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A novel relationship between O-antigen variation, matrix formation, and invasiveness of Salmonella enteritidis

Published online by Cambridge University Press:  15 May 2009

J. Guard-Petter ,
L. H. Keller ,
M. Mahbubur Rahman ,
R. W. Carlson  and
S. Silvers
J. Guard-Petter
Affiliation:
USDA/ARS, Southeast Poultry Research Laboratory, 934 College Station Road, Athens, GA 30605
L. H. Keller
Affiliation:
University of Pennsylvania, New Bolton Center, Kennett Square, PA
M. Mahbubur Rahman
Affiliation:
University of Georgia, Complex Carbohydrate Research Center, Athens, GA
R. W. Carlson
Affiliation:
University of Georgia, Complex Carbohydrate Research Center, Athens, GA
S. Silvers
Affiliation:
USDA/ARS, Russell Research Center, Athens, GA
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Salmonella enterica Enteritidis in chickens serves as a reservoir for salmonellosis in humans and the structure of its lipopolysaccharide (LPS) has been used to assess invasiveness. Culture from chick spleens generated colonies with an unusual wrinkled morphology, and it is designated the lacy phenotype. To characterize the nature of the morphological change, three isogenic variants were compared. Only the lacy phenotype produced a temperature-dependent cell surface matrix composed of several proteins in association with LPS high molecular weight O-antigen.

Flagellin and a 35 kDa protein were identified as specific proteinaceous components of matrix. Both proteins cross-reacted with a monoclonal antibody previously determined to specifically detect the g-epitope of the Enteritidis monophasic flagella (H-antigen). These results suggest that O-antigen in association with protein contributes to cross-reactivity between molecules. The lacy phenotype was more organ invasive in 5-day-old chicks than isogenic variants producing low molecular weight O-antigen. However, it was no more efficient at contaminating eggs after oral inoculation of hens than a variant that completely lacked O-antigen, thus the lacy phenotype is classified as an intermediately invasive organism. The distinctive colonial phenotype of SE6-E21lacy was used to investigate environmental factors that decreased O/C ratios and contributed to attenuation. In so doing, it was found that growth in complement at 46°C caused matrix producing cells to hyperflagellate and migrate across agar surfaces. These results suggest that the structure of O-antigen might influence the secretion and/or the function of Enteritidis cell-surface proteins. The data also reveal a greater heterogeneity than has been assumed in the phenotype, and possibly the infectious behaviour, of Enteritidis.

Type
Research Article
Information
Epidemiology & Infection , Volume 117 , Issue 2 , October 1996 , pp. 219 - 231
Copyright
Copyright © Cambridge University Press 1996

