Versatility of biofilm matrix molecules in Staphylococcus epidermidis clinical isolates and importance of polysaccharide intercellular adhesin expression during high shear stress

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

Research output: Contribution to journalArticle

7 Citations (Scopus)

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 PIAmediated 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.

Original languageEnglish (US)
Article numbere00165-16
JournalmSphere
Volume1
Issue number5
DOIs
StatePublished - Sep 1 2016

Fingerprint

Staphylococcus epidermidis
Biofilms
Operon
Cerebrospinal Fluid Shunts
polysaccharide intercellular adhesin
Cross Infection
Nucleic Acids
Orthopedics
Polysaccharides
Catheters

Keywords

  • Accumulation-associated protein
  • Biofilms
  • Catheter-associated infections
  • Polysaccharide intercellular adhesin
  • Staphylococcus epidermidis

ASJC Scopus subject areas

  • Microbiology
  • Molecular Biology

Cite this

Versatility of biofilm matrix molecules in Staphylococcus epidermidis clinical isolates and importance of polysaccharide intercellular adhesin expression during high shear stress. / Schaeffer, Carolyn R.; Hoang, Tra My N.; Sudbeck, Craig M.; Alawi, Malik; Tolo, Isaiah E.; Robinson, D. Ashley; Horswill, Alexander R.; Rohde, Holger; Fey, Paul D.

In: mSphere, Vol. 1, No. 5, e00165-16, 01.09.2016.

Research output: Contribution to journalArticle

Schaeffer, Carolyn R. ; Hoang, Tra My N. ; Sudbeck, Craig M. ; Alawi, Malik ; Tolo, Isaiah E. ; Robinson, D. Ashley ; Horswill, Alexander R. ; Rohde, Holger ; Fey, Paul D. / Versatility of biofilm matrix molecules in Staphylococcus epidermidis clinical isolates and importance of polysaccharide intercellular adhesin expression during high shear stress. In: mSphere. 2016 ; Vol. 1, No. 5.
@article{395cb1dd4043470dab61faf8d4d9a2ef,
title = "Versatility of biofilm matrix molecules in Staphylococcus epidermidis 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 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 PIAmediated 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.",
keywords = "Accumulation-associated protein, Biofilms, Catheter-associated infections, Polysaccharide intercellular adhesin, Staphylococcus epidermidis",
author = "Schaeffer, {Carolyn R.} and Hoang, {Tra My N.} and Sudbeck, {Craig M.} and Malik Alawi and Tolo, {Isaiah E.} and Robinson, {D. Ashley} and Horswill, {Alexander R.} and Holger Rohde and Fey, {Paul D}",
year = "2016",
month = "9",
day = "1",
doi = "10.1128/mSphere.00165-16",
language = "English (US)",
volume = "1",
journal = "mSphere",
issn = "2379-5042",
publisher = "American Society for Microbiology",
number = "5",

}

TY - JOUR

T1 - Versatility of biofilm matrix molecules in Staphylococcus epidermidis clinical isolates and importance of polysaccharide intercellular adhesin expression during high shear stress

AU - Schaeffer, Carolyn R.

AU - Hoang, Tra My N.

AU - Sudbeck, Craig M.

AU - Alawi, Malik

AU - Tolo, Isaiah E.

AU - Robinson, D. Ashley

AU - Horswill, Alexander R.

AU - Rohde, Holger

AU - Fey, Paul D

PY - 2016/9/1

Y1 - 2016/9/1

N2 - 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 PIAmediated 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.

AB - 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 PIAmediated 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.

KW - Accumulation-associated protein

KW - Biofilms

KW - Catheter-associated infections

KW - Polysaccharide intercellular adhesin

KW - Staphylococcus epidermidis

UR - http://www.scopus.com/inward/record.url?scp=85013777303&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85013777303&partnerID=8YFLogxK

U2 - 10.1128/mSphere.00165-16

DO - 10.1128/mSphere.00165-16

M3 - Article

VL - 1

JO - mSphere

JF - mSphere

SN - 2379-5042

IS - 5

M1 - e00165-16

ER -