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Published in: Medical Microbiology and Immunology 3/2009

01-08-2009 | Original Investigation

RfaB, a galactosyltransferase, contributes to the resistance to detergent and the virulence of Salmonella enterica serovar Enteritidis

Authors: Jing Su, Dommo Timbely, Minmin Zhu, Xiaomei Hua, Biao Liu, Yanjun Pang, Hengguan Shen, Jinliang Qi, Yonghua Yang

Published in: Medical Microbiology and Immunology | Issue 3/2009

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Abstract

In this study, a deletion mutant of rfaBrfaB) was observed to be susceptible to sodium dodecyl sulfate and less tolerant to bile salts. In addition, pre-incubation in 10% bile salts increased bacterial tolerance to 30% bile salts. We also showed that the ΔrfaB mutant invaded HeLa cells less than the wild type and resulted in a lower ratio of intracellular bacteria. Competitive infection of mice showed that the ΔrfaB mutant was defective in the colonization of host organs and was cleared more quickly in fecal shedding. Transforming of a plasmid containing a wild-type allele of rfaB (pRB3-rfaB) partially rescued the defect of the ΔrfaB mutant. The results suggest that RfaB, which is responsible to add the glycosyl residue to the core lipopolysaccharide, contributes to the tolerance to detergent and the virulence of Salmonella enterica serovar Enteritidis.
Literature
1.
go back to reference Trevejo RT, Courtney JG, Starr M, Vugia DJ (2003) Epidemiology of Salmonellosis in California, 1990–1999: morbidity, mortality, and hospitalization costs. Am J Epidemiol 157:48–57. doi:10.1093/aje/kwf155 PubMedCrossRef Trevejo RT, Courtney JG, Starr M, Vugia DJ (2003) Epidemiology of Salmonellosis in California, 1990–1999: morbidity, mortality, and hospitalization costs. Am J Epidemiol 157:48–57. doi:10.​1093/​aje/​kwf155 PubMedCrossRef
2.
go back to reference CDC (2003) Outbreaks of Salmonella serotype enteritidis infection associated with eating shell eggs—United States, 1999–2001. MMWR 51:1149–1152 CDC (2003) Outbreaks of Salmonella serotype enteritidis infection associated with eating shell eggs—United States, 1999–2001. MMWR 51:1149–1152
3.
go back to reference CDC (2007) Multistate outbreak of Salmonella serotype Tennessee infections associated with peanut butter—United States, 2006–2007. MMWR 56:521–524 CDC (2007) Multistate outbreak of Salmonella serotype Tennessee infections associated with peanut butter—United States, 2006–2007. MMWR 56:521–524
4.
go back to reference Nikaido H, Vaara M (1985) Molecular basis of bacterial outer membrane permeability. Microbiol Rev 49:1–32PubMed Nikaido H, Vaara M (1985) Molecular basis of bacterial outer membrane permeability. Microbiol Rev 49:1–32PubMed
5.
go back to reference Nikaido H (1989) Outer membrane barrier as a mechanism of antimicrobial resistance. Antimicrob Agents Chemother 33:1831–1836PubMed Nikaido H (1989) Outer membrane barrier as a mechanism of antimicrobial resistance. Antimicrob Agents Chemother 33:1831–1836PubMed
6.
go back to reference Procyk KJ, Kovarik P, Gabain AV, Baccarini M (1999) Salmonella typhimurium and lipopolysaccharide stimulate extracellularly regulated kinase activation in macrophages by a mechanism involving phosphatidylinositol 3-kinase and phospholipase D as novel intermediates. Infect Immun 67:1011–1017PubMed Procyk KJ, Kovarik P, Gabain AV, Baccarini M (1999) Salmonella typhimurium and lipopolysaccharide stimulate extracellularly regulated kinase activation in macrophages by a mechanism involving phosphatidylinositol 3-kinase and phospholipase D as novel intermediates. Infect Immun 67:1011–1017PubMed
7.
go back to reference Rosenberger CM, Scott MG, Gold MR, Hancock REW, Finlay BB (2000) Salmonella typhimurium infection and lipopolysaccharide stimulation induce similar changes in macrophage gene expression. J Immunol 164:5894–5904PubMed Rosenberger CM, Scott MG, Gold MR, Hancock REW, Finlay BB (2000) Salmonella typhimurium infection and lipopolysaccharide stimulation induce similar changes in macrophage gene expression. J Immunol 164:5894–5904PubMed
8.