References

1.St Louise, ME, Morse, DL, Potter, ME, et al. The emergence of grade A eggs as a major source of Salmonella enteriridis infections: new implications for the control of salmonellosis. JAMA 1988; 259: 2103–7.CrossRefGoogle Scholar
2.Shivaprasad, HL, Timoney, JF, Morales, S, Lucio, B, Baker, RC. Pathogenesis of Salmonella enteritidis infection in laying chickens. I. Studies on egg transmission, clinical signs, fecal shedding, and serological responses. Avian Dis 1990; 34: 548–57.CrossRefGoogle Scholar
3.Humphrey, TJ, Whitehead, A, Gawler, AH, Henley, A, Rowe, B. Numbers of Salmonella enteritidis in the contents of naturally contaminated hens' eggs. Epidemiol Infect 1991; 106: 489–96.Google ScholarPubMed
4.Mishu, B, Koehier, J, Lee, LA, Rodrigue, D, Brenner, FH, Tauxe, RV. Outbreaks of Salmonella enteritidis infections in the United States, 1985–1991. J Infect Dis 1994; 169: 547–52.CrossRefGoogle ScholarPubMed
5.Threlfall, EJ, Powell, NG, Rowe, B. Differentiation of Salmonella by molecular methods. PHLS Microbiol Digest 1995; 11: 199–202.Google Scholar
6.Ward, LR, DeSa, JDH, Rowe, B. A phage-typing scheme for Salmonella enteritidis. Epidemiol Infect 1987; 99: 291–4.CrossRefGoogle ScholarPubMed
7.Adams, MH. Bacteriophages. Interscience Publishers, Inc., 1959.Google Scholar
8.Petter, JG, Vimr, ER. Complete nucleotide sequence of bacteriophage K1F tail gene encoding endo-N-acylneuraminidase (Endo-N) and comparison to an Endo-N Homolog in bacteriophage PK1E. J Bacteriol 1993; 176: 4354–63.Google Scholar
9.Guard-Petter, J, Lakshmi, BSK, Carlson, R, Ingram, K. Characterization of lipopolysaccharide heterogeneity in Salmonella enteritidis by an improved gel electrophoresis method. Appl Environ Microbiol 1995; 61: 2845–51.CrossRefGoogle ScholarPubMed
10.Subbs, AD, Hickman-Brenner, FW, Cameron, DN, Farmer, JJ, 3rd. Differentiation of Salmonella enteritidis phage type 8 strains: evaluation of three additional phage typing systems, plasmid profiles, antibiotic susceptibility patterns, and biotyping. J Clin Microbiol 1994; 32: 199–201.CrossRefGoogle Scholar
11.Stanley, J, Burnens, AP, Threlfall, EJ, Chowdry, N, Goldsworthy, MGenetic relationships among strains of Salmonella enteritidis in a national epidemic in Switzerland. Epidemiol Infect 1992; 108: 213–20.Google Scholar
12.Stanley, J, Goldsworthy, M, Threlfall, EJ. Molecular phylogenetic typing of pandemic isolates of Salmonella enteritidis 1992. FEMS Microbiol Lett 1992; 69: 153–60.CrossRefGoogle Scholar
13.Katauli, M, Seufer, RH, Wollin, R, Kuhn, I, Mollby, RVariations in biochemical phenotypes and phage types of Salmonella enteritidis in Germany 1980–1992. Epidemiol Infect 1993; 11: 199–207.CrossRefGoogle Scholar
14.Petter, JG.Detection of two smooth colony phenotypes in a Salmonella enteritidis isolate which vary in their ability to contaminate eggs. Appi Environ Microbiol 1993; 59: 2884–90.CrossRefGoogle Scholar
15.Reeves, P. 1994. Biosynthesis and assembly of lipopolysaccharide. In Bacterial cell wall. Ghysen, JM, Hakenbeck, R, eds. Vol. 27: 281–317.CrossRefGoogle Scholar
16.Humphrey, TJ, Slater, E, McAlpine, K, Rowbury, RJ, Gilbert, RJ. Salmonella enteritidis PT4 isolates more tolerant of heat, acid or hydrogen peroxide also survive longer on surfaces. Appl Environ Microbiol 1995; 61: 3161–4.CrossRefGoogle ScholarPubMed
17.Portnoy, DA, Moseley, SL, Falkow, S. Characterization of plasmid-associated determinants of Yersinia enterocolitica pathogenesis. Infect Immun 1981; 31: 775–82.CrossRefGoogle ScholarPubMed
18.Gast, RK. Recovery of Salmonella enteritidis from inoculated pools of egg contents. J Food Protect 1993; 56: 21–4.CrossRefGoogle ScholarPubMed
19.Ausubel, F, Brent, R, Kingston, RE, et al. In Current protocols in molecular biology. New York: John Wiley and Sons, 1993.Google Scholar
20.Laemmli, UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227: 680–5.CrossRefGoogle ScholarPubMed
21.Keller, LH, Benson, CE, Garcia, V, Nocks, E, Battenfelder, P, Eckroade, RJMonoclonal antibody-based detection system for Salmonella enteritidis. Avian Dis 1993; 37: 501–7.CrossRefGoogle ScholarPubMed
22.York, WS, Darvill, AG, McNeil, M, Stevenson, TT, Albersheim, P. Isolation and characterization of plant cell walls and cell wall components. Methods Enzymol 1985; 118: 3–40.Google Scholar
23.Darveau, RP, Hancock, REW. Procedure for isolation of bacterial lipopolysaccharides from both smooth and rough Pseudomonas aeruginosa and Salmonella typhimurium strains. J Bacteriol 1983; 155: 831–8.CrossRefGoogle ScholarPubMed
