Molecular Characteristics, Virulence Gene and Wall Teichoic Acid Glycosyltransferase Profiles of Staphylococcus aureus: A Multicenter Study in China

Xiong, Mengyuan; Jin, Zhao; Huang, Tao; Wang, Lijun; Zhang, Zhao; Li, Xuehan; Zhou, Jihua; Xiao, Xiao; Pan, Yunbao; Lin, Jie; Li, Yirong

doi:10.3389/fmicb.2020.02013

Cited by 16 publications

(23 citation statements)

References 45 publications

(63 reference statements)

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“…In China, methicillin-susceptible S. aureus (MSSA) CC398 with spa type t011, t899, and t034 have been more frequently reported to be the cause of human infections, occupying approximately 20% of the infection cases in the hospital [ 10 ]. MRSA CC398 has also been reported to infect children and patients in Chinese hospitals [ 11 , 12 ]. S. aureus CC398 has been reported as one of the predominate CC types causing bovine mastitis [ 13 ].…”

Section: Introductionmentioning

confidence: 99%

The Prevalence of Staphylococcus aureus and the Occurrence of MRSA CC398 in Monkey Feces in a Zoo Park in Eastern China

Tang

Qiao

Wang

et al. 2021

Animals

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Methicillin-resistant Staphylococcus aureus (MRSA) is one of the important antibiotic resistant pathogens causing infections in humans and animals. The increasing observation of MRSA in wildlife species has raised the concern of its impact on animal health and the potential of zoonotic transmission. This study investigated the prevalence of S. aureus in fecal samples from non-human primates in a zoo located in Jiangsu, China, in which 6 out of 31 (19.4%) fecal samples, and 2 out of 14 (14.3%) indoor room floor swab samples were S. aureus-positive. The antibiotic susceptibility tests of the eight isolates showed that the two isolates were resistant to both penicillin and cefoxitin, the three isolates were resistant only to penicillin, while three isolates were susceptible to all detected antibiotics. The two isolates resistant to cefoxitin were further identified as MRSA by the presence of mecA. Five different spa types were identified including t034 of two MRSA isolates from Trachypithecus francoisi, t189 of two methicillin-susceptible S. aureus (MSSA) isolates from Rhinopithecus roxellana, t377 of two MSSA isolates from Colobus guereza, and two novel spa types t19488 and t19499 from Papio anubis. Whole genome sequencing analysis showed that MRSA t034 isolates belonged to ST398 clustered in clonal complex 398 (CC398) and carried the type B ΦSa3 prophage. The phylogenetic analysis showed that the two MRSA t034/ST398 isolates were closely related to the human-associated MSSA in China. Moreover, two MRSA isolates contained the virulence genes relating to the cell adherence, biofilm formation, toxins, and the human-associated immune evasion cluster, which indicated the potential of bidirectional transfer of MRSA between monkeys and humans. This study is the first to report MRSA CC398 from monkey feces in China, indicating that MRSA CC398 could colonize in monkey and have the risk of transmission between humans and monkeys.

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Section: Introductionmentioning

confidence: 99%

The Prevalence of Staphylococcus aureus and the Occurrence of MRSA CC398 in Monkey Feces in a Zoo Park in Eastern China

Tang

Qiao

Wang

et al. 2021

Animals

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“…TarP modifies the WTA backbone with β-linked GlcNAc residues similar to TarS but at the C3 position of RboP instead of C4. TarP is always co-expressed with tarS and is associated with, but not limited to, healthcare-associated and livestock-associated MRSA strains belonging to clonal complexes 5 and 398 (31,32). TarP can functionally replace TarS with regard to β-lactam resistance and phage susceptibility (31).…”

Section: Introductionmentioning

confidence: 99%

“…However, whether the same applies to immune recognition remains to be fully elucidated. For example, TarP-modified WTA displayed attenuated immunogenicity in mice compared to TarS-modified WTA and co-modification of WTA by TarP may lower S. aureus antibody recognition despite the presence of antibodies to both WTA glycoforms in serum from healthy individuals (23,32).…”

Section: Introductionmentioning

confidence: 99%

The impact ofStaphylococcus aureuscell wall glycosylation on langerin recognition and Langerhans cell activation

