Open Access

Genome sequencing and molecular characterisation of Staphylococcus aureus ST772-MRSA-V, “Bengal Bay Clone”

  • Stefan Monecke1, 2Email author,
  • Vico Baier2,
  • Geoffrey W Coombs3, 4,
  • Peter Slickers2,
  • Albrecht Ziegler2 and
  • Ralf Ehricht2
BMC Research Notes20136:548

https://doi.org/10.1186/1756-0500-6-548

Received: 20 June 2013

Accepted: 17 December 2013

Published: 20 December 2013

Abstract

Background

The PVL-positive ST772-MRSA-V is an emerging community-associated (CA-) MRSA clone that has been named Bengal Bay Clone since most patients have epidemiological connections to the Indian subcontinent. It is found increasingly common in other areas of the world.

Methods

One isolate of ST772-MRSA-V was sequenced using the Illumina Genome Analyzer System. After initial assembling the multiple sequence contigs were analysed using different in-house annotation scripts. Results were compared to microarray hybridisation results of clinical isolates of ST772-MRSA-V, of related strains and to another ST772-MRSA-V genome sequence.

Results

According to MLST e-burst analysis, ST772-MRSA-V belongs to Clonal Complex (CC)1, differing from ST1 only in one MLST allele (pta-22). However, there are several additional differences including agr alleles (group II rather than III), capsule type (5 rather than 8), the presence of the egc enterotoxin gene cluster and of the enterotoxin homologue ORF CM14 as well as the absence of the enterotoxin H gene seh. Enterotoxin genes sec and sel are present. ST772-MRSA-V harbours the genes encoding enterotoxin A (sea) and PVL (lukS/F-PV). Both are located on the same prophage.

Conclusions

ST772-MRSA-V may have emerged from the same lineage as globally spread CC1 and CC5 strains. It has acquired a variety of virulence factors, and for a CA-MRSA strain it has an unusually high number of genes associated with antibiotic resistance.

Background

In recent years the epidemiology of methicillin-resistant Staphylococcus aureus (MRSA) has changed with the emergence of community associated MRSA (CA-MRSA) strains. Unlike the original healthcare associated MRSA strains, CA-MRSA strains are no longer restricted to the hospital setting and can persist in and be transmitted by healthy individuals in the community. Some of these strains exhibit an enhanced virulence due to the carriage of a number of virulence genes, including the Panton Valentine leukocidin (PVL) lukF-PV and lukS-PV determinants. PVL is a phage-borne, bi-component toxin [1] associated with chronic/recurrent skin and soft tissue infections and with necrotising pneumonia and fasciitis [2].

ST772-MRSA-V, colloquially known as the Bengal Bay Clone [3], is a multiresistant PVL-positive CA-MRSA initially isolated in India in 2004/2005 [4]. Transmission of Bengal Bay MRSA has subsequently occurred in several countries including England [3], Ireland [5], Germany (H.J. Linde, Regensburg, Germany, pers. communication; [6]), Norway (H. Aamot, pers. communication), Italy [7, 8], Abu Dhabi [6, 9], Saudi Arabia [10], Hong Kong [6], Malaysia [11], Australia [12] and New Zealand [13]. Many patients had a travel history or family background suggesting an infection in India, Pakistan or Bangladesh ([3, 5, 12]; H.J. Linde, Regensburg, Germany, pers. communication; author’s unpublished observations), where this strain appears to be increasingly common [14, 15].

In order to identify possible factors promoting its recent emergence and spread we have sequenced the ST772-MRSA-V genome.

Methods

Strains

One isolate of ST772-MRSA-V (07–17048) was selected for next generation genome sequencing. It was isolated from an Indian healthcare worker in Western Australia as part of standard patient care in 2007 and submitted to the Australian Collaborating Centre for Enterococcus and Staphylococcus Species for typing. Thirteen related isolates that were previously submitted for typing purposes to the participating institutions were selected. Their microarray hybridisation profiles where compared to isolate 07–17048 especially with regard to genes associated with resistance or virulence (Table 1, Additional file 1).
Table 1

Overview on typing and microarray hybridisation data for CC1 reference strains (nr. 1 and 2), CC5 reference strains (nr. 3 and 4), the strain described herein (nr. 5), other Bengal Bay isolates (nr. 6 to 14) and other, related strains (nr. 15 to 18)

Nr.

