Title: Streptococcus gordonii Type I Lipoteichoic Acid Contributes to Surface Protein Biogenesis

Journal Article · · mSphere
ORCiD logo [1]; ORCiD logo [2];  [3];  [4];  [5];  [3];  [3];  [3];  [2];  [3];  [6]
  1. Univ. of Minnesota, Minneapolis, MN (United States). Dept. of Diagnostic and Biological Sciences, School of Dentistry; DOE/OSTI
  2. Pennsylvania State Univ., State College, PA (United States). Dept. of Biochemistry and Molecular Biology
  3. Univ. of Minnesota, Minneapolis, MN (United States). Dept. of Diagnostic and Biological Sciences, School of Dentistry
  4. Univ. of Malmo (Sweden). Dept. of Oral Biology, Faculty of Odontology
  5. Univ. of Malmo (Sweden). Dept. of Oral Biology, Faculty of Odontology
  6. Univ. of Iowa, Iowa City, IA (United States)
+ Show Author Affiliations

Lipoteichoic acid (LTA) is an abundant polymer of the Gram-positive bacterial cell envelope and is essential for many species. Whereas the exact function of LTA has not been elucidated, loss of LTA in some species affects hydrophobicity, biofilm formation, and cell division. Using a viable LTA-deficient strain of the human oral commensal Streptococcus gordonii, we demonstrated that LTA plays an important role in surface protein presentation. Cell wall fractions derived from the wild-type and LTA-deficient strains of S. gordonii were analyzed using label-free mass spectroscopy. Comparisons showed that the abundances of many proteins differed, including (i) SspA, SspB, and S. gordonii 0707 (SGO_0707) (biofilm formation); (ii) FtsE (cell division); (iii) Pbp1a and Pbp2a (cell wall biosynthesis and remodeling); and (iv) DegP (envelope stress response). These changes in cell surface protein presentation appear to explain our observations of altered cell envelope homeostasis, biofilm formation, and adhesion to eukaryotic cells, without affecting binding and coaggregation with other bacterial species, and provide insight into the phenotypes revealed by the loss of LTA in other species of Gram-positive bacteria. We also characterized the chemical structure of the LTA expressed by S. gordonii. Similarly to Streptococcus suis, S. gordonii produced a complex type I LTA, decorated with multiple d-alanylations and glycosylations. Hence, the S. gordonii LTA appears to orchestrate expression and presentation of cell surface-associated proteins and functions.

Research Organization:
Univ. of Georgia, Athens, GA (United States); Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center
Sponsoring Organization:
USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES)
Grant/Contract Number:
SC0015662
OSTI ID:
1626161
Journal Information:
mSphere, Journal Name: mSphere Journal Issue: 6 Vol. 4; ISSN 2379-5042
Publisher:
American Society for MicrobiologyCopyright Statement
Country of Publication:
United States
Language:
English

References (126)

