Emergence of scarlet fever Streptococcus pyogenes emm12 clones in Hong Kong is associated with toxin acquisition and multidrug resistance

Mark R Davies; Matthew T Holden; Paul Coupland; Jonathan H K Chen; Carola Venturini; Timothy C Barnett; Nouri L Ben Zakour; Herman Tse; Gordon Dougan; Kwok-Yung Yuen; Mark J Walker

doi:10.1038/ng.3147

Emergence of scarlet fever Streptococcus pyogenes emm12 clones in Hong Kong is associated with toxin acquisition and multidrug resistance

Nat Genet. 2015 Jan;47(1):84-7. doi: 10.1038/ng.3147. Epub 2014 Nov 17.

Authors

Affiliations

¹ 1] Australian Infectious Diseases Research Centre, School of Chemistry and Molecular Biosciences, University of Queensland, St. Lucia, Queensland, Australia. [2] Wellcome Trust Sanger Institute, Hinxton, UK.
² Wellcome Trust Sanger Institute, Hinxton, UK.
³ Department of Microbiology, Queen Mary Hospital, Hong Kong, China.
⁴ Australian Infectious Diseases Research Centre, School of Chemistry and Molecular Biosciences, University of Queensland, St. Lucia, Queensland, Australia.
⁵ 1] Department of Microbiology, Queen Mary Hospital, Hong Kong, China. [2] Carol Yu Centre for Infection, The University of Hong Kong, Hong Kong, China. [3] State Key Laboratory for Emerging Infectious Diseases, Hong Kong, China.

PMID: 25401300
DOI: 10.1038/ng.3147

Abstract

A scarlet fever outbreak began in mainland China and Hong Kong in 2011 (refs. 1-6). Macrolide- and tetracycline-resistant Streptococcus pyogenes emm12 isolates represent the majority of clinical cases. Recently, we identified two mobile genetic elements that were closely associated with emm12 outbreak isolates: the integrative and conjugative element ICE-emm12, encoding genes for tetracycline and macrolide resistance, and prophage ΦHKU.vir, encoding the superantigens SSA and SpeC, as well as the DNase Spd1 (ref. 4). Here we sequenced the genomes of 141 emm12 isolates, including 132 isolated in Hong Kong between 2005 and 2011. We found that the introduction of several ICE-emm12 variants, ΦHKU.vir and a new prophage, ΦHKU.ssa, occurred in three distinct emm12 lineages late in the twentieth century. Acquisition of ssa and transposable elements encoding multidrug resistance genes triggered the expansion of scarlet fever-associated emm12 lineages in Hong Kong. The occurrence of multidrug-resistant ssa-harboring scarlet fever strains should prompt heightened surveillance within China and abroad for the dissemination of these mobile genetic elements.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Adolescent
Adult
Aged
Antigens, Bacterial / genetics
Bacterial Outer Membrane Proteins / genetics
Bacterial Proteins / genetics
Bacterial Toxins / genetics*
Carrier Proteins / genetics
Child
Child, Preschool
DNA, Bacterial / genetics
Disease Outbreaks
Drug Resistance, Multiple, Bacterial / genetics*
Exotoxins / genetics
Genetic Drift
Hong Kong / epidemiology
Humans
Interspersed Repetitive Sequences / genetics*
Middle Aged
Molecular Sequence Data
Mutation Rate
Phylogeny
Polymorphism, Single Nucleotide
Population Surveillance
Prophages / genetics*
Scarlet Fever / epidemiology
Scarlet Fever / microbiology*
Streptococcal Infections / epidemiology
Streptococcal Infections / microbiology
Streptococcus pyogenes / classification
Streptococcus pyogenes / drug effects
Streptococcus pyogenes / genetics*
Streptococcus pyogenes / isolation & purification
Streptococcus pyogenes / metabolism
Streptococcus pyogenes / virology
Young Adult

Substances

Antigens, Bacterial
Bacterial Outer Membrane Proteins
Bacterial Proteins
Bacterial Toxins
Carrier Proteins
DNA, Bacterial
Exotoxins
erythrogenic toxin
streptococcal M protein
streptococcal superantigen SSA

Associated data

GENBANK/CP009612

Grants and funding

100891/Wellcome Trust/United Kingdom