Isolate

Origin

Reference

RIDOM spa

MLST

agr

capsule type

mecA

Delta mecR

ccrA/B-1

ccrA/B-2

ccrAA/C

kdp SCC locus

blaZ/R/I

erm(C)

msr(A) + mph(C)

aacA-aphD

aadD

aphA3 + sat

fusC(Q6GD50)

tet(K)

tet(M)

tst1

sea

sea (N315)/sep

sec/sel

sed/j/r

egc (total)

seh

sek/q

ORF CM14

lukF/S-PV

lukD/E

sak

chp

scn

splA + splB

1

MW2

US

[16]

t128

ST1

III

8

+

+

-

+

-

-

+

-

-

-

-

-

-

-

-

-

+

-

+

-

-

+

+

-

+

+

+

-

+

+

2

Sanger 476

UK

[17]

t607

ST1

III

8

-

-

+

-

-

-

+

-

-

-

-

-

+

-

-

-

+

-

-

-

-

+

+

-

-

+

+

-

+

+

3

N315

Japan

[18]

t002

ST5

II

5

+

+

-

+

-

+

+

-

-

-

+

-

-

-

-

+

-

+

+

-

+

-

-

-

-

+

+

+

+

+

4

Mu50

Japan

[18]

t002

ST5

II

5

+

+

-

+

-

+

-

-

-

+

+

-

-

-

+

+

+

-

+

-

+

-

-

-

-

+

+

-

+

+

5

07-17048

WA/India

[6, 12]

t3387

ST772

II

5

+

-

-

-

+

-

+

-

+

+

-

+

-

-

-

-

+

-

+

-

+

-

-

+

+

-

-

-

+

-

6

09 V32405

Saxony

[6]

n.a.

n.a.

II

5

+

-

-

-

+

-

+

+

+

+

-

+

-

-

-

-

+

-

+

-

+

-

-

+

+

-

-

-

+

-

7

10 V3510

Saxony/India

[6]

n.a.

n.a.

II

5

+

-

-

-

+

-

+

-

+

+

-

+

-

-

-

-

+

-

+

-

+

-

-

+

+

-

-

-

+

-

8

11ANR12420

Saxony

-

n.a.

n.a.

II

5

+

-

-

-

+

-

+

-

+

+

-

+

-

-

-

-

+

-

+

-

+

-

-

+

+

-

-

-

+

-

9

12ANR75832

Saxony

-

n.a.

n.a.

II

5

+

-

-

-

+

-

+

-

+

+

-

+

-

-

-

-

+

-

+

-

+

-

-

+

+

-

-

-

+

-

10

11-18844

WA

-

t657

n.a.

II

5

+

-

-

-

+

-

+

-

+

-

-

+

-

-

-

-

+

-

+

-

+

-

-

+

+

-

-

-

+

-

11

11-18907

WA

-

t657

n.a.

II

5

+

-

-

-

+

-

+

-

+

+

-

+

-

-

-

-

+

-

+

-

+

-

-

+

+

-

-

-

+

-

12

11-19350

WA

-

t4599

n.a.

II

5

+

-

-

-

+

-

+

-

-

+

-

-

-

-

-

-

+

-

+

-

+

-

-

+

+

-

-

-

+

-

13

11-19415

WA

-

t657

n.a.

II

5

+

-

-

-

+

-

+

-

+

+

-

+

-

-

-

-

+

-

+

-

+

-

-

+

+

-

-

-

+

-

14

11-19454

WA

-

t1075

n.a.

II

5

+

-

-

-

+

-

+

+

+

+

-

+

-

-

-

-

+

-

+

-

+

-

-

+

+

-

-

-

+

-

15

03-16918 (WA-10)

WA

[6, 19]

t5073

ST573

II

5

+

-

-

-

+

-

+

-

-

-

-

-

-

-

-

-

-

-

+

-

+

-

-

+

-

-

-

-

+

-

16

11-16548

WA

-

n.a.

