SpyB, a small heme-binding protein, affects the composition of the cell wall in Streptococcus pyogenes
Abstract
Streptococcus pyogenes (Group A Streptococcus or GAS) is a hemolytic human pathogen associated with a wide variety of infections ranging from minor skin and throat infections to life-threatening invasive diseases. The cell wall of GAS consists of peptidoglycan sacculus decorated with a carbohydrate comprising a polyrhamnose backbone with immunodominant N-acetylglucosamine side-chains. All GAS genomes contain the spyBA operon, which encodes a 35-amino-acid membrane protein SpyB, and a membrane-bound C3-like ADP-ribosyltransferase SpyA. In this study, we addressed the function of SpyB in GAS. Phenotypic analysis of a spyB deletion mutant revealed increased bacterial aggregation, and reduced sensitivity to β-lactams of the cephalosporin class and peptidoglycan hydrolase PlyC. Glycosyl composition analysis of cell wall isolated from the spyB mutant suggested an altered carbohydrate structure compared with the wild-type strain. Furthermore, we found that SpyB associates with heme and protoporphyrin IX. Heme binding induces SpyB dimerization, which involves disulfide bond formation between the subunits. Furthermore, our data suggest the possibility that SpyB activity is regulated by heme.
- Authors:
-
- Univ. of Kentucky, Lexington, KY (United States)
- The Ohio State Univ., Columbus, OH (United States)
- Univ. of Washington, Seattle, WA (United States)
- Univ. of Georgia, Athens, GA (United States)
- Publication Date:
- Research Org.:
- Univ. of Georgia, Athens, GA (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1365842
- Grant/Contract Number:
- FG02-93ER20097
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Frontiers in Cellular and Infection Microbiology
- Additional Journal Information:
- Journal Volume: 6; Journal ID: ISSN 2235-2988
- Publisher:
- Frontiers Research Foundation
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 60 APPLIED LIFE SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; SpyA; SpyB; heme; ADP-ribosyltransferase; Group A carbohydrate; Streptococcus pyogenes; cell wall
Citation Formats
Edgar, Rebecca J., Chen, Jing, Kant, Sashi, Rechkina, Elena, Rush, Jeffrey S., Forsberg, Lennart S., Jaehrig, Bernhard, Azadi, Parastoo, Tchesnokova, Veronika, Sokurenko, Evgeni V., Zhu, Haining, Korotkov, Konstantin V., Pancholi, Vijay, and Korotkova, Natalia. SpyB, a small heme-binding protein, affects the composition of the cell wall in Streptococcus pyogenes. United States: N. p., 2016.
Web. doi:10.3389/fcimb.2016.00126.
Edgar, Rebecca J., Chen, Jing, Kant, Sashi, Rechkina, Elena, Rush, Jeffrey S., Forsberg, Lennart S., Jaehrig, Bernhard, Azadi, Parastoo, Tchesnokova, Veronika, Sokurenko, Evgeni V., Zhu, Haining, Korotkov, Konstantin V., Pancholi, Vijay, & Korotkova, Natalia. SpyB, a small heme-binding protein, affects the composition of the cell wall in Streptococcus pyogenes. United States. https://doi.org/10.3389/fcimb.2016.00126
Edgar, Rebecca J., Chen, Jing, Kant, Sashi, Rechkina, Elena, Rush, Jeffrey S., Forsberg, Lennart S., Jaehrig, Bernhard, Azadi, Parastoo, Tchesnokova, Veronika, Sokurenko, Evgeni V., Zhu, Haining, Korotkov, Konstantin V., Pancholi, Vijay, and Korotkova, Natalia. Thu .
"SpyB, a small heme-binding protein, affects the composition of the cell wall in Streptococcus pyogenes". United States. https://doi.org/10.3389/fcimb.2016.00126. https://www.osti.gov/servlets/purl/1365842.
@article{osti_1365842,
title = {SpyB, a small heme-binding protein, affects the composition of the cell wall in Streptococcus pyogenes},
author = {Edgar, Rebecca J. and Chen, Jing and Kant, Sashi and Rechkina, Elena and Rush, Jeffrey S. and Forsberg, Lennart S. and Jaehrig, Bernhard and Azadi, Parastoo and Tchesnokova, Veronika and Sokurenko, Evgeni V. and Zhu, Haining and Korotkov, Konstantin V. and Pancholi, Vijay and Korotkova, Natalia},
abstractNote = {Streptococcus pyogenes (Group A Streptococcus or GAS) is a hemolytic human pathogen associated with a wide variety of infections ranging from minor skin and throat infections to life-threatening invasive diseases. The cell wall of GAS consists of peptidoglycan sacculus decorated with a carbohydrate comprising a polyrhamnose backbone with immunodominant N-acetylglucosamine side-chains. All GAS genomes contain the spyBA operon, which encodes a 35-amino-acid membrane protein SpyB, and a membrane-bound C3-like ADP-ribosyltransferase SpyA. In this study, we addressed the function of SpyB in GAS. Phenotypic analysis of a spyB deletion mutant revealed increased bacterial aggregation, and reduced sensitivity to β-lactams of the cephalosporin class and peptidoglycan hydrolase PlyC. Glycosyl composition analysis of cell wall isolated from the spyB mutant suggested an altered carbohydrate structure compared with the wild-type strain. Furthermore, we found that SpyB associates with heme and protoporphyrin IX. Heme binding induces SpyB dimerization, which involves disulfide bond formation between the subunits. Furthermore, our data suggest the possibility that SpyB activity is regulated by heme.},
doi = {10.3389/fcimb.2016.00126},
journal = {Frontiers in Cellular and Infection Microbiology},
number = ,
volume = 6,
place = {United States},
year = {Thu Oct 13 00:00:00 EDT 2016},
month = {Thu Oct 13 00:00:00 EDT 2016}
}
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Bacterial glycobiology: rhamnose-containing cell wall polysaccharides in Gram-positive bacteria
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Two Group A Streptococcal Peptide Pheromones Act through Opposing Rgg Regulators to Control Biofilm Development
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Assembly of the Type II Secretion System such as Found in Vibrio cholerae Depends on the Novel Pilotin AspS
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Molecular mechanisms of β-lactam resistance in Streptococcus pneumoniae
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The crimson conundrum: heme toxicity and tolerance in GAS
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- Frontiers in Cellular and Infection Microbiology, Vol. 4
Works referencing / citing this record:
The molecular mechanism of N -acetylglucosamine side-chain attachment to the Lancefield group A carbohydrate in Streptococcus pyogenes
journal, October 2017
- Rush, Jeffrey S.; Edgar, Rebecca J.; Deng, Pan
- Journal of Biological Chemistry, Vol. 292, Issue 47
Genome sequence analysis of emm89 Streptococcus pyogenes strains causing infections in Scotland, 2010–2016
journal, December 2017
- Beres, Stephen B.; Olsen, Randall J.; Ojeda Saavedra, Matthew
- Journal of Medical Microbiology, Vol. 66, Issue 12
An In-Silico Sequence-Structure-Function Analysis of the N-Terminal Lobe in CT Group Bacterial ADP-Ribosyltransferase Toxins
journal, June 2019
- Lugo, Miguel R.; Merrill, A. Rod
- Toxins, Vol. 11, Issue 6
The molecular mechanism of N-acetylglucosamine side-chain attachment to the Lancefield group A Carbohydrate in Streptococcus pyogenes
journal, October 2017
- Rush, Jeffrey S.; Edgar, Rebecca J.; Deng, Pan
- Journal of Biological Chemistry