A novel comprehensive analysis method for <i>Staphylococcus aureus</i> pathogenicity islands

Sato’o, Yusuke; Omoe, Katsuhiko; Ono, Hisaya K.; Nakane, Akio; Hu, Dong‐Liang

doi:10.1111/1348-0421.12007

Cited by 48 publications

(46 citation statements)

References 34 publications

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“…1). In the erm(45)-carrying island, they consisted of one putative integrase (Pfam signature cd00397), a putative cro repressor and c1 antirepressor (PROSITE signature PS50943), one putative primase (PS51206), and two ORFs containing the conserved DNAbinding domains KilA-N (PS51301) and Bro-N (SMART accession number 01040; no defined PS), domains which have been found in proteins of bacterial DNA viruses (20)(21)(22)(23). The integrase, harboring the conserved similarity regions of tyrosine recombinases (24), was most likely responsible for integration into the S. fleurettii chromosome and the formation of a circular intermediate of the erm(45)-containing island.…”

Section: Cloning and Expression Of Erm(45)mentioning

confidence: 99%

The New Macrolide-Lincosamide-Streptogramin B Resistance Gene erm (45) Is Located within a Genomic Island in Staphylococcus fleurettii

Wipf

Schwendener

Nielsen

et al. 2015

Antimicrob Agents Chemother

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Genome alignment of a macrolide, lincosamide, and streptogramin B (MLS B )-resistant Staphylococcus fleurettii strain with an MLS B -susceptible S. fleurettii strain revealed a novel 11,513-bp genomic island carrying the new erythromycin resistance methylase gene erm(45). This gene was shown to confer inducible MLS B resistance when cloned into Staphylococcus aureus. The erm(45)-containing island was integrated into the housekeeping gene guaA in S. fleurettii and was able to form a circular intermediate but was not transmissible to S. aureus. Staphylococcus fleurettii is a commensal bacterium of various animal species and an occasional cause of bovine mastitis (1-3). It naturally contains the methicillin resistance gene mecA within its chromosome and is therefore suspected to have been the source of the mecA gene found in staphylococcal cassette chromosome mec (SCCmec) of methicillin-resistant staphylococci, including methicillin-resistant Staphylococcus aureus (MRSA) (4).Due to this intrinsic resistance to ␤-lactams, other antibiotic classes such as macrolides or lincosamides are being used for the treatment of mastitis caused by S. fleurettii (5, 6).S. fleurettii strain JW205, recently isolated from bovine milk in Switzerland, exhibited resistance to erythromycin and inducible resistance to clindamycin (3). This suggested the presence of a macrolide, lincosamide, and streptogramin B (MLS B ) resistance methylase (Erm) (7). However, none of the erm genes commonly occurring in staphylococci were detected by microarray analysis (8, 9). We therefore examined S. fleurettii strain JW205 for a novel MLS B resistance mechanism by genome comparison with MLS Bsusceptible S. fleurettii strain JW404 (Table 1).Detection and characterization of erm(45). Genomes of strain JW205 and JW404 were sequenced using Ion Torrent (Life Technologies, Grand Island, NY) at the UZH/ETH Functional Genomics Center (Zurich, Switzerland) and Illumina MiSeq (Illumina, San Diego, CA) at the Department of Clinical Microbiology at Hvidovre Hospital (Hvidovre, Denmark), respectively. Contigs of the sequenced strains were aligned using the progressive Mauve algorithm (10). This revealed an 11,513-bp integrated genomic island in JW205, which was absent in strain JW404. The island contained 18 open reading frames (ORFs) (Fig. 1), which were identified by the Prokaryotic Dynamic Programming Genefinding Algorithm (Prodigal) (11) and compared to protein sequences and conserved domains in the BLASTp program (http: //blast.ncbi.nlm.nih.gov/Blast.cgi) and the Swiss Institute of Bioinformatics PROSITE database (http://prosite.expasy.org/). The rightmost ORF of the island encoded a 245-amino-acid (aa) protein, which contained the rRNA adenine dimethylase PROSITE signature PS01131, which is present in nearly all Erm 23S rRNA methylases (12). Of all 36 currently described Erm determinants, this methylase exhibited the highest similarity to Erm(B), with 64% aa and 67% nucleotide (nt) identity (Fig. 2).The novel gene was assigned the name erm(45) according to th...

