Versatility of Biofilm Matrix Molecules in <named-content content-type="genus-species">Staphylococcus epidermidis</named-content> Clinical Isolates and Importance of Polysaccharide Intercellular Adhesin Expression during High Shear Stress
ABSTRACT Staphylococcus epidermidis is a leading cause of hospital-associated infections, including those of intravascular catheters, cerebrospinal fluid shunts, and orthopedic implants. Multiple biofilm matrix molecules with heterogeneous characteristics have been identified, including proteinaceou...
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American Society for Microbiology
2016
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oai:doaj.org-article:7dc689804f6944a98059b6a858274e362021-11-15T15:21:29ZVersatility of Biofilm Matrix Molecules in <named-content content-type="genus-species">Staphylococcus epidermidis</named-content> Clinical Isolates and Importance of Polysaccharide Intercellular Adhesin Expression during High Shear Stress10.1128/mSphere.00165-162379-5042https://doaj.org/article/7dc689804f6944a98059b6a858274e362016-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00165-16https://doaj.org/toc/2379-5042ABSTRACT Staphylococcus epidermidis is a leading cause of hospital-associated infections, including those of intravascular catheters, cerebrospinal fluid shunts, and orthopedic implants. Multiple biofilm matrix molecules with heterogeneous characteristics have been identified, including proteinaceous, polysaccharide, and nucleic acid factors. Two of the best-studied components in S. epidermidis include accumulation-associated protein (Aap) and polysaccharide intercellular adhesin (PIA), produced by the enzymatic products of the icaADBC operon. Biofilm composition varies by strain as well as environmental conditions, and strains producing PIA-mediated biofilms are more robust. Clinically, biofilm-mediated infections occur in a variety of anatomical sites with diverse physiological properties. To test the hypothesis that matrix composition exhibits niche specificity, biofilm-related genetic and physical properties were compared between S. epidermidis strains isolated from high-shear and low-shear environments. Among a collection of 105 clinical strains, significantly more isolates from high-shear environments carried the icaADBC operon than did those from low-shear settings (43.9% versus 22.9%, P < 0.05), while there was no significant difference in the presence of aap (77.2% versus 75.0%, P > 0.05). Additionally, a significantly greater number of high-shear isolates were capable of forming biofilm in vitro in a microtiter assay (82.5% versus 45.8%, P < 0.0001). However, even among high-shear clinical isolates, less than half contained the icaADBC locus; therefore, we selected for ica-negative variants with increased attachment to abiotic surfaces to examine PIA-independent biofilm mechanisms. Sequencing of selected variants identified substitutions capable of enhancing biofilm formation in multiple genes, further highlighting the heterogeneity of S. epidermidis biofilm molecules and mechanisms. IMPORTANCE Staphylococcus epidermidis is a leading cause of infections related to biomaterials, mostly due to their ability to form biofilm. Biofilm accumulation mechanisms vary, including those that are dependent on specific proteins, environmental DNA (eDNA), or polysaccharide intercellular adhesin (PIA). We found that those isolates obtained from high-shear environments, such as the lumen of a catheter, are more likely to produce PIA-mediated biofilms than those isolates obtained from a low-shear biomaterial-related infection. This suggests that PIA functions as a mechanism that is protective against shear flow. Finally, we performed selection experiments documenting the heterogeneity of biofilm accumulation molecules that function in the absence of PIA, further documenting the biofilm-forming potential of S. epidermidis.Carolyn R. SchaefferTra-My N. HoangCraig M. SudbeckMalik AlawiIsaiah E. ToloD. Ashley RobinsonAlexander R. HorswillHolger RohdePaul D. FeyAmerican Society for Microbiologyarticleaccumulation-associated proteinStaphylococcus epidermidisbiofilmscatheter-associated infectionspolysaccharide intercellular adhesinMicrobiologyQR1-502ENmSphere, Vol 1, Iss 5 (2016) |
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accumulation-associated protein Staphylococcus epidermidis biofilms catheter-associated infections polysaccharide intercellular adhesin Microbiology QR1-502 |
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accumulation-associated protein Staphylococcus epidermidis biofilms catheter-associated infections polysaccharide intercellular adhesin Microbiology QR1-502 Carolyn R. Schaeffer Tra-My N. Hoang Craig M. Sudbeck Malik Alawi Isaiah E. Tolo D. Ashley Robinson Alexander R. Horswill Holger Rohde Paul D. Fey Versatility of Biofilm Matrix Molecules in <named-content content-type="genus-species">Staphylococcus epidermidis</named-content> Clinical Isolates and Importance of Polysaccharide Intercellular Adhesin Expression during High Shear Stress |
