Population Biology of Intestinal Enterococcus Isolates from Hospitalized and Nonhospitalized Individuals in Different Age Groups

Tedim, Ana P.; Ruíz-Garbajosa, Patricia; Corander, Jukka; Rodríguez, C; Cantón, Rafael; Willems, Rob J. L.; Baquero, Fernando; Coque, Teresa M.

doi:10.1128/aem.03661-14

Cited by 83 publications

(79 citation statements)

References 81 publications

(113 reference statements)

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“…In this aspect, the Bac41 gene element is, at least in theory, suspected to be freely disseminated among E. faecalis lineages without restriction by host background. Indeed, the epigenetic backgrounds of our collected isolates were geographically diverse, and the isolates varied as to the characteristics of the individual inpatients (gender and age) and the hospitals from which they were obtained, suggesting that they were independent and unlikely to belong to certain clonal strains (see Table S1 in the supplemental material) (41). However, the collected isolates were largely from urineassociated specimens, and fewer were obtained from blood or cases of infective endocarditis.…”

Section: Discussionmentioning

confidence: 99%

Partial Diversity Generates Effector Immunity Specificity of the Bac41-Like Bacteriocins of Enterococcus faecalis Clinical Strains

2016

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Bacteriocin 41 (Bac41) is the plasmid-encoded bacteriocin produced by the opportunistic pathogen Enterococcus faecalis. Its genetic determinant consists of bacL 1 (effector), bacL 2 (regulator), bacA (effector), and bacI (immunity). The secreted effectors BacL 1 and BacA coordinate to induce the lytic cell death of E. faecalis. Meanwhile, the immunity factor BacI provides self-resistance to the Bac41 producer, E. faecalis, against the action of BacL 1 and BacA. In this study, we demonstrated that more than half of the 327 clinical strains of E. faecalis screened had functional Bac41 genes. Analysis of the genetic structure of the Bac41 genes in the DNA sequences of the E. faecalis strains revealed that the Bac41-like genes consist of a relatively conserved region and a variable region located downstream from bacA. Based on similarities in the variable region, the Bac41-like genes could be classified into type I, type IIa, and type IIb. Interestingly, the distinct Bac41 types had specific immunity factors for self-resistance, BacI1 or BacI2, and did not show cross-immunity to the other type of effector. We also demonstrated experimentally that the specificity of the immunity was determined by the combination of the C-terminal region of BacA and the presence of the unique BacI1 or BacI2 factor. These observations suggested that Bac41-like bacteriocin genes are extensively disseminated among E. faecalis strains in the clinical environment and can be grouped into at least three types. It was also indicated that the partial diversity results in specificity of self-resistance which may offer these strains a competitive advantage. IMPORTANCEBacteriocins are antibacterial effectors produced by bacteria. In general, a bacteriocin-coding gene is accompanied by a cognate immunity gene that confers self-resistance on the bacteriocin-producing bacterium itself. We demonstrated that one of the bacteriocins, Bac41, is disseminated among E. faecalis clinical strains and the Bac41 subtypes with partial diversity. The Bac41-like bacteriocins were found to be classified into type I, type IIa, and type IIb by variation of the cognate immunity factors. The antibacterial activity of the respective effectors was specifically inhibited by the immunity factor from the same type of Bac41 but not the other types. This specificity of effector-immunity pairs suggests that bacteriocin genes might have evolved to change the immunity specificity to acquire an advantage in interbacterial competition. Enterococcus faecalis is a Gram-positive commensal bacterium present in the intestinal tract of healthy humans or animals, but it is also a causative agent of opportunistic infectious diseases, including urinary infectious disease, bacteremia, infective endocarditis, and others (1-4). As represented by the development of drug resistance, the acquisition of new genes via mobile genetic elements (MGEs), such as plasmids, raises the concern of increased severity of these enterococcal diseases (5). Enterococcal plasmids also encode various bact...

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Section: Discussionmentioning

confidence: 99%

Partial Diversity Generates Effector Immunity Specificity of the Bac41-Like Bacteriocins of Enterococcus faecalis Clinical Strains

2016

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“…To test the applicability of the E. faecium cgMLST scheme to distinguish epidemiologically linked isolates from unlinked isolates, i.e., to identify isolates belonging to a single outbreak, we sequenced a collection of 103 hospital-associated VRE strains that had been isolated from different hospitals in Germany, Denmark, and the Netherlands. Based on the STs of these strains, they are all expected to belong to the hospital-associated clade A1 and BAPS groups 2.1a and 3.3a, respectively (16,17). An overview of these isolates is provided in Table S2 in the supplemental material.…”

Section: Resultsmentioning

confidence: 99%

“…NZ_AHWU00000000]), the set of 40 strains used for building the cgMLST scheme included clade A1 (9 isolates), clade A2 (18 isolates), clade B (12 isolates), and one strain that appears to be a hybrid of clades A and B. In total, 36 different STs were represented, and these were previously allocated to 11 different BAPS groups (16). All of the selected strains had high-quality genome sequences, as reflected by the relatively low number of contigs or scaffolds (median, 13; range, 3 to 109) for the 37 draft genome sequences (see Table S1 in the supplemental material).…”

