Skip to main content

Advertisement

SpringerLink
Log in

Leuconostoc mesenteroides SJRP55: A Bacteriocinogenic Strain Isolated from Brazilian Water Buffalo Mozzarella Cheese

  • Published:
Probiotics and Antimicrobial Proteins Aims and scope Submit manuscript

Abstract

The production of bacteriocins by Leuconostoc mesenteroides represents an important opportunity for exploration of their potential use for industrial purpose. The antimicrobial compounds produced by L. mesenteroides subsp. mesenteroides SJRP55 strain were characterized and purified. Cell-free supernatant of Leuc. mesenteroides subsp. mesenteroides SJRP55 produced antibacterial compounds against Listeria spp. strains and not inhibiting against Lactobacillus spp. The antimicrobial substances were stable at high temperatures (100 °C for 2 h and 121 °C for 20 min) and low pH (pH 2–4) values, but sensitive to proteolytic enzymes and resistant to α-amylase, lipase and catalase enzymes. The optimal temperature for active peptides production was 25 °C. The antimicrobial compounds were purified by ammonium sulfate precipitation, affinity column and reverse-phase chromatography. Mass spectrometry and amino acids analyses showed that the bacteriocins were identical to mesentericin Y105 and B105. The producer strain’s DNA analysis revealed presence of open reading frames possibly coding for virulence factors, such as enterococcal surface protein (esp), collagen adhesion (ace) and intrinsic vancomycin resistance (vanA); however, biogenic amines encoding genes were not observed. Leuc. mesenteroides subsp. mesenteroides SJRP55 is a promising biopreservative culture in fermented milk, and the purified bacteriocins can also be applied in food preservation.

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
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Adimpong DB, Nielsen DS, Sorensen KI, Derkx PM, Jespersen L (2012) Genotypic characterization and safety assessment of lactic acid bacteria from indigenous African fermented food products. BMC Microbiol 12:75. doi:10.1186/1471-2180-12-75

    Article  CAS  Google Scholar 

  2. de Vuyst L, Callewaert R, Crabbé K (1996) Primary metabolite kinetics of bacteriocin biosynthesis by Lactobacillus amylovorus and evidence for stimulation of bacteriocin production under unfavourable growth conditions. Microbiology 142(2):817–827

    Article  Google Scholar 

  3. Dobson A, Cotter PD, Ross RP, Hill C (2012) Bacteriocin production: a probiotic trait? Appl Environ Microbiol 78(1):1–6. doi:10.1128/AEM.05576-11

    Article  CAS  Google Scholar 

  4. Masuda Y, Ono H, Kitagawa H, Ito H, Mu F, Sawa N, Zendo T, Sonomoto K (2011) Identification and characterization of leucocyclicin Q, a novel cyclic bacteriocin produced by Leuconostoc mesenteroides TK41401. Appl Environ Microbiol 77(22):8164–8170. doi:10.1128/AEM.06348-11

    Article  CAS  Google Scholar 

  5. Zouhir A, Hammami R, Fliss I, Hamida JB (2010) A new structure-based classification of gram-positive bacteriocins. Protein J 29(6):432–439. doi:10.1007/s10930-010-9270-4

    Article  CAS  Google Scholar 

  6. Daba H, Pandian S, Gosselin JF, Simard RE, Huang J, Lacroix C (1991) Detection and activity of a bacteriocin produced by Leuconostoc mesenteroides. Appl Environ Microbiol 57(12):3450–3455

    CAS  Google Scholar 

  7. Fimland G, Sletten K, Nissen-Meyer J (2002) The complete amino acid sequence of the pediocin-like antimicrobial peptide leucocin C. Biochem Biophys Res Commun 295(4):826–827

    Article  CAS  Google Scholar 

  8. Hastings JW, Stiles ME, von Holy A (1994) Bacteriocins of leuconostocs isolated from meat. Int J Food Microbiol 24(1–2):75–81

    Article  CAS  Google Scholar 

  9. Héchard Y, Berjeaud JM, Cenatiempo Y (1999) Characterization of the mesB gene and expression of bacteriocins by Leuconostoc mesenteroides Y105. Curr Microbiol 39(5):265–269

    Article  Google Scholar 

  10. Héchard Y, Derijard B, Letellier F, Cenatiempo Y (1992) Characterization and purification of mesentericin Y105, an anti-Listeria bacteriocin from Leuconostoc mesenteroides. J Gen Microbiol 138(12):2725–2731

    Article  Google Scholar 

  11. Papathanasopoulos MA, Revol-Junelles AM, Lefebvre G, Le Caer JP, von Holy A, Hastings JW (1997) Multiple bacteriocin production by Leuconostoc mesenteroides TA33a, and other Leuconostoc/Weissella strains. Curr Microbiol 6(35):331–335

