense mutations in bacteriophage T7.Mol. Biol. Evol.141997113116 (10.1093/oxfordjournals.molbev.a025697) / Mol. Biol. Evol. / Parallel molecular evolution of deletions and nonsense mutations in bacteriophage T7 by Cunningham C. W. (1997)
  10. De Visser J. A. G. M. Zeyl C. W. Gerrish P. J. Blanchard J. L. Lenski R. E. Diminishing returns from mutation supply rate in asexual populations.Science2831999404406 (10.1126/science.283.5400.404) / Science / Diminishing returns from mutation supply rate in asexual populations by De Visser J. A. G. M. (1999)
  11. 10.1128/IAI.59.12.4310-4317.1991
  12. Drake J. W. A constant rate of spontaneous mutation in DNA-based microbes.Proc. Natl. Acad. Sci. USA88199171607164 (10.1073/pnas.88.16.7160) / Proc. Natl. Acad. Sci. USA / A constant rate of spontaneous mutation in DNA-based microbes by Drake J. W. (1991)
  13. Dykhuizen D. E. Experimental studies of natural selection in bacteria.Annu. Rev. Ecol. Syst.211990378398 (10.1146/annurev.es.21.110190.002105) / Annu. Rev. Ecol. Syst. / Experimental studies of natural selection in bacteria by Dykhuizen D. E. (1990)
  14. 10.1128/mr.47.2.150-168.1983
  15. Elena S. F. Lenski R. E. Test of synergistic interactions among deleterious mutations in bacteria.Nature3901997395398 (10.1038/37108) / Nature / Test of synergistic interactions among deleterious mutations in bacteria by Elena S. F. (1997)
  16. 10.1023/A:1017067816551
  17. Goodrich-Blair H. Kolter R. Homocysteine thiolactone is a positive effector of ςs levels in Escherichia coli.FEMS Microbiol. Lett.1852000117121 / FEMS Microbiol. Lett. / Homocysteine thiolactone is a positive effector of ςs levels in Escherichia coli by Goodrich-Blair H. (2000)
  18. Harvey P. H. Pagel M. D. The comparative method in evolutionary biology. 1991 Oxford University Press Oxford United Kingdom (10.1093/oso/9780198546412.001.0001)
  19. Huey R. B. Gilchrist G. W. Carson M. L. Berrigan D. Serra L. Rapid evolution of a geographic cline in size in an introduced fly.Science2872000308309 (10.1126/science.287.5451.308) / Science / Rapid evolution of a geographic cline in size in an introduced fly by Huey R. B. (2000)
  20. 10.1128/jb.158.2.674-682.1984
  21. 10.1007/BF02986080
  22. 10.1128/jb.91.3.1029-1036.1966
  23. Lenski R. E. Travisano M. Dynamics of adaptation and diversification: a 10,000-generation experiment with bacterial populations.Proc. Natl. Acad. Sci. USA91199468086814 (10.1073/pnas.91.15.6808) / Proc. Natl. Acad. Sci. USA / Dynamics of adaptation and diversification: a 10,000-generation experiment with bacterial populations by Lenski R. E. (1994)
  24. 10.1086/285289
  25. Lin E. C. C. Dissimilatory pathways for sugars polyols and carboxylates Escherichia coli and Salmonella: cellular and molecular biology 2nd ed. Neidhardt F. C. Curtiss R. III Ingraham J. L. Lin E. C. C. Low K. B. Magasanik B. Reznikoff W. S. Riley M. Schaechter M. Umbarger H. E. 1996 307 342 ASM Press Washington D.C.
