The DOI matches its Crossref record; 44 of the 44 references it cites were found in a registry or an index.
The generation of multiple co‐existing mal ‐regulatory mutations through polygenic evolution in glucose‐limited populations of Escherichia coli
Abstract
The multicomponent glucose transport system of Escherichia coli was used to study the polygenic basis of increased fitness in prolonged nutrient‐limited, continuous cultures. After 280 generations of glucose‐limited growth, nearly all bacteria in four independent chemostat populations exhibited increased glucose transport and contained multiple, stable mutations. Fitter bacteria increased outer membrane permeability for glucose through overexpression of the LamB glycoporin. Three classes of mutation influenced LamB levels as well as regulation of other mal genes. Low‐level mal/lamB constitutivity resulted from mlc mutations acquired in all populations as well as changes at another uncharacterized locus. Larger increases in transporter content resulted from widespread acquisition of a regulatory malT–con mutation in fit isolates. The malT mutations sequenced from 67 adapted isolates were all single base substitutions resulting in amino acid replacements in the N‐terminal third of the MalT activator protein. Analysis of malT–con sequences revealed a mutational spectrum distinct from that found in plate‐selected malT mutants, suggesting that mutational pathways were affected by environmental factors. A second major finding was the remarkable allele diversity in malT within a population derived from a single clone, with at least 11 different alleles co‐existing in a population. The multiplicity of alleles (as well as those found in adaptive mgl changes in the accompanying study) suggest that the periodic selection events observed previously in such populations are not a major factor in reducing genetic diversity. A simple model is presented for the generation of genetic heterogeneity in bacterial populations undergoing polygenic selection.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
During ALE, clonal interference, bet hedging, genetic hitchhiking and fluctuating growth environments can lead to significant population heterogeneity.
“Stable phenotypes will accumulate rapidly, although clonal interference [42], bet hedging [43,60], genetic hitchhiking [61] and fluctuating growth environments can lead to significant population heterogeneity [22,62,63].”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [43]
Citations
Cites
Experiments in molecular genetics
Miller, J. H. (1972) · Medical Entomology and Zoology · Cited by 27,157
Escherichia coli and Salmonella typhimurium: Cellular and molecular biology
Lejeune, P. (1988) · Biochimie · doi:10.1016/0300-9084(88)90119-8 · Cited by 4,086
Cairns, J., Overbaugh, J., & Miller, S. (1988) · Nature · doi:10.1038/335142a0 · Cited by 1,025
Evolution of high mutation rates in experimental populations of E. coli
Sniegowski, P. D., Gerrish, P. J., & Lenski, R. E. (1997) · Nature · doi:10.1038/42701 · Cited by 879
Role of mutator alleles in adaptive evolution
Taddéi, F., Radman, M., Smith, J. M., Toupance, B., Gouyon, P. H., & Godelle, B. (1997) · Nature · doi:10.1038/42696 · Cited by 678
Rosenzweig, R. F., Sharp, R. R., Treves, D. S., & Adams, J. (1994) · Genetics · doi:10.1093/genetics/137.4.903 · Cited by 357
Dykhuizen, D. E., & Hartl, D. L. (1983) · Microbiological Reviews · doi:10.1128/mr.47.2.150-168.1983 · Cited by 324
Schaaper, R. M., Danforth, B. N., & Glickman, B. W. (1986) · Journal of Molecular Biology · doi:10.1016/0022-2836(86)90509-7 · Cited by 303
Evolution of Escherichia coli During Growth in a Constant Environment
Helling, R. B., Vargas, C. N., & Adams, J. (1987) · Genetics · doi:10.1093/genetics/116.3.349 · Cited by 283
ADAPTIVE MUTATION: The Uses of Adversity
Foster, P. L. (1993) · Annual Review of Microbiology · doi:10.1146/annurev.mi.47.100193.002343 · Cited by 262
SPONTANEOUS MUTATORS IN BACTERIA: Insights into Pathways of Mutagenesis and Repair
Miller, J. H. (1996) · Annual Review of Microbiology · doi:10.1146/annurev.micro.50.1.625 · Cited by 256
SELECTIVE MECHANISMS IN BACTERIAPreprint