Lipoteichoic acid and lipids in the membrane of Staphylococcus aureus journal May 1994
The essential nature of teichoic acids in Bacillus subtilis as revealed by insertional mutagenesis journal February 1989
Inhibition of bacterial wall lysins by lipoteichoic acids and related compounds journal December 1975
Occurrence and function of membrane teichoic acids journal May 1977
Novel series of plasmid vectors for gene inactivation and expression analysis in group A streptococci (GAS) journal January 1996
Slx5/Slx8 Promotes Replication Stress Tolerance by Facilitating Mitotic Progression journal May 2016
Streptococcus gordonii induces nitric oxide production through its lipoproteins stimulating Toll-like receptor 2 in murine macrophages journal February 2017
Streptococcus gordonii lipoproteins induce IL-8 in human periodontal ligament cells journal November 2017
Staphylococcal biofilm disassembly journal September 2011
Dental plaque formation journal November 2000
Oral multispecies biofilm development and the key role of cell–cell distance journal June 2010
From the regulation of peptidoglycan synthesis to bacterial growth and morphology journal December 2011
Hepatitis C virus enhances Rubicon expression, leading to autophagy inhibition and intracellular innate immune activation journal September 2020
Cell wall stress responses in Bacillus subtilis: the regulatory network of the bacitracin stimulon: B. subtilis bacitracin stimulon journal November 2003
An ATP-binding cassette transporter-like complex governs cell-wall hydrolysis at the bacterial cytokinetic ring journal October 2011
Small molecule inhibitor of lipoteichoic acid synthesis is an antibiotic for Gram-positive bacteria journal February 2013
Structural analysis and immunostimulatory potency of lipoteichoic acids isolated from three Streptococcus suis serotype 2 strains journal June 2018
Interactions of Fibronectin with Streptococci: The Role of Fibronectin as a Receptor for Streptococcus pyogenes journal July 1987
Identity of viridans streptococci isolated from cases of infective endocarditis journal September 1993
Identification of novel LPXTG-linked surface proteins from Streptococcus gordonii journal June 2009
Mechanisms of intrinsic resistance to antimicrobial peptides of Edwardsiella ictaluri and its influence on fish gut inflammation and virulence journal July 2013
Consequences of a sortase A mutation in Streptococcus gordonii journal December 2007
The Bacterial Cell Envelope journal April 2010
The Cpx two-component signal transduction pathway of Escherichia coli regulates transcription of the gene specifying the stress-inducible periplasmic protease, DegP. journal February 1995
MicroReview: Envelope stress responses and Gram-negative bacterial pathogenesis: Envelope stress responses and virulence journal March 2005
A Staphylococcus aureus ypfP mutant with strongly reduced lipoteichoic acid (LTA) content: LTA governs bacterial surface properties and autolysin activity journal August 2007
Evidence for a dual role of PBP1 in the cell division and cell separation of Staphylococcus aureus journal May 2009
Cell envelope stress response in Gram-positive bacteria journal January 2008
Differential localization of LTA synthesis proteins and their interaction with the cell division machinery in Staphylococcus aureus: Localization and interactions of LTA proteins journal March 2014
Cloning-Independent and Counterselectable Markerless Mutagenesis System in Streptococcus mutans journal September 2011
Cell Surface-Associated Lipoteichoic Acid Acts as an Adhesion Factor for Attachment of Lactobacillus johnsonii La1 to Human Enterocyte-Like Caco-2 Cells journal March 1999
Bacillus subtilis α-Phosphoglucomutase Is Required for Normal Cell Morphology and Biofilm Formation journal January 2005
Induction of Experimental Endocarditis by Continuous Low-Grade Bacteremia Mimicking Spontaneous Bacteremia in Humans journal February 2011
Growth of several cariogenic strains of oral streptococci in a chemically defined medium. journal January 1975
Lipoteichoic acid is the major cell wall component responsible for surface hydrophobicity of group A streptococci journal January 1983
Platelet-interactive products of Streptococcus sanguis protoplasts journal December 1990
Multiple adhesins of streptococci journal June 1992
Porphyromonas gingivalis invasion of gingival epithelial cells journal October 1995
Role of PBP1 in Cell Division of Staphylococcus aureus journal February 2007
Streptococcal Antagonism in Oral Biofilms: Streptococcus sanguinis and Streptococcus gordonii Interference with Streptococcus mutans journal April 2008
Pleiotropic Roles of Polyglycerolphosphate Synthase of Lipoteichoic Acid in Growth of Staphylococcus aureus Cells journal October 2008
Genes Required for Glycolipid Synthesis and Lipoteichoic Acid Anchoring in Staphylococcus aureus journal January 2007
Hydrophobic interactions of group A streptococci with hexadecane droplets journal April 1983
Effect of lipoteichoic acid on thermotropic membrane properties. journal January 1997
