The Staphylococcus aureus CC398 Lineage: An Evolution Driven by the Acquisition of Prophages and Other Mobile Genetic Elements

Among clinically relevant lineages of Staphylococcus aureus, the lineage or clonal complex 398 (CC398) is of particular interest. Strains from this lineage were only described as livestock colonizers until 2007. Progressively, cases of infection were reported in humans in contact with farm animals, and now, CC398 isolates are increasingly identified as the cause of severe infections even in patients without any contact with animals. These observations suggest that CC398 isolates have spread not only in the community but also in the hospital setting. In addition, several recent studies have reported that CC398 strains are evolving towards increased virulence and antibiotic resistance. Identification of the origin and emergence of this clonal complex could probably benefit future large-scale studies that aim to detect sources of contamination and infection. Current evidence indicates that the evolution of CC398 strains towards these phenotypes has been driven by the acquisition of prophages and other mobile genetic elements. In this short review, we summarize the main knowledge of this major lineage of S. aureus that has become predominant in the human clinic worldwide within a single decade.

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The Mobile Genetic Elements of Staphylococcus aureus

Horizontal Gene Transfer in the Evolution of Pathogenesis ◽

10.1017/cbo9780511541520.011 ◽

2009 ◽

pp. 237-272 ◽

Cited By ~ 1

Author(s):

Richard P. Novick

Keyword(s):

Staphylococcus Aureus ◽

Mobile Genetic Elements ◽

Genetic Elements

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The Virulence Potential of Livestock-Associated Methicillin-Resistant Staphylococcus aureus Cultured from the Airways of Cystic Fibrosis Patients

Toxins ◽

10.3390/toxins12060360 ◽

2020 ◽

Vol 12 (6) ◽

pp. 360

Author(s):

Janina Treffon ◽

Sarah Ann Fotiadis ◽

Sarah van Alen ◽

Karsten Becker ◽

Barbara C. Kahl

Keyword(s):

Cystic Fibrosis ◽

Staphylococcus Aureus ◽

Airway Epithelial Cells ◽

Farm Animals ◽

Airway Epithelial ◽

Methicillin Resistant ◽

Virulence Potential ◽

Airway Infections ◽

Severe Infections

Staphylococcus aureus is one of the most common pathogens that infects the airways of patients with cystic fibrosis (CF) and contributes to respiratory failure. Recently, livestock-associated methicillin-resistant S. aureus (LA-MRSA), usually cultured in farm animals, were detected in CF airways. Although some of these strains are able to establish severe infections in humans, there is limited knowledge about the role of LA-MRSA virulence in CF lung disease. To address this issue, we analyzed LA-MRSA, hospital-associated (HA-) MRSA and methicillin-susceptible S. aureus (MSSA) clinical isolates recovered early in the course of airway infection and several years after persistence in this hostile environment from pulmonary specimens of nine CF patients regarding important virulence traits such as their hemolytic activity, biofilm formation, invasion in airway epithelial cells, cytotoxicity, and antibiotic susceptibility. We detected that CF LA-MRSA isolates were resistant to tetracycline, more hemolytic and cytotoxic than HA-MRSA, and more invasive than MSSA. Despite the residence in the animal host, LA-MRSA still represent a serious threat to humans, as such clones possess a virulence potential similar or even higher than that of HA-MRSA. Furthermore, we confirmed that S. aureus individually adapts to the airways of CF patients, which eventually impedes the success of antistaphylococcal therapy of airway infections in CF.

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Comparative genomic analysis reveals significant enrichment of mobile genetic elements and genes encoding surface structure-proteins in hospital-associated clonal complex 2 Enterococcus faecalis

BMC Microbiology ◽

10.1186/1471-2180-11-3 ◽

2011 ◽

Vol 11 (1) ◽

pp. 3 ◽

Cited By ~ 35

Author(s):

Margrete Solheim ◽

Mari C Brekke ◽

Lars G Snipen ◽

Rob JL Willems ◽

Ingolf F Nes ◽

...