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Section: Cloning and Expression Of Erm(45)mentioning

confidence: 99%

The New Macrolide-Lincosamide-Streptogramin B Resistance Gene erm (45) Is Located within a Genomic Island in Staphylococcus fleurettii

Wipf

Schwendener

Nielsen

et al. 2015

Antimicrob Agents Chemother

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“…Moreover, superantigen-related genes, such as staphylococcal superantigen-like protein (SSL) genes (ssl1 to ssl26), were discovered during determination of the complete genome sequences of several S. aureus strains (9)(10)(11). It has been recognized that the superantigen genes are associated with mobile genetic elements (MGEs), such as pathogenicity islands, prophages, or plasmids (5,(11)(12)(13)(14). This fact implies that these superantigen genes move among S. aureus strains by horizontal transfer and that such MGEs play an important role in the evolution of S. aureus as a pathogen.…”

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Identification and Characterization of a Novel Staphylococcal Emetic Toxin

Ono

Sato’o

Narita

et al. 2015

Appl Environ Microbiol

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e Staphylococcal enterotoxins (SEs) produced by Staphylococcus aureus have superantigenic and emetic activities, which cause toxic shock syndrome and staphylococcal food poisoning, respectively. Our previous study demonstrated that the sequence of SET has a low level of similarity to the sequences of other SEs and exhibits atypical bioactivities. Hence, we further explored whether there is an additional SET-related gene in S. aureus strains. One SET-like gene was found in the genome of S. aureus isolates that originated from a case of food poisoning, a human nasal swab, and a case of bovine mastitis. The deduced amino acid sequence of the SET-like gene showed 32% identity with the amino acid sequence of SET. The SET-like gene product was designated SElY. In the food poisoning and nasal swab isolates, mRNA encoding SElY was highly expressed in the early log phase of cultivation, whereas a high level of expression of this mRNA was found in the bovine mastitis isolate at the early stationary phase. To estimate whether SElY has both superantigenic and emetic activities, recombinant SElY was prepared. Cell proliferation and cytokine production were examined to assess the superantigenic activity of SElY. SElY exhibited superantigenic activity in human peripheral blood mononuclear cells but not in mouse splenocytes. In addition, SElY exhibited emetic activity in house musk shrews after intraperitoneal and oral administration. However, the stability of SElY against heating and pepsin and trypsin digestion was different from that of SET and SEA. From these results, we identified SElY to be a novel staphylococcal emetic toxin. Staphylococcus aureus produces a variety of exotoxins, including staphylococcal enterotoxins (SEs) and toxic shock syndrome toxin 1 (TSST-1) (1). These toxins are superantigens, which have the ability to stimulate a large repertoire of the V␤ elements of T cell receptor (TCR)-bearing T cells. SEs are also emetic toxins causing staphylococcal food poisoning in humans, although the mechanism of SE-induced emesis has not been entirely verified (2). Due to these properties, SEs are assumed to be a menace to public health. Five major serological types (SEA to SEE) have been characterized (2), and new types of SE-related toxins (SEG to SEI, SElJ, SEK to SET, SElU, SElV, and SElX) have recently been reported (2-8). Moreover, superantigen-related genes, such as staphylococcal superantigen-like protein (SSL) genes (ssl1 to ssl26), were discovered during determination of the complete genome sequences of several S. aureus strains (9-11). It has been recognized that the superantigen genes are associated with mobile genetic elements (MGEs), such as pathogenicity islands, prophages, or plasmids (5,(11)(12)(13)(14). This fact implies that these superantigen genes move among S. aureus strains by horizontal transfer and that such MGEs play an important role in the evolution of S. aureus as a pathogen.We have reported that SET shows mitogenicity to human T cells and requires major histocompatibility complex (MHC) cla...

