Role of anionic charges of osmoregulated periplasmic glucans of Salmonella enterica serovar Typhimurium SL1344 in mice virulence
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Abstract
opgB gene of Salmonella enterica serovar Typhimurium was identified earlier in a genome-wide screen for mice virulence (Valentine et al. in Infect Immun 66:3378–3383, 1998). Although mutation in opgB resulted in avirulent Salmonella strain, how this gene contributes to pathogenesis remains unclear. Based on DNA homology, opgB is predicted to be responsible for adding phosphoglycerate residues to osmoregulated periplasmic glucans (OPGs) giving them anionic characteristics. In Escherichia coli, yet another gene, opgC, is also reported to contribute to anionic characteristics of OPGs by adding succinic acid residues. We constructed opgB, opgC, and opgBC double mutants of S. enterica serovar Typhimurium strain SL1344. As predicted opgBC mutant synthesized neutral OPGs that were devoid of any anionic substituents. However, opgB, opgC, and opgBC mutations had no significant impact on mice virulence as well as on competitive organ colonization. In low osmotic conditions, opgB, opgC, and opgBC mutants exhibited delay in growth initiation in the presence of sodium deoxycholate. Anionic substituents of OPGs from Salmonella although appear to be needed to overcome resistance of deoxycholate in hypoosmotic growth media, no evidence was found for their role in mice virulence.
Keywords
Periplasmicglucans Low osmolarity Bile salt sensitivity Salmonellosis Food microbiology Microbial food safetyReferences
- Badie G, Heithoff DM, Sinsheimer RL, Mahan MJ (2007) Altered levels of Salmonella DNA adenine methylase are associated with defects in gene expression, motility, flagellar synthesis, and bile resistance in the pathogenic strain 14028 but not in thelaboratory strain LT2. J Bacteriol 189:1556–1564PubMedCrossRefGoogle Scholar
- Baumler AJ, Tsolis RM, Valentine PJ, Ficht TA, Heffron F (1997) Synergistic effect of mutations in invA and lpfC on the ability of Salmonella typhimurium to cause murine typhoid. Infect Immun 65:2254–2259PubMedGoogle Scholar
- Beuzon CR, Holden DW (2001) Use of mixed infections with Salmonella strains to study virulence genes and their interactions in vivo. Microbes Infect 3:1345–1352PubMedCrossRefGoogle Scholar
- Bhagwat AA (2006) Microbiological safety of fresh-cut produce: where are we now? In: Matthews KR (ed) Microbiology of fresh produce. Am Soc Microbiol, Washington, pp 121–165Google Scholar
- Bhagwat AA, Tully RE, Keister DL (1992) Isolation and chracterization of an ndvB locus from Rhizobium fredii. Molec Microbiol 6:2159–2165CrossRefGoogle Scholar
- Bhagwat AA, Gross KC, Tully RE, Keister DL (1996) ß-Glucan synthesis in Bradyrhizobium japonicum: Characterization of a new locus (ndvC) influencing ß-(1,6)-linkages. J Bacteriol 178:4635–4642PubMedGoogle Scholar
- Bhagwat AA et al (2006) Functional heterogeneity of RpoS in stress tolerance of enterohemorrhagic Escherichia coli strains. Appl Environ Microbiol 72:4978–4986PubMedCrossRefGoogle Scholar
- Bhagwat AA et al (2009) Osmoregulated periplasmic glucans of Salmonella enterica serovar Typhimurium are required for optimal virulence in mice. Microbiology 155:229–237PubMedCrossRefGoogle Scholar
- Bohin J-P (2000) Osmoregulated periplasmic glucans in Proteobacteria. FEMS Microbiol Lett 186:11–19PubMedGoogle Scholar
- Bohin J-P, Lacroix J-M (2007) Osmoregulation in the periplasm. In: Ehrmann M (ed) The periplasm. ASM Press, Washington, pp 325–341Google Scholar