Keyword(s):

Surface Structure ◽

Enterococcus Faecalis ◽

Clonal Complex ◽

Genomic Analysis ◽

Mobile Genetic Elements ◽

Comparative Genomic Analysis ◽

Comparative Genomic ◽

Genetic Elements ◽

Genes Encoding ◽

Significant Enrichment

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A Small RNA-Based Immune System Defends Germ Cells against Mobile Genetic Elements

Stem Cells International ◽

10.1155/2016/7595791 ◽

2016 ◽

Vol 2016 ◽

pp. 1-9 ◽

Cited By ~ 7

Author(s):

Astrid D. Haase

Keyword(s):

Immune System ◽

Germ Cells ◽

Mobile Genetic Elements ◽

Short Review ◽

Loss Of Function ◽

Adaptation Mechanism ◽

Genetic Elements ◽

Small Regulatory Rna ◽

Rna Pathways ◽

Transposon Activity

Transposons are mobile genetic elements that threaten the survival of species by destabilizing the germline genomes. Limiting the spread of these selfish elements is imperative. Germ cells employ specialized small regulatory RNA pathways to restrain transposon activity. PIWI proteins and Piwi-interacting RNAs (piRNAs) silence transposons at the transcriptional and posttranscriptional level with loss-of-function mutant animals universally exhibiting sterility often associated with germ cell defects. This short review aims to illustrate basic strategies of piRNA-guided defense against transposons. Mechanisms of piRNA silencing are most readily studied inDrosophila melanogaster, which serves as a model to delineate molecular concepts and as a reference for mammalian piRNA systems. PiRNA pathways utilize two major strategies to handle the challenges of transposon control: (1) the hard-wired molecular memory of prior transpositions enables recognition of mobile genetic elements and discriminates transposons from host genes; (2) a feed-forward adaptation mechanism shapes piRNA populations to selectively combat the immediate threat of transposon transcripts. In flies, maternally contributed PIWI-piRNA complexes bolster both of these lines of defense and ensure transgenerational immunity. While recent studies have provided a conceptual framework of what could be viewed as an ancient immune system, we are just beginning to appreciate its many molecular innovations.

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Non-canonical Staphylococcus aureus pathogenicity island repression

10.1101/2021.09.07.459249 ◽

2021 ◽

Author(s):

Laura Miguel-Romero ◽

Mohammed Alqasmi ◽

Julio Bacarizo ◽

Jason A. Tan ◽

Richard J. Cogdell ◽

...

Keyword(s):

Staphylococcus Aureus ◽

Dna Binding ◽

Virulence Factors ◽

Pathogenicity Island ◽

Mobile Genetic Elements ◽

Life Cycles ◽

Genetic Elements ◽

Dna Binding Domains ◽

Binding Domains ◽

Induction System

ABSTRACTMobile genetic elements (MGEs) control their life cycles by the expression of a master repressor, whose function must be disabled to allow the spread of these elements in nature. Here we describe an unprecedented repression-derepression mechanism involved in the transfer of the Staphylococcus aureus pathogenicity islands (SaPIs). Contrary to the classical phage and SaPI repressors, which are dimers, the SaPI1 repressor StlSaPI1 presents a unique tetrameric conformation, never seen before. Importantly, not just one but two tetramers are required for SaPI1 repression, which increases the novelty of the system. To derepress SaPI1, the phage-encoded protein Sri binds to and induces a conformational change in the DNA binding domains of StlSaPI1, preventing the binding of the repressor to its cognate StlSaPI1 sites. Finally, our findings demonstrate that this system is not exclusive to SaPI1 but widespread in nature. Overall, our results characterise a novel repression-induction system involved in the transfer of MGE-encoded virulence factors in nature.SignificanceWhile most repressors controlling the transfer of mobile genetic elements are dimers, we demonstrate here that the Staphylococcal pathogenicity island 1 (SaPI1) is repressed by two tetramers, which have a novel structural fold in their body that has never been seen before in other proteins. Moreover, by solving the structure of the SaPI1 repressor in complex with its inducing protein Sri, we have demonstrated that Sri forces the SaPI1 repressor to adopt a conformation that is incompatible with DNA binding, explaining how SaPI1 is induced. Finally, our results demonstrate that this repression system is not exclusive of the SaPIs but widespread in nature. Our studies provide important insights understanding how SaPIs spread in nature.