go back to reference Xie H, Rath NC, Huff GR, Huff WE, Balog JM (2000) Effects of Salmonella typhimurium lipopolysaccharide on broiler chickens. Poult Sci 79:33–40PubMed Xie H, Rath NC, Huff GR, Huff WE, Balog JM (2000) Effects of Salmonella typhimurium lipopolysaccharide on broiler chickens. Poult Sci 79:33–40PubMed
9.
go back to reference Brazas R, Davie E, Farewell A, Rothfield LI (1991) Transcriptional organization of the rfaGBIJ locus of Salmonella typhimurium. J Bacteriol 173:6168–6173PubMed Brazas R, Davie E, Farewell A, Rothfield LI (1991) Transcriptional organization of the rfaGBIJ locus of Salmonella typhimurium. J Bacteriol 173:6168–6173PubMed
12.
go back to reference Valtonen MV, Plosila M, Valtonen VV, Makela PH (1975) Effect of the quality of the lipopolysaccharide on mouse virulence of Salmonella enteritidis. Infect Immun 12:828–832PubMed Valtonen MV, Plosila M, Valtonen VV, Makela PH (1975) Effect of the quality of the lipopolysaccharide on mouse virulence of Salmonella enteritidis. Infect Immun 12:828–832PubMed
13.
go back to reference Mintz CS, Deibel RH (1983) Effect of lipopolysaccharide mutations on the pathogenesis of experimental Salmonella gastroenteritis. Infect Immun 40:236–244PubMed Mintz CS, Deibel RH (1983) Effect of lipopolysaccharide mutations on the pathogenesis of experimental Salmonella gastroenteritis. Infect Immun 40:236–244PubMed
16.
go back to reference Devyatyarova-Johnson M, Rees IH, Robertson BD, Turner MW, Klein NJ, Jack DL (2000) The lipopolysaccharide structures of Salmonella enterica serovar Typhimurium and Neisseria gonorrhoeae determine the attachment of human mannose-binding lectin to intact organisms. Infect Immun 68:3894–3899. doi:10.1128/IAI.68.7.3894-3899.2000 PubMedCrossRef Devyatyarova-Johnson M, Rees IH, Robertson BD, Turner MW, Klein NJ, Jack DL (2000) The lipopolysaccharide structures of Salmonella enterica serovar Typhimurium and Neisseria gonorrhoeae determine the attachment of human mannose-binding lectin to intact organisms. Infect Immun 68:3894–3899. doi:10.​1128/​IAI.​68.​7.​3894-3899.​2000 PubMedCrossRef
18.
go back to reference Schnaitman CA, Klena JD (1993) Genetics of lipopolysaccharide biosynthesis in enteric bacteria. Microbiol Rev 57:655–682PubMed Schnaitman CA, Klena JD (1993) Genetics of lipopolysaccharide biosynthesis in enteric bacteria. Microbiol Rev 57:655–682PubMed
19.
go back to reference Kadam SK, Rehemtulla A, Sanderson KE (1985) Cloning of rfaG, B, I, and J genes for glycosyltransferase enzymes for synthesis of the lipopolysaccharide core of Salmonella typhimurium. J Bacteriol 161:277–284PubMed Kadam SK, Rehemtulla A, Sanderson KE (1985) Cloning of rfaG, B, I, and J genes for glycosyltransferase enzymes for synthesis of the lipopolysaccharide core of Salmonella typhimurium. J Bacteriol 161:277–284PubMed
20.
go back to reference Pradel E, Parker CT, Schnaitman CA (1992) Structures of the rfaB, rfaI, rfaJ, and rfaS genes of Escherichia coli K-12 and their roles in assembly of the lipopolysaccharide core. J Bacteriol 174:4736–4745PubMed Pradel E, Parker CT, Schnaitman CA (1992) Structures of the rfaB, rfaI, rfaJ, and rfaS genes of Escherichia coli K-12 and their roles in assembly of the lipopolysaccharide core. J Bacteriol 174:4736–4745PubMed
21.
go back to reference Wollin R, Creeger ES, Rothfield LI, Stocker BAD, Lindberg AA (1983) Salmonella typhimurium mutants defective in UDP-D-galactose:lipopolysaccharide alpha 1, 6-D-galactosyltransferase. Structural, immunochemical, and enzymologic studies of rfaB mutants. J Biol Chem 258:3769–3774PubMed Wollin R, Creeger ES, Rothfield LI, Stocker BAD, Lindberg AA (1983) Salmonella typhimurium mutants defective in UDP-D-galactose:lipopolysaccharide alpha 1, 6-D-galactosyltransferase. Structural, immunochemical, and enzymologic studies of rfaB mutants. J Biol Chem 258:3769–3774PubMed
22.
go back to reference Carnell SC, Bowen A, Morgan E, Maskell DJ, Wallis TS, Stevens MP (2007) Role in virulence and protective efficacy in pigs of Salmonella enterica serovar Typhimurium secreted components identified by signature-tagged mutagenesis. Microbiology 153:1940–1952. doi:10.1099/mic.0.2006/006726-0 PubMedCrossRef Carnell SC, Bowen A, Morgan E, Maskell DJ, Wallis TS, Stevens MP (2007) Role in virulence and protective efficacy in pigs of Salmonella enterica serovar Typhimurium secreted components identified by signature-tagged mutagenesis. Microbiology 153:1940–1952. doi:10.​1099/​mic.​0.​2006/​006726-0 PubMedCrossRef