- Bowe F, Lipps CJ, Tsolis RM, Groisman E, Heffron F, Kusters JG (1998) At least four percent of the Salmonella typhimurium genome is required for fatal infection of mice. Infect Immun 66:3372–3377PubMedGoogle Scholar
- Cangelosi GA, Martinetti G, Nester EW (1990) Osmosensitivity phenotypes of Agrobacterium tumefaciens mutants that lack periplasmic beta-1,2-glucan. J Bacteriol 172:2172–2174PubMedGoogle Scholar
- Crawford RW, Gibson DL, Kay WW, Gunn JS (2008) Identification of a bile-induced exopolysaccharide required for Salmonella biofilm formation on gallstone surfaces. Infect Immun 76:5341–5349PubMedCrossRefGoogle Scholar
- Cronan JE (2006) A family of arabinose-inducible Escherichia coli expression vectors having pBR322 copy control. Pasmid 55:152–157CrossRefGoogle Scholar
- Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97:6640–6645PubMedCrossRefGoogle Scholar
- Gunn JS (2000) Mechanism of bacterial resistance and response to bile. Microbes Infect 2:907–913PubMedCrossRefGoogle Scholar
- Kannan P, Dharne M, Smith A, Karns J, Bhagwat AA (2009) Motility revertants of opgGH mutants of Salmonella enterica serovar Typhimurium remain defective in mice virulence. Curr Microbiol 59:641–645PubMedCrossRefGoogle Scholar
- Kennedy EP (1996) Membrane-derived oligosaccharides (periplasmic beta-D-glucans) of Escherichia coli. In: Neidhardt FC et al (eds) Escherichia coli and Salmonella cellular and molecular biology, 2nd edn. American Society for Microbiology, Washigton, pp 1064–1074Google Scholar
- Lacorix J, Lanfroy E, Cogez V, Lequette Y, Bohin A, Bohin J-P (1999) The mdoC gene of Escherichia coli encodes a membrane protein that is required for succinylation of osmoregulated periplasmic glucans. J Bacteriol 181:3626–3631Google Scholar
- Lequette Y, Odberg-Ferragut C, Bohin J-P, Lacorix J (2004) Identification of mdoD, an mdoG paralog which encodes a twin-arginine-dependent periplasmic protein that controls osmoregulated periplasmic glucan backbone structures. J Bacteriol 186:3695–9702PubMedCrossRefGoogle Scholar
- Liu L, Tan S, Jun W, Smith A, Meng J, Bhagwat AA (2009) Osmoregulated periplasmic glucans are needed for competitive growth and biofilm formation by Salmonella enterica serovar Typhimurium in leafy-green vegetable wash waters and colonization in mice. FEMS Microbiol Lett 292:13–20PubMedCrossRefGoogle Scholar
- Liu L et al (2010) Osmoregulated periplasmic glucans synthesis gene family of Shigella flexneri. Arch Microbiol 192:167–174PubMedCrossRefGoogle Scholar
- Merritt ME, Donaldson JR (2009) Effect of bile salts on the DNA and membrane integrity of enteric bacteria. J Med Microbiol 58:1533–1541PubMedCrossRefGoogle Scholar
- Rajagopal S, Eis N, Bhattacharya M, Nickerson KW (2003) Membrane-derived oligosaccharides (MDOs) are essential for sodium dodecyl sulfate resistance in Escherichia coli. FEMS Microbiol Lett 223:25–31PubMedCrossRefGoogle Scholar
- Ramos-Morales F, Prieto AI, Beuzon CR, Holden DW, Casadesus J (2003) Role for Salmonella enterica enterobacterial common antigen in bile resistance and virulence. J Bacteriol 185:5328–5332PubMedCrossRefGoogle Scholar
- Shea JE, Beuzon CR, Gleeson C, Mundy R, Holden DW (1999) Influence of the Salmonella typhimurium pathogenicity island 2 type III secretion system on bacterial growth in the mouse. Infect Immun 67:213–219PubMedGoogle Scholar
- Valentine PJ, Devore BP, Heffron F (1998) Identification of three highly attenuated Salmonella typhimurium mutants that are more immunogenic and protective in mice than a prototypical aroA mutant. Infect Immun 66:3378–3383PubMedGoogle Scholar