Skip to main content
Log in

Permeabilization and lysis induced by bacteriocins and its effect on aldehyde formation by Lactococcus lactis

  • Original paper
  • Published:
Biotechnology Letters Aims and scope Submit manuscript

Abstract

Permeabilization induced by lacticin 3147, lactococcins A, B and M, enterocin AS-48 and nisin, bacteriocins described as cell membrane-pore forming and lytic agents, enhanced in all cases aldehyde formation by Lactococcus lactis IFPL730. Nevertheless, the conversion of isoleucine into 2-methylbutyraldehyde depended not only on the degree of permeabilization but also on the bacteriocin that caused the cell membrane damage. The highest values of 2-methylbutyraldehyde corresponded to cell suspensions containing lacticin 3147 and lactococcins, treatments that provoked further lysis in addition to induced permeabilization.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abee T (1995) Pore-forming bacteriocins of Gram-positive bacteria and self-protection mechanisms of producer organisms. FEMS Microbiol Lett 129:1–10

    PubMed  CAS  Google Scholar 

  • Abriouel H, Valdivia E, Gálvez A, Maqueda M (2001) Influence of physico-chemical factors on the oligomerization and biological activity of bacteriocin AS-48. Curr Microbiol 42:89–95

    PubMed  CAS  Google Scholar 

  • Atiles MW, Dudley E, Steele J (2000) Gene cloning, sequencing and inactivation of the branched chain aminotransferase of Lactococcus lactis LM0230. Appl Environ Microbiol 66:2325–2329

    Article  PubMed  CAS  Google Scholar 

  • Bauer R, Dicks LMT (2005) Mode of action of lipid II-targeting lantibiotics. Int J Food Microbiol 101:201–216

    Article  PubMed  CAS  Google Scholar 

  • Ben Amor K, Breeuwer P, Verbaarschot P, Rombouts FM, Akkermans ADL, de Vos WM, Abee T (2002) Multiparametric flow cytometry and cell sorting for the assessment of viable, injured, and dead Bifidobacterium cells during bile salt stress. Appl Environ Microbiol 68:5209–5216

    Article  CAS  Google Scholar 

  • Bierbaum G, Sahl HG (1987) Autolytic system of Staphylococcus simulans 22: influence of cationic peptides on activity of N-acetylmuramoyl-l-alanine amidase. J␣Bacteriol 169:5452–5458

    PubMed  CAS  Google Scholar 

  • Bourdat-Deschamps M, Le Bars D, Yvon M, Chapot-Chartier MP (2004) Autolysis of Lactococcus lactis AM2 stimulates the formation of certain aroma compounds from amino acids in a cheese model. Int Dairy J 14:791–800

    Article  CAS  Google Scholar 

  • Bunthof CJ, Van Schalkwijk S, Meijer W, Abee T, Hugenholtz J (2001) Fluorescent method for monitoring cheese starter permeabilization and lysis. Appl Environ Microbiol 67:4264–4271

    Article  PubMed  CAS  Google Scholar 

  • Casla D, Requena T, Gómez R (1996) Antimicrobial activity of lactic acid bacteria isolated from goat’s milk and artisanal cheeses: characterisitcs of a bacteriocin produced by Lactobacillus curvatus IFPL105. J␣Appl Bacteriol 81:35–41

    PubMed  CAS  Google Scholar 

  • Chapot-Chartier MP, Deniel C, Rousseau M, Vassal L, Gripon JC (1994) Autolysis of two strains of Lactococcus lactis during cheese ripening. Int Dairy J 4:251–269

    Article  CAS  Google Scholar 

  • Daeschel MA (1993) Applications and interactions of bacteriocins from lactic acid bacteria in foods and beverages. In: Hoover D, Steenson L (eds) Bacteriocins of lactic acid bacteria. Academic Press, New York, N.Y., pp 63–91

