Abstract
A bacterial insertion sequence (IS) is a mobile DNA sequence carrying only the transposase gene (tnp) that acts as a mutator to disrupt genes, alter gene expressions, and cause genomic rearrangements. “Canonical” ISs have historically been characterized by their terminal inverted repeats (IRs), which may form a stem-loop structure, and duplications of a short (non-IR) target sequence at both ends, called target site duplications (TSDs). The IS distributions and virulence potentials of Staphylococcus aureus genomes in familial infection cases are unclear. Here, we determined the complete circular genome sequences of familial strains from a Panton-Valentine leukocidin (PVL)-positive ST50/agr4 S. aureus (GN) infection of a 4-year old boy with skin abscesses. The genomes of the patient strain (GN1) and parent strain (GN3) were rich for “canonical” IS1272 with terminal IRs, both having 13 commonly-existing copies (ce-IS1272). Moreover, GN1 had a newly-inserted IS1272 (ni-IS1272) on the PVL-converting prophage, while GN3 had two copies of ni-IS1272 within the DNA helicase gene and near rot. The GN3 genome also had a small deletion. The targets of ni-IS1272 transposition were IR structures, in contrast with previous “canonical” ISs. There were no TSDs. Based on a database search, the targets for ce-IS1272 were IRs or “non-IRs”. IS1272 included a larger structure with tandem duplications of the left (IRL) side sequence; tnp included minor cases of a long fusion form and truncated form. One ce-IS1272 was associated with the segments responsible for immune evasion and drug resistance. Regarding virulence, GN1 expressed cytolytic peptides (phenol-soluble modulin α and δ-hemolysin) and PVL more strongly than some other familial strains. These results suggest that IS1272 transposes through an IR-replacing mechanism, with an irreversible process unlike that of “canonical” transpositions, resulting in genomic variations, and that, among the familial strains, the patient strain has strong virulence potential based on community-associated virulence factors.
Highlights
Staphylococcus aureus is a common human pathogen that colonizes the nasal mucosa and skin and causes a wide spectrum of diseases, including skin and soft tissue infections (SSTIs) such as furuncles and cellulitis, systemic infections including bacteremia, sepsis, osteomyelitis, bacteremic pneumonia, and endocarditis, and exotoxin-related diseases such as toxic shock syndrome and food poisoning [1,2,3,4,5]
Among the nine members from three families who were living together within the same house, five were positive for Panton-Valentine leukocidin (PVL)-positive CA-methicillin-susceptible S. aureus (MSSA), and the strains isolated from these individuals were named strains GN1 to GN5 (Fig 1A)
A pulsed-field gel electrophoresis (PFGE) analysis revealed that the five PVLpositive CA-MSSA strains GN1 to GN5 were the same (Fig 1B), indicating the intrafamilial spread
Summary
Staphylococcus aureus is a common human pathogen that colonizes the nasal mucosa and skin and causes a wide spectrum of diseases, including skin and soft tissue infections (SSTIs) such as furuncles and cellulitis, systemic infections including bacteremia, sepsis, osteomyelitis, bacteremic pneumonia, and endocarditis, and exotoxin-related diseases such as toxic shock syndrome and food poisoning [1,2,3,4,5]. Most community-associated infections of S. aureus in the United States are those that affect skin and soft tissues [4]. S. aureus poses a threat because many of its strains are drug-resistant, most notably methicillin-resistant S. aureus (MRSA) with staphylococcal cassette chromosome mec (SCCmec) [6], which emerged as healthcareassociated MRSA (HA-MRSA) in the early 1960s and as community-associated MRSA (CA-MRSA) in the late 1990s [7,8,9,10]. S. aureus, both methicillin-susceptible S. aureus (MSSA) and CA-MRSA, often produce Panton-Valentine leukocidin (PVL), which is associated with pyogenic skin infections (large abscesses) [11,12,13]. The strong expression of peptide cytolysins, such as phenol-soluble modulins (PSMs) and δ-hemolysin (Hld), is associated with CA-MRSA [12,19,20,21,22] and CA-MSSA [20,22]
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