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Phylogenetic analysis and virulence determinant of the host-adapted Staphylococcus aureus lineage ST188 in China.

ABSTRACT: Staphylococcus aureus (S. aureus) is an important pathogen of humans and livestock species, but an understanding of the clonal distribution of S. aureus causing different host-species infections in the same geographical environment and within the same period is lacking. By characterizing infections caused by S. aureus in bovine, pediatric, and adult patients in Shanghai, China, between 2012 and 2014, we identified methicillin-sensitive S. aureus (MSSA) ST188 as the major lineage causing infections in multiple host species. Whole-genome sequencing and phenotypic analyses demonstrated that ST188 might evolve from livestock, and there was no significant genomic or virulence difference between ST188 isolated from livestock and humans. The virulence of ST188 is related to its adhesion and nasal colonization ability. This result is in accord with the strong epithelial cell adhesion and biofilm formation properties of ST188. Furthermore, the adhesion- and biofilm-formation-related genes are present in multiple copies and exhibit significantly increased expression in ST188. In conclusion, S. aureus ST188 is the major lineage causing human and livestock infections in Shanghai, China. Due to its high expression of the factors associated with bacterial adhesion and biofilm formation, ST188 has the ability to colonize and infect different host species.

SUBMITTER: Wang Y

PROVIDER: S-EPMC5874244 | biostudies-literature | 2018 Mar

REPOSITORIES: biostudies-literature

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Phylogenetic analysis and virulence determinant of the host-adapted Staphylococcus aureus lineage ST188 in China.

Wang Yanan Y Liu Qingyun Q Liu Qian Q Gao Qianqian Q Lu Huiying H Meng Hongwei H Xie Yihui Y Huang Qian Q Ma Xiaowei X Wang Hua H Qin Juanxiu J Li Qiong Q Li Tianming T Xia Qiang Q Li Min M

Emerging microbes & infections 20180329 1

Staphylococcus aureus (S. aureus) is an important pathogen of humans and livestock species, but an understanding of the clonal distribution of S. aureus causing different host-species infections in the same geographical environment and within the same period is lacking. By characterizing infections caused by S. aureus in bovine, pediatric, and adult patients in Shanghai, China, between 2012 and 2014, we identified methicillin-sensitive S. aureus (MSSA) ST188 as the major lineage causing infectio ...[more]

PMID: 29593254

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Project description:Methicillin-resistant Staphylococcus aureus (MRSA) sequence type 45 (ST45) was rarely found in China. This study was conducted to trace the transmission and evolution of emerging MRSA ST45 strains in mainland China and explore its virulence. A total of 27 ST45 isolates were included for whole-genome sequencing and genetic characteristic analysis. Epidemiological results showed that MRSA ST45 isolates were often obtained from blood, primarily originated in Guangzhou, and carried diverse virulence and drug resistance genes. Staphylococcal cassette chromosome mec type IV (SCCmec IV) dominated in MRSA ST45 (23/27, 85.2%). ST45-SCCmec V was located on a phylogenetic clade distinct from the SCCmec IV cluster. We selected two representative isolates, MR370 (ST45-SCCmec IV) and MR387 (ST45-SCCmec V), and performed hemolysin activity, a blood killing assay, a Galleria mellonella infection model, and a mouse bacteremia model, as well as real-time fluorescence quantitative PCR. MR370 was proved to have extreme virulence in the phenotypic assays and at the mRNA level compared with ST59, ST5, and USA300 MRSA strains. MR387 was comparable to USA300-LAC on the phenotype and was verified to have higher expression of scn, chp, sak, saeR, agrA, and RNAIII than USA300-LAC. The results emphasized the extraordinary performance of MR370 and the good potential of MR387 in virulence causing bloodstream infection. Meanwhile, we conclude that China MRSA ST45 showed two different clonotypes, which may be widespread in the future. The entire study is valuable as a timely reminder and reports virulence phenotypes of China MRSA ST45 for the first time. IMPORTANCE Methicillin-resistant Staphylococcus aureus ST45 is epidemic worldwide. This study contributed to the awareness of the Chinese hyper-virulent MRSA ST45 strains and served as a timely reminder of its wide dissemination of clonotypes. Further, we provide novel insights for prevention from the perspective of bloodstream infections. ST45-SCCmec V is a clonotype deserving special attention in China, and we performed genetic and phenotypic analyses for the first time on it.

Project description:BackgroundMethicillin-resistant Staphylococcus aureus (MRSA) is a major nosocomial pathogen subdivided into lineages termed sequence types (STs). Since the 1950s, successive waves of STs have appeared and replaced previously dominant lineages. One such event has been occurring in China since 2013, with community-associated (CA-MRSA) strains including ST59 largely replacing the previously dominant healthcare-associated (HA-MRSA) ST239. We previously showed that ST59 isolates tend to have a competitive advantage in growth experiments against ST239. However, the underlying genomic and phenotypic drivers of this replacement event are unclear.MethodsHere, we investigated the replacement of ST239 using whole-genome sequencing data from 204 ST239 and ST59 isolates collected in Chinese hospitals between 1994 and 2016. We reconstructed the evolutionary history of each ST and considered two non-mutually exclusive hypotheses for ST59 replacing ST239: antimicrobial resistance (AMR) profile and/or ability to colonise and persist in the environment through biofilm formation. We also investigated the differences in cytolytic activity, linked to higher virulence, between STs. We performed an association study using the presence and absence of accessory virulence genes.ResultsST59 isolates carried fewer AMR genes than ST239 and showed no evidence of evolving towards higher AMR. Biofilm production was marginally higher in ST59 overall, though this effect was not consistent across sub-lineages so is unlikely to be a sole driver of replacement. Consistent with previous observations of higher virulence in CA-MRSA STs, we observed that ST59 isolates exhibit significantly higher cytolytic activity than ST239 isolates, despite carrying on average fewer putative virulence genes. Our association study identified the chemotaxis inhibitory protein (chp) as a strong candidate for involvement in the increased virulence potential of ST59. We experimentally validated the role of chp in increasing the virulence potential of ST59 by creating Δchp knockout mutants, confirming that ST59 can carry chp without a measurable impact on fitness.ConclusionsOur results suggest that the ongoing replacement of ST239 by ST59 in China is not associated to higher AMR carriage or biofilm production. However, the increase in ST59 prevalence is concerning since it is linked to a higher potential for virulence, aided by the carriage of the chp gene.

Dataset Information

Phylogenetic analysis and virulence determinant of the host-adapted Staphylococcus aureus lineage ST188 in China.

Publications

Phylogenetic analysis and virulence determinant of the host-adapted Staphylococcus aureus lineage ST188 in China.

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