Skip to main content
SpringerLink
Log in

Sialic Acid-Containing Lipopolysaccharides of Salmonella O48 Strains—Potential Role in Camouflage and Susceptibility to the Bactericidal Effect of Normal Human Serum

  • Host Microbe Interactions
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Sialic acid (N-acetylneuraminic acid, NeuAc) plays an essential role in protecting gram-negative bacteria against the bactericidal activity of serum and may contribute to the pathogenicity of bacteria by mimicking epitopes that resemble host tissue components (molecular mimicry). The role of sialic acid (NeuAc)-containing lipopolysaccharides (LPS) of Salmonella O48 strains in the complement activation of normal human serum (NHS) was investigated. NeuAc-containing lipooligosaccharides cause a downregulation of complement activation and may serve to camouflage the bacterial surface from the immunological response of the host. Serotype O48 Salmonella strains have the O-antigen structure containing NeuAc while its serovars differ in outer membrane protein composition. In this study, the mechanisms of complement activation responsible for killing Salmonella O48 serum-sensitive rods by NHS were established. Four of such mechanisms involving pathways, which are important in the bactericidal mechanism of complement activation, were distinguished: only the classical/lectin pathways, independent activation of the classical/lectin or alternative pathway, parallel activation of the classical/lectin and alternative pathways, and only the alternative pathway important in the bactericidal action of human serum. To further study the role of NeuAc, its content in bacterial cells was determined by gas-liquid chromatography-mass spectrometry in relation to 3-deoxy-D-manno-2-octulosonic acid (Kdo), an inherent constituent of LPS. The results indicate that neither the presence of sialic acid in LPS nor the length of the O-specific part of LPS containing NeuAc plays a decisive role in determining bacterial resistance to the bactericidal activity of complement and that the presence of sialic acid in the structure of LPS is not sufficient to block the activation of the alternative pathway of complement. We observed that for three strains with a very high NeuAc/Kdo ratio the alternative pathways were decisive in the bactericidal action of human serum. The results indicated that those strains are not capable of inhibiting the alternative pathway very effectively. As the pathogenicity of most Salmonella serotypes remains undefined, research into the interactions between these bacterial cells and host organisms is indispensable.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

References

  1. Bugla-Płoskońska G, Kiersnowski A, Futoma-Kołoch B, Doroszkiewicz W (2009) Killing of gram-negative bacteria with normal human serum and normal bovine serum: use of lysozyme and complement protein in the death of Salmonella strains O48. Microb Ecol 58:276–289

    Article  PubMed  Google Scholar 

  2. Bugla-Płoskońska G, Doroszkiewicz W (2006) Bactericidal activity of normal bovine serum (NBS) directed against some Enterobacteriaceae with sialic acid-containing lipopolysaccharides (LPS) as a component of cell wall. Pol J Microb 55:169–174

    Google Scholar 

  3. Bugla-Płoskońska G, Cisowska A, Karpińska K, Jankowski S, Doroszkiewicz W (2006) The mechanisms of the activation of normal human serum complement by Escherichia coli strains with K1 surface antigen. Folia Microbiol 51:627–632

    Article  Google Scholar 

  4. Bugla-Płoskońska G, Korzeniowska-Kowal A, Gamian A, Doroszkiewicz W (2004) Bactericidal activity of serum against Salmonella O48 serovars. Int J Antimicrobiol Ag 24:203

    Google Scholar 

  5. Ciurana B, Tomás JM (1987) Role of lipopolysaccharide and complement in susceptibility of Klebsiella pneumoniae to nonimmune serum. Infect Immun 11:2741–2746

    Google Scholar 

  6. Doroszkiewicz W (1997) Mechanism of antigenic variation in Shigella flexneri bacilli. IV. Role lipopolysaccharides and their components in the sensitivity of Shigella flexneri 1b and its Lac + recombinant to killing action of serum. Arch Immunol Ther Exp 45:235–242

    CAS  Google Scholar 

  7. Edinger D, Bello E, Mates A (1977) The heterocytotoxicity of human serum. I. Activation of the alternative complement pathway by heterologous target cells. Cell Immunol 29:174–186

    Article  Google Scholar 

  8. Erridge C, Bennett-Guerrero E, Paxton IR (2002) Structure and function of lipopolysaccharides. Microb Infect 4:837–851

    Article  CAS  Google Scholar 

  9. Fine DP, Marney SR, Colley DG, Sergent JS, Des Prez RM (1972) C3 shunt activation in human serum chelated with EGTA. J Immunol 109:807–809

