Emergence of a New Highly Successful Acapsular Group A <italic toggle="yes">Streptococcus</italic> Clade of Genotype <italic toggle="yes">emm</italic>89 in the United Kingdom

ABSTRACT Group A Streptococcus (GAS) genotype emm89 is increasingly recognized as a leading cause of disease worldwide, yet factors that underlie the success of this emm type are unknown. Surveillance identified a sustained nationwide increase in emm89 invasive GAS disease in the United Kingdom, pro...

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Autores principales:	Claire E. Turner, James Abbott, Theresa Lamagni, Matthew T. G. Holden, Sophia David, Michael D. Jones, Laurence Game, Androulla Efstratiou, Shiranee Sriskandan
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Lenguaje:	EN
Publicado:	American Society for Microbiology 2015
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/2ceb8adf72f24ed59097bfe910f0225a
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spelling	oai:doaj.org-article:2ceb8adf72f24ed59097bfe910f0225a2021-11-15T15:41:26ZEmergence of a New Highly Successful Acapsular Group A <italic toggle="yes">Streptococcus</italic> Clade of Genotype <italic toggle="yes">emm</italic>89 in the United Kingdom10.1128/mBio.00622-152150-7511https://doaj.org/article/2ceb8adf72f24ed59097bfe910f0225a2015-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00622-15https://doaj.org/toc/2150-7511ABSTRACT Group A Streptococcus (GAS) genotype emm89 is increasingly recognized as a leading cause of disease worldwide, yet factors that underlie the success of this emm type are unknown. Surveillance identified a sustained nationwide increase in emm89 invasive GAS disease in the United Kingdom, prompting longitudinal investigation of this genotype. Whole-genome sequencing revealed a recent dramatic shift in the emm89 population with the emergence of a new clade that increased to dominance over previous emm89 variants. Temporal analysis indicated that the clade arose in the early 1990s but abruptly increased in prevalence in 2008, coinciding with an increased incidence of emm89 infections. Although standard variable typing regions (emm subtype, tee type, sof type, and multilocus sequence typing [MLST]) remained unchanged, uniquely the emergent clade had undergone six distinct regions of homologous recombination across the genome compared to the rest of the sequenced emm89 population. Two of these regions affected known virulence factors, the hyaluronic acid capsule and the toxins NADase and streptolysin O. Unexpectedly, and in contrast to the rest of the sequenced emm89 population, the emergent clade-associated strains were genetically acapsular, rendering them unable to produce the hyaluronic acid capsule. The emergent clade-associated strains had also acquired an NADase/streptolysin O locus nearly identical to that found in emm12 and modern emm1 strains but different from the rest of the sequenced emm89 population. The emergent clade-associated strains had enhanced expression of NADase and streptolysin O. The genome remodeling in the new clade variant and the resultant altered phenotype appear to have conferred a selective advantage over other emm89 variants and may explain the changes observed in emm89 GAS epidemiology. IMPORTANCE Sudden upsurges or epidemic waves are common features of group A streptococcal disease. Although the mechanisms behind such changes are largely unknown, they are often associated with an expansion of a single genotype within the population. Using whole-genome sequencing, we investigated a nationwide increase in invasive disease caused by the genotype emm89 in the United Kingdom. We identified a new clade variant that had recently emerged in the emm89 population after having undergone several core genomic recombination-related changes, two of which affected known virulence factors. An unusual finding of the new variant was the loss of the hyaluronic acid capsule, previously thought to be essential for causing invasive disease. A further genomic adaptation in the NADase/streptolysin O locus resulted in enhanced production of these toxins. Recombination-related genome remodeling is clearly an important mechanism in group A Streptococcus that can give rise to more successful and potentially more pathogenic variants.Claire E. TurnerJames AbbottTheresa LamagniMatthew T. G. HoldenSophia DavidMichael D. JonesLaurence GameAndroulla EfstratiouShiranee SriskandanAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 4 (2015)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Claire E. Turner James Abbott Theresa Lamagni Matthew T. G. Holden Sophia David Michael D. Jones Laurence Game Androulla Efstratiou Shiranee Sriskandan Emergence of a New Highly Successful Acapsular Group A <italic toggle="yes">Streptococcus</italic> Clade of Genotype <italic toggle="yes">emm</italic>89 in the United Kingdom