24.Cole, G. Preparation of microfungi for SEM. In Ultrastucture techniques for microorganisms. New York, NY: Plenum Press, 1986.Google Scholar
25.Li, J, Nelson, K, McWhorter, AC, Whittam, TS, Selander, RK. Recombinational basis of serovar diversity in Salmonella enterica. Proc Natl Acad Sci 1994; 91: 2552–6.CrossRefGoogle ScholarPubMed
26.Meyer, TF. Variation in pilin and opacity-associated protein in pathogenic Neisseria species. In The bacteria, vol. 9. New York: Academic Press, 1990.Google Scholar
27.Humphrey, TJ, Rawkins, A, McAlpine, K, Lever, S, Guard-Petter, J, Cox, JM. Isolates of Salmonella enteritidis PT4 with enhanced heat and acid tolerance are more virulent in mice and more invasive in chickens. (In Press.)Google Scholar
28.Massol-Deya, AA, Whallon, J, Hickey, RF, Tiedje, JM. Biofilm architecture: a fortuitous engineering feature. ASM News 1995; 60: 206.Google Scholar
29.Keller, LH, Benson, CE, Krotec, K, Eckroade, RJ. Salmonella enteritidis colonization of the reproductive tract and forming and freshly laid eggs of chickens. Infect Immun 1995; 63: 2443–9.CrossRefGoogle ScholarPubMed
30.Masten, BJ, Joys, TM. Molecular analyses of the Salmonella g… flagellar antigen complex. J Bacteriol 1993; 175: 5359–65.CrossRefGoogle ScholarPubMed
31.Allison, C, Lai, HC, Hughes, C. Coordinate expression of virulence genes during swarm cell differentiation and population migration of Proteus mirabilis. Mol Microbiol 1992; 6: 1583–91.Google ScholarPubMed
32.Allison, C, Jones, P, Emody, L, Hughes, C. The role of swarm cell differentiation and multicellular migration in the uropathogenicity of Proteus mirabilis. J Infect Dis 1994; 169: 1155–8.CrossRefGoogle ScholarPubMed
33.Collinson, SK, Doig, PC, Doran, JL, Cluthier, S, Trust, TJ, Kay, WW. Thin, aggregative fimbriae mediate binding of Salmonella enteritidis to fibronectin. J Bacteriol 1993; 175: 12–8.CrossRefGoogle ScholarPubMed
34.Muscas, P, Rossolini, GM, Chiesurin, A, Santucci, A, Satta, G. Purification and characterization of type-l fimbriae of Salmonella typhi. Microbial Immunol 1994; 38: 353–8.CrossRefGoogle Scholar
35.Cluthier, SC, Collinson, SK, Day, WW. Unique fimbriae like structures encoded by sefD of the sef14 fimbrial gene cluster of Salmonella enteritidis. Mol Microbial 1994; 12: 893–901.Google Scholar
36.Valtonen, MV, Plosila, M, Valtonen, VV, Makela, PH. Effect of the quality of the lipopolysaccharide on mouse virulence of Salmonella enteritidis. Infect Immun 1975; 12: 828–32.CrossRefGoogle ScholarPubMed
37.Jimenez-Lucho, VE, Leive, LL. Role of the O-antigen of lipopolysaccharide in Salmonella in protection against complement action. In The bacteria, vol. 9. New York: Academic Press, 1990.Google Scholar
38.Wandersman, C, Delepelaire, P TolC. an Escherichia coli outer membrane protein required for hemolysin secretion. Proc Natl Acad Sci USA 1990; 87: 4776–80.CrossRefGoogle ScholarPubMed
39.Stone, BJ, Miller, V. Salmonella enteritidis has a homologue of toiC that is required for virulence in BALB/c mice. Mol Microbiol 1995; 17: 701–12.CrossRefGoogle Scholar
40.Wandersman, C, Letoffe, S. Involvement of lipopolysaccharides in the secretion of Escherichia coli alphahemolysin and Erwinia chrysanthemi proteases. Mol Microbiol 1993; 7: 141–50.CrossRefGoogle Scholar
41.Koranakis, V, Hughes, C. Secretion of hemolysin and other proteins out of the gram-negative bacterial cell. In Bacterial cell wall. Ghysen, JM, Hakenbeck, R. eds, vol. 27. New York: Elsevier, 1994: 425–46.CrossRefGoogle Scholar
42.Slauch, JM, Mahan, MJ, Mekalanos, JJ. In vivo expression technology for selection of bacterial genes specifically induced in host tissues. Methods Enzymol 1994; 235: 481–92.CrossRefGoogle ScholarPubMed
43.Hormaeche, CE, Joysey, HS, Desilva, L, Izhar, M, Stocker, BA. Immunity induced by live attenuated Salmonella vaccines. Res Microbiol 1990; 141: 757–64.CrossRefGoogle ScholarPubMed
44.Barrow, PA, Lovell, MA, Berchieri, A. The use of two live attenuated vaccines to immunize egg-laying hens against Salmonella enteritidis phage type 4. Avian Path 1991; 20: 681–92.Google ScholarPubMed
45.Hinton, M, Pearson, GR, Threlfall, EJ, Rowe, B. Experimental Salmonella enteritidis infection in chicks. Vet Rec 1989; 124: 223.CrossRefGoogle ScholarPubMed
46.Hinton, M, Threlfall, EJ, Rowe, B. The invasiveness of different strains of Salmonella enteritidis phage type 4 for young chickens. FEMS Microbiol Lett 1990; 70: 193–6.Google Scholar
47.Cox, JM, Woolcock, JB. Lipopolysaccharide expression and virulence in mice of Australian isolates of Salmonella enteritidis. Lett Appl Microbiol 1994; 19: 95–8.CrossRefGoogle Scholar