    CAS  PubMed  Google Scholar 

  10. Gamian A, Jones C, Lipiński T, Korzeniowska-Kowal A, Ravenscroft N (2000) Structure of the sialic acid-containing O-specific polysaccharide from Salmonella enterica serovar Toucra O48 lipopolysaccharide. Eur J Biochem 267:3160–3167

    Article  CAS  PubMed  Google Scholar 

  11. Gamian A, Kenne L (1993) Analysis of 7-substituted sialic acid in some enterobacterial lipopolysaccharides. J Bacteriol 175:1508–1513

    CAS  PubMed  Google Scholar 

  12. Gamian A, Romanowska A, Romanowska E (1992) Immunochemical studies on sialic acid-containing lipopolysaccharides from enterobacterial species. FEMS Microbiol Immunol 89:323–328

    Article  Google Scholar 

  13. Giammanco GM, Pignato S, Mammina C, Grimont F, Grimont PA, Nastasi A, Giammanco G (2002) Persistent endemicity of Salmonella bongori 48:z35 in Southern Italy: molecular characterization of human, animal and environmental isolates. J Clin Microbiol 9:3502–3505

    Article  Google Scholar 

  14. Grimond PD, Weill FX (2007) Antigenic formulae of the Salmonella serovars, 9th ed.WHO Collaborating Centre for Reference and Research on Salmonella

  15. Holland MCH, Lambris JD (2005) Complement: Encyclopedia of life sciences. Wiley, UK

    Google Scholar 

  16. Joiner KA, Hammer CH, Brown EJ, Cole RJ, Frank MM (1982) Studies on the mechanism of bacterial resistance to complement mediated-killing. I. Terminal complement components are deposited and released from Salmonella Minnesota S218 without causing bacterial death. J Exp Med 155:797–808

    Article  CAS  PubMed  Google Scholar 

  17. Koistinen V (1992) Limited tryptic cleavage of complement factor H abrogates recognition of sialic acid-containing surfaces by the alternative pathway of complement. Biochem J 283:317–319

    CAS  PubMed  Google Scholar 

  18. Meri S, Pangburn MK (1990) Discrimination between activators and nonactivators of the alternative pathway of complement: regulation via a sialic acid/polyanion binding site on factor H. Proc Natl Acad Sci USA 87:3982–3986

    Article  CAS  PubMed  Google Scholar 

  19. Mielnik G, Gamian A, Doroszkiewicz W (2001) Bactericidal activity of normal cord serum (NCS) against Gram-negative rods with sialic acid-containing lipopolysaccharides (LPS). FEMS Immunol Med Microbiol 31:169–173

    Article  CAS  PubMed  Google Scholar 

  20. Moran AP, Prendergast MM, Appelmelk BJ (1996) Molecular mimicry of host structures by bacterial lipopolysaccharides and its contribution to disease. FEMS Immunol Med Microbiol 16:105–115

    Article  CAS  PubMed  Google Scholar 

  21. Odumeru JA, Wiseman GM, Ronald AR (1985) Role of lipopolysaccharide and complement in susceptibility of Haemophilus ducrei to human serum. Infect Immun 50:495–499

    CAS  PubMed  Google Scholar 

  22. Ourth DD, Bachinski LM (1987) Bacterial sialic acid modulates activation of the alternative complement pathway of channel catfish (Ictalurus punctatus). Dev Comp Immunol 11:551–564

    Article  CAS  PubMed  Google Scholar 

  23. Prescott LM, Harley JP, Klein DA (2002) Microbiology, 5th edn. McGraw-Hill, Boston

    Google Scholar 

  24. Ram S, Sharma AK, Simpson SD, Gulati S, Mcquillen DP, Pangburn MK, Rice PA (1998) A novel sialic acid binding site on factor H mediates serum resistance of sialylated Neisseria gonorrhoeae. J Exp Med 187:743–752

    Article  CAS  PubMed  Google Scholar 

  25. Rautemaa R, Meri S (1999) Complement-resistance mechanisms of bacteria. Microb Infect 1:785–794

    Article  CAS  Google Scholar 

  26. Ringenberg MA, Steenbergen SM, Vimr ER (2003) The first committed step in the biosynthesis of sialic acid by Escherichia coli K1 does not involve a phosphorylated N-acetylmannosamine intermediate. Mol Microbiol 50:961–975