ST772

II

5

+

-

-

-

+

-

+

-

+

+

-

+

-

-

-

-

-

-

+

-

+

-

-

+

-

-

-

(+)

+

-

17

05 V02622

Saxony

-

n.a.

n.a.

II

5

-

-

-

-

-

-

+

-

-

-

-

-

-

-

-

-

-

-

+

-

+

-

-

+

-

-

-

-

+

-

18

DP15

Australia

-

n.a.

ST772

II

5

-

-

-

-

-

-

+

-

+

-

-

+

-

-

-

-

+

-

+

-

+

-

-

+

+

-

-

-

+

-

Methods

High-throughput de novo sequencing was undertaken commercially by Geneservice Source BioScience plc (Nottingham, United Kingdom) using the Illumina Genome Analyzer System (Illumina Hiseq 2000 platform, Illumina, Essex, United Kingdom). The average genome coverage was ca. 105. The reads were assembled to contigs using the Velvet de novo genome assembler (vers.1.0.15; Illumina). The project was registered with the NCBI BioProject database under the provisional accession number PRJNA207032 and has been deposited at DDBJ/EMBL/GenBank under the accession number AZBT00000000.

Microarray procedures have been previously described in detail [6].

Analysis

Analysis was performed using automated scripts for full text comparison and BLAST analysis and an in-house database of known, annotated and previously identified S. aureus genomes, genes and gene fragments to the query sequence. This allows determination of identity, clonal parentage and (given the constant order of core genomic genes in S. aureus) position within the genome of each contig (Additional file 2). In parallel, iterated BLAST searches were used for analysis of individual contigs in order to confirm results (http://blast.ncbi.nlm.nih.gov/Blast.cgi; [20]).

Results and discussion

In terms of microarray hybridisation patterns, the sequenced strain represents the typical and most common variant of the Bengal Bay Clone (Table 1 and Additional file 1). The isolate 07–17048 was found to belong to the multilocus sequence type (MLST) ST772 (1-1-1-1-22-1-1), spa type t3387 (RIDOM nomenclature, [21], repeat sequence 26-16-21-17-34-33-34) and dru type dt10ao (5a-4a-0-2d-5b-3a-2 g-3b-4e-3e). According to MLST e-burst analysis, ST772 is considered to belong to CC 1 as it differs from ST1 only in one MLST allele (pta-22). However, because of several differences, as shown below, its inclusion into CC1 needs to be re-assessed.

A total of 340 contigs were obtained after initial assembling. Seventy contigs consisting of 2,741,418 base pairs have been analysed (Additional file 2). The overall G/C content was 33%. 1,946 protein coding sequences have been identified (Additional file 3). 1,234 protein coding sequences were completely identical to previously identified genes from other S. aureus strains. A total number of 416, 239 and 101 protein coding sequences were completely identical to alleles from CC1 genome sequences (from MSSA476, GenBank accession number BX571857 and MW2-USA400, BA000033), CC5 genome sequences (from Mu50, BA000017; ED98, CP001781 and N315, BA000018) and CC8 genome sequences (from COL, CP000046; Newman, AP009351 and NCTC8325, CP000253) respectively. Three-hundred eighty-three genes were identical only to another ST772-MRSA-V sequence (strain 118, whole genome shotgun project AJGE00000000, [22]). Based on identities to previously published gene sequences, ST772-MRSA-V is most closely related to CC1 and CC5. Genes of CC1 and CC5 backgrounds are scattered across the genome, and no evidence for a distinct part of the genome being affected by a genomic replacement (as observed in, for instance, ST239; [23]) can be found. Theoretically, this may be attributed to a high number of recombination events involving CC1 and CC5 strains, or may indicate a common ancestry for both lineages and subsequent accumulation of random mutations in genes that are essentially orthologs in CC1, CC5 and ST772. The question whether the presence of different capsule types and agr groups in otherwise closely related strains (such as ST1 and ST772) can be attributed to recombination or to convergent evolution justifies further study.

