Upregulation of <i>ica</i> Operon Governs Biofilm Formation by a Coagulase-Negative <i>Staphylococcus caprae</i>

<i>Staphylococcus caprae</i> is a Gram-positive, coagulase-negative staphylococci (CoNS), which appears as commensal in the skin, as well as a prevalent mastitis pathogen of goats. Occasionally, it is also associated with infections in humans. Biofilm formation has been identified as a p...

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Main Authors: Hilla Oknin, Yulia Kroupitski, Moshe Shemesh, Shlomo Blum
Format: Article
Language:English
Published: MDPI AG 2023-06-01
Series:Microorganisms
Subjects:
Online Access:https://www.mdpi.com/2076-2607/11/6/1533
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author Hilla Oknin
Yulia Kroupitski
Moshe Shemesh
Shlomo Blum
author_facet Hilla Oknin
Yulia Kroupitski
Moshe Shemesh
Shlomo Blum
author_sort Hilla Oknin
collection DOAJ
description <i>Staphylococcus caprae</i> is a Gram-positive, coagulase-negative staphylococci (CoNS), which appears as commensal in the skin, as well as a prevalent mastitis pathogen of goats. Occasionally, it is also associated with infections in humans. Biofilm formation has been identified as a putative virulence factor in <i>S. caprae</i>. Biofilms are multicellular communities protected by a self-produced extracellular matrix (ECM), which facilitates the resistance of bacterial cells to antimicrobial treatments. The ECM is constructed by exopolysaccharides, including the major exopolysaccharide—polysaccharide intercellular adhesion (PIA), regulated by the <i>ica</i> operon in <i>Staphylococcus</i> species. The aim of this study was to characterize the expression of the <i>ica</i> operon in relation to biofilm formation in <i>S. caprae</i>. Results showed that within a few hours of growth, <i>S. caprae</i> could adhere to polystyrene surfaces, start to accumulate, and form biofilm. Peak biofilm biomass and maturation were reached after 48 h, followed by a reduction in biomass after 72 h. Confocal laser scanning microscopy showed the expression of matrix-associated proteins and polysaccharides at various time points. The expression dynamics of the <i>ica</i> operon were investigated using real-time reverse transcriptase PCR (RT)-qPCR, which showed elevated expression during the early stages of biofilm formation and subsequent downregulation throughout the biofilm aging process. In conclusion, our results show that the <i>ica</i> operon is essential in regulating biofilm formation in <i>S. caprae</i>, similar to other <i>Staphylococcus</i> species. Furthermore, the robustness of the observed biofilm phenotype could account for the successful intramammary colonization and may explain disease persistence caused by this pathogenic bacterium.
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spelling doaj.art-1da3b01ad7ec4fb594624919997e348c2023-11-18T11:43:12ZengMDPI AGMicroorganisms2076-26072023-06-01116153310.3390/microorganisms11061533Upregulation of <i>ica</i> Operon Governs Biofilm Formation by a Coagulase-Negative <i>Staphylococcus caprae</i>Hilla Oknin0Yulia Kroupitski1Moshe Shemesh2Shlomo Blum3Institute for Postharvest Technology and Food Sciences, Department of Food Science, Agricultural Research Organization, Volcani Institute, Rishon LeZion 7505101, IsraelInstitute for Postharvest Technology and Food Sciences, Department of Food Science, Agricultural Research Organization, Volcani Institute, Rishon LeZion 7505101, IsraelInstitute for Postharvest Technology and Food Sciences, Department of Food Science, Agricultural Research Organization, Volcani Institute, Rishon LeZion 7505101, IsraelDepartment of Bacteriology and Mycology, Kimron Veterinary Institute, Rishon LeZion 7534503, Israel<i>Staphylococcus caprae</i> is a Gram-positive, coagulase-negative staphylococci (CoNS), which appears as commensal in the skin, as well as a prevalent mastitis pathogen of goats. Occasionally, it is also associated with infections in humans. Biofilm formation has been identified as a putative virulence factor in <i>S. caprae</i>. Biofilms are multicellular communities protected by a self-produced extracellular matrix (ECM), which facilitates the resistance of bacterial cells to antimicrobial treatments. The ECM is constructed by exopolysaccharides, including the major exopolysaccharide—polysaccharide intercellular adhesion (PIA), regulated by the <i>ica</i> operon in <i>Staphylococcus</i> species. The aim of this study was to characterize the expression of the <i>ica</i> operon in relation to biofilm formation in <i>S. caprae</i>. Results showed that within a few hours of growth, <i>S. caprae</i> could adhere to polystyrene surfaces, start to accumulate, and form biofilm. Peak biofilm biomass and maturation were reached after 48 h, followed by a reduction in biomass after 72 h. Confocal laser scanning microscopy showed the expression of matrix-associated proteins and polysaccharides at various time points. The expression dynamics of the <i>ica</i> operon were investigated using real-time reverse transcriptase PCR (RT)-qPCR, which showed elevated expression during the early stages of biofilm formation and subsequent downregulation throughout the biofilm aging process. In conclusion, our results show that the <i>ica</i> operon is essential in regulating biofilm formation in <i>S. caprae</i>, similar to other <i>Staphylococcus</i> species. Furthermore, the robustness of the observed biofilm phenotype could account for the successful intramammary colonization and may explain disease persistence caused by this pathogenic bacterium.https://www.mdpi.com/2076-2607/11/6/1533CoNSbiofilm formationextracellular matrixsub-clinical mastitisPIAdairy food safety
spellingShingle Hilla Oknin
Yulia Kroupitski
Moshe Shemesh
Shlomo Blum
Upregulation of <i>ica</i> Operon Governs Biofilm Formation by a Coagulase-Negative <i>Staphylococcus caprae</i>
Microorganisms
CoNS
biofilm formation
extracellular matrix
sub-clinical mastitis
PIA
dairy food safety
title Upregulation of <i>ica</i> Operon Governs Biofilm Formation by a Coagulase-Negative <i>Staphylococcus caprae</i>
title_full Upregulation of <i>ica</i> Operon Governs Biofilm Formation by a Coagulase-Negative <i>Staphylococcus caprae</i>
title_fullStr Upregulation of <i>ica</i> Operon Governs Biofilm Formation by a Coagulase-Negative <i>Staphylococcus caprae</i>
title_full_unstemmed Upregulation of <i>ica</i> Operon Governs Biofilm Formation by a Coagulase-Negative <i>Staphylococcus caprae</i>
title_short Upregulation of <i>ica</i> Operon Governs Biofilm Formation by a Coagulase-Negative <i>Staphylococcus caprae</i>
title_sort upregulation of i ica i operon governs biofilm formation by a coagulase negative i staphylococcus caprae i
topic CoNS
biofilm formation
extracellular matrix
sub-clinical mastitis
PIA
dairy food safety
url https://www.mdpi.com/2076-2607/11/6/1533
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AT mosheshemesh upregulationofiicaioperongovernsbiofilmformationbyacoagulasenegativeistaphylococcuscapraei
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