skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

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

Abstract

ABSTRACT 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 commensalStreptococcus 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 ofS. gordoniiwere analyzed using label-free mass spectroscopy. Comparisons showed that the abundances of many proteins differed, including (i) SspA, SspB, andS. gordonii0707 (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 byS. gordonii. Similarly toStreptococcus suis,S. gordoniiproduced a complex type I LTA, decorated with multipled-alanylations and glycosylations. Hence, theS. gordoniiLTAmore » appears to orchestrate expression and presentation of cell surface-associated proteins and functions. IMPORTANCEDiscovered over a half-century ago, lipoteichoic acid (LTA) is an abundant polymer found on the surface of Gram-positive bacteria. Although LTA is essential for the survival of many Gram-positive species, knowledge of how LTA contributes to bacterial physiology has remained elusive. Recently, LTA-deficient strains have been generated in some Gram-positive species, including the human oral commensalStreptococcus gordonii. The significance of our research is that we utilized an LTA-deficient strain ofS. gordoniito address why LTA is physiologically important to Gram-positive bacteria. We demonstrate that inS. gordonii, LTA plays an important role in the presentation of many cell surface-associated proteins, contributing to cell envelope homeostasis, cell-to-cell interactions in biofilms, and adhesion to eukaryotic cells. These data may broadly reflect a physiological role of LTA in Gram-positive bacteria.« less

Authors:
ORCiD logo [1]; ORCiD logo [2];  [1];  [3];  [4];  [1];  [1];  [1];  [2];  [1];  [5]
  1. Univ. of Minnesota, Minneapolis, MN (United States). Dept. of Diagnostic and Biological Sciences, School of Dentistry
  2. Pennsylvania State Univ., State College, PA (United States). Dept. of Biochemistry and Molecular Biology
  3. Univ. of Malmo (Sweden). Dept. of Oral Biology, Faculty of Odontology
  4. Univ. of Malmo (Sweden). Dept. of Oral Biology, Faculty of Odontology
  5. Univ. of Iowa, Iowa City, IA (United States)
Publication Date:
Research Org.:
Univ. of Georgia, Athens, GA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1626161
Grant/Contract Number:  
SC0015662; R01 DE02561; K08DE027705
Resource Type:
Accepted Manuscript
Journal Name:
mSphere
Additional Journal Information:
Journal Volume: 4; Journal Issue: 6; Journal ID: ISSN 2379-5042
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
Microbiology; Gram-positive bacteria; LTA; Streptococcus gordonii; cell wall; lipoteichoicacid; surface protein

Citation Formats

Lima, Bruno P., Kho, Kelvin, Nairn, Brittany L., Davies, Julia R., Svensäter, Gunnel, Chen, Ruoqiong, Steffes, Amanda, Vreeman, Gerrit W., Meredith, Timothy C., Herzberg, Mark C., and Ellermeier, Craig D. Streptococcus gordonii Type I Lipoteichoic Acid Contributes to Surface Protein Biogenesis. United States: N. p., 2019. Web. https://doi.org/10.1128/msphere.00814-19.
Lima, Bruno P., Kho, Kelvin, Nairn, Brittany L., Davies, Julia R., Svensäter, Gunnel, Chen, Ruoqiong, Steffes, Amanda, Vreeman, Gerrit W., Meredith, Timothy C., Herzberg, Mark C., & Ellermeier, Craig D. Streptococcus gordonii Type I Lipoteichoic Acid Contributes to Surface Protein Biogenesis. United States. https://doi.org/10.1128/msphere.00814-19
Lima, Bruno P., Kho, Kelvin, Nairn, Brittany L., Davies, Julia R., Svensäter, Gunnel, Chen, Ruoqiong, Steffes, Amanda, Vreeman, Gerrit W., Meredith, Timothy C., Herzberg, Mark C., and Ellermeier, Craig D. Wed . "Streptococcus gordonii Type I Lipoteichoic Acid Contributes to Surface Protein Biogenesis". United States. https://doi.org/10.1128/msphere.00814-19. https://www.osti.gov/servlets/purl/1626161.
@article{osti_1626161,
title = {Streptococcus gordonii Type I Lipoteichoic Acid Contributes to Surface Protein Biogenesis},
author = {Lima, Bruno P. and Kho, Kelvin and Nairn, Brittany L. and Davies, Julia R. and Svensäter, Gunnel and Chen, Ruoqiong and Steffes, Amanda and Vreeman, Gerrit W. and Meredith, Timothy C. and Herzberg, Mark C. and Ellermeier, Craig D.},
abstractNote = {ABSTRACT 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 commensalStreptococcus 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 ofS. gordoniiwere analyzed using label-free mass spectroscopy. Comparisons showed that the abundances of many proteins differed, including (i) SspA, SspB, andS. gordonii0707 (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 byS. gordonii. Similarly toStreptococcus suis,S. gordoniiproduced a complex type I LTA, decorated with multipled-alanylations and glycosylations. Hence, theS. gordoniiLTA appears to orchestrate expression and presentation of cell surface-associated proteins and functions. IMPORTANCEDiscovered over a half-century ago, lipoteichoic acid (LTA) is an abundant polymer found on the surface of Gram-positive bacteria. Although LTA is essential for the survival of many Gram-positive species, knowledge of how LTA contributes to bacterial physiology has remained elusive. Recently, LTA-deficient strains have been generated in some Gram-positive species, including the human oral commensalStreptococcus gordonii. The significance of our research is that we utilized an LTA-deficient strain ofS. gordoniito address why LTA is physiologically important to Gram-positive bacteria. We demonstrate that inS. gordonii, LTA plays an important role in the presentation of many cell surface-associated proteins, contributing to cell envelope homeostasis, cell-to-cell interactions in biofilms, and adhesion to eukaryotic cells. These data may broadly reflect a physiological role of LTA in Gram-positive bacteria.},
doi = {10.1128/msphere.00814-19},
journal = {mSphere},
number = 6,
volume = 4,
place = {United States},
year = {2019},
month = {12}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Figures / Tables:

FIG 1 FIG 1: ltaS deletion leads to loss of LTA. (A) ltaS deletion was confirmed by PCR amplification of the wild-type (WT) and the LTA-deficient (ΔltaS) genomic DNA with the primer pair ltaS up For and ltaS Dn Rev. (B) Mouse anti-LTA antibody was used to detect LTA presence on cellmore » wall fractions from the WT strain, the ΔltaS strain, and the complemented LTA deletion strain (ΔltaSc) using Western blotting.« less

Save / Share:

Works referenced in this record:

From the regulation of peptidoglycan synthesis to bacterial growth and morphology
journal, December 2011

  • Typas, Athanasios; Banzhaf, Manuel; Gross, Carol A.
  • Nature Reviews Microbiology, Vol. 10, Issue 2
  • DOI: 10.1038/nrmicro2677

Novel series of plasmid vectors for gene inactivation and expression analysis in group A streptococci (GAS)
journal, January 1996


The essential nature of teichoic acids in Bacillus subtilis as revealed by insertional mutagenesis
journal, February 1989

  • Mauël, Catherine; Young, Michael; Margot, Philippe
  • Molecular and General Genetics MGG, Vol. 215, Issue 3
  • DOI: 10.1007/bf00427034

Lipoteichoic acid and lipids in the membrane of Staphylococcus aureus
journal, May 1994

  • Fischer, Werner
  • Medical Microbiology and Immunology, Vol. 183, Issue 2
  • DOI: 10.1007/bf00277157

The Bacterial Cell Envelope
journal, April 2010


Inactivation of Streptococcusgordonii SspAB Alters Expression of Multiple Adhesin Genes
journal, June 2005


Induction of Experimental Endocarditis by Continuous Low-Grade Bacteremia Mimicking Spontaneous Bacteremia in Humans
journal, February 2011

  • Veloso, T. R.; Amiguet, M.; Rousson, V.
  • Infection and Immunity, Vol. 79, Issue 5
  • DOI: 10.1128/IAI.01208-10

Genes Involved in Formation of Structured Multicellular Communities by Bacillus subtilis
journal, June 2004


Essential PcsB putative peptidoglycan hydrolase interacts with the essential FtsXSpn cell division protein in Streptococcus pneumoniae D39
journal, October 2011

  • Sham, L. -T.; Barendt, S. M.; Kopecky, K. E.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 45
  • DOI: 10.1073/pnas.1108323108

Small molecule inhibitor of lipoteichoic acid synthesis is an antibiotic for Gram-positive bacteria
journal, February 2013