Several fundamental differences in the ST772 and CC1 core genomic markers have already been identified by microarray DNA [6] and have been confirmed by sequencing. These differences include agr alleles (group II rather than III), the capsule type (5 rather than 8) and the presence of different allelic variants of hlb, ssl01/set6, bbp, clfB, fnbB, sdrC, sdrD, vwb and hsdS. The egc enterotoxin gene cluster, Q7A4X2 (a hypothetical protein localised close to egc), the metallothiol transferase gene fosB and the enterotoxin homologue ORF CM14 are present in ST772 but absent from other CC1 strains. The genes seh (encoding enterotoxin H), lukD/E (a leukocidin homologue), splA/B/F (serine proteases), ssl11/set2, ssl06/set21 (superantigen-like proteins), and Q2FXC0 (hypothetical protein, located next to serine protease operon) are absent in ST772, but present in other CC1 strains. In lieu of seh, the enterotoxin homologue ORF CM14 was identified in a similar position, i.e., closely downstream of the integration site of the SCCmec element. ORF CM14, absent in the related and possibly parental lineages CC1 and CC5 can be found in a number of different lineages including CC12, ST93, CC121, CC395 and CC705. This may indicate a small scale genomic replacement in a region close/downstream to oriC. Alternatively, ORF CM14 may have been replaced by seh in ancestors of CC1 or entirely deleted in CC5, but retained only in ST772.

Isolate 07–17048 harbours the enterotoxin A and PVL encoding sea and lukF/S-PV genes. Both genes are located on the same contig, and together with several other phage-associated genes, appear to be on a novel prophage. The phage is integrated into a gene of the putative protein A5IT17 which contains an attachment site of the PVL-carrying phage previously identified in other strains (un-truncated in the CC1 strain MSSA476, BX571857.1: SAS1429; truncated in the CC1 strain MW2-USA400, BA000033.2: MW1377/1443). All phage-associated genes identified are shown in Table 2.
Table 2

Genes associated with the PVL prophage in isolate 07-17048

Designation

Explanation

Position in contig

Length

Best match

tx_lukF-PV

Rho-independent terminator of lukF-PV

89974…90030

56

MW2-USA400, BA000033.2 [1529274:1529329:r]RC

lukF-PV

Panton-Valentine leukocidin F

90081…91059

978

MW2-USA400, BA000033.2 [1529381:1530358:r]RC

lukS-PV

Panton-Valentine leukocidin S

91060…91999

939

CIGC128, AHVY01000005.1 [221466:222404:r]RC

O80065

Putative protein directly upstream of lukS-PV - leader-peptide of lukPV

92106…92239

133

CIGC128, AHVY01000005.1 [222512:222644:r]RC

tx_amidase1-phiSLT

Rho-independent terminator of bacteriophage amidase

92327…92383

56

TCH1516, CP000730.1 [1562363:1562418:r]RC

amidase1-phi12

Bacteriophage amidase

92388…93843

1455

MW2-USA400, BA000033.2 [1531688:1533142:r]RC

holin1-phiL54a

Bacteriophage holin

93853…94156

303

MSSA476, BX571857.1 [1023464:1023766]RC

sprFG

Small pathogenicity island RNA F and G

94155…94266

211

ED98, CP001781.1 [892742:892952:r]