Atwood, K. C., Schneider, L. K., & Rryan, F. J. (1951) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.1951.016.01.026 · Cited by 196
Ferenci, T. (1996) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.1996.tb00246.x · Cited by 184
Self-citationMUTATION AND ADAPTATION: The Directed Mutation Controversy in Evolutionary Perspective
Sniegowski, P., & Lenski, R. E. (1995) · Annual Review of Ecology and Systematics · doi:10.1146/annurev.es.26.110195.003005 · Cited by 167
Débarbouillé, M., Shuman, H. A., Silhavy, T. J., et al. (1978) · Journal of Molecular Biology · doi:10.1016/0022-2836(78)90304-2 · Cited by 163
Dykhuizen, D. E., & Hartl, D. L. (1983) · Microbiological Reviews · doi:10.1128/mmbr.47.2.150-168.1983 · Cited by 162
Sonti, R. V., & Roth, J. R. (1989) · Genetics · doi:10.1093/genetics/123.1.19 · Cited by 159
McRobb, L. S., Death, A. K., & Ferenci, T. (1997) · Microbiology · doi:10.1099/00221287-143-6-1909 · Cited by 153
Self-citationSenn, H. P., Lendenmann, U., Snozzi, M., et al. (1994) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/0304-4165(94)90072-8 · Cited by 146
PLUMBRIDGE, J. A. (1998) · Molecular Microbiology · doi:10.1046/j.1365-2958.1998.00685.x · Cited by 132
Kühnau, S., Reyes, M., Sievertsen, A., et al. (1991) · Journal of Bacteriology · doi:10.1128/jb.173.7.2180-2186.1991 · Cited by 129
Death, A. K., Notley, L., & Ferenci, T. (1993) · Journal of Bacteriology · doi:10.1128/jb.175.5.1475-1483.1993 · Cited by 116
Self-citationNotley, L., & Ferenci, T. (1996) · Journal of Bacteriology · doi:10.1128/jb.178.5.1465-1468.1996 · Cited by 111
Self-citationMcRobb, L. S., & Ferenci, T. (1999) · Environmental Microbiology · doi:10.1046/j.1462-2920.1999.00002.x · Cited by 109
Self-citationDecker, K., PLUMBRIDGE, J. A., & Boos, W. (1998) · Molecular Microbiology · doi:10.1046/j.1365-2958.1998.00694.x · Cited by 106
Maltotriose is the inducer of the maltose regulon of Escherichia coli
Raibaud, O., & Richet, E. (1987) · Journal of Bacteriology · doi:10.1128/jb.169.7.3059-3061.1987 · Cited by 93
Role of the catabolite activator protein in the maltose regulon of Escherichia coli
Chapon, C. (1982) · Journal of Bacteriology · doi:10.1128/jb.150.2.722-729.1982 · Cited by 91
Fitness of an Escherichia coli Mutator Gene
Gibson, T. C., Scheppe, M. L., & Cox, E. C. (1970) · Science · doi:10.1126/science.169.3946.686 · Cited by 88
Decker, K., Peist, R., Reidl, J., et al. (1993) · Journal of Bacteriology · doi:10.1128/jb.175.17.5655-5665.1993 · Cited by 77
Reidl, J., Römisch, K., Ehrmann, M., & Boos, W. (1989) · Journal of Bacteriology · doi:10.1128/jb.171.9.4888-4899.1989 · Cited by 74
Notley, L., & Ferenci, T. (1995) · Molecular Microbiology · doi:10.1111/j.1365-2958.1995.tb02397.x · Cited by 74
Self-citationDeath, A. K., & Ferenci, T. (1993) · Research in Microbiology · doi:10.1016/0923-2508(93)90002-j · Cited by 61
Self-citationGenetic analysis of sequences in maltoporin that contribute to binding domains and pore structure
Heine, H. G., Francis, G., Lee, K. S., et al. (1988) · Journal of Bacteriology · doi:10.1128/jb.170.4.1730-1738.1988 · Cited by 57
Ferenci, T., & Lee, K.-S. (1982) · Journal of Molecular Biology · doi:10.1016/0022-2836(82)90306-0 · Cited by 57
Self-citationH-NS and RpoS regulate emergence of Lac Ara+ mutants of Escherichia coli MCS2
Gómez-Gómez, J., Blázquez, J., Baquero, F., & Martínez, J. (1997) · Journal of Bacteriology · doi:10.1128/jb.179.14.4620-4622.1997 · Cited by 49
Kurlandzka, A., Rosenzweig, R., & Adams, J. (1991) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a040650 · Cited by 47
Bridges, B. A. (1994) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/0027-5107(94)90287-9 · Cited by 43
Dardonville, B., & Raibaud, O. (1990) · Journal of Bacteriology · doi:10.1128/jb.172.4.1846-1852.1990 · Cited by 42
Tröbner, W., & Piechocki, R. (1984) · Molecular and General Genetics MGG · doi:10.1007/bf00328719 · Cited by 38
Indications that mutagenesis in Salmonella may be subject to catabolite repression
MacPhee, D. G. (1985) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/0027-5107(85)90179-4 · Cited by 19
Takimoto, K., Tachibana, A., Ayaki, H., & Yamamoto, K. (1997) · Journal of Radiation Research · doi:10.1269/jrr.38.27 · Cited by 11
Adaptive mutation: a general phenomenon or special case?
