Role of the LytSR Two-Component Regulatory System in Staphylococcus lugdunensis Biofilm Formation and Pathogenesis
Staphylococcus lugdunensis is a coagulase negative Staphylococcus recognized as a virulent pathogen. It is responsible for a wide variety of infections, some of which are associated with biofilm production, such as implanted medical device infections or endocarditis. However, little is known about S...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2020-01-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2020.00039/full |
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| author | Sandrine Dahyot Virginie Oxaran Maïté Niepceron Eddy Dupart Stéphanie Legris Laurie Destruel Jennifer Didi Thomas Clamens Olivier Lesouhaitier Yasmine Zerdoumi Jean-Michel Flaman Martine Pestel-Caron |
| author_facet | Sandrine Dahyot Virginie Oxaran Maïté Niepceron Eddy Dupart Stéphanie Legris Laurie Destruel Jennifer Didi Thomas Clamens Olivier Lesouhaitier Yasmine Zerdoumi Jean-Michel Flaman Martine Pestel-Caron |
| author_sort | Sandrine Dahyot |
| collection | DOAJ |
| description | Staphylococcus lugdunensis is a coagulase negative Staphylococcus recognized as a virulent pathogen. It is responsible for a wide variety of infections, some of which are associated with biofilm production, such as implanted medical device infections or endocarditis. However, little is known about S. lugdunensis regulation of virulence factor expression. Two-component regulatory systems (TCS) play a critical role in bacterial adaptation, survival, and virulence. Among them, LytSR is widely conserved but has variable roles in different organisms, all connected to metabolism or cell death and lysis occurring during biofilm development. Therefore, we investigated here the functions of LytSR in S. lugdunensis pathogenesis. Deletion of lytSR in S. lugdunensis DSM 4804 strain did not alter either susceptibility to Triton X-100 induced autolysis or death induced by antibiotics targeting cell wall synthesis. Interestingly, ΔlytSR biofilm was characterized by a lower biomass, a lack of tower structures, and a higher rate of dead cells compared to the wild-type strain. Virulence toward Caenorhabditis elegans using a slow-killing assay was significantly reduced for the mutant compared to the wild-type strain. By contrast, the deletion of lytSR had no effect on the cytotoxicity of S. lugdunensis toward the human keratinocyte cell line HaCaT. Transcriptional analyses conducted at mid- and late-exponential phases showed that lytSR deletion affected the expression of 286 genes. Most of them were involved in basic functions such as the metabolism of amino acids, carbohydrates, and nucleotides. Furthermore, LytSR appeared to be involved in the regulation of genes encoding known or putative virulence and colonization factors, including the fibrinogen-binding protein Fbl, the major autolysin AtlL, and the type VII secretion system. Overall, our data suggest that the LytSR TCS is implicated in S. lugdunensis pathogenesis, through its involvement in biofilm formation and potentially by the control of genes encoding putative virulence factors. |
| first_indexed | 2024-12-22T20:16:32Z |
| format | Article |
| id | doaj.art-9ebca7eb9af340beaa80a2b894305902 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-22T20:16:32Z |
| publishDate | 2020-01-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-9ebca7eb9af340beaa80a2b8943059022022-12-21T18:13:57ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-01-011110.3389/fmicb.2020.00039504168Role of the LytSR Two-Component Regulatory System in Staphylococcus lugdunensis Biofilm Formation and PathogenesisSandrine Dahyot0Virginie Oxaran1Maïté Niepceron2Eddy Dupart3Stéphanie Legris4Laurie Destruel5Jennifer Didi6Thomas Clamens7Olivier Lesouhaitier8Yasmine Zerdoumi9Jean-Michel Flaman10Martine Pestel-Caron11Groupe de Recherche sur l’Adaptation Microbienne (GRAM 2.0), Department of Bacteriology, Rouen University Hospital, Normandie University, UNIROUEN, UNICAEN, Rouen, FranceDepartment of Biological Sciences, Border Biomedical Research Center, University of Texas at El Paso, El Paso, TX, United StatesGroupe de Recherche sur l’Adaptation Microbienne (GRAM 2.0), Normandie University, UNIROUEN, UNICAEN, Rouen, FranceGroupe de Recherche sur l’Adaptation Microbienne (GRAM 2.0), Normandie University, UNIROUEN, UNICAEN, Rouen, FranceGroupe de Recherche sur l’Adaptation Microbienne (GRAM 2.0), Normandie University, UNIROUEN, UNICAEN, Rouen, FranceGroupe de Recherche sur