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Case-control study: Determination of potential risk factors for the colonization of healthy volunteers with Streptococcus gallolyticus subsp. gallolyticus.

ABSTRACT: Streptococcus gallolyticus subsp. gallolyticus was identified in humans and animals as commensal of the gut and can act as a causative agent of endocarditis and septicemia. A case-control study was performed to identify yet unknown risk factors for the transmission of this facultative pathogen. The prevalence in the gut of 99 healthy volunteers was determined using real-time polymerase chain reaction resulting in 62.5% S. gallolyticus subsp. gallolyticus positive excrements. Subsequent cultivation offered three isolates and epidemiological analysis based on MLST revealed sequence type (ST) 3 and ST 7, previously detected from bovine and endocarditis patients. These results support the hypotheses of the zoonotic potential of this bacterium. Participant questionnaires were evaluated concerning personal characteristics, nutritional habits and animal contact. Specifically, closer contact between participants and animals influenced the colonization of the human gut significantly and was further affected if volunteers used excrement for the fertilization of plants.

SUBMITTER: Dumke J

PROVIDER: S-EPMC5411088 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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Case-control study: Determination of potential risk factors for the colonization of healthy volunteers with Streptococcus gallolyticus subsp. gallolyticus.

Dumke Jessika J Vollmer Tanja T Akkermann Oke O Knabbe Cornelius C Dreier Jens J

PloS one 20170501 5

Streptococcus gallolyticus subsp. gallolyticus was identified in humans and animals as commensal of the gut and can act as a causative agent of endocarditis and septicemia. A case-control study was performed to identify yet unknown risk factors for the transmission of this facultative pathogen. The prevalence in the gut of 99 healthy volunteers was determined using real-time polymerase chain reaction resulting in 62.5% S. gallolyticus subsp. gallolyticus positive excrements. Subsequent cultivati ...[more]

PMID: 28459818

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Project description:Streptococcus gallolyticus subsp. gallolyticus, a member of the group D streptococci, is normally found in the bovine rumen and human gut. It is an opportunistic pathogen that was recently determined to be a bacterial driver of colorectal cancer, in addition to causing other diseases, such as infective endocarditis, bacteremia, neonatal meningitis, and septicemia. As an emerging pathogen, not much is known about this bacterium, its virulence mechanisms, or its virulence regulatory pathways. Previous studies suggest that S. gallolyticus subsp. gallolyticus uses a ComRS pathway, one of many Streptococcus quorum-sensing circuitries, for competence. However, thus far, the ubiquitous ComABCDE pathway has not been studied, nor has its regulatory role in S. gallolyticus subsp. gallolyticus We therefore sought to study the S. gallolyticus subsp. gallolyticus ComABCDE quorum-sensing pathway and have identified its peptide pheromone, which is termed the competence-stimulating peptide (CSP). We further determined that this peptide regulates the production of bacteriocin-like inhibitory substances (BLISs), a phenotype that has been linked with the ComABCDE pathway in both Streptococcus pneumoniae and Streptococcus mutans Our data show that S. gallolyticus subsp. gallolyticus TX20005 produces a 21-mer CSP signal, which differs from CSP signals of other Streptococcus species in that its active form begins three residues after the double-glycine leader signal of the ComC precursor peptide. Additionally, our data suggest that this peptide might not be related to competence induction, as opposed to CSP signaling peptides in other Streptococcus species. This study provides the first evidence that S. gallolyticus subsp. gallolyticus utilizes quorum sensing to eliminate competitors, presenting a potential pathway to target this emerging human pathogen.IMPORTANCEStreptococcus gallolyticus subsp. gallolyticus is an emerging human pathogen known as a causative agent of infective endocarditis, and recently, of colorectal cancer. In this work, we revealed a functional quorum-sensing circuitry in S. gallolyticus subsp. gallolyticus, including the identification of the central signaling peptide pheromone, competence-stimulating peptide (CSP), and the regulatory role of this circuitry in the production of bacteriocin-like inhibitory substances (BLISs). This work uncovered a mechanism by which this bacterium outcompetes other bacterial species and thus provides a potential tool to study this opportunistic pathogen.