Section: Resultsmentioning

confidence: 99%

“…Extensive MLST analyses revealed that the majority of isolates causing clinical infections in hospitalized patients and hospital outbreaks are genotypically different from commensal isolates from healthy humans and isolates from farm animals, and they formed a distinct subpopulation, which was initially termed clonal complex 17 (CC17) (14). Subsequent Bayesian analysis of the population structure (BAPS) of E. faecium confirmed the separate grouping of hospital, commensal, and farm animal isolates in distinct BAPS groups, of which BAPS groups 2.1a and 3.3a represent the isolates previously contained in CC17 (15,16). Whole-genome sequence (WGS)-based phylogenomics corroborated MLST analyses, since the majority of hospitalderived isolates (from clinical sites and hospital outbreaks), farm animal isolates, and commensal isolates from healthy humans clustered in the distinct clades A1, A2, and B, respectively (17).…”

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confidence: 97%

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Core Genome Multilocus Sequence Typing Scheme for High-Resolution Typing of Enterococcus faecium

et al. 2015

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Enterococcus faecium, a common inhabitant of the human gut, has emerged in the last 2 decades as an important multidrugresistant nosocomial pathogen. Since the start of the 21st century, multilocus sequence typing (MLST) has been used to study the molecular epidemiology of E. faecium. However, due to the use of a small number of genes, the resolution of MLST is limited. Whole-genome sequencing (WGS) now allows for high-resolution tracing of outbreaks, but current WGS-based approaches lack standardization, rendering them less suitable for interlaboratory prospective surveillance. To overcome this limitation, we developed a core genome MLST (cgMLST) scheme for E. faecium. cgMLST transfers genome-wide single nucleotide polymorphism (SNP) diversity into a standardized and portable allele numbering system that is far less computationally intensive than SNPbased analysis of WGS data. The E. faecium cgMLST scheme was built using 40 genome sequences that represented the diversity of the species. The scheme consists of 1,423 cgMLST target genes. To test the performance of the scheme, we performed WGS analysis of 103 outbreak isolates from five different hospitals in the Netherlands, Denmark, and Germany. The cgMLST scheme performed well in distinguishing between epidemiologically related and unrelated isolates, even between those that had the same sequence type (ST), which denotes the higher discriminatory power of this cgMLST scheme over that of conventional MLST. We also show that in terms of resolution, the performance of the E. faecium cgMLST scheme is equivalent to that of an SNP-based approach. In conclusion, the cgMLST scheme developed in this study facilitates rapid, standardized, and high-resolution tracing of E. faecium outbreaks. In the last 2 decades, Enterococcus faecium has emerged as an important multidrug-resistant nosocomial pathogen causing an increasing number of bloodstream infections, mainly in debilitated patients (1-3). Currently, Ͼ90% of the E. faecium strains causing infections have acquired ampicillin resistance, and an increasing number of health care-associated infections and outbreaks are caused by E. faecium strains that are resistant to both ampicillin and vancomycin (4). The global emergence of ampicillin-and vancomycin-resistant E. faecium (VRE) as nosocomial pathogens started in the United States in the late 1980s/early 1990s and occurred in other parts in the world 1 or 2 decades later. In Europe, more particularly in France, Germany, Denmark, and the Netherlands, VRE first spread among livestock due to the use of the vancomycin analog avoparcin as a growth promoter, and it only relatively recently became an important nosocomial pathogen (5, 6). Different molecular typing methods have been used to study the epidemiology of E. faecium, ranging from fingerprint-based methods, like pulsed-field gel electrophoresis (PFGE) (7), ribotyping (8), and amplified fragment length polymorphism (9), to PCR-based methods, like multilocus variable-number tandemrepeat analysis (10) and the sequenced-bas...

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“…Most enterococcal plasmids are able to acquire and disseminate AbR genes by different mechanisms of genetic exchange. However, the role of plasmids in the population structure and evolvability of these enterococcal species has been poorly addressed (194)(195)(196)(197) due to the overrepresentation of recent clinical and animal isolates of specific lineages commonly associated with AbR included in most studies (7,141) and due to the lack of available plasmid sequences. Similar plasmids have been found in E. faecium and other enterococcal species that may play equivalent functional roles in the gastrointestinal tract such as Enterococcus avium, Enterococcus raffinosus, E. durans, and E. hirae (195,198).…”

Section: Enterococcusmentioning

confidence: 99%

The Plasmidome of Firmicutes: Impact on the Emergence and the Spread of Resistance to Antimicrobials

et al. 2015

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The phylum Firmicutes is one of the most abundant groups of prokaryotes in the microbiota of humans and animals and includes genera of outstanding relevance in biomedicine, health care, and industry. Antimicrobial drug resistance is now considered a global health security challenge of the 21st century, and this heterogeneous group of microorganisms represents a significant part of this public health issue.

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Population Biology of Intestinal Enterococcus Isolates from Hospitalized and Nonhospitalized Individuals in Different Age Groups

Cited by 83 publications

References 81 publications

Partial Diversity Generates Effector Immunity Specificity of the Bac41-Like Bacteriocins of Enterococcus faecalis Clinical Strains

Partial Diversity Generates Effector Immunity Specificity of the Bac41-Like Bacteriocins of Enterococcus faecalis Clinical Strains

Core Genome Multilocus Sequence Typing Scheme for High-Resolution Typing of Enterococcus faecium

The Plasmidome of Firmicutes: Impact on the Emergence and the Spread of Resistance to Antimicrobials

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