  26. 10.1093/genetics/28.6.491
  27. Ma W. T. Sandri G. H. Sarkar S. Analysis of the Luria-Delbrück distribution using discrete convolution powers.J. Appl. Prob.291992254267 / J. Appl. Prob. / Analysis of the Luria-Delbrück distribution using discrete convolution powers by Ma W. T. (1992)
  28. Miller J. H. Experiments in molecular genetics. 1972 Cold Spring Harbor Laboratory Cold Spring Harbor N.Y
  29. 10.1128/JB.180.17.4325-4331.1998
  30. Papadopoulos D. Schneider D. Meier-Eiss J. Arber W. Lenski R. E. Blot M. Genomic evolution during a 10,000-generation experiment with bacteria.Proc. Natl. Acad. Sci. USA96199938073812 (10.1073/pnas.96.7.3807) / Proc. Natl. Acad. Sci. USA / Genomic evolution during a 10,000-generation experiment with bacteria by Papadopoulos D. (1999)
  31. Sambrook J. Fritsch E. F. Maniatis T. Molecular cloning: a laboratory manual 2nd ed. 1989 Cold Spring Harbor Laboratory Press Cold Spring Harbor N.Y
  32. Sanger F. Nicklen S. Coulson A. R. DNA sequencing with chain-terminating inhibitors.Proc. Natl. Acad. Sci. USA74197754635467 (10.1073/pnas.74.12.5463) / Proc. Natl. Acad. Sci. USA / DNA sequencing with chain-terminating inhibitors by Sanger F. (1977)
  33. Schneider D. Duperchy E. Coursange E. Lenski R. E. Blot M. Long-term experimental evolution in Escherichia coli. IX. Characterization of IS-mediated mutations and rearrangements.Genetics1562000477488 (10.1093/genetics/156.2.477) / Genetics / Long-term experimental evolution in Escherichia coli. IX. Characterization of IS-mediated mutations and rearrangements by Schneider D. (2000)
  34. Simpson G. G. The major features of evolution. 1953 Columbia University Press New York N.Y (10.7312/simp93764)
  35. Sniegowski P. D Gerrish P. J. Lenski R. E. Evolution of high mutation rates in experimental populations of Escherichia coli.Nature3871997703705 (10.1038/42701) / Nature / Evolution of high mutation rates in experimental populations of Escherichia coli by Sniegowski P. D (1997)
  36. Stewart F. M. Fluctuation tests: how reliable are the estimates of mutation rates? Genetics 137 1994 1139 1146 (10.1093/genetics/137.4.1139) / Genetics / Fluctuation tests: how reliable are the estimates of mutation rates? by Stewart F. M. (1994)
  37. Taddei F. Radman M. Maynard Smith J. Toupance B. Gouyon P. H. Godelle B. Role of mutator alleles in adaptive evolution.Nature3871997700702 (10.1038/42696) / Nature / Role of mutator alleles in adaptive evolution by Taddei F. (1997)
  38. Travisano M. Vasi F. Lenski R. E. Long-term experimental evolution in Escherichia coli. III. Variation among replicate populations in correlated responses to novel environments.Evolution491995189200 / Evolution / Long-term experimental evolution in Escherichia coli. III. Variation among replicate populations in correlated responses to novel environments by Travisano M. (1995)
  39. Treves D. S. Manning S. Adams J. Repeated evolution of an acetate-crossfeeding polymorphism in long-term populations of Escherichia coli.Mol. Biol. Evol.151998789797 (10.1093/oxfordjournals.molbev.a025984) / Mol. Biol. Evol. / Repeated evolution of an acetate-crossfeeding polymorphism in long-term populations of Escherichia coli by Treves D. S. (1998)
Dates
Type When
Created 23 years, 1 month ago (July 27, 2002, 5:58 a.m.)
Deposited 1 year, 7 months ago (Jan. 5, 2024, 6:54 p.m.)
Indexed 3 weeks ago (Aug. 6, 2025, 8:30 a.m.)
Issued 24 years, 3 months ago (May 1, 2001)
Published 24 years, 3 months ago (May 1, 2001)
Published Print 24 years, 3 months ago (May 1, 2001)
Funders 0

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@article{Cooper_2001, title={Mechanisms Causing Rapid and Parallel Losses of Ribose Catabolism in Evolving Populations ofEscherichia coliB}, volume={183}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.183.9.2834-2841.2001}, DOI={10.1128/jb.183.9.2834-2841.2001}, number={9}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Cooper, Vaughn S. and Schneider, Dominique and Blot, Michel and Lenski, Richard E.}, year={2001}, month=may, pages={2834–2841} }