Project description:BackgroundStreptococcus gallolyticus subsp. gallolyticus is an important causative agent of infective endocarditis (IE) but the knowledge on virulence factors is limited and the pathogenesis of the infection is poorly understood. In the present study, we established an experimental in vitro IE cell culture model using EA.hy926 and HUVEC cells to investigate the adhesion and invasion characteristics of 23 Streptococcus gallolyticus subsp. gallolyticus strains from different origins (human IE-derived isolates, other human clinical isolates, animal isolates). Adhesion to eight components of the extracellular matrix (ECM) and the ability to form biofilms in vitro was examined in order to reveal features of S. gallolyticus subsp. gallolyticus endothelial infection. In addition, the strains were analyzed for the presence of the three virulence factors gtf, pilB, and fimB by PCR.ResultsThe adherence to and invasion characteristics of the examined S. gallolyticus subsp. gallolyticus strains to the endothelial cell line EA.hy926 differ significantly among themselves. In contrast, the usage of three different in vitro models (EA.hy926 cells, primary endothelial cells (HUVECs), mechanical stretched cells) revealed no differences regarding the adherence to and invasion characteristics of different strains. Adherence to the ECM proteins collagen I, II and IV revealed the highest values, followed by fibrinogen, tenascin and laminin. Moreover, a strong correlation was observed in binding to these proteins by the analyzed strains. All strains show the capability to adhere to polystyrole surfaces and form biofilms. We further confirmed the presence of the genes of two known virulence factors (fimB: all strains, gtf: 19 of 23 strains) and demonstrated the presence of the gene of one new putative virulence factor (pilB: 9 of 23 strains) by PCR.ConclusionOur study provides the first description of S. gallolyticus subsp. gallolyticus adhesion and invasion of human endothelial cells, revealing important initial information of strain variability, behaviour and characteristics of this as yet barely analyzed pathogen.

Project description:Streptococcus gallolyticus subsp. gallolyticus is a commensal bacterium of the human gastrointestinal tract, and a pathogen causing infective endocarditis and other biofilm-associated infections via exposed collagen. This study focuses on the characterization of the biofilm formation and collagen adhesion of S. gallolyticus subsp. gallolyticus under different conditions. In this study, it has been observed that the isolate UCN 34 is resistant to 20 mg/ml lysozyme in BHI medium, whereas the strain BAA-2069 builds more biofilm in the presence of lysozyme compared to in a control of BHI without lysozyme. A transcriptome analysis with whole genome microarrays of these two isolates in BHI medium with lysozyme compared to control without lysozyme revealed changes in gene expression levels. In the isolate BAA-2069, 67 genes showed increased expression in the presence of lysozyme, while in the isolate UCN 34, 165 genes showed increased expression and 30 genes showed decreased expression through lysozyme treatment. Products of genes which were higher expressed are in involved in transcription and translation, in cell-wall modification, in hydrogen peroxide resistance and in bacterial immunity. Furthermore, the adhesion ability of different strains of S. gallolyticus subsp. gallolyticus to collagen type I and IV was analyzed. Thereby, we compared the adhesion of 46 human isolates with 23 isolates from animals. It was shown that the adhesion ability depends significantly on whether the isolate was isolated from human or animal. For example, high adhesion ability was observed for strain UCN 34 isolated from an infective endocarditis patient, whereas strain DSM 16831 isolated from koala feces adhered only marginally to collagen. Full genome microarray analysis of these two strains revealed strain-dependent gene expression due to adhesion. The expression of 25 genes of a transposon and 15 genes of a phage region in strain DSM 16831 were increased, which corresponds to horizontal gene transfer. Adherence to collagen in strain UCN 34 led to higher expression of 27 genes and lower expression of 31 genes. This was suggestive of a change in nutrient uptake.

Dataset Information

Case-control study: Determination of potential risk factors for the colonization of healthy volunteers with Streptococcus gallolyticus subsp. gallolyticus.

Publications

Case-control study: Determination of potential risk factors for the colonization of healthy volunteers with Streptococcus gallolyticus subsp. gallolyticus.

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