Skip to main content
SpringerLink
Log in

Changes associated with cell membrane composition of Staphylococcus aureus on acquisition of resistance against class IIa bacteriocin and its in vitro substantiation

  • Original Paper
  • Published:
European Food Research and Technology Aims and scope Submit manuscript

Abstract

The emergence and spread of bacteria resistant to bacteriocins would threaten the safety of using them as food preservatives. To determine the physiological characteristics of resistant strain, resistance of Staphylococcus aureus NCDC 133 against pediocin, a class IIa bacteriocin, was isolated. A significant amplification in unsaturated fatty acid and hydroxy fatty acid in addition to branched chain fatty acid was observed in resistant which validates enhanced fluid membrane of resistant strain. Increased membrane fluidity leads to unstable oligomerization of bacteriocin which ceases pore formation. The composition of the phospholipids in resistant strain also differed from those in the wild-type strain. The putative zwitterionic amino-containing phospholipid in the resistant significantly increased, whereas amounts of amino-lacking phospholipids decreased which could be correlated to reduced negative charge making bacteriocin unable to associate optimally with bacterial membrane. Increased percent colorimetric response in resistant variant indicates that bacteriocin was positioned predominantly at the lipid–water interface rather than penetrating deep inside. Both physiological study and in vitro results confirm membrane changes during resistance acquisition which could be utilized to establish structure activity relationship and henceforth to develop potent peptide with suitable amino acid substitutes with enhanced stability and activity features.

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

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Bayer AS, Prasad R, Chandra J, Koul A et al (2000) In vitro resistance of Staphylococcus aureus to thrombin-induced platelet microbicidal protein is associated with alterations in cytoplasmic membrane fluidity. Infect Immun 68(6):3548–3553

    Article  CAS  Google Scholar 

  2. Bligh EG, Dyer EJ (1959) A rapid method for total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    Article  CAS  Google Scholar 

  3. Cabo ML, Murado MA, González MP, Pastoriza L (1999) A method for bacteriocin quantification. J Appl Microbiol 87(6):907–914

    Article  CAS  Google Scholar 

  4. Collins LV, Kristian A, Weidenmaier C, Faigle M et al (2002) Staphylococcus aureus strains lacking D-alanine modifications of teichoic acids are highly susceptible to human neutrophil killing and are virulence attenuated in mice. J Infect Dis 186:214–219

    Article  CAS  Google Scholar 

  5. Chen Y, Ludescher RD, Montville TJ (1998) Influence of lipid composition on pediocin PA-1 binding to phospholipid vesicles. Appl Environ Microbiol 64:3530–3532

    CAS  Google Scholar 

  6. Crandall AD, Montville TJ (1998) Nisin resistance in Listeria monocytogenes ATCC 700302 is a complex phenotype. Appl Environ Microbiol 64:231–237

    CAS  Google Scholar 

  7. Gidalevitz D, Ishitsuka Y, Muresan AS, Konovalov O et al (2003) Interaction of antimicrobial peptide protegrin with biomembranes. PNAS 100(11):6302–6307

    Article  CAS  Google Scholar 

  8. Jenssen H, Gutteberg TJ, Lejon T (2006) Modelling the anti-herpes simplex virus activity of small cationic peptides using amino acid descriptors. J Pept Res 66(1):48–56

    Google Scholar 

  9. Katz SS, Weinrauch Y, Munford RS, Weiss EP (1999) Deacylation of LPS in whole E. coli during destruction by cellular and extracellular components of a rabbit peritoneal inflammatory exudate. J Biol Chem 274:36579–36584

    Article  CAS  Google Scholar 

  10. Kolusheva S, Boyer L, Jelinek R (2000) A colorimetric assay for rapid screening of antimicrobial peptides. Nat Biotechnol 18:225–227

    Article  CAS  Google Scholar 

  11. Lehrer RI, Ganz T (2002) Defensins of vertebrate animals. Curr Opin Immunol 14:96–102

    Article  CAS  Google Scholar 

  12. Levy SB (1998) Antibiotic resistance: an ecological imbalance. In: Chadwick DJ, Good J (eds) Antibiotic resistance: origins, evolution, selection and spread. Wiley, Chichester, pp 1–14

    Google Scholar 

  13. Li J, Chikindas ML, Ludescher RD, Montville TJ (2002) Temperature and surfactant induced membrane modifications that alter Listeria monocytogenes nisin sensitivity by different mechanisms. Appl Environ Microbiol 68(12):5904–5910

    Article  CAS  Google Scholar 

  14. Limonet M, Junelles AM, Milliere JB (2002) Variations in the membrane fatty acid composition of resistant or susceptible Leuconostoc or Weissela strains in presence or absence of Mesenterocin 52A and Mesenterocin 52B produced by Leuconostoc mesenteroides subsp. Mesenteroides FR52. Appl Enrivon Microbiol 68:2910–2916

    Article  CAS  Google Scholar 

  15. Loir YL, Baron F, Gautier M (2003) Staphylococcus aureus and food poisoning. Genet Mol Res 2(1):63–76

    Google Scholar 

  16. Lowy FD (1998) Staphylococcus aureus infections. N Engl J Med 339:520–532

    Article  CAS  Google Scholar 

  17. Mazzotta AS, Montville TJ (1997) Nisin induces changes in membrane fatty acid composition of Listeria monocytogenes nisin-resistant strains at 10°C and 30°C. J Appl Microbiol 82:32–38

    Article  CAS  Google Scholar 

  18. Mehla J, Sood SK (2011) Acidic pH enhances activity/yield of an YGNGV motif containing antimicrobial peptide isolated and purified from Pediococcus pentosaceus NCDC 273, a dairy strain. Int J Prob Preb 6(2):81–88