    Google Scholar 

  • De la Plaza M, Fernández de Palencia P, Peláez C, Requena T (2004) Biochemical and molecular characterization of α-ketoisovalerate decarboxylase, an enzyme involved in the formation of aldehydes from amino acids by Lactococcus lactis. FEMS Microbiol Lett 238:367–374

    Article  Google Scholar 

  • Fernández de Palencia P, de la Plaza M, Mohedano ML, Martínez-Cuesta MC, Requena T, López P, Peláez C (2004) Enhancement of 2-methylbutanal formation in cheese by using a fluorescently tagged Lacticin 3147 producing Lactococcus lactis strain. Int J Food Microbiol 93:335–347

    Article  CAS  Google Scholar 

  • Gálvez A, Maqueda M, Martínez-Bueno M, Valdivia E (1991) Permeation of bacterial cells, permeation of cytoplasmic and artificial membrana vesicles, and channel formation on lipid bilayers by peptide antibiotic AS-48. J Bacteriol 173:886–892

    PubMed  Google Scholar 

  • Gálvez A, Valdivia E, Martínez-Bueno M, Maqueda M (1990) Induction of autolysis in Enterococcus faecalis S-47 by peptide AS-48. J Appl Bacteriol 69:406–413

    PubMed  Google Scholar 

  • Gao S, Mooberry ES, Steele JL (1998) Use of 13C Nuclear magnetic resonance and gas chromatography to examine methionine catabolism in lactococci. Appl Environ Microbiol 64:4670–4675

    PubMed  CAS  Google Scholar 

  • Garde S, Gaya P, Medina M, Nuñez M (1997) Acceleration of flavour formation in cheese by a bacteriocin-producing adjunct lactic culture. Biotechnol Lett 19:1011–1014

    Article  CAS  Google Scholar 

  • Hurst A (1981) Nisin. Adv Appl Microbiol 27:25–163

    Google Scholar 

  • Joux F, Lebaron P (2000) Use of fluorescent probes to assess physiological functions of bacteria at a single-cell level. Microbes Infect 2:1523–1535

    Article  PubMed  CAS  Google Scholar 

  • Kabuki T, Saito T, Kawai Y, Uemura J, Itoh T (1997) Production, purification and characterization of reutericin 6, a bacteriocin with lytic activity produced by Lactobacillus reuteri LA6. Int J Food Microbiol 34:145–156

    Article  PubMed  CAS  Google Scholar 

  • Kok J, Holo H, van Belkum MJ, Haandrikman AJ, Nes IF (1993) Non nisin bacteriocins in lactococci: biochemistry, genetics and mode of action. In: Hoover D, Steenson L (eds) Bacteriocins of lactic acid bacteria. Academic Press, New York, N.Y., pp 121–150

    Google Scholar 

  • Kuntz DA, Chen JL, Pan G (1998) Accumulation of α-ketoacids as essential components in cyanide assimilation by Pseudomonas fluorescens. Appl Environ Microbiol 64:4452–4459

    Google Scholar 

  • Langsrud T, Landaas A, Castberg HB (1987) Autolytic properties of different strains of group N streptococci. Milchwiss 42:556–560

    Google Scholar 

  • Liu W, Hansen NJ (1990) Some chemical and physical properties of nisin, a small-protein antibiotic produced by Lactococcus lactis. Appl Environ Microbiol 56:2551–2558

    PubMed  CAS  Google Scholar 

  • Lortal S, Chapot-Chartier MP (2005) Role, mechanisms and control of lactic acid bacteria lysis in cheese. Int Dairy J 15:857–871

    Article  CAS  Google Scholar 

  • Martínez-Cuesta MC, Kok J, Herranz E, Peláez C, Requena T, Buist G (2000) Requirement of autolytic activity for bacteriocin induced lysis. Appl Environ Microbiol 66:3174–3179

