Population and Whole Genome Sequence Based Characterization of Invasive Group A Streptococci Recovered in the United States during 2015

ABSTRACT Group A streptococci (GAS) are genetically diverse. Determination of strain features can reveal associations with disease and resistance and assist in vaccine formulation. We employed whole-genome sequence (WGS)-based characterization of 1,454 invasive GAS isolates recovered in 2015 by Acti...

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Autores principales:	Sopio Chochua, Ben J. Metcalf, Zhongya Li, Joy Rivers, Saundra Mathis, Delois Jackson, Robert E. Gertz, Velusamy Srinivasan, Ruth Lynfield, Chris Van Beneden, Lesley McGee, Bernard Beall
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	streptococcal disease seasonality Streptococcus pyogenes vaccines invasive group A streptococci streptococcal genetics streptococcal resistance streptococcal virulence features Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/ee6bf7bb66684e4889972696d53e9da6
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spelling	oai:doaj.org-article:ee6bf7bb66684e4889972696d53e9da62021-11-15T15:51:51ZPopulation and Whole Genome Sequence Based Characterization of Invasive Group A Streptococci Recovered in the United States during 201510.1128/mBio.01422-172150-7511https://doaj.org/article/ee6bf7bb66684e4889972696d53e9da62017-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01422-17https://doaj.org/toc/2150-7511ABSTRACT Group A streptococci (GAS) are genetically diverse. Determination of strain features can reveal associations with disease and resistance and assist in vaccine formulation. We employed whole-genome sequence (WGS)-based characterization of 1,454 invasive GAS isolates recovered in 2015 by Active Bacterial Core Surveillance and performed conventional antimicrobial susceptibility testing. Predictions were made for genotype, GAS carbohydrate, antimicrobial resistance, surface proteins (M family, fibronectin binding, T, R28), secreted virulence proteins (Sda1, Sic, exotoxins), hyaluronate capsule, and an upregulated nga operon (encodes NADase and streptolysin O) promoter (Pnga3). Sixty-four M protein gene (emm) types were identified among 69 clonal complexes (CCs), including one CC of Streptococcus dysgalactiae subsp. equisimilis. emm types predicted the presence or absence of active sof determinants and were segregated into sof-positive or sof-negative genetic complexes. Only one “emm type switch” between strains was apparent. sof-negative strains showed a propensity to cause infections in the first quarter of the year, while sof+ strain infections were more likely in summer. Of 1,454 isolates, 808 (55.6%) were Pnga3 positive and 637 (78.9%) were accounted for by types emm1, emm89, and emm12. Theoretical coverage of a 30-valent M vaccine combined with an M-related protein (Mrp) vaccine encompassed 98% of the isolates. WGS data predicted that 15.3, 13.8, 12.7, and 0.6% of the isolates were nonsusceptible to tetracycline, erythromycin plus clindamycin, erythromycin, and fluoroquinolones, respectively, with only 19 discordant phenotypic results. Close phylogenetic clustering of emm59 isolates was consistent with recent regional emergence. This study revealed strain traits informative for GAS disease incidence tracking, outbreak detection, vaccine strategy, and antimicrobial therapy. IMPORTANCE The current population-based WGS data from GAS strains causing invasive disease in the United States provide insights important for prevention and control strategies. Strain distribution data support recently proposed multivalent M type-specific and conserved M-like protein vaccine formulations that could potentially protect against nearly all invasive U.S. strains. The three most prevalent clonal complexes share key polymorphisms in the nga operon encoding two secreted virulence factors (NADase and streptolysin O) that have been previously associated with high strain virulence and transmissibility. We find that Streptococcus pyogenes is phylogenetically subdivided into loosely defined multilocus sequence type-based clusters consisting of solely sof-negative or sof-positive strains; with sof-negative strains demonstrating differential seasonal preference for infection, consistent with the recently demonstrated differential seasonal preference based on phylogenetic clustering of full-length M proteins. This might relate to the differences in GAS strain compositions found in different geographic settings and could further inform prevention strategies.Sopio ChochuaBen J. MetcalfZhongya LiJoy RiversSaundra MathisDelois JacksonRobert E. GertzVelusamy SrinivasanRuth LynfieldChris Van BenedenLesley McGeeBernard BeallAmerican Society for Microbiologyarticlestreptococcal disease seasonalityStreptococcus pyogenes vaccinesinvasive group A streptococcistreptococcal geneticsstreptococcal resistancestreptococcal virulence featuresMicrobiologyQR1-502ENmBio, Vol 8, Iss 5 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	streptococcal disease seasonality Streptococcus pyogenes vaccines invasive group A streptococci streptococcal genetics streptococcal resistance streptococcal virulence features Microbiology QR1-502