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

Microorganisms ◽

10.3390/microorganisms8111737 ◽

2020 ◽

Vol 8 (11) ◽

pp. 1737

Author(s):

Kevin Bouiller ◽

Xavier Bertrand ◽

Didier Hocquet ◽

Catherine Chirouze

Keyword(s):

Staphylococcus Aureus ◽

Common Ancestor ◽

Clonal Complex ◽

Bloodstream Infections ◽

Human Infection ◽

Last Common Ancestor ◽

Joint Infections ◽

Global Epidemiology ◽

The World ◽

Severe Infections

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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Epidemiological survey of the first case of vancomycin-resistant Staphylococcus aureus infection in Europe

Epidemiology and Infection ◽

10.1017/s0950268814001423 ◽

2014 ◽

Vol 143 (4) ◽

pp. 745-748 ◽

Cited By ~ 24

Author(s):

A. FRIÃES ◽

C. RESINA ◽

V. MANUEL ◽

L. LITO ◽

M. RAMIREZ ◽

...

Keyword(s):

Staphylococcus Aureus ◽

Clonal Complex ◽

Hospital Setting ◽

Epidemiological Survey ◽

Aureus Infection ◽

First Case ◽

Typing Methods ◽

Vancomycin Resistant ◽

Close Contacts

SUMMARYWe report on the follow-up and epidemiological study triggered by the isolation of the first vancomycin-resistant Staphylococcus aureus (VRSA) detected in Europe. The patient and 53 close contacts were screened for S. aureus colonization and all isolates recovered were characterized by multiple molecular typing methods. The VRSA remained confined to the infected foot of the patient and was not detected in any of the close contacts. Nasal colonization with S. aureus was detected in 20 subjects, of whom 15 carried methicilin-susceptible isolates with the remaining five harbouring methicilin-resistant S. aureus (MRSA). The majority of the isolates belonged to clones that have been previously shown to be prevalent in Portugal, both in the hospital setting and in the community. Only one isolate, an MRSA, was closely related to the VRSA. Like most of the characterized VRSA isolates from other countries, the VRSA isolated in Portugal belonged to clonal complex (CC) 5. Despite the absence of VRSA dissemination, the recent increase in the incidence of lineages belonging to CC5 in some European countries, including Portugal, may result in more frequent opportunities for the emergence of VRSA.

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Draft Genome Sequences of 14 Staphylococcus aureus Sequence Type 5 Isolates from California, USA

Genome Announcements ◽

10.1128/genomea.00098-17 ◽

2017 ◽

Vol 5 (13) ◽

Cited By ~ 4

Author(s):

Samantha J. Hau ◽

Darrell O. Bayles ◽

David P. Alt ◽

Tracy L. Nicholson

Keyword(s):

Staphylococcus Aureus ◽

Draft Genome ◽

Mobile Genetic Elements ◽

Sequence Type ◽

Genome Sequences ◽

Content Type ◽

Genetic Elements

ABSTRACT Staphylococcus aureus is part of the human epithelial microbiota; however, it is also a pathogen. The acquisition of mobile genetic elements plays a role in the virulence of S. aureus isolates and contributes to treatment failures. This report details the draft genome sequences of 14 clinical S. aureus isolates.

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Complete Genome Sequences of Two Staphylococcus aureus Sequence Type 5 Isolates from California, USA

Genome Announcements ◽

10.1128/genomea.00099-17 ◽

2017 ◽

Vol 5 (13) ◽

Cited By ~ 1

Author(s):

Samantha J. Hau ◽

Darrell O. Bayles ◽

David P. Alt ◽

Tracy L. Nicholson

Keyword(s):

Staphylococcus Aureus ◽

Complete Genome ◽

Mobile Genetic Elements ◽

Sequence Type ◽

Human Diseases ◽

Genome Sequences ◽

Content Type ◽

Genetic Elements

ABSTRACT Staphylococcus aureus causes a variety of human diseases ranging in severity. The pathogenicity of S. aureus can be partially attributed to the acquisition of mobile genetic elements. In this report, we provide two complete genome sequences from human clinical S. aureus isolates.

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