Multiple Antibiotic Resistance Gene Transfer from Animal to Human Enterococci in the Digestive Tract of Gnotobiotic Mice

Moubareck, Carole Ayoub; Bourgeois, N.; Courvalin, Patrice; Doucet‐Populaire, Florence

doi:10.1128/aac.47.9.2993-2996.2003

Cited by 108 publications

(76 citation statements)

References 24 publications

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“…Thus, in complex bacterial ecosystems, low densities of donor and recipient bacteria may lower the frequency of direct bacterial encounters and thus decrease the chance of conjugation-mediated HGT. Several studies reported inefficient enterobacterial HGT in the normal mammalian gut (15)(16)(17), whereas others identified higher rates of HGT (18,19). This suggested that particular conditions exist that might favor plasmid exchange between Enterobacteriaceae.…”

mentioning

confidence: 94%

Gut inflammation can boost horizontal gene transfer between pathogenic and commensal Enterobacteriaceae

Stecher

Denzler

Maier

et al. 2012

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

432

399

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The mammalian gut harbors a dense microbial community interacting in multiple ways, including horizontal gene transfer (HGT). Pangenome analyses established particularly high levels of genetic flux between Gram-negative Enterobacteriaceae. However, the mechanisms fostering intraenterobacterial HGT are incompletely understood. Using a mouse colitis model, we found that Salmonella-inflicted enteropathy elicits parallel blooms of the pathogen and of resident commensal Escherichia coli. These blooms boosted conjugative HGT of the colicin-plasmid p2 from Salmonella enterica serovar Typhimurium to E. coli. Transconjugation efficiencies of ∼100% in vivo were attributable to high intrinsic p2-transfer rates. Plasmid-encoded fitness benefits contributed little. Under normal conditions, HGT was blocked by the commensal microbiota inhibiting contact-dependent conjugation between Enterobacteriaceae. Our data show that pathogen-driven inflammatory responses in the gut can generate transient enterobacterial blooms in which conjugative transfer occurs at unprecedented rates. These blooms may favor reassortment of plasmid-encoded genes between pathogens and commensals fostering the spread of fitness-, virulence-, and antibiotic-resistance determinants.bacterial evolution | hospital-acquired infection | mucosal immune response | plasmid spread

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mentioning

confidence: 94%

Gut inflammation can boost horizontal gene transfer between pathogenic and commensal Enterobacteriaceae

Stecher

Denzler

Maier

et al. 2012

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

432

399

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“…Similar levels of gut colonization of gnotobiotic mice by Enterococcus spp. have been reported (18). Expression of VanB-type resistance impairs colonization.…”

Section: Impact Of Vancomycin Resistance On Fitness Of Enterococci Inmentioning

confidence: 99%

Inducible expression eliminates the fitness cost of vancomycin resistance in enterococci

Foucault

Depardieu

Courvalin

et al. 2010

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

108

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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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“…These bacteria are of particular concern in human and animal medicine because some strains have constitutive antimicrobial resistance traits, and others carry inducible resistance traits (Eisner et al, 2005). Another concern is that these organisms can transfer resistance genes to other bacterial species including pathogens (Moubareck et al, 2003;Lester et al, 2006). Although opinions differ in defining the source of resistant Enterococcus spp., increasing development of antimicrobial resistance and transferable resistance genes are points of concern (O'Brien, 2002).…”

Section: Introductionmentioning

confidence: 99%

Prevalence and Antibiotic-Resistance Characteristics of Enterococcus Spp. Isolated From Free-Living and Captive Raptors in Central Illinois

Marrow

Whittington

Mitchell

et al. 2009

Journal of Wildlife Diseases

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ABSTRACT:Due to their predatory nature, raptor species may serve as important indicators of environmental contamination with antimicrobial-resistant bacteria. Raptors prey on small rodents and birds that have diverse habitat ranges, including urban and rural environments, and their intestinal microflora can reflect that of the animals on which they feed. Enterococcus spp. were selected as target organisms because they have been isolated from the avian gastrointestinal tract, can be conferred by prey items, and because they are capable of multiple resistance patterns. They are also a concerning source of human antimicrobial resistance. In this study fecal cultures were obtained from 15 May 2004 to 31 August 2004, from 21 free-living raptors and four captive raptors. Enterococcus was isolated from 21 (84%) of the 25 birds, and 54 isolates were chosen for further study based upon unique colony morphology. The most common isolate recovered was Enterococcus faecalis (95%, 95% confidence interval [CI]: 89-100). One bird in the study was determined to have Enterococcus gallinarum. Two distinct ribotypes of E. faecalis were identified, one with unique bands at 11 and 13 kb and the other with unique bands at 14 and 20 kb. Both ribotypes were found in free-living and captive birds. The Enterococcus isolates in this study demonstrated a variety of antimicrobial-resistance characteristics, including almost complete resistance to amikacin, first-generation cephalosporins, spectinomycin, and sulphadimethoxime. Isolates demonstrated variable resistance to chloramphenicol, gentamicin, enrofloxacin, erythromycin, and ticarcillin. No phenotypically vancomycin-resistant E. faecalis isolates were recovered from any of the raptors; three isolates had intermediate level susceptibility. A significantly higher number of isolates collected from captive birds demonstrated resistance to chloramphenicol than those obtained from free-living birds. This trend was not duplicated with any of the remaining 18 antimicrobial drugs tested. The results of this study suggest that raptors in central Illinois are coming into contact with antimicrobials, prey exposed to antimicrobials, or bacteria that are capable of transferring resistance genes. Further study is needed to determine the source of antimicrobial-resistant Enterococcus in free-living raptors but the limited data reflecting few differences between birds with and without antimicrobial exposure suggests that treatment and release of treated wild raptors is not contributing significantly to antimicrobial resistance in the environment.

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Multiple Antibiotic Resistance Gene Transfer from Animal to Human Enterococci in the Digestive Tract of Gnotobiotic Mice

Cited by 108 publications

References 24 publications

Gut inflammation can boost horizontal gene transfer between pathogenic and commensal Enterobacteriaceae

Gut inflammation can boost horizontal gene transfer between pathogenic and commensal Enterobacteriaceae

Inducible expression eliminates the fitness cost of vancomycin resistance in enterococci

Prevalence and Antibiotic-Resistance Characteristics of Enterococcus Spp. Isolated From Free-Living and Captive Raptors in Central Illinois

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