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Pathologic and molecular characterization of Streptococcus dysgalactiae subsp. equisimilis infection in neonatal piglets.

ABSTRACT: Streptococcus dysgalactiae subspecies equisimilis (SDSE) is an emerging pathogen in animals and humans. Herein, we describe two clinical swine cases of SDSE infection presenting with lameness, neurological signs, or sudden death. Pathological examination indicated suppurative arthritis, encephalitis, and multifocal abscesses in kidney and heart. The ?-hemolytic colonies obtained from joint samples of each case were identified as SDSE. The two isolates had low minimum inhibitory concentrations for ?-lactams, and they presented the same virulence gene profile (slo-/sagA?/pSTKP8?). Molecular analysis by multilocus sequence typing identified the SDSE isolates from cases 1 and 2 as sequence types 315 and 252, respectively.

SUBMITTER: Oh SI

PROVIDER: S-EPMC5879081 | biostudies-literature | 2018 Mar

REPOSITORIES: biostudies-literature

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Pathologic and molecular characterization of Streptococcus dysgalactiae subsp. equisimilis infection in neonatal piglets.

Oh Sang-Ik SI Kim Jong Wan JW Jung Ji-Youl JY Chae Myeongju M Lee Yu-Ran YR Kim Jong Ho JH So ByungJae B Kim Ha-Young HY

Journal of veterinary science 20180301 2

Streptococcus dysgalactiae subspecies equisimilis (SDSE) is an emerging pathogen in animals and humans. Herein, we describe two clinical swine cases of SDSE infection presenting with lameness, neurological signs, or sudden death. Pathological examination indicated suppurative arthritis, encephalitis, and multifocal abscesses in kidney and heart. The β-hemolytic colonies obtained from joint samples of each case were identified as SDSE. The two isolates had low minimum inhibitory con ...[more]

PMID: 29284213

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Project description:Streptococcus dysgalactiae subsp. equisimilis (SDSE) is an emerging human pathogen that causes severe invasive streptococcal diseases. Recent reports have shown that SDSE exhibits high pathogenicity with different mechanisms from that of Streptococcus pyogenes, although the two streptococci possess some common virulence factors such as streptolysin, streptokinase, and cell-binding proteins. To date, only a few studies have examined the variety of mechanisms expressing the pathogenicity of SDSE. Among nine SDSE clinical isolates sequenced in this study, we present in vitro and in vivo analyses of KNZ01 and KNZ03, whose emm and multilocus species types (MLSTs) are prevalent in Japan and other countries. For the comparison of pathogenicity, we also utilized the ATCC 12394 strain. The whole-genome analysis showed that KNZ03 and ATCC 12394 are categorized into an identical clonal complex by MLST and are phylogenetically close. However, the three strains exhibited different characteristics for pathogenicity in vitro; ATCC 12394 showed significant cytotoxicity to human keratinocytes and release of streptolysin O (SLO) compared to KNZ01 and KNZ03; KNZ03 exhibited significantly high hemolytic activity, but did not secrete SLO. KNZ01 and KNZ03 adhered to human keratinocytes at a higher rate than ATCC 12394; KNZ03 showed a higher rate of survival after a brief (30 min) incubation with human neutrophils compared to the other two strains; also, KNZ01 grew more rapidly in the presence of human serum. In vivo subcutaneous infection commonly resulted in ulcer formation in the three strains 7 days after infection. KNZ01-infected mice showed significant body weight loss 2 days after infection. Besides, on post-infection day 2, only KNZ01 remained in the cutaneous tissues of mice. Scanning electron microscopy analysis revealed that KNZ01 formed an extracellular structure (biofilm), which was probably composed of cell wall-anchoring proteins, in the presence of glucose and human serum. The extracellular structure of ATCC 12394 was also changed dramatically in response to culture conditions, whereas that of KNZ03 did not. Our study proposed that each SDSE strain possesses different virulence factors characteristics for mediating pathogenicity in humans.

Project description:Streptococcus dysgalactiae subsp. equisimilis (SDSE) causes cellulitis, bacteremia, and invasive diseases, such as streptococcal toxic shock syndrome. Although SDSE infection is more prevalent among elderly individuals and those with diabetes mellitus than infections with Streptococcus pyogenes (Group A streptococci; GAS) and Streptococcus agalactiae (Group B streptococci; GBS), the mechanisms underlying the pathogenicity of SDSE remain unknown. SDSE possesses a gene hylD encoding a hyaluronate lyase (HylD), whose homologue (HylB) is involved in pathogenicity of GBS, while the role of HylD has not been characterized. In this study, we focused on the enzyme HylD produced by SDSE; HylD cleaves hyaluronate (HA) and generates unsaturated disaccharides via a ?-elimination reaction. Hyaluronate-agar plate assays revealed that SDSE promoted dramatic HA degradation. SDSE expresses both HylD and an unsaturated glucuronyl hydrolase (UGL) that catalyzes the degradation of HA-derived oligosaccharides; as such, SDSE was more effective at HA degradation than other ?-hemolytic streptococci, including GAS and GBS. Although HylD shows some homology to HylB, a similar enzyme produced by GBS, HylD exhibited significantly higher enzymatic activity than HylB at pH 6.0, conditions that are detected in the skin of both elderly individuals and those with diabetes mellitus. We also detected upregulation of transcripts from hylD and ugl genes from SDSE wild-type collected from the mouse peritoneal cavity; upregulated expression of ugl was not observed in ?hylD SDSE mutants. These results suggested that disaccharides produced by the actions of HylD are capable of triggering downstream pathways that catalyze their destruction. Furthermore, we determined that infection with SDSE?hylD was significantly less lethal than infection with the parent strain. When mouse skin wounds were infected for 2 days, intensive infiltration of neutrophils was observed around the wound areas infected with SDSE wild-type but not SDSE?hylD. Our investigation suggested that HylD and UGL play important roles in nutrient acquisition from hosts, followed by the bacterial pathogenicity damaging host tissues.

Dataset Information

Pathologic and molecular characterization of Streptococcus dysgalactiae subsp. equisimilis infection in neonatal piglets.

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Pathologic and molecular characterization of <i>Streptococcus dysgalactiae</i> subsp. <i>equisimilis</i> infection in neonatal piglets.

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