    Article  Google Scholar 

  12. Revol-Junelles AM, Mathis R, Krier F, Fleury Y, Delfour A, Lefebvre G (1996) Leuconostoc mesenteroides subsp. mesenteroides FR52 synthesizes two distinct bacteriocins. Lett Appl Microbiol 23(2):120–124

    Article  CAS  Google Scholar 

  13. Todorov SD, Dicks LM (2004) Characterization of mesentericin ST99, a bacteriocin produced by Leuconostoc mesenteroides subsp. dextranicum ST99 isolated from boza. J Ind Microbiol Biotechnol 31(7):323–329. doi:10.1007/s10295-004-0153-6

    CAS  Google Scholar 

  14. Trias R, Badosa E, Montesinos E, Baneras L (2008) Bioprotective Leuconostoc strains against Listeria monocytogenes in fresh fruits and vegetables. Int J Food Microbiol 127(1–2):91–98. doi:10.1016/j.ijfoodmicro.2008.06.011

    Article  CAS  Google Scholar 

  15. Xiraphi N, Georgalaki M, Rantsiou K, Cocolin L, Tsakalidou E, Drosinos EH (2008) Purification and characterization of a bacteriocin produced by Leuconostoc mesenteroides E131. Meat Sci 80(2):194–203. doi:10.1016/j.meatsci.2007.11.020

    Article  CAS  Google Scholar 

  16. Klaenhammer TR (1993) Genetics of bacteriocins produced by lactic acid bacteria. FEMS Microbiol Rev 12(1–3):39–85

    Article  CAS  Google Scholar 

  17. Sip A, Więckowicz M, Olejnik-Schmidt A, Grajek W (2012) Anti-Listeria activity of lactic acid bacteria isolated from golka, a regional cheese produced in Poland. Food Control 26(1):117–124. doi:10.1016/j.foodcont.2012.01.014

    Article  CAS  Google Scholar 

  18. Nieto-Arribas P, Sesena S, Poveda JM, Palop L, Cabezas L (2010) Genotypic and technological characterization of Leuconostoc isolates to be used as adjunct starters in Manchego cheese manufacture. Food Microbiol 27(1):85–93. doi:10.1016/j.fm.2009.08.006

    Article  CAS  Google Scholar 

  19. Galvez A, Abriouel H, Benomar N, Lucas R (2010) Microbial antagonists to food-borne pathogens and biocontrol. Curr Opin Biotechnol 21(2):142–148. doi:10.1016/j.copbio.2010.01.005

    Article  CAS  Google Scholar 

  20. Silva LF (2010) Identificação e caracterização da microbiota lática isolada de queijo mussarela de búfala. Universidade Estadual Paulista, São José do Rio Preto

    Google Scholar 

  21. Schillinger U, Lücke FK (1989) Antibacterial activity of Lactobacillus sakei isolated from meat. Appl Environ Microbiol 55(8):1901–1906

    CAS  Google Scholar 

  22. Todorov SD, Dicks LM (2006) Parameters affecting the adsorption of plantaricin 423, a bacteriocin produced by Lactobacillus plantarum 423 isolated from sorghum beer. Biotechnol J 1(4):405–409. doi:10.1002/biot.200500026

    Article  CAS  Google Scholar 

  23. Batdorj B, Dalgalarrondo M, Choiset Y, Pedroche J, Metro F, Prevost H, Chobert JM, Haertle T (2006) Purification and characterization of two bacteriocins produced by lactic acid bacteria isolated from Mongolian airag. J Appl Microbiol 101(4):837–848. doi:10.1111/j.1365-2672.2006.02966.x

    Article  CAS  Google Scholar 

  24. Todorov SD, Wachsman M, Tome E, Dousset X, Destro MT, Dicks LM, Franco BD, Vaz-Velho M, Drider D (2010) Characterisation of an antiviral pediocin-like bacteriocin produced by Enterococcus faecium. Food Microbiol 27(7):869–879. doi:10.1016/j.fm.2010.05.001

    Article  CAS  Google Scholar 

  25. Vankerckhoven V, van Autgaerden T, Vael C, Lammens C, Chapelle S, Rossi R, Jabes D, Goossens H (2004) Development of a multiplex PCR for the detection of asa1, gelE, cylA, esp, and hyl genes in enterococci and survey for virulence determinants among European hospital isolates of Enterococcus faecium. J Clin Microbiol 42(10):4473–4479. doi:10.1128/JCM.42.10.4473-4479.2004

    Article  CAS  Google Scholar 

  26. Martín-Platero AM, Valdivia E, Maqueda M, Martínez-Bueno M (2009) Characterization and safety evaluation of enterococci isolated from Spanish goats’ milk cheeses. Int J Food Microbiol 132(1):24–32