rli28

Listeria sRNA rli28 homolog, locus 2

94395…94574

179

MW2-USA400, BA000033.2 [2051199:2051377:r]RC

txpA-phage

Toxin involved in plasmid maintenance

94400…94535

1662

MW2-USA400 BA000033.2[2051171:2051305:r]RC

sea

Enterotoxin A

94652…95426

774

ST772 strain 118, AJGE01000058.1 [57550:58323]RC

minor-phiNM3

Bacteriophage minor structural protein

96751…100537

3786

TCH70-ST1, ACHH02000016.1 [79909:83694]RC

Q8SDK3-phiNM3

Putative bacteriophagal protein

100552…102037

1485

ST772 strain 118, AJGE01000058.1 [50939:52423]RC

measure1-phiNM3

Bacteriophage tail length tape measure protein

102033…106578

4545

04-02981, CP001844.2 [2051791:2056320:r]RC

tailL-CC5

Bacteriophage major tail protein

107488…108133

645

N315, BA000018.3 [2024201:2024845:r]RC

A0EWZ3

Bacteriophage major capsid protein

109862…111008

1146

Mu50-VRSA, BA000017.4 [2103511:2104656:r]RC

Q6GF91

Putative protease

111031…111769

738

A9299, ACKH01000012.1 [7311:8048]RC

portal1-phiNM3

Bacteriophage portal protein type 1

111752…112940

1188

Mu50-VRSA, BA000017.4 [2105401:2106588:r]RC

terminase-phiNM3

Bacteriophagal terminase

112955…114617

1662

Mu50-VRSA, BA000017.4 [2106604:2108265:r]RC

rinB-phiPVL

Bacteriophage transcript activator B

116263…116413

150

TCH1516, CP000730.1 [2111630:2111779:r]RC

dut-phi

Phage dUTP pyrophosphatase

117277…117820

543

MRSA252, BX571856.1 [2152883:2153425:r]RC

sri

Staphylococcal replication inhibitor

120465…120624

159

AP009351.1 [1110173:1110331]RC

istB

Replicative DNA helicase

120617…121397

780

phage, FJ713816.1 [12631:13404]RC and 04–02981, CP001844.2 [886487:887266]RC

Q4ZAK4

Putative bacteriophagal protein

121406…122177

771

04-02981, CP001844.2 [885707:886477]RC

ssb3-phage

Putative DNA binding protein

123346…123898

552

NCTC8325, CP000253.1 [2065949:2066500:r]RC

DUF2483-phi80a

Putative bacteriophagal protein

124707…124929

222

H19, ACSS01000056.1 [6024:6245:r]RC

ant-phiPV83

Bacteriophage antirepressor

127131…127929

798

phage, AY508486.1 [26092:26889]RC

repressor-var3

Bacteriophage repressor

128338…129067

729

phage, AP001553.1 [2342:3070:r]

int1-phiPVL01

Bacteriophage integrase

131132…132338

1206

ST772 strain 118, AJGE01000058.1 [20637:21842:r]

Genes sea and sprFG are normally associated with haemolysin beta converting phages rather than with PVL phages. In ST772-MRSA-V, haemolysin beta is interrupted, but there is no complete phage integrated into that gene. Only genes encoding the staphylococcal complement inhibitor scn, the putative membrane protein Q6GFB6 (usually located next to scn on hlb- converting phages, e.g., in genomes of USA300 and USA400, N315, Mu50, NCTC8325, MRSA252, MSSA476) and sprD (coding for small pathogenicity island RNA D) can be found within hlb. A possible assembly error affecting both phage integration sites is highly unlikely. Several other ST772-MRSA-V genome sequences [22, 24] also show this association of lukF/S-PV with sea. Besides, rare naturally occurring variants of ST772-MRSA-V and the related (single locus variant) ST573-MRSA-V (WA MRSA-10, [19]) lack lukS/F-PV and sea while still harbouring scn. Similar constellations can also be observed in ST573/772 MSSA (Table 1). Thus it is more likely that a part of the hlb-converting phage was translocated into a PVL phage that is integrated into a different position of the staphylococcal genome.

Other genes that are associated with mobile genetic elements include enterotoxin genes sec and sel. They are localised in similar position and context as in MW2, where they are also accompanied by phage derived genes and by the gene ear encoding the enterotoxin-linked ampicillin resistance protein. For resistance genes blaZ/I/R, msr(A), mph(C), aacA-aphD, aphA3, sat and aadE it was not possible to unambiguously determine with the given set of contigs whether they were situated on the chromosome or on plasmids. The macrolide/clindamycin resistance gene erm(C), and msr(A), mph(C), aacA-aphD, aphA3 and sat genes have been shown by microarray hybridisation to occur variably in ST772-MRSA-V (Table 1).

