Dataset Information

Detection of Streptococcus pyogenes M1_UK in Australia and characterization of the mutation driving enhanced expression of superantigen SpeA.

ABSTRACT: A new variant of Streptococcus pyogenes serotype M1 (designated 'M1_UK') has been reported in the United Kingdom, linked with seasonal scarlet fever surges, marked increase in invasive infections, and exhibiting enhanced expression of the superantigen SpeA. The progenitor S. pyogenes 'M1_global' and M1_UK clones can be differentiated by 27 SNPs and 4 indels, yet the mechanism for speA upregulation is unknown. Here we investigate the previously unappreciated expansion of M1_UK in Australia, now isolated from the majority of serious infections caused by serotype M1 S. pyogenes. M1_UK sub-lineages circulating in Australia also contain a novel toxin repertoire associated with epidemic scarlet fever causing S. pyogenes in Asia. A single SNP in the 5' transcriptional leader sequence of the transfer-messenger RNA gene ssrA drives enhanced SpeA superantigen expression as a result of ssrA terminator read-through in the M1_UK lineage. This represents a previously unappreciated mechanism of toxin expression and urges enhanced international surveillance.

SUBMITTER: Davies MR

PROVIDER: S-EPMC9951164 | biostudies-literature | 2023 Feb

REPOSITORIES: biostudies-literature

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Detection of Streptococcus pyogenes M1UK in Australia and characterization of the mutation driving enhanced expression of superantigen SpeA.

Davies Mark R MR Keller Nadia N Brouwer Stephan S Jespersen Magnus G MG Cork Amanda J AJ Hayes Andrew J AJ Pitt Miranda E ME De Oliveira David M P DMP Harbison-Price Nichaela N Bertolla Olivia M OM Mediati Daniel G DG Curren Bodie F BF Taiaroa George G Lacey Jake A JA Smith Helen V HV Fang Ning-Xia NX Coin Lachlan J M LJM Stevens Kerrie K Tong Steven Y C SYC Sanderson-Smith Martina M Tree Jai J JJ Irwin Adam D AD Grimwood Keith K Howden Benjamin P BP Jennison Amy V AV Walker Mark J MJ

Nature communications 20230224 1

A new variant of Streptococcus pyogenes serotype M1 (designated 'M1UK') has been reported in the United Kingdom, linked with seasonal scarlet fever surges, marked increase in invasive infections, and exhibiting enhanced expression of the superantigen SpeA. The progenitor S. pyogenes 'M1global' and M1UK clones can be differentiated by 27 SNPs and 4 indels, yet the mechanism for speA upregulation is unknown. Here we investigate the previously unappreciated expansio ...[more]

PMID: 36828918

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Project description:Streptococcus pyogenes genotype emm1 is a successful, globally distributed epidemic clone that is regarded as inherently virulent. An emm1 sublineage, M1UK, that produces increased levels of SpeA toxin was associated with increased scarlet fever and invasive infections in England in 2015/2016. Defined by 27 SNPs in the core genome, M1UK is now dominant in England. To more fully characterize M1UK, we undertook comparative transcriptomic and proteomic analyses of M1UK and contemporary non-M1UK emm1 strains (M1global). Just seven genes were differentially expressed by M1UK compared with contemporary M1global strains. In addition to speA, five genes in the operon that includes glycerol dehydrogenase were upregulated in M1UK (gldA, mipB/talC, pflD, and phosphotransferase system IIC and IIB components), while aquaporin (glpF2) was downregulated. M1UK strains have a stop codon in gldA. Deletion of gldA in M1global abrogated glycerol dehydrogenase activity, and recapitulated upregulation of gene expression within the operon that includes gldA, consistent with a feedback effect. Phylogenetic analysis identified two intermediate emm1 sublineages in England comprising 13/27 (M113SNPs) and 23/27 SNPs (M123SNPs), respectively, that had failed to expand in the population. Proteomic analysis of invasive strains from the four phylogenetic emm1 groups highlighted sublineage-specific changes in carbohydrate metabolism, protein synthesis and protein processing; upregulation of SpeA was not observed in chemically defined medium. In rich broth, however, expression of SpeA was upregulated ~10-fold in both M123SNPs and M1UK sublineages, compared with M113SNPs and M1global. We conclude that stepwise accumulation of SNPs led to the emergence of M1UK. While increased expression of SpeA is a key indicator of M1UK and undoubtedly important, M1UK strains have outcompeted M123SNPs and other emm types that produce similar or more superantigen toxin. We speculate that an accumulation of adaptive SNPs has contributed to a wider fitness advantage in M1UK on an inherently successful emm1 streptococcal background.

Dataset Information

Detection of Streptococcus pyogenes M1_UK in Australia and characterization of the mutation driving enhanced expression of superantigen SpeA.

Publications

Detection of Streptococcus pyogenes M1<sub>UK</sub> in Australia and characterization of the mutation driving enhanced expression of superantigen SpeA.

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