Complementation of the Essential Peptidoglycan Transpeptidase Function of Penicillin-Binding Protein 2 (PBP2) by the Drug Resistance Protein PBP2A in Staphylococcus aureus journal November 2001
Genes Involved in Formation of Structured Multicellular Communities by Bacillus subtilis journal June 2004
Identification of clinically relevant viridans group streptococci to the species level by PCR journal September 1997
Streptococcus Adherence and Colonization journal September 2009
A Continuum of Anionic Charge: Structures and Functions of D-Alanyl-Teichoic Acids in Gram-Positive Bacteria journal December 2003
Teichoic and teichuronic acids: biosynthesis, assembly, and location journal June 1981
Lipoteichoic Acid Synthesis and Function in Gram-Positive Bacteria journal September 2014
High-resolution Visualization of the Microbial Glycocalyx with Low-voltage Scanning Electron Microscopy: Dependence on Cationic Dyes journal November 2004
Identification and characterization of a novel Fusobacterium nucleatum adhesin involved in physical interaction and biofilm formation with Streptococcus gordonii journal February 2017
Lipoteichoic acid and lipids in the membrane of Staphylococcus aureus journal May 1994
The essential nature of teichoic acids in Bacillus subtilis as revealed by insertional mutagenesis journal February 1989
Inhibition of bacterial wall lysins by lipoteichoic acids and related compounds journal December 1975
Occurrence and function of membrane teichoic acids journal May 1977
Novel series of plasmid vectors for gene inactivation and expression analysis in group A streptococci (GAS) journal January 1996
The biosynthesis of nascent membrane lipoteichoic acid of Streptococcus faecium (S. faecalis ATCC 9790) from phosphatidylkojibiosyl diacylglycerol and phosphatidylglycerol. journal June 1980
Slx5/Slx8 Promotes Replication Stress Tolerance by Facilitating Mitotic Progression journal May 2016
Streptococcus gordonii induces nitric oxide production through its lipoproteins stimulating Toll-like receptor 2 in murine macrophages journal February 2017
Streptococcus gordonii lipoproteins induce IL-8 in human periodontal ligament cells journal November 2017
Lipoproteins in Streptococcus gordonii are critical in the infection and inflammatory responses journal September 2018
Staphylococcal biofilm disassembly journal September 2011
Dental plaque formation journal November 2000
Teichoic Acids from Bacterial Walls: Composition of Teichoic Acids from a Number of Bacterial Walls journal July 1959
MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification journal November 2008
Oral multispecies biofilm development and the key role of cell–cell distance journal June 2010
From the regulation of peptidoglycan synthesis to bacterial growth and morphology journal December 2011
Cell wall stress responses in Bacillus subtilis: the regulatory network of the bacitracin stimulon: B. subtilis bacitracin stimulon journal November 2003
An ATP-binding cassette transporter-like complex governs cell-wall hydrolysis at the bacterial cytokinetic ring journal October 2011
Essential PcsB putative peptidoglycan hydrolase interacts with the essential FtsXSpn cell division protein in Streptococcus pneumoniae D39 journal October 2011
Small molecule inhibitor of lipoteichoic acid synthesis is an antibiotic for Gram-positive bacteria journal February 2013
Re-evaluation of the Role of Calcium Homeostasis Endoplasmic Reticulum Protein (CHERP) in Cellular Calcium Signaling journal November 2012
Structural analysis and immunostimulatory potency of lipoteichoic acids isolated from three Streptococcus suis serotype 2 strains journal June 2018
A combinatorial approach to the peptide feature matching problem for label-free quantification journal May 2013
Interactions of Fibronectin with Streptococci: The Role of Fibronectin as a Receptor for Streptococcus pyogenes journal July 1987
Identity of viridans streptococci isolated from cases of infective endocarditis journal September 1993
Identification of novel LPXTG-linked surface proteins from Streptococcus gordonii journal June 2009
Mechanisms of intrinsic resistance to antimicrobial peptides of Edwardsiella ictaluri and its influence on fish gut inflammation and virulence journal July 2013
Consequences of a sortase A mutation in Streptococcus gordonii journal December 2007
The Bacterial Cell Envelope journal April 2010
The Cpx two-component signal transduction pathway of Escherichia coli regulates transcription of the gene specifying the stress-inducible periplasmic protease, DegP. journal February 1995
A reproducible oral microcosm biofilm model for testing dental materials journal September 2012
MicroReview: Envelope stress responses and Gram-negative bacterial pathogenesis: Envelope stress responses and virulence journal March 2005
A Staphylococcus aureus ypfP mutant with strongly reduced lipoteichoic acid (LTA) content: LTA governs bacterial surface properties and autolysin activity journal August 2007
The Fusobacterium nucleatum outer membrane protein RadD is an arginine-inhibitable adhesin required for inter-species adherence and the structured architecture of multispecies biofilm journal January 2009