The isolate 07–17048 harbours a SCCmec V element. Its terminal sequence towards orfX was also present in another ST772-MRSA-V sequence (strain 118, [22]) and appears to be unique to ST772-MRSA-V. The SCCmec V element consists of a tnpIS431-04, mvaS- SCC (a truncated 3-hydroxy-3-methylglutaryl CoA synthase), a putative protein Q5HJW6, dru (SCC-associated direct repeat units), ugpQ (glycerophosphoryl diester phosphodiesterase), ydeM (a putative dehydratase), a bidirectional rho-independent terminator of mecA followed by mecA in an allelic variant identical to GQ902038 and AM990992 [25], a series of genes coding for putative proteins (Q4LAG7, Q3T2N0, Q4LAG4, Q4LAG3, Q3T2M7), a recombinase homologue “ccrAA” [26], a SCCmec type V recombinase ccrC, further genes encoding putative proteins (Q4LAF9, Q7A206, Q7A207, Q9KX75, A9UFT0), a bidirectional rho-independent terminator of hsdR and three genes (hsdR, hsdS, hsdM2) of a type I restriction-modification system.

Conclusion

In conclusion, ST772-MRSA-V may have emerged from the same root or lineage as the global CC1 and CC5 strains. It has acquired a variety of virulence factors, and, compared to other CA-MRSA strains, it has an unusually high number of genes associated with antibiotic resistance. Whether it evolved in a hospital setting or acquired these genes in community cannot be decided based on a single sequence. Therefore, more epidemiological data and possibly the sequencing of a number of additional isolates are warranted in order to understand the evolution and spread of this conspicuous strain.

Declarations

Acknowledgements

We acknowledge A. Ruppelt, B. Stieber (Dresden), A. Reissig, J. Sachtschal and E. Mueller (Jena) as well as H.L. Tan and J. Pearson (Perth) for excellent technical assistance as well as Prof. Dr. E. Jacobs (Dresden) and E. Ermantraut (Jena) for their support. We thank Geneservice Source BioScience for their efforts, A. Shore and Peter Kinnevey (Dublin) for help and information as well as C. Scott and S. Proft for proofreading the manuscript.

Authors’ Affiliations

(1)
Institute for Medical Microbiology and Hygiene, Technical University of Dresden
(2)
Alere Technologies GmbH
(3)
Australian Collaborating Centre for Enterococcus and Staphylococcus Species (ACCESS) Typing and Research, Curtin University
(4)
Department of Microbiology and Infectious Diseases, PathWest Laboratory Medicine - WA, Royal Perth Hospital

