Fitness Trade-Offs in<i>bla</i><sub>TEM</sub>Evolution

Mroczkowska, Joanna E.; Barlow, Miriam

doi:10.1128/aac.00018-08

Cited by 49 publications

(26 citation statements)

References 27 publications

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“…Most such studies have focused on trade-offs in plants and animals, whereas the operation of trade-offs has been much less systematically studied with microorganisms. This is unfortunate because in the examples using bacteria and phages, it is clear that microbes are much more amenable to the analysis of not just the effects but also the potential molecular causes of trade-offs (De Paepe and Taddei, 2006;Jessup and Bohannan, 2008;Mroczkowska and Barlow, 2008;Tree et al, 2008;Lang et al, 2009;Lee et al, 2009;Kang and Park, 2010;De Paepe et al, 2011;Taylor and Buckling, 2011). Here, we identify mutually exclusive traits in Escherichia coli to define an ecological trade-off between self-protection and growth affinity in species-wide terms as well as in molecular detail.…”

Section: Introductionmentioning

confidence: 99%

A design-constraint trade-off underpins the diversity in ecologically important traits in species Escherichia coli

Phan

Ferenci

2013

The ISME Journal

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Bacterial species are internally diverse in genomic and multi-locus gene comparisons. The ecological causes of phenotypic and genotypic diversity within species are far less well understood. Here, we focus on the competitive fitness for growth on nutrients within Escherichia coli, an internally rich species. Competition experiments in nutrient-limited chemostats revealed that members of the ECOR collection exhibited a wide continuum of competitive abilities, with some fitter and some less fit than the lab strain MG1655. We observed an inverse relationship between competitiveness and the resistance of strains to detergent and antibiotic, consistent with the notion that membrane permeability and competitive fitness are linked by a trade-off between selfpreservation and nutritional competence (SPANC); high permeability has a postulated cost in antibacterial sensitivity whereas a low permeability has a cost in nutrient affinity. Isolates moved along the markedly nonlinear trade-off curve by mutational adaptation; an ECOR strain sensitive to antibacterials and a good competitor was easily converted by mutation into a mutant with higher resistance but poorer competition in the presence of low antibiotic concentrations. Conversely, a resistant ECOR strain changed into a better competitor after a short period of selection under nutrient limitation. In both directions, mutations can affect porin proteins and outer membrane permeability, as indicated by protein analysis, gene sequencing and an independent assay of outer membrane permeability. The extensive, species-wide diversity of E. coli in ecologically important traits can thus be explained as an evolutionary consequence of a SPANC trade-off driven by antagonistic pleiotropy.

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Section: Introductionmentioning

confidence: 99%

A design-constraint trade-off underpins the diversity in ecologically important traits in species Escherichia coli

Phan

Ferenci

2013

The ISME Journal

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“…Based on results from previous competition experiments (13) and enzymatic studies (8,12), we predicted that for bacteria passaged through ampicillin, bla TEM-12 would be eliminated from the plasmid and population and that for bacteria passaged through ceftazidime, bla TEM-1 would be eliminated from the plasmid and population.…”

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Recombination and Selection Can Removebla_TEMAlleles from Bacterial Populations