    Article  Google Scholar 

  27. de Las Rivas B, Marcobal A, Munoz R (2005) Improved multiplex-PCR method for the simultaneous detection of food bacteria producing biogenic amines. FEMS Microbiol Rev 244(2):367–372. doi:10.1016/j.femsle.2005.02.012

    Article  Google Scholar 

  28. van Laack RL, Schillinger U, Holzapfel WH (1992) Characterization and partial purification of a bacteriocin produced by Leuconostoc carnosum LA44A. Int J Food Microbiol 16(3):183–195

    Article  Google Scholar 

  29. Chang JY, Lee HJ, Chang HC (2007) Identification of the agent from Lactobacillus plantarum KFRI464 that enhances bacteriocin production by Leuconostoc citreum GJ7. J Appl Microbiol 103(6):2504–2515. doi:10.1111/j.1365-2672.2007.03543.x

    Article  CAS  Google Scholar 

  30. Hartmann HA, Wilke T, Erdmann R (2011) Efficacy of bacteriocin-containing cell-free culture supernatants from lactic acid bacteria to control Listeria monocytogenes in food. Int J Food Microbiol 146(2):192–199. doi:10.1016/j.ijfoodmicro.2011.02.031

    Article  CAS  Google Scholar 

  31. Parente E, Moles M, Ricciardi A (1996) Leucocin F 10, a bacteriocin from Leuconostoc carnosum. Int J Food Microbiol 33(2–3):231–243

    Article  CAS  Google Scholar 

  32. Cotter PD, Hill C, Ross RP (2005) Bacteriocins: developing innate immunity for food. Nat Rev Microbiol 3(10):777–788

    Article  CAS  Google Scholar 

  33. Mataragas M, Metaxopoulos J, Drosinos EH (2002) Characterization of two bacteriocins produced by Leuconostoc mesenteroides L124 and Lactobacillus curvatus L442, isolated from dry fermented sausages. World J Microbiol Biotechnol 18(9):847–856

    Article  CAS  Google Scholar 

  34. Aasen IM, Moretro T, Katla T, Axelsson L, Storro I (2000) Influence of complex nutrients, temperature and pH on bacteriocin production by Lactobacillus sakei CCUG 42687. Appl Microbiol Biotechnol 53(2):159–166

    Article  CAS  Google Scholar 

  35. Drosinos EH, Mataragas M, Metaxopoulos J (2006) Modeling of growth and bacteriocin production by Leuconostoc mesenteroides E131. Meat Sci 74(4):690–696. doi:10.1016/j.meatsci.2006.05.022

    Article  CAS  Google Scholar 

  36. Maftah A, Renault D, Vignoles C, Hechard Y, Bressollier P, Ratinaud MH, Cenatiempo Y, Julien R (1993) Membrane permeabilization of Listeria monocytogenes and mitochondria by the bacteriocin mesentericin Y105. J Bacteriol 175(10):3232–3235

    CAS  Google Scholar 

  37. Ennahar S, Deschamps N, Richard J (2000) Natural variation in susceptibility of Listeria strains to class IIa bacteriocins. Curr Microbiol 41(1):1–4

    Article  CAS  Google Scholar 

  38. Ray B (2004) Fundamental food microbiology. CRC Press, New York

    Google Scholar 

  39. Inglis RF, Bayramoglu B, Gillor O, Ackermann M (2013) The role of bacteriocins as selfish genetic elements. Biol Lett 18(9):1–4

    Google Scholar 

  40. Limonet M, Revol-Junelles AM, Cailliez-Grimal C, Milliere JB (2004) Synergistic mode of action of mesenterocins 52A and 52B produced by Leuconostoc mesenteroides subsp. mesenteroides FR 52. Curr Microbiol 48(3):204–207. doi:10.1007/s00284-003-4165-7

    Article  CAS  Google Scholar 

  41. Renye JA Jr, Somkuti GA, Paul M, Van Hekken DL (2009) Characterization of antilisterial bacteriocins produced by Enterococcus faecium and Enterococcus durans isolates from Hispanic-style cheeses. J Ind Microbiol Biotechnol 36(2):261–268

    Article  CAS  Google Scholar 

  42. Pogacic T, Mancini A, Santarelli M, Bottari B, Lazzi C, Neviani E, Gatti M (2013) Diversity and dynamic of lactic acid bacteria strains during aging of a long ripened hard cheese produced from raw milk and undefined natural starter. Food Microbiol 36(2):207–215

    Article  CAS  Google Scholar 

  43. Muñoz-Atienza E, Gómez-Sala B, Araújo C, Campanero C, Del Campo R, Hernández PE, Carmen H, Luis MC (2013) Antimicrobial activity, antibiotic susceptibility and virulence factors of lactic acid bacteria of aquatic origin intended for use as probiotics in aquaculture. BMC Microbiol 13(1):1–22