References

  1. Kaneko J, Kamio Y: Bacterial two-component and hetero-heptameric pore-forming cytolytic toxins: structures, pore-forming mechanism, and organization of the genes. Biosci Biotechnol Biochem. 2004, 68 (5): 981-1003. 10.1271/bbb.68.981.PubMedView ArticleGoogle Scholar
  2. Boyle-Vavra S, Daum RS: Community-acquired methicillin-resistant Staphylococcus aureus: the role of Panton-Valentine leukocidin. Lab Invest. 2007, 87 (1): 3-9. 10.1038/labinvest.3700501.PubMedView ArticleGoogle Scholar
  3. Ellington MJ, Ganner M, Warner M, Cookson BD, Kearns AM: Polyclonal multiply antibiotic-resistant methicillin-resistant Staphylococcus aureu s with Panton-Valentine leucocidin in England. J Antimicrob Chemother. 2010, 65 (1): 46-50. 10.1093/jac/dkp386.PubMedView ArticleGoogle Scholar
  4. Goering RV, Shawar RM, Scangarella NE, O’Hara FP, Amrine-Madsen H, West JM, Dalessandro M, Becker JA, Walsh SL, Miller LA, et al: Molecular Epidemiology of Methicillin-Resistant and Methicillin-Susceptible Staphylococcus aureus Isolates from Global Clinical Trials. J Clin Microbiol. 2008, 46 (9): 2842-2847. 10.1128/JCM.00521-08.PubMedPubMed CentralView ArticleGoogle Scholar
  5. Brennan GI, Shore AC, Corcoran S, Tecklenborg S, Coleman DC, O’Connell B: Emergence of Hospital- and Community-Associated Panton-Valentine Leukocidin-Positive Methicillin-Resistant Staphylococcus aureus Genotype ST772-MRSA-V in Ireland and Detailed Investigation of an ST772-MRSA-V Cluster in a Neonatal Intensive Care Unit. J Clin Microbiol. 2012, 50 (3): 841-847. 10.1128/JCM.06354-11.PubMedPubMed CentralView ArticleGoogle Scholar
  6. Monecke S, Coombs G, Shore AC, Coleman DC, Akpaka P, Borg M, Chow H, Ip M, Jatzwauk L, Jonas D, et al: A Field Guide to Pandemic, Epidemic and Sporadic Clones of Methicillin-Resistant Staphylococcus aureus. PLoS One. 2011, 6 (4): e17936-10.1371/journal.pone.0017936.PubMedPubMed CentralView ArticleGoogle Scholar
  7. Sanchini A, Campanile F, Monaco M, Cafiso V, Rasigade JP, Laurent F, Etienne J, Stefani S, Pantosti A: DNA microarray-based characterisation of Panton-Valentine leukocidin-positive community-acquired methicillin-resistant Staphylococcus aureus from Italy. Eur J Clin Microbiol Infect Dis. 2011, 30 (11): 1399-1408. 10.1007/s10096-011-1234-x.PubMedView ArticleGoogle Scholar
  8. Aschbacher R, Pichon B, Spoladore G, Pagani E, Innocenti P, Moroder L, Ganner M, Hill R, Pike R, Ganthaler O, et al: High clonal heterogeneity of Panton–Valentine leukocidin-positive meticillin-resistant Staphylococcus aureus strains from skin and soft-tissue infections in the Province of Bolzano, Northern Italy. Int J Antimicrob Agents. 2012, 39 (6): 522-525. 10.1016/j.ijantimicag.2012.02.004.PubMedView ArticleGoogle Scholar
  9. Weber S, Ehricht R, Slickers P, Abdel-Wareth L, Donnelly G, Pitout M, Monecke S: Genetic fingerprinting of MRSA from Abu Dhabi. ECCMID: 2010; Vienna. 2010Google Scholar
  10. Monecke S, Skakni L, Hasan R, Ruppelt A, Ghazal SS, Hakawi A, Slickers P, Ehricht R: Characterisation of MRSA strains isolated from patients in a hospital in Riyadh, Kingdom of Saudi Arabia. BMC Microbiol. 2012, 12 (1): 146-10.1186/1471-2180-12-146.PubMedPubMed CentralView ArticleGoogle Scholar
  11. Neela V, Ehsanollah GR, Zamberi S, Van Belkum A, Mariana NS: Prevalence of Panton–Valentine leukocidin genes among carriage and invasive Staphylococcus aureus isolates in Malaysia. Int J Infect Dis. 2009, 13 (3): e131-e132. 10.1016/j.ijid.2008.07.009.PubMedView ArticleGoogle Scholar
  12. Coombs GW, Monecke S, Pearson JC, Tan HL, Chew YK, Wilson L, Ehricht R, O’Brien FG, Christiansen KJ: Evolution and diversity of community-associated methicillin-resistant Staphylococcus aureus in a geographical region. BMC Microbiol. 2011, 11: 215-10.1186/1471-2180-11-215.PubMedPubMed CentralView ArticleGoogle Scholar
  13. Williamson DA, Roberts SA, Ritchie SR, Coombs GW, Fraser JD, Heffernan H: Clinical and molecular epidemiology of methicillin-resistant Staphylococcus aureus in New Zealand: rapid emergence of sequence type 5 (ST5)-SCCmec IV as the dominant community-associated MRSA clone. PLoS One. 2013, 8 (4): e62020-10.1371/journal.pone.0062020.PubMedPubMed CentralView ArticleGoogle Scholar