Mroczkowska

Barlow

2008

Antimicrob Agents Chemother

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We passaged cells expressing TEM-1 and TEM-12 from a single plasmid through either ampicillin or ceftazidime. We found that the combined effects of recombination and selection removed the bla TEM-1 allele from the bacterial population when it was passaged through ceftazidime or the bla TEM-12 allele when cultures were passaged through ampicillin.The overall abundance of bla TEM alleles in bacterial populations has caused multiple bla TEM alleles to coexist in single strains of bacteria (1, 4-7, 9-11, 15, 16), which has created the opportunity for recombination to occur among bla TEM alleles. The occurrence of recombination between two bla TEM alleles on a single plasmid strongly resembles gene conversion (14) and will cause the fragment between the recombination sites to be removed if the alleles are oriented in the same direction (3). This will typically result in the removal of one bla TEM allele from the plasmid while the remaining allele will usually be a chimera (Fig. 1). The potential for the removal of one bla TEM allele from a plasmid creates a situation in which closely related alleles may compete directly for retention in bacterial plasmids. While the bla TEM allele that is left on a plasmid following recombination is random, subsequent selection is not. Therefore, the combined effects of recombination and selection could result in the presence of a single allele on each copy of the plasmid and the removal of one of the alleles entirely from the population.To experimentally investigate whether allelic competition occurs in an environment with potential for both recombination and selection, we cloned the two bla TEM alleles bla TEM-1 and bla TEM-12 into the pAC3 vector (2) in the same orientation (Fig. 1A), validated the construction by sequencing, and expressed them from wild-type E. coli K-12. We passaged these bacteria through L broth containing either 32 g/ml ampicillin or 4 g/ml ceftazidime. Every 24 h, the saturated cultures were diluted 100 times in fresh broth, and the remaining bacteria were used to isolate plasmid for quantitative PCR (qPCR) analysis.Each 25-l qPCR reaction mixture contained 10 6 to 10 7 copies (60 pg of DNA) of the plasmid, 1ϫ Brilliant master mixture (Stratagene, La Jolla, CA), 200 nmol of each molecular beacon probe (Biosearch Technologies), and 900 nmol of each primer (Table 1). To measure the ratio between the origin of replication (Ori) and TEM alleles, recombination markers, and TET amplicons (Fig. 1), real-time PCR with TaqMan probes was performed. Each 25-l qPCR reaction mixture contained 10 6 to 10 7 copies of the plasmid DNA, 1ϫ Brilliant multiplex master mixture (Stratagene, La Jolla, CA), 200 nmol of each TaqMan probe (Biosearch Technologies), and appropriate concentrations of each primer (Table 1). The specificity of all primers and probes for the appropriate sequence was verified. Real-time PCR experiments were performed on a Stratagene Mx3000 multiplex qPCR system, with the quantitative PCR setting. The cycling conditions were either 1 cycle of 10 min at 95°C, ...

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“…Measurement of bacterial fitness competition between bacteria expressing different ␤-lactamases provides a sensitive method for detecting phenotypic differences (34). Furthermore, the acquisition of plasmids with antibiotic resistance genes may have several effects on bacterial fitness (2,25).…”

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confidence: 99%

Expression of OXA-Type and SFO-1 β-Lactamases Induces Changes in Peptidoglycan Composition and Affects Bacterial Fitness

Fernández

Pérez

Ayala

et al. 2012

Antimicrob Agents Chemother

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b␤-Lactamases and penicillin-binding proteins (PBPs) have evolved from a common ancestor. ␤-Lactamases are enzymes that degrade ␤-lactam antibiotics, whereas PBPs are involved in the synthesis and processing of peptidoglycan, which forms an elastic network in the bacterial cell wall. This study analyzed the interaction between ␤-lactamases and peptidoglycan and the impact on fitness and biofilm production. A representative set of all classes of ␤-lactamases was cloned in the expression vector pBGS18 under the control of the CTX-M promoter and expressed in Escherichia coli MG1655. The peptidoglycan composition of all clones was evaluated, and quantitative changes were found in E. coli strains expressing OXA-24, OXA-10-like, and SFO-1 (with its upstream regulator AmpR) ␤-lactamases; the level of cross-linked muropeptides decreased, and their average length increased. These changes were associated with a statistically significant fitness cost, which was demonstrated in both in vitro and in vivo experiments. The observed changes in peptidoglycan may be explained by the presence of residual DD-endopeptidase activity in these ␤-lactamases, which may result in hydrolysis of the peptide cross bridge. The biological cost associated with these changes provides important data regarding the interaction between ␤-lactamases and the metabolism of peptidoglycan and may provide an explanation for the epidemiology of these ␤-lactamases in Enterobacteriaceae.

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Fitness Trade-Offs inbla_TEMEvolution

Cited by 49 publications

References 27 publications

A design-constraint trade-off underpins the diversity in ecologically important traits in species Escherichia coli

A design-constraint trade-off underpins the diversity in ecologically important traits in species Escherichia coli

Recombination and Selection Can Removebla_TEMAlleles from Bacterial Populations

Expression of OXA-Type and SFO-1 β-Lactamases Induces Changes in Peptidoglycan Composition and Affects Bacterial Fitness

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Fitness Trade-Offs inblaTEMEvolution

Cited by 49 publications

References 27 publications

A design-constraint trade-off underpins the diversity in ecologically important traits in species Escherichia coli

A design-constraint trade-off underpins the diversity in ecologically important traits in species Escherichia coli

Recombination and Selection Can RemoveblaTEMAlleles from Bacterial Populations

Expression of OXA-Type and SFO-1 β-Lactamases Induces Changes in Peptidoglycan Composition and Affects Bacterial Fitness

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Fitness Trade-Offs inbla_TEMEvolution

Recombination and Selection Can Removebla_TEMAlleles from Bacterial Populations