    Article  CAS  PubMed  Google Scholar 

  27. Rybka J, Gamian A (2006) Determination of endotoxin by the measurement of the acetylated methyl glycoside derivative of Kdo with gas–liquid chromatography-mass spectrometry. J Microbiol Meth 64:171–184

    Article  CAS  Google Scholar 

  28. Schmidt BZ, Colten HR (2000) Complement: a critical test of its biological importance. Immunol Rev 178:166–176

    Article  CAS  PubMed  Google Scholar 

  29. Schröter M, Roggentin P, Hofman J, Speicher A, Laufs R, Mack D (2004) Pet snakes as a reservoir for Salmonella enterica subsp. diarizonae (serogroup IIIb): a prospective study. Appl Environ Microb 70:613–615

    Article  Google Scholar 

  30. Selander B, Martensson U, Wientraub A, Holmström E, Matsushita M, Thiel S, Jensenius JC, Truedsson L, Sjöholm AG (2006) Mannan-binding lectin activates C3 and the alternative complement pathway without involvement of C2. J Clin Invest 116:1425–1434

    Article  CAS  PubMed  Google Scholar 

  31. Ślopek S (1970) Immunologia praktyczna. Państwowy Zakład Wydawnictw Lekarskich, Warszawa in Polish

    Google Scholar 

  32. Taylor PW (1983) Bactericidal and bacteriolytic activity of serum against gram-negative bacteria. Microb Rev 1:46–83

    Google Scholar 

  33. Taylor PW, Kroll HP, Tomlinson S (1982) Effect of subinhibitory concentrations of mecillinam on expression of Escherichia coli surface components associated with serum resistance. Drugs Exp Clin Res 8:625–631

    CAS  Google Scholar 

  34. Taylor PW, Gaunt H, Unger FM (1981) Effect of subinhibitory concentration of meticillinam on the serum susceptibility of Escherichia coli strains. Antimicrob Ag Chemother 19:786–788

    CAS  Google Scholar 

  35. Uzzau S, Brown DJ, Wallis T, Rubino S, Leori G, Bernerd S, Casadesus J, Platt DJ, Olsen JE (2000) Host adapted serotypes of Salmonella enterica. Epidemiol Infect 125:229–255

    Article  CAS  PubMed  Google Scholar 

  36. Waterman SH, Juarez G, Carr SJ, Kilman L (1990) Salmonella ariozona infections in Latinos associated with rattlesnake folk medicine. Am J Pub Health 80:286–289

    Article  CAS  Google Scholar 

  37. World Health Organization. Drug-resistant Salmonella. Fact sheet N°139. Revised April 2005

  38. World Health Organization. Food and Agriculture Organization of the United Nations. FAO/WHO Expert Meeting on Salmonella and Campylobacter in chicken meat. FAO Headquarters, Rome, Italy, 4–9 May 2009

Download references

Author information

Authors and Affiliations

  1. Department of Microbiology, Institute of Genetics and Microbiology, University of Wrocław, Przybyszewskiego 63/77, 51-148, Wrocław, Poland

    Gabriela Bugla-Płoskońska, Bożena Futoma-Kołoch & Włodzimierz Doroszkiewicz

  2. Ludwik Hirszfeld Institute of Immunology and Experimental Therapy, Polish Academy of Sciences, Weigla 12, 53-114, Wrocław, Poland

    Jacek Rybka & Andrzej Gamian

  3. Department of Biology and Medical Parasitology, Medical University, Radeckiego 9, 50-367, Wrocław, Poland

    Agnieszka Cisowska

  4. Department of Medical Biochemistry, Medical University, Wroclaw, Poland

    Andrzej Gamian

  5. Institute of Genetics and Microbiology, University of Wroclaw, Przybyszewskiego 63/72, 51-148, Wroclaw, Poland

    Gabriela Bugla-Płoskońska

Authors
  1. Gabriela Bugla-Płoskońska
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jacek Rybka
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bożena Futoma-Kołoch
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Agnieszka Cisowska
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Andrzej Gamian
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Włodzimierz Doroszkiewicz
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gabriela Bugla-Płoskońska.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bugla-Płoskońska, G., Rybka, J., Futoma-Kołoch, B. et al. Sialic Acid-Containing Lipopolysaccharides of Salmonella O48 Strains—Potential Role in Camouflage and Susceptibility to the Bactericidal Effect of Normal Human Serum. Microb Ecol 59, 601–613 (2010). https://doi.org/10.1007/s00248-009-9600-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-009-9600-2

Keywords

Search

Navigation