Hendriks

Ali

et al. 2020

Preprint

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Staphylococcus aureus is the leading cause of skin and soft tissue infections. It remains incompletely understood how skin-resident immune cells respond to S. aureus invasion and contribute to an effective immune response. Langerhans cells (LCs), the only professional antigen-presenting cell type in the epidermis, sense S. aureus through their pattern-recognition receptor langerin, triggering a pro-inflammatory response. Langerin specifically recognizes the β-1,4-linked N-acetylglucosamine (β-GlcNAc) modification, which requires the glycosyltransferase TarS, on the cell wall glycopolymer Wall Teichoic Acid (WTA). Recently, an alternative WTA glycosyltransferase, TarP, was identified in methicillin-resistant S. aureus strains belonging to clonal complexes (CC) 5 and CC398. TarP also modifies WTA with β-GlcNAc but at the C-3 position of the WTA ribitol phosphate (RboP) subunit. Here, we aimed to unravel the impact of β-GlcNAc linkage position for langerin binding and LC activation. In addition, we performed structure-binding studies using a small panel of unique chemically-synthesized WTA molecules to assess langerin-WTA binding requirements. Using FITC-labeled recombinant human langerin and genetically-modified S. aureus strains, we observed that langerin similarly recognized bacteria that produce either TarS- or TarP-modified WTA. Furthermore, using chemically-synthesized WTA, representative of the different S. aureus WTA glycosylation patterns, established that β-GlcNAc is sufficient to confer langerin binding. Functionally, tarP-expressing S. aureus induce increased cytokine production and maturation of in vitro-generated LCs compared to tarS-expressing S. aureus. Overall, our data suggest that LCs are able to sense all β-GlcNAc-WTA producing S. aureus strains, likely performing an important role as first responders upon S. aureus skin invasion.

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“…TarP is always coexpressed with tarS and is associated with, but not limited to, healthcare-associated and livestock-associated MRSA strains belonging to clonal complexes 5 and 398. 32 , 33 TarP can functionally replace TarS with regard to β-lactam resistance and phage susceptibility via the decoration of WTA with β-GlcNAc moieties. 30 , 32 However, whether the same applies to immune recognition remains to be fully elucidated.…”

mentioning

confidence: 99%

“…For example, TarP-modified WTA displayed attenuated immunogenicity in mice compared to TarS-modified WTA and comodification of WTA by TarP may lower S. aureus antibody recognition despite the presence of antibodies to both WTA glycoforms in serum from healthy individuals. 24 , 33 …”

mentioning

confidence: 99%

Impact of Glycan Linkage to Staphylococcus aureus Wall Teichoic Acid on Langerin Recognition and Langerhans Cell Activation

et al. 2021

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Staphylococcus aureus is the leading cause of skin and soft tissue infections. It remains incompletely understood how skin-resident immune cells respond to invading S. aureus and contribute to an effective immune response. Langerhans cells (LCs), the only professional antigen-presenting cell type in the epidermis, sense S. aureus through their pattern-recognition receptor langerin, triggering a proinflammatory response. Langerin recognizes the β-1,4-linked N -acetylglucosamine (β1,4-GlcNAc) but not α-1,4-linked GlcNAc (α1,4-GlcNAc) modifications, which are added by dedicated glycosyltransferases TarS and TarM, respectively, on the cell wall glycopolymer wall teichoic acid (WTA). Recently, an alternative WTA glycosyltransferase, TarP, was identified, which also modifies WTA with β-GlcNAc but at the C-3 position (β1,3-GlcNAc) of the WTA ribitol phosphate (RboP) subunit. Here, we aimed to unravel the impact of β-GlcNAc linkage position for langerin binding and LC activation. Using genetically modified S. aureus strains, we observed that langerin similarly recognized bacteria that produce either TarS- or TarP-modified WTA, yet tarP -expressing S. aureus induced increased cytokine production and maturation of in vitro -generated LCs compared to tarS -expressing S. aureus . Chemically synthesized WTA molecules, representative of the different S. aureus WTA glycosylation patterns, were used to identify langerin-WTA binding requirements. We established that β-GlcNAc is sufficient to confer langerin binding, thereby presenting synthetic WTA molecules as a novel glycobiology tool for structure-binding studies and for elucidating S. aureus molecular pathogenesis. Overall, our data suggest that LCs are able to sense all β-GlcNAc-WTA producing S. aureus strains, likely performing an important role as first responders upon S. aureus skin invasion.

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Molecular Characteristics, Virulence Gene and Wall Teichoic Acid Glycosyltransferase Profiles of Staphylococcus aureus: A Multicenter Study in China

Cited by 16 publications

References 45 publications

The Prevalence of Staphylococcus aureus and the Occurrence of MRSA CC398 in Monkey Feces in a Zoo Park in Eastern China

The Prevalence of Staphylococcus aureus and the Occurrence of MRSA CC398 in Monkey Feces in a Zoo Park in Eastern China

The impact ofStaphylococcus aureuscell wall glycosylation on langerin recognition and Langerhans cell activation

Impact of Glycan Linkage to Staphylococcus aureus Wall Teichoic Acid on Langerin Recognition and Langerhans Cell Activation

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