A Novel Gene, fudoh, in the SCCmec Region Suppresses the Colony Spreading Ability and Virulence of Staphylococcus aureus

Kaito, Chikara; Omae, Yosuke; Matsumoto, Yasuhiko; Nagata, Mizuki; Yamaguchi, Hiroki; Aoto, Taiji; Ito, Teruyo; Hiramatsu, Kazumasa; Sekimizu, Kazuhisa

doi:10.1371/journal.pone.0003921

Cited by 41 publications

(64 citation statements)

References 28 publications

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“…We show that the large hospital-associated type II SCCmec element has a significant effect on the toxicity and growth rate of MRSAs. The mechanism by which the type II element reduces toxin expression is not fully understood but is possibly a consequence of the presence of the recently identified fudoh gene (Kaito et al, 2008). We believe the fitness burden associated with carrying the large type II SCCmec element is partially compensated for by the reduction in toxin expression, and that this contributes to the restriction of these MRSA strains to health-care settings where transmission is often through health-care workers and a large pool of susceptible hosts are available.…”

Section: Discussionmentioning

confidence: 99%

Offsetting virulence and antibiotic resistance costs by MRSA

et al. 2010

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The prevalence of diverse MRSA (methicillin-resistant Staphylococcus aureus) types in both hospital and community settings is a major health problem worldwide. Here we compare hospitalacquired MRSAs with large type II SCCmec elements with those prevalent in both hospital and community settings with smaller type IV SCCmec elements. We find that the type II but not the type IV SCCmec element causes the bacteria to reduce their levels of costly toxin expression. We compare the relative growth rates of these MRSA types and show that the type II SCCmec carrying MRSAs are more affected than those carrying type IV elements and from this we hypothesize that offsetting the costs associated with antibiotic resistance and toxin expression is why the type II are confined to hospital environments where antibiotic use, the prevalence of immunocompromised individuals and vector-mediated transmission is high. In contrast, those MRSAs that are also successful in the community can maintain their high levels of toxin expression due to a lower fitness burden associated with the smaller SCCmec element.

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Section: Discussionmentioning

confidence: 99%

Offsetting virulence and antibiotic resistance costs by MRSA

et al. 2010

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“…Although S. aureus was originally believed to be nonmotile, recent studies have shown that this organism is capable of spreading over wet surfaces (25)(26)(27). We have previously shown that a mix of the four PSM␣ peptides can promote this so-called colony spreading phenotype (27), and we hypothesized that this relates to their strong surfactant properties (9).…”

Section: S Taphylococcus Aureus Is An Opportunistic Human Pathogen Thatmentioning

confidence: 99%

“…The PSM␤ peptides appear less important for cytolysis and inflammation but, in low concentrations, they seem to promote biofilm formation by Staphylococcus epidermidis. High amounts of the same PSM␤ peptides do, however, promote the detachment of staphylococcal cells from biofilms both in vitro and in vivo (24).Although S. aureus was originally believed to be nonmotile, recent studies have shown that this organism is capable of spreading over wet surfaces (25)(26)(27). We have previously shown that a mix of the four PSM␣ peptides can promote this so-called colony spreading phenotype (27), and we hypothesized that this relates to their strong surfactant properties (9).…”

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confidence: 99%

Distinct Roles of Phenol-Soluble Modulins in Spreading of Staphylococcus aureus on Wet Surfaces

Tsompanidou

Denham

Becher

et al. 2013

Appl Environ Microbiol

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The human pathogen Staphylococcus aureus is renowned for the rapid colonization of contaminated wounds, medical implants, and food products. Nevertheless, little is known about the mechanisms that allow S. aureus to colonize the respective wet surfaces. The present studies were therefore aimed at identifying factors used by S. aureus cells to spread over wet surfaces, starting either from planktonic or biofilm-associated states. Through proteomics analyses we pinpoint phenol-soluble modulins (PSMs) as prime facilitators of the spreading process. To dissect the roles of the eight PSMs produced by S. aureus, these peptides were chemically synthesized and tested in spreading assays with different psm mutant strains. The results show that PSM␣3 and PSM␥ are the strongest facilitators of spreading both for planktonic cells and cells in catheter-associated biofilms. Compared to the six other PSMs of S. aureus, PSM␣3 and PSM␥ combine strong surfactant activities with a relatively low overall hydropathicity. Importantly, we show that PSM-mediated motility of S. aureus facilitates the rapid colonization of wet surfaces next to catheters and the colonization of fresh meat. S taphylococcus aureus is an opportunistic human pathogen thatcan cause a wide range of acute and chronic diseases, which range from superficial skin infections to life-threatening endocarditis and sepsis (1, 2). The ability of this Gram-positive bacterium to cause these infections depends on the production of secreted and cell wall-associated virulence factors. Of increasing concern is the ability of S. aureus to acquire resistance against antibiotics, as underscored by the global spread of methicillin-resistant S. aureus (MRSA) lineages.Intriguingly, recent proteomics studies have revealed an enormous diversity in the production of virulence factors by different isolates of S. aureus, and only a few of these seem to be invariantly produced (3-5). Among the most commonly identified staphylococcal virulence factors, especially in the community-associated (CA)-MRSA lineages, are the so-called phenol-soluble modulins (PSMs) (6). These PSMs are short, amphipathic, ␣-helical peptides that have leukocidal activity and biosurfactant properties (7-9). The growth media of S. aureus cultures contain both N-terminally formylated and deformylated PSMs, suggesting that these virulence factors are substrates for the bacterial N-formylmethionine deformylase (9, 10).To date, eight PSMs have been identified in S. aureus. These include the four PSM␣1 to PSM␣4 peptides (22 residues each), the PSM␤1 and PSM␤2 peptides (44 residues each), PSM␥ (25 residues) and the recently reported PSM-mec (22 residues). The PSM␣ peptides are encoded by the psm␣ operon, the PSM␤ peptides by the psm␤ operon, and PSM␥ by the hld gene. Notably, the hld gene is embedded within the regulatory RNAIII molecule that is encoded by the agr locus. The gene for PSM-mec was identified in MRSA strains carrying the staphylococcal cassette chromosome mec (SCCmec) types II or III. The expression of all ps...

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“…Hospital-associated methicillin-resistant S. aureus (HA-MRSA) 2 strains have lower colony-spreading ability than community-acquired MRSA (CA-MRSA) strains that cause severe diseases (10). The correlation between high colony-spreading activity and high virulence of S. aureus strains suggests that colony spreading has a role in the infectious processes of S. aureus (10).…”

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confidence: 99%

“…The correlation between high colony-spreading activity and high virulence of S. aureus strains suggests that colony spreading has a role in the infectious processes of S. aureus (10). The difference in colony-spreading activity and virulence between HA-MRSA and CA-MRSA is attributed to the virulence regulatory RNA harbored specifically in the SCCmec region of the HA-MRSA strain (11).…”

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confidence: 99%