Evidence for a dual role of PBP1 in the cell division and cell separation of Staphylococcus aureus journal May 2009
Location, synthesis and function of glycolipids and polyglycerolphosphate lipoteichoic acid in Gram-positive bacteria of the phylum Firmicutes: Synthesis and function of glycolipid and PGP-LTA journal March 2011
Cell envelope stress response in Gram-positive bacteria journal January 2008
Differential localization of LTA synthesis proteins and their interaction with the cell division machinery in Staphylococcus aureus: Localization and interactions of LTA proteins journal March 2014
An intramembrane sensory circuit monitors sortase A–mediated processing of streptococcal adhesins journal May 2019
Cloning-Independent and Counterselectable Markerless Mutagenesis System in Streptococcus mutans journal September 2011
Cell Surface-Associated Lipoteichoic Acid Acts as an Adhesion Factor for Attachment of Lactobacillus johnsonii La1 to Human Enterocyte-Like Caco-2 Cells journal March 1999
Bacillus subtilis α-Phosphoglucomutase Is Required for Normal Cell Morphology and Biofilm Formation journal January 2005
Induction of Experimental Endocarditis by Continuous Low-Grade Bacteremia Mimicking Spontaneous Bacteremia in Humans journal February 2011
Inactivation of Streptococcusgordonii SspAB Alters Expression of Multiple Adhesin Genes journal June 2005
Salt-Induced Stress Stimulates a Lipoteichoic Acid-Specific Three-Component Glycosylation System in Staphylococcus aureus journal April 2018
Role of PBP1 in Cell Division of Staphylococcus aureus journal February 2007
Streptococcal Antagonism in Oral Biofilms: Streptococcus sanguinis and Streptococcus gordonii Interference with Streptococcus mutans journal April 2008
Lipoteichoic Acids, Phosphate-Containing Polymers in the Envelope of Gram-Positive Bacteria journal January 2014
Pleiotropic Roles of Polyglycerolphosphate Synthase of Lipoteichoic Acid in Growth of Staphylococcus aureus Cells journal October 2008
Genes Required for Glycolipid Synthesis and Lipoteichoic Acid Anchoring in Staphylococcus aureus journal January 2007
Complementation of the Essential Peptidoglycan Transpeptidase Function of Penicillin-Binding Protein 2 (PBP2) by the Drug Resistance Protein PBP2A in Staphylococcus aureus journal November 2001
Genes Involved in Formation of Structured Multicellular Communities by Bacillus subtilis journal June 2004
Role of Penicillin-Binding Protein 2 (PBP2) in the Antibiotic Susceptibility and Cell Wall Cross-Linking of Staphylococcus aureus: Evidence for the Cooperative Functioning of PBP2, PBP4, and PBP2A journal March 2005
Streptococcus Adherence and Colonization journal September 2009
Growth of several cariogenic strains of oral streptococci in a chemically defined medium. journal January 1975
Lipoteichoic acid is the major cell wall component responsible for surface hydrophobicity of group A streptococci journal January 1983
Platelet-interactive products of Streptococcus sanguis protoplasts journal December 1990
Multiple adhesins of streptococci journal June 1992
Porphyromonas gingivalis invasion of gingival epithelial cells journal October 1995
Hydrophobic interactions of group A streptococci with hexadecane droplets journal April 1983
Comparative studies of lipoteichoic acids from several Bacillus strains. journal January 1986
Effect of lipoteichoic acid on thermotropic membrane properties. journal January 1997
Identification of clinically relevant viridans group streptococci to the species level by PCR journal September 1997
Involvement of FtsE ATPase and FtsX Extracellular Loops 1 and 2 in FtsEX-PcsB Complex Function in Cell Division of Streptococcus pneumoniae D39 journal July 2013
Staphylococcal Biofilms journal July 2018
A Continuum of Anionic Charge: Structures and Functions of D-Alanyl-Teichoic Acids in Gram-Positive Bacteria journal December 2003
Teichoic and teichuronic acids: biosynthesis, assembly, and location journal June 1981
Lipoteichoic Acid Synthesis and Function in Gram-Positive Bacteria journal September 2014
Deletion of the glycosyltransferase bgsB of Enterococcus faecalis leads to a complete loss of glycolipids from the cell membrane and to impaired biofilm formation journal January 2011
Oral keratinocytes support non-replicative infection and transfer of harbored HIV-1 to permissive cells journal January 2008
High-resolution Visualization of the Microbial Glycocalyx with Low-voltage Scanning Electron Microscopy: Dependence on Cationic Dyes journal November 2004
FtsEX-mediated regulation of the final stages of cell division reveals morphogenetic plasticity in Caulobacter crescentus journal September 2017
Extraction and Analysis of Bacterial Teichoic Acids journal January 2018

Cited By (1)

Additional file 1 of Lipoteichoic acids influence cell shape and bacterial division of Streptococcus suis serotype 2, but play a limited role in the pathogenesis of the infection image January 2024

Similar Records

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Streptococcus gordonii
Gram-positive bacteria
LTA
Microbiology
cell wall
lipoteichoicacid
surface protein