  • Richter, Stefan G.; Elli, Derek; Kim, Hwan Keun
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 9
  • DOI: 10.1073/pnas.1217337110

Pleiotropic Roles of Polyglycerolphosphate Synthase of Lipoteichoic Acid in Growth of Staphylococcus aureus Cells
journal, October 2008

  • Oku, Yusuke; Kurokawa, Kenji; Matsuo, Miki
  • Journal of Bacteriology, Vol. 191, Issue 1
  • DOI: 10.1128/JB.01221-08

Identity of viridans streptococci isolated from cases of infective endocarditis
journal, September 1993

  • Douglas, C. W. I.; Heath, J.; Hampton, K. K.
  • Journal of Medical Microbiology, Vol. 39, Issue 3
  • DOI: 10.1099/00222615-39-3-179

Teichoic Acids from Bacterial Walls: Composition of Teichoic Acids from a Number of Bacterial Walls
journal, July 1959

  • Armstrong, J. J.; Baddiley, J.; Buchanan, J. G.
  • Nature, Vol. 184, Issue 4682
  • DOI: 10.1038/184247a0

High-resolution Visualization of the Microbial Glycocalyx with Low-voltage Scanning Electron Microscopy: Dependence on Cationic Dyes
journal, November 2004

  • Erlandsen, Stanley L.; Kristich, Christopher J.; Dunny, Gary M.
  • Journal of Histochemistry & Cytochemistry, Vol. 52, Issue 11
  • DOI: 10.1369/jhc.4A6428.2004

Interactions of Fibronectin with Streptococci: The Role of Fibronectin as a Receptor for Streptococcus pyogenes
journal, July 1987


Genes Required for Glycolipid Synthesis and Lipoteichoic Acid Anchoring in Staphylococcus aureus
journal, January 2007

  • Grundling, A.; Schneewind, O.
  • Journal of Bacteriology, Vol. 189, Issue 6
  • DOI: 10.1128/JB.01683-06

Cell envelope stress response in Gram-positive bacteria
journal, January 2008


Comparative studies of lipoteichoic acids from several Bacillus strains.
journal, January 1986


FtsEX-mediated regulation of the final stages of cell division reveals morphogenetic plasticity in Caulobacter crescentus
journal, September 2017


Mechanisms of intrinsic resistance to antimicrobial peptides of Edwardsiella ictaluri and its influence on fish gut inflammation and virulence
journal, July 2013

  • Gatlin, Delbert M.; Santander, Javier; Loh, Amanda
  • Microbiology, Vol. 159, Issue 7
  • DOI: 10.1099/mic.0.066639-0

Role of PBP1 in Cell Division of Staphylococcus aureus
journal, February 2007

  • Pereira, S. F. F.; Henriques, A. O.; Pinho, M. G.
  • Journal of Bacteriology, Vol. 189, Issue 9
  • DOI: 10.1128/JB.00044-07

Bacillus subtilis α-Phosphoglucomutase Is Required for Normal Cell Morphology and Biofilm Formation
journal, January 2005

  • Lazarevic, Vladimir; Soldo, Blazenka; M�dico, No�l
  • Applied and Environmental Microbiology, Vol. 71, Issue 1
  • DOI: 10.1128/AEM.71.1.39-45.2005

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

  • Xie, Zhoujie; Okinaga, Toshinori; Qi, Fengxia
  • Applied and Environmental Microbiology, Vol. 77, Issue 22
  • DOI: 10.1128/AEM.06362-11

Slx5/Slx8 Promotes Replication Stress Tolerance by Facilitating Mitotic Progression
journal, May 2016


Lipoteichoic Acids, Phosphate-Containing Polymers in the Envelope of Gram-Positive Bacteria
journal, January 2014

  • Schneewind, O.; Missiakas, D.
  • Journal of Bacteriology, Vol. 196, Issue 6
  • DOI: 10.1128/JB.01155-13

Salt-Induced Stress Stimulates a Lipoteichoic Acid-Specific Three-Component Glycosylation System in Staphylococcus aureus
journal, April 2018

  • Kho, Kelvin; Meredith, Timothy C.
  • Journal of Bacteriology, Vol. 200, Issue 12
  • DOI: 10.1128/JB.00017-18

Consequences of a sortase A mutation in Streptococcus gordonii
journal, December 2007


Effect of lipoteichoic acid on thermotropic membrane properties.
journal, January 1997


