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...

Descripción completa

Guardado en:
Detalles Bibliográficos
Autores principales: 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
Formato: article
Lenguaje:EN
Publicado: American Society for Microbiology 2016
Materias:
Acceso en línea:https://doaj.org/article/7dc689804f6944a98059b6a858274e36
Etiquetas: Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
id oai:doaj.org-article:7dc689804f6944a98059b6a858274e36
record_format dspace
spelling 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)
institution DOAJ
collection DOAJ
language EN
topic accumulation-associated protein
Staphylococcus epidermidis
biofilms
catheter-associated infections
polysaccharide intercellular adhesin
Microbiology
QR1-502
spellingShingle 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 AT carolynrschaeffer versatilityofbiofilmmatrixmoleculesinnamedcontentcontenttypegenusspeciesstaphylococcusepidermidisnamedcontentclinicalisolatesandimportanceofpolysaccharideintercellularadhesinexpressionduringhighshearstress
AT tramynhoang versatilityofbiofilmmatrixmoleculesinnamedcontentcontenttypegenusspeciesstaphylococcusepidermidisnamedcontentclinicalisolatesandimportanceofpolysaccharideintercellularadhesinexpressionduringhighshearstress
AT craigmsudbeck versatilityofbiofilmmatrixmoleculesinnamedcontentcontenttypegenusspeciesstaphylococcusepidermidisnamedcontentclinicalisolatesandimportanceofpolysaccharideintercellularadhesinexpressionduringhighshearstress
AT malikalawi versatilityofbiofilmmatrixmoleculesinnamedcontentcontenttypegenusspeciesstaphylococcusepidermidisnamedcontentclinicalisolatesandimportanceofpolysaccharideintercellularadhesinexpressionduringhighshearstress
AT isaiahetolo versatilityofbiofilmmatrixmoleculesinnamedcontentcontenttypegenusspeciesstaphylococcusepidermidisnamedcontentclinicalisolatesandimportanceofpolysaccharideintercellularadhesinexpressionduringhighshearstress
AT dashleyrobinson versatilityofbiofilmmatrixmoleculesinnamedcontentcontenttypegenusspeciesstaphylococcusepidermidisnamedcontentclinicalisolatesandimportanceofpolysaccharideintercellularadhesinexpressionduringhighshearstress
AT alexanderrhorswill versatilityofbiofilmmatrixmoleculesinnamedcontentcontenttypegenusspeciesstaphylococcusepidermidisnamedcontentclinicalisolatesandimportanceofpolysaccharideintercellularadhesinexpressionduringhighshearstress
AT holgerrohde versatilityofbiofilmmatrixmoleculesinnamedcontentcontenttypegenusspeciesstaphylococcusepidermidisnamedcontentclinicalisolatesandimportanceofpolysaccharideintercellularadhesinexpressionduringhighshearstress
AT pauldfey versatilityofbiofilmmatrixmoleculesinnamedcontentcontenttypegenusspeciesstaphylococcusepidermidisnamedcontentclinicalisolatesandimportanceofpolysaccharideintercellularadhesinexpressionduringhighshearstress
_version_ 1718428139375296512