Temperate Prophages Increase Bacterial Adhesin Expression and Virulence in an Experimental Model of Endocarditis Due to Staphylococcus aureus From the CC398 Lineage

Laumay, Floriane; Corvaglia, Anna‐Rita; Diène, Seydina M.; Girard, Myriam; Oechslin, Frank; Mee-Marquet, Nathalie van der; Entenza, José M.; François, Patrice

doi:10.3389/fmicb.2019.00742

Cited by 39 publications

(23 citation statements)

References 40 publications

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“…In Staphylococcus aureus , a closely related species to S . epidermidis , prophages increase virulence of their bacterial host, most probably by promoting interaction with extracellular matrix components or by integration of phage-encoded virulence determinants into the staphylococcal genome [ 75 , 76 ]. Future studies will therefore need to address whether prophages may at least partly explain the over-representation of ST2 in S .…”

Section: Discussionmentioning

confidence: 99%

Distinct clonal lineages and within-host diversification shape invasive Staphylococcus epidermidis populations

Both

Huang

et al. 2021

PLoS Pathog

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S. epidermidis is a substantial component of the human skin microbiota, but also one of the major causes of nosocomial infection in the context of implanted medical devices. We here aimed to advance the understanding of S. epidermidis genotypes and phenotypes conducive to infection establishment. Furthermore, we investigate the adaptation of individual clonal lines to the infection lifestyle based on the detailed analysis of individual S. epidermidis populations of 23 patients suffering from prosthetic joint infection. Analysis of invasive and colonizing S. epidermidis provided evidence that invasive S. epidermidis are characterized by infection-supporting phenotypes (e.g. increased biofilm formation, growth in nutrient poor media and antibiotic resistance), as well as specific genetic traits. The discriminating gene loci were almost exclusively assigned to the mobilome. Here, in addition to IS256 and SCCmec, chromosomally integrated phages was identified for the first time. These phenotypic and genotypic features were more likely present in isolates belonging to sequence type (ST) 2. By comparing seven patient-matched nasal and invasive S. epidermidis isolates belonging to identical genetic lineages, infection-associated phenotypic and genotypic changes were documented. Besides increased biofilm production, the invasive isolates were characterized by better growth in nutrient-poor media and reduced hemolysis. By examining several colonies grown in parallel from each infection, evidence for genetic within-host population heterogeneity was obtained. Importantly, subpopulations carrying IS insertions in agrC, mutations in the acetate kinase (AckA) and deletions in the SCCmec element emerged in several infections. In summary, these results shed light on the multifactorial processes of infection adaptation and demonstrate how S. epidermidis is able to flexibly repurpose and edit factors important for colonization to facilitate survival in hostile infection environments.

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Section: Discussionmentioning

confidence: 99%

Distinct clonal lineages and within-host diversification shape invasive Staphylococcus epidermidis populations

Both

Huang

et al. 2021

PLoS Pathog

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“…Interestingly, human SA CC398 had a higher capacity for binding to human cytokeratin-10 than LA SA CC398, mediated by the clumping factor B (ClfB) and very likely important for nasal colonization of humans [9]. Recently, Laumay and colleagues showed that the introduction of bacteriophages from the genomes of human-adapted SA to that of a naive SA animal colonizer increased the transcription of clfA (encoding the clumping factor A precursor) and fnbA (encoding the fibronectin binding protein), which in turn increased the bacterial virulence in a rat model of infectious endocarditis [89]. This study confirmed the role of MGE in the virulence of SA CC398.…”

Section: Virulence Factorsmentioning

confidence: 99%

Human Infection of Methicillin-Susceptible Staphylococcus aureus CC398: A Review

et al. 2020

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Staphylococcus aureus (SA) belonging to the clonal complex 398 (CC398) took a special place within the species due to its spread throughout the world. SA CC398 is broadly separated in two subpopulations: livestock-associated methicillin-resistant SA (MRSA) and human-associated methicillin-susceptible SA (MSSA). Here, we reviewed the global epidemiology of SA CC398 in human clinical infections and focused on MSSA CC398. The last common ancestor of SA CC398 was probably a human-adapted prophage φSa3-positive MSSA CC398 strain, but the multiple transmissions between human and animal made its evolution complex. MSSA and MRSA CC398 had different geographical evolutions. Although MSSA was present in several countries all over the world, it was mainly reported in China and in France with a prevalence about 20%. MSSA CC398 was frequently implicated in severe infections such as bloodstream infections, endocarditis, and bone joint infections whereas MRSA CC398 was mainly reported in skin and soft tissue. The spread of the MSSA CC398 clone is worldwide but with a heterogeneous prevalence. The prophage φSa3 played a crucial role in the adaptation to the human niche and in the virulence of MSSA CC398. However, the biological features that allowed the recent spread of this lineage are still far from being fully understood.

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“…An increase in the production of virulence factors was observed, which could not be attributed to insertional effects. Hence, it is tempting to hypothesize that those phages carry uncharacterized regulators influencing the expression of bacterial adhesins and so increase the ability to adhere to human extracellular matrix proteins 79 .…”

Section: Prophages Impact Bacterial Infectivitymentioning

confidence: 99%

Bacteriophages as drivers of bacterial virulence and their potential for biotechnological exploitation

Schroven

Aertsen

Lavigne

2020

FEMS Microbiology Reviews

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Bacteria-infecting viruses (phages) and their hosts maintain an ancient and complex relationship. Bacterial predation by lytic phages drives an ongoing phage-host arms race, whereas temperate phages initiate mutualistic relationships with their hosts upon lysogenisation as prophages. In human pathogens, these prophages impact bacterial virulence in distinct ways: by secretion of phage-encoded toxins, modulation of the bacterial envelope, mediation of bacterial infectivity and the control of bacterial cell regulation. This review builds the argument that virulence-influencing prophages hold extensive, unexplored potential for biotechnology. More specifically, it highlights the development potential of novel therapies against infectious diseases, to address the current antibiotic resistance crisis. First, designer bacteriophages may serve to deliver genes encoding cargo proteins which repress bacterial virulence. Secondly, one may develop small molecules mimicking phage-derived proteins targeting central regulators of bacterial virulence. Thirdly, bacteria equipped with phage-derived synthetic circuits which modulate key virulence factors could serve as vaccine candidates to prevent bacterial infections. The development and exploitation of such antibacterial strategies will depend on the discovery of other prophage-derived, virulence control mechanisms and, more generally, on the dissection of the mutualistic relationship between temperate phages and bacteria, as well as on continuing developments in the synthetic biology field.

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Temperate Prophages Increase Bacterial Adhesin Expression and Virulence in an Experimental Model of Endocarditis Due to Staphylococcus aureus From the CC398 Lineage

Cited by 39 publications

References 40 publications

Distinct clonal lineages and within-host diversification shape invasive Staphylococcus epidermidis populations

Distinct clonal lineages and within-host diversification shape invasive Staphylococcus epidermidis populations

Human Infection of Methicillin-Susceptible Staphylococcus aureus CC398: A Review

Bacteriophages as drivers of bacterial virulence and their potential for biotechnological exploitation

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