    Article  PubMed  Google Scholar 

  • Martínez-Cuesta MC, Requena T, Peláez C (2001) Use of a bacteriocin-producing transconjugant as starter in acceleration of cheese ripening. Int J Food Microbiol 70:79–88

    Article  PubMed  Google Scholar 

  • Martínez-Cuesta MC, Requena T, Peláez C (2006) Cell membrane damage induced by lacticin 3147 enhances aldehyde formation in Lactococcus lactis IFPL730. Int J Food Microbiol (in press) Doi:10.1016/j.ijfoodmicro.2006.01.028

  • Moll G, Hildeng-Hauge H, Nissen-Meyer J, Nes IF, Konings WN, Driessen AJM (1998) Mechanistic properties of the two-component bacteriocin lactococcin G. J Bacteriol 180:96–99

    PubMed  CAS  Google Scholar 

  • Morgan SM, O’Connor PM, Cotter PD, Ross RP, Hill C (2005) Sequential actions of the two component peptides of the lantibiotic lacticin 3147 explains its antimicrobial activity at nanomolar concentrations. Antimicrob Ag Chemother 49:2606–2611

    Article  CAS  Google Scholar 

  • Morgan S, Ross RP, Hill C (1995) Bacteriolytic activity caused by the presence of a novel lactococcal plasmid encoding lactococcins A, B, and M. Appl Environ Microbiol 61:2995–3001

    PubMed  CAS  Google Scholar 

  • Morgan S, Ross RP, Hill C (1997) Increasing starter cell lysis in Cheddar cheese using a bacteriocin-producing adjunct. J Dairy Sci 80:1–10

    Article  CAS  Google Scholar 

  • Rijnen L, Bonneau S, Yvon M (1999) Genetic characterization of the major lactococcal aromatic aminotransferase and its involvement in conversion of amino acid to aroma compounds. Appl Environ Microbiol 65:4873–4880

    PubMed  CAS  Google Scholar 

  • Ruhr E, Sahl HG (1985) Mode of action of the peptide antibiotic nisin and influence on the membrane potential of whole cells and on cytoplasmic and artificial membrane vesicles. Antimicrob Ag Chemother 27:841–845

    CAS  Google Scholar 

  • Schmidt RH, Davidson SM, Lowry SP (1983) Determination of acetaldehyde in Streptococcus lactis cultures as 2,4-dinitrophenylhydrazone by high-performance liquid chromatography. J Agr Food Chem 31:978–980

    Article  CAS  Google Scholar 

  • Smit BA, van Hylcklama Vlieg JET, Engels WJM, Meijer L, Wouters JTM, Smit G (2005) Identification, cloning and characterization of a Lactococcus lactis branched-chain α-keto acid decarboxylase involved in flavor formation. Appl Environ Microbiol 71:303–311

    Article  PubMed  CAS  Google Scholar 

  • Umemoto Y, Sato Y, Kito J (1978) Direct observation of fine-structures of bacteria in ripened cheddar cheese by electron-microscopy. J Biol Chem 42:227–232

    Google Scholar 

  • Yvon M, Thirouin S, Rijnen L, Fromentier D, Gripon JC (1997) An aminotransferase from Lactococcus lactis initiates conversion of amino acids to cheese flavour compounds. Appl Environ Microbiol 63:414–419

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the Research Project CICYT AGL2002-03277. The authors also would like to thank Prof. Dr. Jan Kok and Dr.␣Margarita Medina for kindly providing microorganisms L. lactis subsp. cremoris B94 and Enterococcus faecalis INIA4, respectively, and Pedro Lastres for their assistance with the Flow Cytometry analyses.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. Carmen Martínez-Cuesta.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Martínez-Cuesta, M.C., Requena, T. & Peláez, C. Permeabilization and lysis induced by bacteriocins and its effect on aldehyde formation by Lactococcus lactis . Biotechnol Lett 28, 1573–1580 (2006). https://doi.org/10.1007/s10529-006-9131-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10529-006-9131-6

Keywords

Navigation