Benson, S. A. (1997) · Bioessays · doi:10.1002/bies.950190104 · Cited by 9
Notley, L., Hillier, C. J., & Ferenci, T. (1994) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1994.tb07056.x · Cited by 2
Self-citationChan, W. C., Schirmer, T., & Ferenci, T. (1996) · Molecular Membrane Biology · doi:10.3109/09687689609160573 · Cited by 1
Self-citation
Flagged first, then by citations
Research works printed but not linked: 1
- Schwartz M.(1987)The maltose regulon. In Escherichia coliandSalmonella typhimurium:Cellular and Molecular Biology. Neidhardt F.C. Ingraham J.L. Low K.B. Magasanik B. Schaechter M. and Umbarger H.E. (eds). Washington DC: American Society for Microbiology Press pp.1482–1502.
Cited by
Sorted by citations
Molecular Basis of Bacterial Outer Membrane Permeability Revisited
Nikaido, H. (2003) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.67.4.593-656.2003 · Cited by 4,316
Evolution Experiments with Microorganisms: The Dynamics and Genetic Bases of Adaptation
Elena, S. F., & Lenski, R. E. (2003) · Nature Reviews Genetics · doi:10.1038/nrg1088 · Cited by 1,386
Adaptive laboratory evolution—Principles and applications for biotechnology
Dragosits, M., & Mattanovich, D. (2013) · Microbial Cell Factories · doi:10.1186/1475-2859-12-64 · Cited by 827
Parallel changes in gene expression after 20,000 generations of evolution in Escherichia coli
Cooper, T. F., Rozen, D. E., & Lenski, R. E. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0334340100 · Cited by 440
Severe Zinc Depletion of Escherichia coli
Graham, A. I., Hunt, S., Stokes, S. L., Bramall, N., Bunch, J., Cox, A. G., McLeod, C. W., & Poole, R. K. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.001503 · Cited by 156
The functional basis of adaptive evolution in chemostats
Gresham, D., & Hong, J. (2014) · FEMS Microbiology Reviews · doi:10.1111/1574-6976.12082 · Cited by 122
Quan, S., Ray, J. C. J., Kwota, Z., Duong, T., Balázsi, G., Cooper, T. F., & Monds, R. D. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002444 · Cited by 59
Notley-McRobb, L., Pinto, R., Seeto, S., & Ferenci, T. (2002) · Journal of Bacteriology · doi:10.1128/jb.184.3.739-745.2002 · Cited by 31
Self-citation
Metadata
- Authors
- Notley‐McRobb, L., & Ferenci, T.
- Affiliations
- The University of Sydney (AU)
- Corresponding author
- Ferenci, Thomas
- ORCID
- Ferenci, Thomas
- Venue
- Environmental Microbiology
- Publisher
- Wiley
- Published
- 1999-02
- Volume
- 1
- Issue
- 1
- Pages
- 45-52
- ISSN
- 1462-2912 (ISSN-L)
- 1462-2920
- OpenAlex
- W2089307705
- Cited by
- 105
- References
- 44
- Citations by year
- 2026: 1 · 2025: 1 · 2021: 7 · 2020: 3 · 2019: 1 · 2018: 3 · 2017: 1 · 2016: 1 · 2015: 4 · 2014: 5 · 2013: 7 · 2012: 6
- FWCI
- 3.49
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Environmental Microbiology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial Metabolic Engineering and Bioproduction
- Keywords
- glucose transport, Escherichia coli, mutation spectrum, allele diversity, genetic heterogeneity, outer membrane permeability
- MeSH terms
- Adaptation, Physiological, Alleles, Bacterial Outer Membrane Proteins, Bacterial Proteins, Biological Transport, Active, Culture Media, DNA-Binding Proteins, Escherichia coli, Biological Evolution, Genes, Bacterial, Glucose, Mutation, Receptors, Virus, Selection, Genetic, Transcription Factors, Genetic Variation, Porins, Amino Acid Substitution, Escherichia coli Proteins
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review