spellingShingle	streptococcal disease seasonality Streptococcus pyogenes vaccines invasive group A streptococci streptococcal genetics streptococcal resistance streptococcal virulence features Microbiology QR1-502 Sopio Chochua Ben J. Metcalf Zhongya Li Joy Rivers Saundra Mathis Delois Jackson Robert E. Gertz Velusamy Srinivasan Ruth Lynfield Chris Van Beneden Lesley McGee Bernard Beall Population and Whole Genome Sequence Based Characterization of Invasive Group A Streptococci Recovered in the United States during 2015
description	ABSTRACT Group A streptococci (GAS) are genetically diverse. Determination of strain features can reveal associations with disease and resistance and assist in vaccine formulation. We employed whole-genome sequence (WGS)-based characterization of 1,454 invasive GAS isolates recovered in 2015 by Active Bacterial Core Surveillance and performed conventional antimicrobial susceptibility testing. Predictions were made for genotype, GAS carbohydrate, antimicrobial resistance, surface proteins (M family, fibronectin binding, T, R28), secreted virulence proteins (Sda1, Sic, exotoxins), hyaluronate capsule, and an upregulated nga operon (encodes NADase and streptolysin O) promoter (Pnga3). Sixty-four M protein gene (emm) types were identified among 69 clonal complexes (CCs), including one CC of Streptococcus dysgalactiae subsp. equisimilis. emm types predicted the presence or absence of active sof determinants and were segregated into sof-positive or sof-negative genetic complexes. Only one “emm type switch” between strains was apparent. sof-negative strains showed a propensity to cause infections in the first quarter of the year, while sof+ strain infections were more likely in summer. Of 1,454 isolates, 808 (55.6%) were Pnga3 positive and 637 (78.9%) were accounted for by types emm1, emm89, and emm12. Theoretical coverage of a 30-valent M vaccine combined with an M-related protein (Mrp) vaccine encompassed 98% of the isolates. WGS data predicted that 15.3, 13.8, 12.7, and 0.6% of the isolates were nonsusceptible to tetracycline, erythromycin plus clindamycin, erythromycin, and fluoroquinolones, respectively, with only 19 discordant phenotypic results. Close phylogenetic clustering of emm59 isolates was consistent with recent regional emergence. This study revealed strain traits informative for GAS disease incidence tracking, outbreak detection, vaccine strategy, and antimicrobial therapy. IMPORTANCE The current population-based WGS data from GAS strains causing invasive disease in the United States provide insights important for prevention and control strategies. Strain distribution data support recently proposed multivalent M type-specific and conserved M-like protein vaccine formulations that could potentially protect against nearly all invasive U.S. strains. The three most prevalent clonal complexes share key polymorphisms in the nga operon encoding two secreted virulence factors (NADase and streptolysin O) that have been previously associated with high strain virulence and transmissibility. We find that Streptococcus pyogenes is phylogenetically subdivided into loosely defined multilocus sequence type-based clusters consisting of solely sof-negative or sof-positive strains; with sof-negative strains demonstrating differential seasonal preference for infection, consistent with the recently demonstrated differential seasonal preference based on phylogenetic clustering of full-length M proteins. This might relate to the differences in GAS strain compositions found in different geographic settings and could further inform prevention strategies.
format	article
author	Sopio Chochua Ben J. Metcalf Zhongya Li Joy Rivers Saundra Mathis Delois Jackson Robert E. Gertz Velusamy Srinivasan Ruth Lynfield Chris Van Beneden Lesley McGee Bernard Beall
author_facet	Sopio Chochua Ben J. Metcalf Zhongya Li Joy Rivers Saundra Mathis Delois Jackson Robert E. Gertz Velusamy Srinivasan Ruth Lynfield Chris Van Beneden Lesley McGee Bernard Beall
author_sort	Sopio Chochua
title	Population and Whole Genome Sequence Based Characterization of Invasive Group A Streptococci Recovered in the United States during 2015
title_short	Population and Whole Genome Sequence Based Characterization of Invasive Group A Streptococci Recovered in the United States during 2015
title_full	Population and Whole Genome Sequence Based Characterization of Invasive Group A Streptococci Recovered in the United States during 2015
title_fullStr	Population and Whole Genome Sequence Based Characterization of Invasive Group A Streptococci Recovered in the United States during 2015
title_full_unstemmed	Population and Whole Genome Sequence Based Characterization of Invasive Group A Streptococci Recovered in the United States during 2015
title_sort	population and whole genome sequence based characterization of invasive group a streptococci recovered in the united states during 2015
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/ee6bf7bb66684e4889972696d53e9da6
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_version_	1718427373544669184

Population and Whole Genome Sequence Based Characterization of Invasive Group A Streptococci Recovered in the United States during 2015

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