23.
go back to reference Lu S, Manges A, Xu Y, Fang FC, Riley LW (1999) Analysis of virulence of clinical isolates of Salmonella enteritidis in vivo and in vitro. Infect Immun 67:5651–5657PubMed Lu S, Manges A, Xu Y, Fang FC, Riley LW (1999) Analysis of virulence of clinical isolates of Salmonella enteritidis in vivo and in vitro. Infect Immun 67:5651–5657PubMed
25.
go back to reference Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, NY Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, NY
28.
go back to reference Maloy SR, Stewart VJ, Taylor RK (1996) Genetic analysis of pathogenic bacteria: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY Maloy SR, Stewart VJ, Taylor RK (1996) Genetic analysis of pathogenic bacteria: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
29.
go back to reference Hitchcock PJ, Brown TM (1983) Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels. J Bacteriol 154:269–277PubMed Hitchcock PJ, Brown TM (1983) Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels. J Bacteriol 154:269–277PubMed
30.
go back to reference Fomsgaard A, Freudenberg MA, Galanos C (1990) Modification of the silver staining technique to detect lipopolysaccharide in polyacrylamide gels. J Clin Microbiol 28:2627–2631PubMed Fomsgaard A, Freudenberg MA, Galanos C (1990) Modification of the silver staining technique to detect lipopolysaccharide in polyacrylamide gels. J Clin Microbiol 28:2627–2631PubMed
34.
35.
go back to reference Vaara M (1992) Agents that increase the permeability of the outer membrane. Microbiol Rev 56:395–411PubMed Vaara M (1992) Agents that increase the permeability of the outer membrane. Microbiol Rev 56:395–411PubMed
40.
go back to reference Garcia-Quintanilla M, Prieto AI, Barnes L, Ramos-Morales F, Casadesus J (2006) Bile-induced curing of the virulence plasmid in Salmonella enterica serovar Typhimurium. J Bacteriol 188:7963–7965. doi:10.1128/JB.00995-06 PubMedCrossRef Garcia-Quintanilla M, Prieto AI, Barnes L, Ramos-Morales F, Casadesus J (2006) Bile-induced curing of the virulence plasmid in Salmonella enterica serovar Typhimurium. J Bacteriol 188:7963–7965. doi:10.​1128/​JB.​00995-06 PubMedCrossRef
42.
go back to reference Flahaut S, Frere J, Boutibonnes P, Auffray Y (1996) Comparison of the bile salts and sodium dodecyl sulfate stress responses in Enterococcus faecalis. Appl Environ Microbiol 62:2416–2420PubMed Flahaut S, Frere J, Boutibonnes P, Auffray Y (1996) Comparison of the bile salts and sodium dodecyl sulfate stress responses in Enterococcus faecalis. Appl Environ Microbiol 62:2416–2420PubMed
43.
go back to reference Velkinburch JCV, Gunn JS (1999) PhoP-PhoQ-regulated loci are required for enhanced bile resistance in Salmonella spp. Infect Immun 67:1614–1622 Velkinburch JCV, Gunn JS (1999) PhoP-PhoQ-regulated loci are required for enhanced bile resistance in Salmonella spp. Infect Immun 67:1614–1622
48.
go back to reference Prouty AM, Van Velkinburgh JC, Gunn JS (2002) Salmonella enterica serovar typhimurium resistance to bile: identification and characterization of the tolQRA cluster. J Bacteriol 184:1270–1276PubMedCrossRef Prouty AM, Van Velkinburgh JC, Gunn JS (2002) Salmonella enterica serovar typhimurium resistance to bile: identification and characterization of the tolQRA cluster. J Bacteriol 184:1270–1276PubMedCrossRef
Metadata
Title
RfaB, a galactosyltransferase, contributes to the resistance to detergent and the virulence of Salmonella enterica serovar Enteritidis
Authors
Jing Su
Dommo Timbely
Minmin Zhu
Xiaomei Hua
Biao Liu
Yanjun Pang
Hengguan Shen
Jinliang Qi
Yonghua Yang
Publication date
01-08-2009
Publisher
Springer-Verlag
Published in
Medical Microbiology and Immunology / Issue 3/2009
Print ISSN: 0300-8584
Electronic ISSN: 1432-1831
DOI
https://doi.org/10.1007/s00430-009-0115-8

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