Streptococcus gordonii Type I Lipoteichoic Acid Contributes to Surface Protein Biogenesis
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 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,more »
- Authors:
-
[1];
[2];
- Univ. of Minnesota, Minneapolis, MN (United States). Dept. of Diagnostic and Biological Sciences, School of Dentistry
- Pennsylvania State Univ., State College, PA (United States). Dept. of Biochemistry and Molecular Biology
- Univ. of Malmo (Sweden). Dept. of Oral Biology, Faculty of Odontology
- Univ. of Malmo (Sweden). Dept. of Oral Biology, Faculty of Odontology
- Univ. of Iowa, Iowa City, IA (United States)
- Publication Date:
- Research Org.:
- Univ. of Georgia, Athens, GA (United States); Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1626161
- Alternate Identifier(s):
- OSTI ID: 1964101
- 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:
- 59 BASIC BIOLOGICAL SCIENCES; 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. doi: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 = {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.},
doi = {10.1128/msphere.00814-19},
journal = {mSphere},
number = 6,
volume = 4,
place = {United States},
year = {2019},
month = {12}
}
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Figures / Tables:
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 »
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