Catharina E. Exel , Sara M. Tamminga , Sandra Man-Bovenkerk , A. Robin Temming , Astrid Hendriks , Mirlin Spaninks , Nina M. van Sorge , Lindert Benedictus
{"title":"Wall teichoic acid glycosylation of bovine-associated Staphylococcus aureus strains","authors":"Catharina E. Exel , Sara M. Tamminga , Sandra Man-Bovenkerk , A. Robin Temming , Astrid Hendriks , Mirlin Spaninks , Nina M. van Sorge , Lindert Benedictus","doi":"10.1016/j.vetmic.2025.110403","DOIUrl":null,"url":null,"abstract":"<div><div><em>Staphylococcus aureus</em> (<em>S. aureus</em>) is one of the major causes of bovine mastitis, a disease with detrimental effects on health and wellbeing. Current control measures are costly, laborious and not always effective in eradicating <em>S. aureus</em>. The cell wall-linked polysaccharide wall teichoic acid (WTA) is highly immunogenic in humans and is considered as a prospective vaccine antigen based on promising pre-clinical studies in animals. WTA consist of polymerized ribitol-phosphate backbone that is modified with N-acetylglucosamine (GlcNAc) moieties in different configurations by the glycosyltransferases TarS (β−1,4-GlcNAc), TarM (α−1,4-GlcNAc) and TarP (β−1,3-GlcNAc). This study aimed to characterize the presence and genetic variation in <em>tarS</em>, <em>tarM</em> and <em>tarP</em> in bovine-associated <em>S. aureus</em> strains and how this impacts WTA-glycoprofile. Bioinformatic analyses of a whole genome sequence database consisting of 1047 <em>S. aureus</em>, 10 <em>S. schweitzeri,</em> and 6 <em>S. argenteus</em> strains showed that over 99<em>%</em> of strains contained <em>tarS</em>, 34 % also contained <em>tarM</em>, while 5 % of the strains encoded <em>tarP</em> in addition to <em>tarS.</em> The distribution of WTA-glycosyltransferase genes was similar to what has been reported for human-associated <em>S. aureus</em> strains. Phenotypic analysis of WTA glycosylation by flow cytometry corroborated with <em>tarS/tarM/tarP</em> gene presence. The WTA glycoprofile was variable between bovine-associated strains and the levels and ratios of GlcNAcylation were affected by growth conditions. Interestingly, a divergent <em>tarM</em> allele was present in strains of clonal complexes (CC) 49 and the mastitis-associated CC151, but its function was similar to canonical <em>tarM</em>. In conclusion, we demonstrated that bovine-associated <em>S. aureus</em> strains show similar variation in WTA GlcNAc decoration as human <em>S. aureus</em> strains, despite the presence of a divergent <em>tarM</em> allele.</div></div>","PeriodicalId":23551,"journal":{"name":"Veterinary microbiology","volume":"302 ","pages":"Article 110403"},"PeriodicalIF":2.4000,"publicationDate":"2025-01-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Veterinary microbiology","FirstCategoryId":"97","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S0378113525000380","RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q3","JCRName":"MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Staphylococcus aureus (S. aureus) is one of the major causes of bovine mastitis, a disease with detrimental effects on health and wellbeing. Current control measures are costly, laborious and not always effective in eradicating S. aureus. The cell wall-linked polysaccharide wall teichoic acid (WTA) is highly immunogenic in humans and is considered as a prospective vaccine antigen based on promising pre-clinical studies in animals. WTA consist of polymerized ribitol-phosphate backbone that is modified with N-acetylglucosamine (GlcNAc) moieties in different configurations by the glycosyltransferases TarS (β−1,4-GlcNAc), TarM (α−1,4-GlcNAc) and TarP (β−1,3-GlcNAc). This study aimed to characterize the presence and genetic variation in tarS, tarM and tarP in bovine-associated S. aureus strains and how this impacts WTA-glycoprofile. Bioinformatic analyses of a whole genome sequence database consisting of 1047 S. aureus, 10 S. schweitzeri, and 6 S. argenteus strains showed that over 99% of strains contained tarS, 34 % also contained tarM, while 5 % of the strains encoded tarP in addition to tarS. The distribution of WTA-glycosyltransferase genes was similar to what has been reported for human-associated S. aureus strains. Phenotypic analysis of WTA glycosylation by flow cytometry corroborated with tarS/tarM/tarP gene presence. The WTA glycoprofile was variable between bovine-associated strains and the levels and ratios of GlcNAcylation were affected by growth conditions. Interestingly, a divergent tarM allele was present in strains of clonal complexes (CC) 49 and the mastitis-associated CC151, but its function was similar to canonical tarM. In conclusion, we demonstrated that bovine-associated S. aureus strains show similar variation in WTA GlcNAc decoration as human S. aureus strains, despite the presence of a divergent tarM allele.
期刊介绍:
Veterinary Microbiology is concerned with microbial (bacterial, fungal, viral) diseases of domesticated vertebrate animals (livestock, companion animals, fur-bearing animals, game, poultry, fish) that supply food, other useful products or companionship. In addition, Microbial diseases of wild animals living in captivity, or as members of the feral fauna will also be considered if the infections are of interest because of their interrelation with humans (zoonoses) and/or domestic animals. Studies of antimicrobial resistance are also included, provided that the results represent a substantial advance in knowledge. Authors are strongly encouraged to read - prior to submission - the Editorials (''Scope or cope'' and ''Scope or cope II'') published previously in the journal. The Editors reserve the right to suggest submission to another journal for those papers which they feel would be more appropriate for consideration by that journal.
Original research papers of high quality and novelty on aspects of control, host response, molecular biology, pathogenesis, prevention, and treatment of microbial diseases of animals are published. Papers dealing primarily with immunology, epidemiology, molecular biology and antiviral or microbial agents will only be considered if they demonstrate a clear impact on a disease. Papers focusing solely on diagnostic techniques (such as another PCR protocol or ELISA) will not be published - focus should be on a microorganism and not on a particular technique. Papers only reporting microbial sequences, transcriptomics data, or proteomics data will not be considered unless the results represent a substantial advance in knowledge.
Drug trial papers will be considered if they have general application or significance. Papers on the identification of microorganisms will also be considered, but detailed taxonomic studies do not fall within the scope of the journal. Case reports will not be published, unless they have general application or contain novel aspects. Papers of geographically limited interest, which repeat what had been established elsewhere will not be considered. The readership of the journal is global.