description |
ABSTRACT Staphylococcus epidermidis is a leading cause of hospital-associated infections, including those of intravascular catheters, cerebrospinal fluid shunts, and orthopedic implants. Multiple biofilm matrix molecules with heterogeneous characteristics have been identified, including proteinaceous, polysaccharide, and nucleic acid factors. Two of the best-studied components in S. epidermidis include accumulation-associated protein (Aap) and polysaccharide intercellular adhesin (PIA), produced by the enzymatic products of the icaADBC operon. Biofilm composition varies by strain as well as environmental conditions, and strains producing PIA-mediated biofilms are more robust. Clinically, biofilm-mediated infections occur in a variety of anatomical sites with diverse physiological properties. To test the hypothesis that matrix composition exhibits niche specificity, biofilm-related genetic and physical properties were compared between S. epidermidis strains isolated from high-shear and low-shear environments. Among a collection of 105 clinical strains, significantly more isolates from high-shear environments carried the icaADBC operon than did those from low-shear settings (43.9% versus 22.9%, P < 0.05), while there was no significant difference in the presence of aap (77.2% versus 75.0%, P > 0.05). Additionally, a significantly greater number of high-shear isolates were capable of forming biofilm in vitro in a microtiter assay (82.5% versus 45.8%, P < 0.0001). However, even among high-shear clinical isolates, less than half contained the icaADBC locus; therefore, we selected for ica-negative variants with increased attachment to abiotic surfaces to examine PIA-independent biofilm mechanisms. Sequencing of selected variants identified substitutions capable of enhancing biofilm formation in multiple genes, further highlighting the heterogeneity of S. epidermidis biofilm molecules and mechanisms. IMPORTANCE Staphylococcus epidermidis is a leading cause of infections related to biomaterials, mostly due to their ability to form biofilm. Biofilm accumulation mechanisms vary, including those that are dependent on specific proteins, environmental DNA (eDNA), or polysaccharide intercellular adhesin (PIA). We found that those isolates obtained from high-shear environments, such as the lumen of a catheter, are more likely to produce PIA-mediated biofilms than those isolates obtained from a low-shear biomaterial-related infection. This suggests that PIA functions as a mechanism that is protective against shear flow. Finally, we performed selection experiments documenting the heterogeneity of biofilm accumulation molecules that function in the absence of PIA, further documenting the biofilm-forming potential of S. epidermidis. |
format |
article |
author |
Carolyn R. Schaeffer Tra-My N. Hoang Craig M. Sudbeck Malik Alawi Isaiah E. Tolo D. Ashley Robinson Alexander R. Horswill Holger Rohde Paul D. Fey |
author_facet |
Carolyn R. Schaeffer Tra-My N. Hoang Craig M. Sudbeck Malik Alawi Isaiah E. Tolo D. Ashley Robinson Alexander R. Horswill Holger Rohde Paul D. Fey |
author_sort |
Carolyn R. Schaeffer |
title |
Versatility of Biofilm Matrix Molecules in <named-content content-type="genus-species">Staphylococcus epidermidis</named-content> Clinical Isolates and Importance of Polysaccharide Intercellular Adhesin Expression during High Shear Stress |
title_short |
Versatility of Biofilm Matrix Molecules in <named-content content-type="genus-species">Staphylococcus epidermidis</named-content> Clinical Isolates and Importance of Polysaccharide Intercellular Adhesin Expression during High Shear Stress |
title_full |
Versatility of Biofilm Matrix Molecules in <named-content content-type="genus-species">Staphylococcus epidermidis</named-content> Clinical Isolates and Importance of Polysaccharide Intercellular Adhesin Expression during High Shear Stress |
title_fullStr |
Versatility of Biofilm Matrix Molecules in <named-content content-type="genus-species">Staphylococcus epidermidis</named-content> Clinical Isolates and Importance of Polysaccharide Intercellular Adhesin Expression during High Shear Stress |
title_full_unstemmed |
Versatility of Biofilm Matrix Molecules in <named-content content-type="genus-species">Staphylococcus epidermidis</named-content> Clinical Isolates and Importance of Polysaccharide Intercellular Adhesin Expression during High Shear Stress |
title_sort |
versatility of biofilm matrix molecules in <named-content content-type="genus-species">staphylococcus epidermidis</named-content> clinical isolates and importance of polysaccharide intercellular adhesin expression during high shear stress |
publisher |
American Society for Microbiology |
publishDate |
2016 |
url |
https://doaj.org/article/7dc689804f6944a98059b6a858274e36 |
work_keys_str_mv |
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