This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Cooper, V. S.
Right arrow Articles by Lenski, R. E.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Cooper, V. S.
Right arrow Articles by Lenski, R. E.

 Previous Article  |  Next Article 

Journal of Bacteriology, May 2001, p. 2834-2841, Vol. 183, No. 9
0021-9193/01/$04.00+0   DOI: 10.1128/JB.183.9.2834-2841.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

Mechanisms Causing Rapid and Parallel Losses of Ribose Catabolism in Evolving Populations of Escherichia coli B

Vaughn S. Cooper,1,* Dominique Schneider,2 Michel Blot,2 and Richard E. Lenski1

Center for Microbial Ecology, Michigan State University, East Lansing, Michigan 48824,1 and Laboratoire Plasticité et Expression des Génomes Microbiens, CNRS FRE2029, CEA LRC12, Université Joseph Fourier, 38041 Grenoble Cedex 9, France2

Received 7 March 2000/Accepted 14 February 2001

Twelve populations of Escherichia coli B all lost D-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 × 10-5 per 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 (rbs genes). The physical extent of the deletion varied between mutants, but each deletion was associated with an IS150 element located immediately upstream of the rbs operon. The deletions apparently involved transposition into various locations within the rbs operon; recombination between the new IS150 copy and the one upstream of the rbs operon then led to the deletion of the intervening sequence. To confirm that the beneficial fitness effect was caused by deletion of the rbs operon (and not some undetected mutation elsewhere), we used P1 transduction to restore the functional rbs operon 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.

* Corresponding author. Present address: Department of Biology, University of Michigan, Ann Arbor, MI 48109. Phone: (734) 764-8500. Fax: (734) 647-0884. E-mail: vcooper{at}umich.edu.

Journal of Bacteriology, May 2001, p. 2834-2841, Vol. 183, No. 9
0021-9193/01/$04.00+0   DOI: 10.1128/JB.183.9.2834-2841.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.


This article has been cited by other articles:

  • Zhong, S., Miller, S. P., Dykhuizen, D. E., Dean, A. M. (2009). Transcription, Translation, and the Evolution of Specialists and Generalists. Mol Biol Evol 26: 2661-2678 [Abstract] [Full Text]  
  • Vriezen, J. A. C., Valliere, M., Riley, M. A. (2009). The Evolution of Reduced Microbial Killing. Gen Biol Evol 2009: 400-408 [Abstract] [Full Text]  
  • Lang, G. I., Murray, A. W., Botstein, D. (2009). The cost of gene expression underlies a fitness trade-off in yeast. Proc. Natl. Acad. Sci. USA 106: 5755-5760 [Abstract] [Full Text]  
  • Philippe, N., Pelosi, L., Lenski, R. E., Schneider, D. (2009). Evolution of Penicillin-Binding Protein 2 Concentration and Cell Shape during a Long-Term Experiment with Escherichia coli. J. Bacteriol. 191: 909-921 [Abstract] [Full Text]  
  • Sleight, S. C., Orlic, C., Schneider, D., Lenski, R. E. (2008). Genetic Basis of Evolutionary Adaptation by Escherichia coli to Stressful Cycles of Freezing, Thawing and Growth. Genetics 180: 431-443 [Abstract] [Full Text]  
  • Blount, Z. D., Borland, C. Z., Lenski, R. E. (2008). Inaugural Article: Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli. Proc. Natl. Acad. Sci. USA 105: 7899-7906 [Abstract] [Full Text]  
  • Ostrowski, E. A, Woods, R. J, Lenski, R. E (2008). The genetic basis of parallel and divergent phenotypic responses in evolving populations of Escherichia coli. Proc R Soc B 275: 277-284 [Abstract] [Full Text]  
  • Le Gac, M., Brazas, M. D., Bertrand, M., Tyerman, J. G., Spencer, C. C., Hancock, R. E. W., Doebeli, M. (2008). Metabolic Changes Associated With Adaptive Diversification in Escherichia coli. Genetics 178: 1049-1060 [Abstract] [Full Text]  
  • Jasmin, J.-N., Kassen, R. (2007). Evolution of a single niche specialist in variable environments. Proc R Soc B 274: 2761-2767 [Abstract] [Full Text]  
  • Wagner, A., Lewis, C., Bichsel, M. (2007). A survey of bacterial insertion sequences using IScan. Nucleic Acids Res 35: 5284-5293 [Abstract] [Full Text]  
  • Bennett, A. F., Lenski, R. E. (2007). Colloquium Papers: An experimental test of evolutionary trade-offs during temperature adaptation. Proc. Natl. Acad. Sci. USA 104: 8649-8654 [Abstract] [Full Text]  
  • Bantinaki, E., Kassen, R., Knight, C. G., Robinson, Z., Spiers, A. J., Rainey, P. B. (2007). Adaptive Divergence in Experimental Populations of Pseudomonas fluorescens. III. Mutational Origins of Wrinkly Spreader Diversity. Genetics 176: 441-453 [Abstract] [Full Text]  
  • Bacher, J. M., Metzgar, D., de Crecy-Lagard, V. (2006). Rapid Evolution of Diminished Transformability in Acinetobacter baylyi. J. Bacteriol. 188: 8534-8542 [Abstract] [Full Text]  
  • Rath, D., Jawali, N. (2006). Loss of Expression of cspC, a Cold Shock Family Gene, Confers a Gain of Fitness in Escherichia coli K-12 Strains.. J. Bacteriol. 188: 6780-6785 [Abstract] [Full Text]  
  • Domelier, A.-S., van der Mee-Marquet, N., Grandet, A., Mereghetti, L., Rosenau, A., Quentin, R. (2006). Loss of Catabolic Function in Streptococcus agalactiae Strains and Its Association with Neonatal Meningitis.. J. Clin. Microbiol. 44: 3245-3250 [Abstract] [Full Text]  
  • Pelosi, L., Kuhn, L., Guetta, D., Garin, J., Geiselmann, J., Lenski, R. E., Schneider, D. (2006). Parallel Changes in Global Protein Profiles During Long-Term Experimental Evolution in Escherichia coli. Genetics 173: 1851-1869 [Abstract] [Full Text]  
  • Woods, R., Schneider, D., Winkworth, C. L., Riley, M. A., Lenski, R. E. (2006). Tests of parallel molecular evolution in a long-term experiment with Escherichia coli. Proc. Natl. Acad. Sci. USA 103: 9107-9112 [Abstract] [Full Text]  
  • Goymer, P., Kahn, S. G., Malone, J. G., Gehrig, S. M., Spiers, A. J., Rainey, P. B. (2006). Adaptive Divergence in Experimental Populations of Pseudomonas fluorescens. II. Role of the GGDEF Regulator WspR in Evolution and Development of the Wrinkly Spreader Phenotype. Genetics 173: 515-526 [Abstract] [Full Text]  
  • Velicer, G. J., Raddatz, G., Keller, H., Deiss, S., Lanz, C., Dinkelacker, I., Schuster, S. C. (2006). Comprehensive mutation identification in an evolved bacterial cooperator and its cheating ancestor. Proc. Natl. Acad. Sci. USA 103: 8107-8112 [Abstract] [Full Text]  
  • Wagner, A. (2006). Periodic Extinctions of Transposable Elements in Bacterial Lineages: Evidence from Intragenomic Variation in Multiple Genomes. Mol Biol Evol 23: 723-733 [Abstract] [Full Text]  
  • Sliwa, P., Korona, R. (2005). Loss of dispensable genes is not adaptive in yeast. Proc. Natl. Acad. Sci. USA 102: 17670-17674 [Abstract] [Full Text]  
  • Fong, S. S., Joyce, A. R., Palsson, B. O. (2005). Parallel adaptive evolution cultures of Escherichia coli lead to convergent growth phenotypes with different gene expression states. Genome Res 15: 1365-1372 [Abstract] [Full Text]  
  • Cooper, T. F., Beaumont, H. J. E., Rainey, P. B. (2005). Biofilm diversity as a test of the insurance hypothesis. Microbiology 151: 2815-2816 [Full Text]  
  • Crozat, E., Philippe, N., Lenski, R. E., Geiselmann, J., Schneider, D. (2005). Long-Term Experimental Evolution in Escherichia coli. XII. DNA Topology as a Key Target of Selection. Genetics 169: 523-532 [Abstract] [Full Text]  
  • Whitaker, R. J., Banfield, J. F. (2005). Population Dynamics Through the Lens of Extreme Environments. Reviews in Mineralogy and Geochemistry 59: 259-277 [Full Text]  
  • Rezwan, F., Lan, R., Reeves, P. R. (2004). Molecular Basis of the Indole-Negative Reaction in Shigella Strains: Extensive Damages to the tna Operon by Insertion Sequences. J. Bacteriol. 186: 7460-7465 [Abstract] [Full Text]  
  • Nilsson, A. I., Kugelberg, E., Berg, O. G., Andersson, D. I. (2004). Experimental Adaptation of Salmonella typhimurium to Mice. Genetics 168: 1119-1130 [Abstract] [Full Text]  
  • de Visser, J. A. G. M., Akkermans, A. D. L., Hoekstra, R. F., de Vos, W. M. (2004). Insertion-Sequence-Mediated Mutations Isolated During Adaptation to Growth and Starvation in Lactococcus lactis. Genetics 168: 1145-1157 [Abstract] [Full Text]  
  • Hittinger, C. T., Rokas, A., Carroll, S. B. (2004). Parallel inactivation of multiple GAL pathway genes and ecological diversification in yeasts. Proc. Natl. Acad. Sci. USA 101: 14144-14149 [Abstract] [Full Text]  
  • Zhong, S., Khodursky, A., Dykhuizen, D. E., Dean, A. M. (2004). Evolutionary genomics of ecological specialization. Proc. Natl. Acad. Sci. USA 101: 11719-11724 [Abstract] [Full Text]  
  • MacLean, R. C., Bell, G., Rainey, P. B. (2004). The evolution of a pleiotropic fitness tradeoff in Pseudomonas fluorescens. Proc. Natl. Acad. Sci. USA 101: 8072-8077 [Abstract] [Full Text]  
  • Loewe, L. (2004). Response to Comment on "High Deleterious Genomic Mutation Rate in Stationary Phase of Escherichia coli". Science 304: 518d-518d [Full Text]  
  • Datta, S., Khan, A., Nandy, R. K., Rehman, M., Sinha, S., Chattopadhyay, S., Das, S. C., Nair, G. B. (2003). Environmental Isolates of Aeromonas spp. Harboring the cagA-Like Gene of Helicobacter pylori. Appl. Environ. Microbiol. 69: 4291-4295 [Abstract] [Full Text]  
  • Cooper, T. F., Rozen, D. E., Lenski, R. E. (2003). Parallel changes in gene expression after 20,000 generations of evolution in Escherichiacoli. Proc. Natl. Acad. Sci. USA 100: 1072-1077 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»