l’Adaptation Microbienne (GRAM 2.0), Normandie University, UNIROUEN, UNICAEN, Rouen, FranceGroupe de Recherche sur l’Adaptation Microbienne (GRAM 2.0), Normandie University, UNIROUEN, UNICAEN, Rouen, FranceLaboratory of Microbiology Signals and Microenvironment (LMSM), Normandie University, UNIROUEN, Evreux, FranceLaboratory of Microbiology Signals and Microenvironment (LMSM), Normandie University, UNIROUEN, Evreux, FranceINSERM U1245, Normandy Centre for Genomic and Personalized Medicine, Rouen University Hospital, Normandie University, UNIROUEN, Rouen, FranceINSERM U1245, Normandy Centre for Genomic and Personalized Medicine, Rouen University Hospital, Normandie University, UNIROUEN, Rouen, FranceGroupe de Recherche sur l’Adaptation Microbienne (GRAM 2.0), Department of Bacteriology, Rouen University Hospital, Normandie University, UNIROUEN, UNICAEN, Rouen, FranceStaphylococcus lugdunensis is a coagulase negative Staphylococcus recognized as a virulent pathogen. It is responsible for a wide variety of infections, some of which are associated with biofilm production, such as implanted medical device infections or endocarditis. However, little is known about S. lugdunensis regulation of virulence factor expression. Two-component regulatory systems (TCS) play a critical role in bacterial adaptation, survival, and virulence. Among them, LytSR is widely conserved but has variable roles in different organisms, all connected to metabolism or cell death and lysis occurring during biofilm development. Therefore, we investigated here the functions of LytSR in S. lugdunensis pathogenesis. Deletion of lytSR in S. lugdunensis DSM 4804 strain did not alter either susceptibility to Triton X-100 induced autolysis or death induced by antibiotics targeting cell wall synthesis. Interestingly, ΔlytSR biofilm was characterized by a lower biomass, a lack of tower structures, and a higher rate of dead cells compared to the wild-type strain. Virulence toward Caenorhabditis elegans using a slow-killing assay was significantly reduced for the mutant compared to the wild-type strain. By contrast, the deletion of lytSR had no effect on the cytotoxicity of S. lugdunensis toward the human keratinocyte cell line HaCaT. Transcriptional analyses conducted at mid- and late-exponential phases showed that lytSR deletion affected the expression of 286 genes. Most of them were involved in basic functions such as the metabolism of amino acids, carbohydrates, and nucleotides. Furthermore, LytSR appeared to be involved in the regulation of genes encoding known or putative virulence and colonization factors, including the fibrinogen-binding protein Fbl, the major autolysin AtlL, and the type VII secretion system. Overall, our data suggest that the LytSR TCS is implicated in S. lugdunensis pathogenesis, through its involvement in biofilm formation and potentially by the control of genes encoding putative virulence factors.https://www.frontiersin.org/article/10.3389/fmicb.2020.00039/fullS. lugdunensisbiofilmtwo-component systemLytSRCaenorhabditis elegansvirulence |
| spellingShingle | Sandrine Dahyot Virginie Oxaran Maïté Niepceron Eddy Dupart Stéphanie Legris Laurie Destruel Jennifer Didi Thomas Clamens Olivier Lesouhaitier Yasmine Zerdoumi Jean-Michel Flaman Martine Pestel-Caron Role of the LytSR Two-Component Regulatory System in Staphylococcus lugdunensis Biofilm Formation and Pathogenesis Frontiers in Microbiology S. lugdunensis biofilm two-component system LytSR Caenorhabditis elegans virulence |
| title | Role of the LytSR Two-Component Regulatory System in Staphylococcus lugdunensis Biofilm Formation and Pathogenesis |
| title_full | Role of the LytSR Two-Component Regulatory System in Staphylococcus lugdunensis Biofilm Formation and Pathogenesis |
| title_fullStr | Role of the LytSR Two-Component Regulatory System in Staphylococcus lugdunensis Biofilm Formation and Pathogenesis |
| title_full_unstemmed | Role of the LytSR Two-Component Regulatory System in Staphylococcus lugdunensis Biofilm Formation and Pathogenesis |
| title_short | Role of the LytSR Two-Component Regulatory System in Staphylococcus lugdunensis Biofilm Formation and Pathogenesis |
| title_sort | role of the lytsr two component regulatory system in staphylococcus lugdunensis biofilm formation and pathogenesis |
| topic | S. lugdunensis biofilm two-component system LytSR Caenorhabditis elegans virulence |
| url | https://www.frontiersin.org/article/10.3389/fmicb.2020.00039/full |
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