Dimeric c-di-GMP is required for post-translational regulation of alginate production in Pseudomonas aeruginosa
Abstract
Pseudomonas aeruginosa is an opportunistic human pathogen that secretes the exopolysaccharide alginate during infection of the respiratory tract of individuals afflicted with cystic fibrosis and chronic obstructive pulmonary disease. Among the proteins required for alginate production, Alg44 has been identified as an inner membrane protein whose bis-(3',5')-cyclic dimeric guanosine monophosphate (c-di-GMP) binding activity post-translationally regulates alginate secretion. In this study, we report the 1.8 Å crystal structure of the cytoplasmic region of Alg44 in complex with dimeric self-intercalated c-di-GMP and characterize its dinucleotide-binding site using mutational analysis. The structure shows that the c-di-GMP binding region of Alg44 adopts a PilZ domain fold with a dimerization mode not previously observed for this family of proteins. Moreover, calorimetric binding analysis of residues in the c-di-GMP binding site demonstrate that mutation of Arg-17 and Arg-95 alters the binding stoichiometry between c-di-GMP and Alg44 from 2:1 to 1:1. Introduction of these mutant alleles on the P. aeruginosa chromosome show that the residues required for binding of dimeric c-di-GMP in vitro are also required for efficient alginate production in vivo. Our results suggest that the dimeric form of c-di-GMP represents the biologically active signaling molecule needed for the secretion of an important virulence factor producedmore »
- Authors:
-
- Hospital for Sick Children, Toronto, ON (Canada); Univ. of Toronto, ON (Canada)
- Brookhaven National Lab. (BNL), Upton, NY (United States)
- Hospital for Sick Children, Toronto, ON (Canada);
- Hospital for Sick Children, Toronto, ON (Canada)
- Virginia Commonwealth Univ. Medical Center and McGuire Veterans Affairs Medical Center, Richmond, VA (United States)
- Publication Date:
- Research Org.:
- Brookhaven National Laboratory (BNL), Upton, NY (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1237169
- Report Number(s):
- BNL-108277-2015-JA
Journal ID: ISSN 0021-9258; R&D Project: LS001
- Grant/Contract Number:
- SC00112704
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Journal of Biological Chemistry
- Additional Journal Information:
- Journal Volume: 290; Journal Issue: 20; Journal ID: ISSN 0021-9258
- Publisher:
- American Society for Biochemistry and Molecular Biology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 36 MATERIALS SCIENCE
Citation Formats
Whitney, John C., Robinson, Howard, Whitfield, Gregory B., Marmont, Lindsey S., Yip, Patrick, Neculai, A. Mirela, Lobsanov, Yuri D., Ohman, Dennis E., and Howell, P. Lynne. Dimeric c-di-GMP is required for post-translational regulation of alginate production in Pseudomonas aeruginosa. United States: N. p., 2015.
Web. doi:10.1074/jbc.M115.645051.
Whitney, John C., Robinson, Howard, Whitfield, Gregory B., Marmont, Lindsey S., Yip, Patrick, Neculai, A. Mirela, Lobsanov, Yuri D., Ohman, Dennis E., & Howell, P. Lynne. Dimeric c-di-GMP is required for post-translational regulation of alginate production in Pseudomonas aeruginosa. United States. https://doi.org/10.1074/jbc.M115.645051
Whitney, John C., Robinson, Howard, Whitfield, Gregory B., Marmont, Lindsey S., Yip, Patrick, Neculai, A. Mirela, Lobsanov, Yuri D., Ohman, Dennis E., and Howell, P. Lynne. Fri .
"Dimeric c-di-GMP is required for post-translational regulation of alginate production in Pseudomonas aeruginosa". United States. https://doi.org/10.1074/jbc.M115.645051. https://www.osti.gov/servlets/purl/1237169.
@article{osti_1237169,
title = {Dimeric c-di-GMP is required for post-translational regulation of alginate production in Pseudomonas aeruginosa},
author = {Whitney, John C. and Robinson, Howard and Whitfield, Gregory B. and Marmont, Lindsey S. and Yip, Patrick and Neculai, A. Mirela and Lobsanov, Yuri D. and Ohman, Dennis E. and Howell, P. Lynne},
abstractNote = {Pseudomonas aeruginosa is an opportunistic human pathogen that secretes the exopolysaccharide alginate during infection of the respiratory tract of individuals afflicted with cystic fibrosis and chronic obstructive pulmonary disease. Among the proteins required for alginate production, Alg44 has been identified as an inner membrane protein whose bis-(3',5')-cyclic dimeric guanosine monophosphate (c-di-GMP) binding activity post-translationally regulates alginate secretion. In this study, we report the 1.8 Å crystal structure of the cytoplasmic region of Alg44 in complex with dimeric self-intercalated c-di-GMP and characterize its dinucleotide-binding site using mutational analysis. The structure shows that the c-di-GMP binding region of Alg44 adopts a PilZ domain fold with a dimerization mode not previously observed for this family of proteins. Moreover, calorimetric binding analysis of residues in the c-di-GMP binding site demonstrate that mutation of Arg-17 and Arg-95 alters the binding stoichiometry between c-di-GMP and Alg44 from 2:1 to 1:1. Introduction of these mutant alleles on the P. aeruginosa chromosome show that the residues required for binding of dimeric c-di-GMP in vitro are also required for efficient alginate production in vivo. Our results suggest that the dimeric form of c-di-GMP represents the biologically active signaling molecule needed for the secretion of an important virulence factor produced by P. aeruginosa.},
doi = {10.1074/jbc.M115.645051},
journal = {Journal of Biological Chemistry},
number = 20,
volume = 290,
place = {United States},
year = {Fri May 15 00:00:00 EDT 2015},
month = {Fri May 15 00:00:00 EDT 2015}
}
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