Assessment of the fitness impacts on Escherichia coli of acquisition of antibiotic resistance genes encoded by different types of genetic element

Enne, Virve I.; Delsol, Anne A.; Davis, G. R.; Hayward, SusanK.; Roe, John M.; Bennett, PM

doi:10.1093/jac/dki255

Cited by 95 publications

(76 citation statements)

References 31 publications

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“…2). A similar observation has been reported for two derivatives carrying Tn1 (21). Thus, the integration site of a mobile genetic element may have an impact on fitness of the host, a result that emphasizes the importance of studying isogenic strains.…”

Section: Discussionsupporting

confidence: 76%

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Inducible expression eliminates the fitness cost of vancomycin resistance in enterococci

Foucault

Depardieu

Courvalin

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

105

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Inducible vancomycin resistance in enterococci is due to a sophisticated mechanism that combines synthesis of cell wall peptidoglycan precursors with low affinity for glycopeptides and elimination of the normal target precursors. Although this dual mechanism, which involves seven genes organized in two operons, is predicted to have a high fitness cost, resistant enterococci have disseminated worldwide. We have evaluated the biological cost of VanB-type resistance due to acquisition of conjugative transposon Tn1549 in Enterococcus faecium and Enterococcus faecalis. Because fitness was dependent on the integration site of Tn1549, an isogenic set of E. faecalis was constructed to determine the cost of inducible or constitutive expression of resistance or of carriage of Tn1549. A luciferase gene was inserted in the integrase gene of the transposon to allow differential quantification of the strains in cocultures and in the digestive tract of gnotobiotic mice. Both in vitro and in vivo, carriage of inactivated or inducible Tn1549 had no cost for the host in the absence of induction by vancomycin. In contrast, induced or constitutively resistant strains not only had reduced fitness but were severely impaired in colonization ability and dissemination among mice. These data indicate that tight regulation of resistance expression drastically reduces the biological cost associated with vancomycin resistance in Enterococcus spp. and accounts for the widespread dissemination of these strains. Our findings are in agreement with the observation that regulation of expression is common in horizontally acquired resistance and represents an efficient evolutionary pathway for resistance determinants to become selectively neutral.O ne of the key parameters influencing emergence and stability of antibiotic resistance is the biological cost that resistance determinants impose on cell growth (1). Many studies have shown that resistant bacteria are less fit than their susceptible counterpart, although they can acquire compensatory mutations that restore fitness (2). However, most reports have dealt with resistance due to chromosomal mutations, and fewer have evaluated the fitness change due to acquisition of mobile genetic elements conferring clinically relevant resistance (3).Enterococci are commensals of the intestine of humans and animals but can also be opportunistic pathogens. This bacterial genus has acquired resistance to many antibiotics, and glycopeptides are often the ultimate treatment of infections due to these The vanA operon is part of transposon Tn1546, which is often carried by self-transferable plasmids, accounting for its spread (9). Dissemination of VanB-type resistance results from the spread of conjugative transposon Tn1549 (10) located on plasmids or in the chromosome. Despite the sophisticated dual mechanism of resistance, glycopeptide-resistant enterococci have disseminated worldwide.Two studies have investigated the burden of glycopeptide resistance imposed on enterococci, with conflicting results. A fitness di...

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Section: Discussionsupporting

confidence: 76%

“…Acquisition of Tn1 and Tn7, conferring resistance to ampicillin and trimethoprim, respectively, have no impact on the fitness of E. coli (21). In another study, 80% of Tn10 insertional mutants presented a fitness cost that was related to the insertion locus rather than to expression of tetracycline resistance (22).…”

Section: Discussionmentioning

confidence: 94%

Inducible expression eliminates the fitness cost of vancomycin resistance in enterococci

Foucault

Depardieu

Courvalin

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

105

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“…However, the in vitro fitness studies performed indicated that, at least for receptors harbouring three or fewer PAIs, the carriage of a higher number of islands was not directly associated with a higher fitness cost conferred by the acquisition of the plasmid. The absence of a clear fitness burden imposed by the initial acquisition of a resistance-encoding plasmid differs from most of the fitness studies, where it is associated with a biological cost (Dionisio et al, 2005;Enne et al, 2005). Thus, other factors, which may be possibly related to the genetic background of the bacteria, may be responsible for this tendency.…”

Section: Discussionmentioning

confidence: 92%

“…The relative fitness (W) of plasmid-carrying transconjugants was estimated by pairwise competition experiments between the transconjugants and the receptor strain in S2 minimal medium for 24 h, as described elsewhere (Ray et al, 2009), with the exception that 25 mg glucose ml 21 was added to the medium (Enne et al, 2005). Briefly, a single c.f.u.…”

Section: Methodsmentioning

confidence: 99%

Interplay between pathogenicity island carriage, resistance profile and plasmid acquisition in uropathogenic Escherichia coli