Inhibition of bacterial wall lysins by lipoteichoic acids and related compounds
journal, December 1975

  • Cleveland, R. F.; Holtje, J. -V.; Wicken, A. J.
  • Biochemical and Biophysical Research Communications, Vol. 67, Issue 3
  • DOI: 10.1016/0006-291x(75)90791-3

Streptococcus gordonii lipoproteins induce IL-8 in human periodontal ligament cells
journal, November 2017


Staphylococcal biofilm disassembly
journal, September 2011


Streptococcal Antagonism in Oral Biofilms: Streptococcus sanguinis and Streptococcus gordonii Interference with Streptococcus mutans
journal, April 2008

  • Kreth, Jens; Zhang, Yongshu; Herzberg, Mark C.
  • Journal of Bacteriology, Vol. 190, Issue 13
  • DOI: 10.1128/JB.00276-08

Occurrence and function of membrane teichoic acids
journal, May 1977

  • Lambert, Peter A.; Hancock, Ian C.; Baddiley, James
  • Biochimica et Biophysica Acta (BBA) - Reviews on Biomembranes, Vol. 472, Issue 1
  • DOI: 10.1016/0304-4157(77)90012-0

A reproducible oral microcosm biofilm model for testing dental materials
journal, September 2012


Structural analysis and immunostimulatory potency of lipoteichoic acids isolated from three Streptococcus suis serotype 2 strains
journal, June 2018

  • Gisch, Nicolas; Auger, Jean-Philippe; Thomsen, Simone
  • Journal of Biological Chemistry, Vol. 293, Issue 31
  • DOI: 10.1074/jbc.RA118.002174

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


A combinatorial approach to the peptide feature matching problem for label-free quantification
journal, May 2013


Oral keratinocytes support non-replicative infection and transfer of harbored HIV-1 to permissive cells
journal, January 2008

  • Vacharaksa, Anjalee; Asrani, Anil C.; Gebhard, Kristin H.
  • Retrovirology, Vol. 5, Issue 1
  • DOI: 10.1186/1742-4690-5-66

Oral multispecies biofilm development and the key role of cell–cell distance
journal, June 2010

  • Kolenbrander, Paul E.; Palmer, Robert J.; Periasamy, Saravanan
  • Nature Reviews Microbiology, Vol. 8, Issue 7
  • DOI: 10.1038/nrmicro2381

Streptococcus Adherence and Colonization
journal, September 2009

  • Nobbs, Angela H.; Lamont, Richard J.; Jenkinson, Howard F.
  • Microbiology and Molecular Biology Reviews, Vol. 73, Issue 3
  • DOI: 10.1128/MMBR.00014-09

Evidence for a dual role of PBP1 in the cell division and cell separation of Staphylococcus aureus
journal, May 2009


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

  • Reichmann, Nathalie T.; Piçarra Cassona, Carolina; Monteiro, João M.
  • Molecular Microbiology, Vol. 92, Issue 2
  • DOI: 10.1111/mmi.12551

Extraction and Analysis of Bacterial Teichoic Acids
journal, January 2018


Identification of novel LPXTG-linked surface proteins from Streptococcus gordonii
journal, June 2009

  • Davies, Julia R.; Svensäter, Gunnel; Herzberg, Mark C.
  • Microbiology, Vol. 155, Issue 6
  • DOI: 10.1099/mic.0.027854-0

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

  • Theilacker, Christian; Sava, Irina; Sanchez-Carballo, Patricia
  • BMC Microbiology, Vol. 11, Issue 1
  • DOI: 10.1186/1471-2180-11-67

Lipoproteins in Streptococcus gordonii are critical in the infection and inflammatory responses
journal, September 2018


Lipoteichoic Acid Synthesis and Function in Gram-Positive Bacteria
journal, September 2014


Re-evaluation of the Role of Calcium Homeostasis Endoplasmic Reticulum Protein (CHERP) in Cellular Calcium Signaling
journal, November 2012

  • Lin-Moshier, Yaping; Sebastian, Peter J.; Higgins, LeeAnn
  • Journal of Biological Chemistry, Vol. 288, Issue 1
  • DOI: 10.1074/jbc.M112.405761

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

  • Yang, D. C.; Peters, N. T.; Parzych, K. R.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 45
  • DOI: 10.1073/pnas.1107780108