    Google Scholar 

  19. Mehla J, Sood SK (2011) Substantiation in Enterococcus faecalis of dose-dependent resistance and cross-resistance to pore-forming antimicrobial peptides by use of a polydiacetylene-based colorimetric assay. Appl Environ Microbiol 77(3):786–793

    Article  CAS  Google Scholar 

  20. Okada S, Peng S, Spevak W, Charych D (1998) Color and chromism of polydiacetylene vesicles. Acc Chem Res 31:229–239

    Article  CAS  Google Scholar 

  21. Peschel A (2002) How do bacteria resist human antimicrobial peptides? Trends Microbiol 10:179–186

    Article  CAS  Google Scholar 

  22. Peschel A, Sahl HG (2006) The co-evolution of host cationic antimicrobial peptides and microbial resistance. Nat Rev Microbiol 4:529–536

    Article  CAS  Google Scholar 

  23. Peschel A, Otto M, Jack RW, Kalbacher H et al (1999) Determination of impact on bactericidal activity, in vitro secondary structure, and membrane interaction. Appl Environ Microbiol 70:4672–4680

    Google Scholar 

  24. Peschel A, Jack RW, Otto M, Collins LV et al (2001) Membrane phospholipid composition in nisin-resistant Listeria monocytogenes Scott A. Mol Res 2(1):63–76

    Google Scholar 

  25. Rekhiff N, Atrih A, Lefebvre G (1994) Characterization and partial purification of plantaricin LC74, a bacteriocin produced by Lactobacillus plantarum LC74. Biotech Lett 16(8):771–776

    Article  Google Scholar 

  26. Sahl H, Pag U, Bonness U, Wagner S et al (2005) Mammalian defensins: structure and mechanism of antibiotic activity. J Leukocyte Biol 77:466–475

    Article  CAS  Google Scholar 

  27. Sakayori Y, Muramatsu M, Hanada S, Kamagata Y et al (2003) Characterization of Enterococcus faecium mutants resistant to mundticin KS, a class IIa bacteriocin. Microbiol 149:2901–2908

    Article  CAS  Google Scholar 

  28. Satchell DP, Sheynis T, Shirafuji Y, Kolusheva S et al (2003) Interactions of mouse paneth cell α-defensins and α-defensin precursors with membranes: prosegment inhibition of peptide association with biomimetic membranes. J Biol Chem 278:13838–13846

    Article  CAS  Google Scholar 

  29. Sheynis T, Sykora J, Benda A, Kolusheva S et al (2003) Bilayer localization of membrane-active peptides studied in biomimetic vesicles by visible and fluorescence spectroscopies. Eur J Biochem 270:4478–4487

    Article  CAS  Google Scholar 

  30. Staubiz P, Neumann H, Schneider T, Weidemann I et al (2004) MprF mediated biosynthesis of lysylphosphatidyl glycerol, an important determinant in staphylococcal defensing resistance. FEMS Microbiol Lett 231:67–71

    Article  Google Scholar 

  31. Thippeswamy HS, Sood SK, Venkateswarlu R, Raj I (2009) Membranes of five-fold alamethicin-resistant Staphylococcus aureus, Enterococcus faecalis and Bacillus cereus show decreased interactions with alamethicin due to changes in membrane fluidity and surface charge. Ann Microbiol 59(3):593–601

    Article  CAS  Google Scholar 

  32. Vadyvaloo V, Hastings JW, van der Merwe MJ, Rautenbach M (2002) Membranes of class IIa bacteriocin-resistant Listeria monocytogenes cells contain increased levels of desaturated and shortacyl-chain phosphatidylglycerols. Appl Environ Microbiol 8:5223–5230

    Article  Google Scholar 

  33. Verheul A, Russel NJ, Vanthof R, Rombouts FM, Abee T (1997) Modifications of membrane phospholipid composition in nisin resistant Listeria monocytogenes Scott A. Appl Environ Microbiol 63:3451–3457

    CAS  Google Scholar 

  34. Wu CW, Yin LJ, Jiang ST (2004) Purification and characterization of bacteriocin form Pediococcus pentosaceus ACCEL. J Agric Food Chem 52:1146–1154

    Article  CAS  Google Scholar 

  35. Younsi M, Ramandraibe E, Bonaly R, Donner M, Coulon J (2000) Amphotericin B resistance add membrane fluidity in Kluyveromyces lactics strains. Antimicrob Agents Chemother 44:1911–1916

    Article  CAS  Google Scholar 

Download references

Conflict of interest

None.

Compliance with Ethics Requirements

This article does not contain any studies with human or animal subjects.

Author information

Authors and Affiliations

  1. Animal Biochemistry Division, National Dairy Research Institute, Karnal, 132001, Haryana, India

    Puja Lather, Anita Kumari Garsa & S. K. Sood

  2. Animal Biotechnology Division, National Dairy Research Institute, Karnal, 132001, Haryana, India

    A. K. Mohanty

  3. Dairy Cattle Nutrition Division, National Dairy Research Institute, Karnal, 132001, Haryana, India

    Pankaj Jha

Authors
  1. Puja Lather
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. K. Mohanty
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pankaj Jha
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anita Kumari Garsa
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. S. K. Sood
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Puja Lather.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lather, P., Mohanty, A.K., Jha, P. et al. Changes associated with cell membrane composition of Staphylococcus aureus on acquisition of resistance against class IIa bacteriocin and its in vitro substantiation. Eur Food Res Technol 240, 101–107 (2015). https://doi.org/10.1007/s00217-014-2311-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00217-014-2311-z

Keywords

Search

Navigation