The genetic basis of parallel and divergent phenotypic responses in evolving populations of<i>Escherichia coli</i>

Ostrowski, Elizabeth A.; Woods, Robert J.; Lenski, Richard E.

doi:10.1098/rspb.2007.1244

Cited by 73 publications

(81 citation statements)

References 52 publications

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“…Alternatively, a mathematical model of bacterial growth predicts that larger cells result if selection increases both the transport of the limiting nutrient into the cell and the efficiency of biomass conversion (25), without any direct selection on cell morphology per se. The rate of glucose transport presumably increased in the evolved bacteria, given their faster growth on glucose and the specificity of their fitness gains with respect to carbon sources that, like glucose, employ the phosphotransferase system (47,70). Also, the reduced costs of maintaining unused functions have increased the efficiency with which the evolved bacteria convert the limiting glucose into biomass (35,37,46).…”

Section: Discussionmentioning

confidence: 99%

Evolution of Penicillin-Binding Protein 2 Concentration and Cell Shape during a Long-Term Experiment withEscherichia coli

et al. 2009

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Peptidoglycan is the major component of the bacterial cell wall and is involved in osmotic protection and in determining cell shape. Cell shape potentially influences many processes, including nutrient uptake as well as cell survival and growth. Peptidoglycan is a dynamic structure that changes during the growth cycle. Penicillinbinding proteins (PBPs) catalyze the final stages of peptidoglycan synthesis. Although PBPs are biochemically and physiologically well characterized, their broader effects, especially their effects on organismal fitness, are not well understood. In a long-term experiment, 12 populations of Escherichia coli having a common ancestor were allowed to evolve for more than 40,000 generations in a defined environment. We previously identified mutations in the pbpA operon in one-half of these populations; this operon encodes PBP2 and RodA proteins that are involved in cell wall elongation. In this study, we characterized the effects of two of these mutations on competitive fitness and other phenotypes. By constructing and performing competition experiments with strains that are isogenic except for the pbpA alleles, we showed that both mutations that evolved were beneficial in the environment used for the long-term experiment and that these mutations caused parallel phenotypic changes. In particular, they reduced the cellular concentration of PBP2, thereby generating spherical cells with an increased volume. In contrast to their fitness-enhancing effect in the environment where they evolved, both mutations decreased cellular resistance to osmotic stress. Moreover, one mutation reduced fitness during prolonged stationary phase. Therefore, alteration of the PBP2 concentration contributed to physiological trade-offs and ecological specialization during experimental evolution.Bacteria in nature must survive multiple stresses and repeated shifts between feast and famine conditions. When Escherichia coli experiences nutritional deprivation, its growth rate decreases sharply and the cells become more spherical and resistant to various other environmental stresses (27). Many of the morphological and physiological changes that occur during entry into "stationary" phase are associated with the cell envelope, especially the cell wall.Peptidoglycan is the major component of the bacterial cell wall, and it affects osmotic stability and cell shape (78). Many of the final steps of peptidoglycan synthesis are catalyzed in the periplasm by the penicillin-binding proteins (PBPs) (40, 82). These enzymes are named for their binding to ␤-lactam antibiotics that inhibit cell wall biosynthesis. Twelve PBPs have been identified so far in E. coli, and they are classified as high-molecular-weight (HMW) and low-molecular-weight (LMW) PBPs. The HMW PBPs assemble both the glycan chain and the peptide cross-links of peptidoglycan and are further divided into class A PBPs (PBP1a, PBP1b, and PBP1c), which are bifunctional enzymes that perform both transglycosylation and transpeptidation functions, and class B PBPs (PBP2 and PBP...

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Section: Discussionmentioning

confidence: 99%

Evolution of Penicillin-Binding Protein 2 Concentration and Cell Shape during a Long-Term Experiment withEscherichia coli

et al. 2009

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“…For example, in Escherichia coli, on either lactate or glycerol minimal media, growth phenotypes at the evolutionary endpoint were convergent and repeatable, but had different underlying gene expression states [24]. In E. coli evolved in a glucose environment, a candidate gene approach demonstrated widespread parallelism in the direct response to selection, but considerable heterogeneity in (pleiotropic) mutant effects in five novel environments [25].…”

Section: Introductionmentioning

confidence: 99%

How to run far: multiple solutions and sex-specific responses to selective breeding for high voluntary activity levels

et al. 2010

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The response to uniform selection may occur in alternate ways that result in similar performance. We tested for multiple adaptive solutions during artificial selection for high voluntary wheel running in laboratory mice. At generation 43, the four replicate high runner (HR) lines averaged 2.85-fold more revolutions per day as compared with four non-selected control (C) lines, and females ran 1.11-fold more than males, with no sex-by-linetype interaction. Analysis of variance indicated significant differences among C lines but not among HR for revolutions per day. By contrast, average speed varied significantly among HR lines, but not among C, and showed a sex-by-linetype interaction, with the HR/C ratio being 2.02 for males and 2.45 for females. Time spent running varied among both HR and C lines, and showed a sex-by-linetype interaction, with the HR/C ratio being 1.52 for males but only 1.17 for females. Thus, females (speed) and males (speed, but also time) evolved differently, as did the replicate selected lines. Speed and time showed a trade-off among HR but not among C lines. These results demonstrate that uniform selection on a complex trait can cause consistent responses in the trait under direct selection while promoting divergence in the lower-level components of that trait.

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“…E. coli is often used to study bacterial adaptation (49), experimental evolution (9,36), and speciation (11,28,33,43). Comparisons between representative genomes continue to provide valuable information about these processes (58), and as genetic data accumulate, our understanding of how bacteria adapt to change and evolve is clarified.…”

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confidence: 99%

Cryptic Lineages of the Genus Escherichia

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Gordon

et al. 2009

Appl Environ Microbiol

244

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Extended multilocus sequence typing (MLST) analysis of atypical Escherichia isolates was used to identify five novel phylogenetic clades (CI to CV) among isolates from environmental, human, and animal sources. Analysis of individual housekeeping loci showed that E. coli and its sister clade, CI, remain largely indistinguishable and represent nascent evolutionary lineages. Conversely, clades of similar age (CIII and CIV) were found to be phylogenetically distinct. When all Escherichia lineages (named and unnamed) were evaluated, we found evidence that Escherichia fergusonii has evolved at an accelerated rate compared to E. coli, CI, CIII, CIV, and CV, suggesting that this species is younger than estimated by the molecular clock method. Although the five novel clades were phylogenetically distinct, we were unable to identify a discriminating biochemical marker for all but one of them (CIII) with traditional phenotypic profiling. CIII had a statistically different phenotype from E. coli that resulted from the loss of sucrose and sorbitol fermentation and lysine utilization. The lack of phenotypic distinction has likely hindered the ability to differentiate these clades from typical E. coli, and so their ecological significance and importance for applied and clinical microbiology are yet to be determined. However, our sampling suggests that CIII, CIV, and CV represent environmentally adapted Escherichia lineages that may be more abundant outside the host gastrointestinal tract.

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The genetic basis of parallel and divergent phenotypic responses in evolving populations ofEscherichia coli

Cited by 73 publications

References 52 publications

Evolution of Penicillin-Binding Protein 2 Concentration and Cell Shape during a Long-Term Experiment withEscherichia coli

Evolution of Penicillin-Binding Protein 2 Concentration and Cell Shape during a Long-Term Experiment withEscherichia coli

How to run far: multiple solutions and sex-specific responses to selective breeding for high voluntary activity levels

Cryptic Lineages of the Genus Escherichia

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