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“…Forty-two of them were from SFP outbreaks from 1990 to 2010, and the other 329 were collected from the nasal cavities of healthy humans from 2005 to 2010. Bacterial culture conditions, DNA extraction, coagulase typing, SE/SEl genotyping, and multilocus sequence typing (MLST) were performed as described previously (11)(12)(13)(14). SEA production was determined by ELISA according to our previous method (5), with some modification.…”

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confidence: 99%

“…SuperSignal ELISA Femto Maximum Sensitivity Substrate (Thermo Fisher Scientific), Wallac 1420 ARVO MX/Light (PerkinElmer), and Varioskan Flash (Thermo Fisher Scientific) were used for measurement of SEA concentrations. Typing of genomic elements by SaPI scanning was performed as previously described (11). In addition, we designed new primer sets for a putative truncated transposon harboring seh, the enterotoxin gene cluster (egc), and Sa3.…”

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confidence: 99%

“…Two genotypes, sec seg sei sel sem sen seo and seg sei sem sen seo, were found only among the nasal swab isolates. To further clarify the genomic characteristics of the isolates belonging to the CC81 lineages, we typed the genomic elements of all of the CC81 isolates (23 from SFP and 9 from nasal swabs) by PCR (11). This showed that CC81 can be classified into two subtypes, 1 and 2 ( Table 3).…”

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Molecular Epidemiology and Identification of a Staphylococcus aureus Clone Causing Food Poisoning Outbreaks in Japan

et al. 2014

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e Molecular characterization of isolates from staphylococcal food poisoning (SFP) outbreaks in Japan showed that the dominant lineage causing SFP outbreaks is clonal complex 81 (CC81), a single-locus variant of sequence type 1, coagulase type VII, positive for sea and/or seb, and positive for seh. Among various CC lineages producing staphylococcal enterotoxin A, CC81 showed the highest toxin productivity. Staphylococcal food poisoning (SFP), one of the most common food-borne diseases, results from the consumption of foods containing toxic amounts of staphylococcal enterotoxins (SEs) (1-4). SFP is associated with toxigenic Staphylococcus aureus strains that produce one or more members of a family of genes encoding heat-stable SEs. Recently, a superfamily of more than 23 different SEs and SE-like toxins (SEls) was studied for their biological activities (4-8). These bacterial toxins are also known as pyrogenic superantigens that stimulate polyclonal T-cell proliferation and can potentially cause toxic shock syndrome (1-4). The genes for SEs and SEls are harbored by various mobile genetic elements and/or genomic islands, including prophages, plasmids, S. aureus pathogenicity islands (SaPIs), and Sa␤. To date, in addition to the five classical types of SEs (SEA through SEE), 18 new types of SEs and SEls (SEG through SElX) have been described (4-8). Our recent study confirmed the emetic potential of SElK, SElL, SElM, SElN, SElO, SElP, and SElQ in the monkey, and these SEls were renamed SEK, SEL, SEM, SEN, SEO, SEP, and SEQ, respectively (9). Comparing SEs and SEls, SEA is considered the most important SE causing SFP. S. aureus is a common commensal bacterium of the skin and mucosal surfaces of humans, with estimates of 20% persistent and 60% intermittent colonization (10). Food handlers carrying enterotoxin-producing S. aureus in their nasal cavities or on their skin are important sources of food contamination during the cooking process (3). Contamination with S. aureus is believed to be associated primarily with improper handling of cooked or processed foods with improper storage under conditions that allow the growth of S. aureus and the production of SEs. Reports concerning the molecular epidemiology and genetic diversity of the isolates from SFP outbreaks are limited when clinical isolates are compared. In this investigation, we ex-

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A novel comprehensive analysis method for Staphylococcus aureus pathogenicity islands

Cited by 48 publications

References 34 publications

The New Macrolide-Lincosamide-Streptogramin B Resistance Gene erm (45) Is Located within a Genomic Island in Staphylococcus fleurettii

The New Macrolide-Lincosamide-Streptogramin B Resistance Gene erm (45) Is Located within a Genomic Island in Staphylococcus fleurettii

Identification and Characterization of a Novel Staphylococcal Emetic Toxin

Molecular Epidemiology and Identification of a Staphylococcus aureus Clone Causing Food Poisoning Outbreaks in Japan

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