    Article  Google Scholar 

  44. Łysakowska ME, Denys A, Sienkiewicz M (2012) Frequency of ace, epa and elrA genes in clinical and environmental strains of Enterococcus faecalis. Indian J Microbiol 52(4):612–616. doi:10.1007/s12088-012-0285-8

    Article  Google Scholar 

  45. Nallapareddy SR, Singh KV, Sillanpaa J, Zhao M, Murray BE (2011) Relative contributions of Ebp Pili and the collagen adhesin ace to host extracellular matrix protein adherence and experimental urinary tract infection by Enterococcus faecalis OG1RF. Infect Immun 79(7):2901–2910. doi:10.1128/IAI.00038-11

    Article  CAS  Google Scholar 

  46. Aymerich T, Martin B, Garriga M, Vidal-Carou MC, Bover-Cid S, Hugas M (2006) Safety properties and molecular strain typing of lactic acid bacteria from slightly fermented sausages. J Appl Microbiol 100(1):40–49. doi:10.1111/j.1365-2672.2005.02772.x

    Article  CAS  Google Scholar 

  47. Devirgiliis C, Barile S, Perozzi G (2011) Antibiotic resistance determinants in the interplay between food and gut microbiota. Genes Nutr 6(3):275–284. doi:10.1007/s12263-011-0226-x

    Article  CAS  Google Scholar 

  48. Hemme D, Foucaud-Scheunemann C (2004) Leuconostoc, characteristics, use in dairy technology and prospects in functional foods. Int Dairy J 14(6):467–494. doi:10.1016/j.idairyj.2003.10.005

    Article  Google Scholar 

  49. Dicks LMT, Todorov SD, Franco BDGM (2009) Current status of antibiotic resistance in lactic acid bacteria. In: Bonilla AR, Muniz KP (eds) Antibiotic resistance: causes and risk factors. Nova Publisher, New York, pp 1–46

    Google Scholar 

Download references

Acknowledgments

The authors are grateful to the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, Brazil, Project No. 2010/09302-1 and No. 2011/11922-0), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Brazil), for the financial support and to Dra. Elisabetta Tome from Universidad Central de Venezuela, Caracas, Venezuela, for providing Leuc. mesenteroides subsp. mesenteroides UCV10CET strain (CDCH Project No. PG-03.7371.2008). Enterococcus spp. strains used in this study as test organisms in determination of the antibacterial spectrum of activity have been provided by Prof. Dr. Luis Nero from UFV, Viçosa, MG, Brazil.

Conflict of interest

The authors declare that there is no conflict of interest.

Author information

Authors and Affiliations

  1. Food Engineering and Technology Department, UNESP - Sao Paulo State University, Rua Cristovão Colombo, 2265, São José do Rio Preto, 15.054-000, Brazil

    Aline Teodoro de Paula, Ana Beatriz Jeronymo-Ceneviva, Luana Faria Silva & Ana Lúcia Barretto Penna

  2. Department of Food Science and Experimental Nutrition, Faculty of Pharmaceutical Sciences, USP - Sao Paulo University, Av. Prof. Lineu Prestes, 580, bl. 13B, São Paulo, 05508-000, Brazil

    Svetoslav Dimitrov Todorov & Bernadette Dora Gombossy de Melo Franco

  3. UR 1268, INRA Biopolymères Interactions Assemblages Equipe FIP, B.P. 71627, 44316, Nantes Cedex 03, France

    Yvan Choiset, Thomas Haertlé & Jean-Marc Chobert

  4. UMR1014, LUNAM Université, Oniris, Secalim Rue Géraudière, B.P. 82225, 44322, Nantes Cedex 03, France

    Xavier Dousset

  5. INRA, 44307, Nantes, France

    Xavier Dousset

Authors
  1. Aline Teodoro de Paula
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ana Beatriz Jeronymo-Ceneviva
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Luana Faria Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Svetoslav Dimitrov Todorov
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bernadette Dora Gombossy de Melo Franco
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yvan Choiset
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Thomas Haertlé
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jean-Marc Chobert
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Xavier Dousset
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Ana Lúcia Barretto Penna
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ana Lúcia Barretto Penna.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Paula, A.T., Jeronymo-Ceneviva, A.B., Silva, L.F. et al. Leuconostoc mesenteroides SJRP55: A Bacteriocinogenic Strain Isolated from Brazilian Water Buffalo Mozzarella Cheese. Probiotics & Antimicro. Prot. 6, 186–197 (2014). https://doi.org/10.1007/s12602-014-9163-5

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12602-014-9163-5

Keywords

Search

Navigation