Calhau

Domingues

Ribeiro³

et al. 2015

Journal of Medical Microbiology

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This study aimed to characterize the relationship between pathogenicity islands (PAIs), single virulence genes and resistance among uropathogenic Escherichia coli, evaluating the resistance plasmid carriage fitness cost related to PAIs. For 65 urinary E. coli, antimicrobial susceptibility and extended-spectrum b-lactamase production were determined with the Vitek 2 Advanced Expert system. Phylogroup determination, detection of PAIs and virulence genes papAH, papC, sfa/foc, afa/dra, iutA, kpsMII, cnf1, eaeA, hlyA, stx1 and stx2, plasmid replicon typing and screening for plasmidic resistance determinants qnr, aac(69)-Ib-cr, qepA and bla CTX-M were carried out by PCR. Conjugation was performed between a donor carrying IncF, IncK and bla CTX-M-15 , and receptors carrying one to six PAIs. The relative fitness of transconjugants was estimated by pairwise competition experiments. PAI IV 536 (68 %), gene iutA (57 %) and resistance to ampicillin were the most prevalent traits. PAI I 536 , PAI II 536 , PAI III 536 and PAI II J96 were exclusively associated with susceptibility to amoxicillin/clavulanic acid, cefotaxime, ceftazidime, ciprofloxacin, gentamicin and trimethoprim/sulfamethoxazole, and were more prevalent in strains susceptible to ampicillin and cefalotin. PAI IV 536 , PAI II CFT073 and PAI I CFT073 were more prevalent among isolates showing resistance to amoxicillin/clavulanic acid, cefalotin, cefotaxime, ceftazidime and gentamicin. An inverse relationship was observed between the number of plasmids and the number of PAIs carried. Transconjugants were obtained for receptors carrying three or fewer PAIs. The mean relative fitness rates of these transconjugants were 0.87 (two PAIs), 1.00 (one PAI) and 1.09 (three PAI). The interplay between resistance, PAI carriage and fitness cost of plasmid acquisition could be considered PAI specific, and not necessarily associated with the number of PAIs.

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“…En contraste, los genes de resistencia a antibióti-cos localizados en plataformas móviles de DNA extracromosomal, generan menor gasto energético, por lo que tienden a mantenerse y expresarse por más tiempo (Enne et al, 2005).…”

Section: Mecanismos De Resistencia a Antibióticosunclassified

Perspectiva histórica del origen evolutivo de la resistencia a antibióticos

Bustos¹,

Rubio²,

Navarro³

2017

Rev. colomb. biotecnol.

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Perspectiva histórica de la resistencia a antibióticos 105 ARTÍCULO DE REVISIÓN Perspectiva histórica del origen evolutivo de la resistencia a antibióticos Evolutionary origin of antibiotic resistance, a historical perspective Resumen La resistencia a antimicrobianos representa un aspecto natural de evolución bacteriana, que puede resultar de mutaciones o por adquisición de genes foráneos. Hay diferentes posturas sobre el origen de ésta resistencia que explican la habilidad de estos microorganismos de adquirir nuevas características. Las teorías de la evolución de Lamarck y Darwin, han dado pie a experimentos diseñados para explorar el origen de la variación bacteriana y surgimiento de nuevas características. Estos estudios muestran que la resistencia está relacionada con mutaciones en genes cromosomales y/o la transferencia de elementos genéticos extracromosomales, que se expresan según la presión antibiótica ejercida. Está revisión recopila los principales experimentos y las conclusiones derivadas para explicar el fenómeno de resistencia a antibióticos.Palabras clave: resistencia a antibióticos, evolución, adaptación, mutación, transferencia horizontal. AbstractAntimicrobial resistance is a natural aspect of bacterial evolution that can result from mutations or acquisition of foreign genes. Various views on the origin of this resistance explain the ability of these organisms to acquire new features. Lamarck and Darwin's theories of evolution have led to experiments designed to explore the origin of bacterial variation and the emergence of new features. These experiments show that antimicrobial resistance is related to mutations in chromosomal genes and/or transfer of extrachromosomal genetic elements that can be expressed based on the antibiotic pressure exerted. The main experiments and findings that seek to explain the phenomenon of antibiotic resistance are reviewed here in.

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Assessment of the fitness impacts on Escherichia coli of acquisition of antibiotic resistance genes encoded by different types of genetic element

Abstract: The fitness impact imposed on E. coli 345-2 RifC by carriage of antibiotic resistance elements was generally low or non-existent, suggesting that once established, resistance may be difficult to eliminate through reduction in prescribing alone.

Cited by 95 publications

References 31 publications

Inducible expression eliminates the fitness cost of vancomycin resistance in enterococci

Inducible expression eliminates the fitness cost of vancomycin resistance in enterococci

Interplay between pathogenicity island carriage, resistance profile and plasmid acquisition in uropathogenic Escherichia coli

Perspectiva histórica del origen evolutivo de la resistencia a antibióticos

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