  14. Dsouza N, Rodrigues C, Mehta A: Molecular characterization of Methicillin resistant Staphylococcus aureus (MRSA) with emergence of epidemic clones ST 22 and ST 772, in Mumbai, India. J Clin Microbiol. 2010, 48 (5): 1806-1811. 10.1128/JCM.01867-09.View ArticleGoogle Scholar
  15. Shambat S, Nadig S, Prabhakara S, Bes M, Etienne J, Arakere G: Clonal complexes and virulence factors of Staphylococcus aureus from several cities in India. BMC Microbiol. 2012, 12 (1): 64-10.1186/1471-2180-12-64.PubMedPubMed CentralView ArticleGoogle Scholar
  16. Baba T, Takeuchi F, Kuroda M, Yuzawa H, Aoki K, Oguchi A, Nagai Y, Iwama N, Asano K, Naimi T, et al: Genome and virulence determinants of high virulence community-acquired MRSA. Lancet. 2002, 359 (9320): 1819-1827. 10.1016/S0140-6736(02)08713-5.PubMedView ArticleGoogle Scholar
  17. Holden MTG, Feil EJ, Lindsay JA, Peacock SJ, Day NPJ, Enright MC, Foster TJ, Moore CE, Hurst L, Atkin R, et al: Complete genomes of two clinical Staphylococcus aureus strains: Evidence for the rapid evolution of virulence and drug resistance. Proc Natl Acad Sci U S A. 2004, 101 (26): 9786-9791. 10.1073/pnas.0402521101.PubMedPubMed CentralView ArticleGoogle Scholar
  18. Kuroda M, Ohta T, Uchiyama I, Baba T, Yuzawa H, Kobayashi I, Cui L, Oguchi A, Aoki K, Nagai Y, et al: Whole genome sequencing of meticillin-resistant Staphylococcus aureus. Lancet. 2001, 357 (9264): 1225-1240. 10.1016/S0140-6736(00)04403-2.PubMedView ArticleGoogle Scholar
  19. Nimmo GR, Coombs GW: Community-associated methicillin-resistant Staphylococcus aureus (MRSA) in Australia. Int J Antimicrob Agents. 2008, 31 (5): 401-410. 10.1016/j.ijantimicag.2007.08.011.PubMedView ArticleGoogle Scholar
  20. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ: Basic local alignment search tool. J Mol Biol. 1990, 215 (3): 403-410.PubMedView ArticleGoogle Scholar
  21. Harmsen D, Claus H, Witte W, Rothganger J, Claus H, Turnwald D, Vogel U: Typing of Methicillin-Resistant Staphylococcus aureus in a University Hospital Setting by Using Novel Software for spa Repeat Determination and Database Management. J Clin Microbiol. 2003, 41 (12): 5442-5448. 10.1128/JCM.41.12.5442-5448.2003.PubMedPubMed CentralView ArticleGoogle Scholar
  22. Prabhakara S, Khedkar S, Loganathan RM, Chandana S, Gowda M, Arakere G, Seshasayee ASN: Draft Genome Sequence of Staphylococcus aureus 118 (ST772), a Major Disease Clone from India. J Bacteriol. 2012, 194 (14): 3727-3728. 10.1128/JB.00480-12.PubMedPubMed CentralView ArticleGoogle Scholar
  23. Robinson DA, Enright MC: Evolution of Staphylococcus aureus by Large Chromosomal Replacements. J Bacteriol. 2004, 186 (4): 1060-1064. 10.1128/JB.186.4.1060-1064.2004.PubMedPubMed CentralView ArticleGoogle Scholar
  24. Prabhakara S, Khedkar S, Shambat SM, Srinivasan R, Basu A, Norrby-Teglund A, Seshasayee ASN, Arakere G: Genome Sequencing Unveils a Novel Sea Enterotoxin-Carrying PVL Phage in Staphylococcus aureus ST772 from India. PLoS One. 2013, 8 (3): e60013-10.1371/journal.pone.0060013.PubMedPubMed CentralView ArticleGoogle Scholar
  25. Monecke S, Muller E, Schwarz S, Hotzel H, Ehricht R: Rapid microarray based identification of different mecA alleles in Staphylococci. Antimicrob Agents Chemother. 2012, 56 (11): 5547-5554. 10.1128/AAC.00574-12.PubMedPubMed CentralView ArticleGoogle Scholar
  26. Coombs GW, Monecke S, Ehricht R, Slickers P, Pearson JC, Tan HL, Christiansen KJ, O’Brien FG: Differentiation of CC59 community-associated methicillin-resistant Staphylococcus aureus in Western Australia. Antimicrob Agents Chemother. 2010, 54 (5): 1914-1921. 10.1128/AAC.01287-09.PubMedPubMed CentralView ArticleGoogle Scholar

Copyright

© Monecke et al.; licensee BioMed Central Ltd. 2013

This article is published under license to BioMed Central Ltd. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.