description	ABSTRACT Group A Streptococcus (GAS) genotype emm89 is increasingly recognized as a leading cause of disease worldwide, yet factors that underlie the success of this emm type are unknown. Surveillance identified a sustained nationwide increase in emm89 invasive GAS disease in the United Kingdom, prompting longitudinal investigation of this genotype. Whole-genome sequencing revealed a recent dramatic shift in the emm89 population with the emergence of a new clade that increased to dominance over previous emm89 variants. Temporal analysis indicated that the clade arose in the early 1990s but abruptly increased in prevalence in 2008, coinciding with an increased incidence of emm89 infections. Although standard variable typing regions (emm subtype, tee type, sof type, and multilocus sequence typing [MLST]) remained unchanged, uniquely the emergent clade had undergone six distinct regions of homologous recombination across the genome compared to the rest of the sequenced emm89 population. Two of these regions affected known virulence factors, the hyaluronic acid capsule and the toxins NADase and streptolysin O. Unexpectedly, and in contrast to the rest of the sequenced emm89 population, the emergent clade-associated strains were genetically acapsular, rendering them unable to produce the hyaluronic acid capsule. The emergent clade-associated strains had also acquired an NADase/streptolysin O locus nearly identical to that found in emm12 and modern emm1 strains but different from the rest of the sequenced emm89 population. The emergent clade-associated strains had enhanced expression of NADase and streptolysin O. The genome remodeling in the new clade variant and the resultant altered phenotype appear to have conferred a selective advantage over other emm89 variants and may explain the changes observed in emm89 GAS epidemiology. IMPORTANCE Sudden upsurges or epidemic waves are common features of group A streptococcal disease. Although the mechanisms behind such changes are largely unknown, they are often associated with an expansion of a single genotype within the population. Using whole-genome sequencing, we investigated a nationwide increase in invasive disease caused by the genotype emm89 in the United Kingdom. We identified a new clade variant that had recently emerged in the emm89 population after having undergone several core genomic recombination-related changes, two of which affected known virulence factors. An unusual finding of the new variant was the loss of the hyaluronic acid capsule, previously thought to be essential for causing invasive disease. A further genomic adaptation in the NADase/streptolysin O locus resulted in enhanced production of these toxins. Recombination-related genome remodeling is clearly an important mechanism in group A Streptococcus that can give rise to more successful and potentially more pathogenic variants.
format	article
author	Claire E. Turner James Abbott Theresa Lamagni Matthew T. G. Holden Sophia David Michael D. Jones Laurence Game Androulla Efstratiou Shiranee Sriskandan
author_facet	Claire E. Turner James Abbott Theresa Lamagni Matthew T. G. Holden Sophia David Michael D. Jones Laurence Game Androulla Efstratiou Shiranee Sriskandan
author_sort	Claire E. Turner
title	Emergence of a New Highly Successful Acapsular Group A <italic toggle="yes">Streptococcus</italic> Clade of Genotype <italic toggle="yes">emm</italic>89 in the United Kingdom
title_short	Emergence of a New Highly Successful Acapsular Group A <italic toggle="yes">Streptococcus</italic> Clade of Genotype <italic toggle="yes">emm</italic>89 in the United Kingdom
title_full	Emergence of a New Highly Successful Acapsular Group A <italic toggle="yes">Streptococcus</italic> Clade of Genotype <italic toggle="yes">emm</italic>89 in the United Kingdom
title_fullStr	Emergence of a New Highly Successful Acapsular Group A <italic toggle="yes">Streptococcus</italic> Clade of Genotype <italic toggle="yes">emm</italic>89 in the United Kingdom
title_full_unstemmed	Emergence of a New Highly Successful Acapsular Group A <italic toggle="yes">Streptococcus</italic> Clade of Genotype <italic toggle="yes">emm</italic>89 in the United Kingdom
title_sort	emergence of a new highly successful acapsular group a <italic toggle="yes">streptococcus</italic> clade of genotype <italic toggle="yes">emm</italic>89 in the united kingdom
publisher	American Society for Microbiology
publishDate	2015
url	https://doaj.org/article/2ceb8adf72f24ed59097bfe910f0225a
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Emergence of a New Highly Successful Acapsular Group A <italic toggle="yes">Streptococcus</italic> Clade of Genotype <italic toggle="yes">emm</italic>89 in the United Kingdom

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