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Bacteriocinogenic Lactococcus lactis subsp. lactis 3MT isolated from freshwater Nile Tilapia: isolation, safety traits, bacteriocin characterisation, and application for biopreservation in fish pâté

  • Pierre Marie KaktchamEmail author
  • Laverdure Tchamani Piame
  • Guy Merlin Sandjong Sileu
  • Edith Marius Foko Kouam
  • Jules-Bocamdé Temgoua
  • François Zambou Ngoufack
  • María de Lourdes Pérez-Chabela
Original Paper
  • 45 Downloads

Abstract

This work was aimed to screen bacteriocin-producing LAB from freshwater fish, select a prominent strain and evaluate its safety, characterise the bacteriocin produced, and evaluate its potential to be used as biopreservatives. Isolate 3MT showed the ability to produce bacteriocin-like substances and was identified as Lactococcus lactis subsp. lactis. This strain proved to be free from virulence factors as well as biogenic amine production and antibiotic resistance patterns. The bacteriocin produced displayed high resistance to heat, pH, detergents, and its partial purification led to a 4.35-fold increase in specific activity. Moreover, this bacteriocin showed the ability to inhibit the growth of Vibrio sp. 1T1 in fish pâté stored at 10 °C for 20 days, without altering its sensory properties. The bacteriocin can be used successfully as a preservative to improve the hygienic quality and enhance the shelf life of fish paté in particular and food products in general. Lactococcus lactis subsp. lactis strain 3MT can also be safely used as a protective culture.

Keywords

Freshwater fish Lactococcus lactis subsp. lactis Bacteriocins Biopreservative Fish pâté 

Notes

Acknowledgements

The authors are grateful to TWAS (The World Academy of Sciences for the development of science in developing countries) and CONACyT (Consejo Nacional de Ciencia y Tecnología, México) for their support.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Adedeji OB, Musefiu TA, Emikpe BO (2011) The antibiotic resistant patterns of bacterial flora of fish from different aquatic environments from Ibadan, South-west Nigeria. Adv Environ Biol 5(8):2039–2047Google Scholar
  2. Araújo C, Muñoz-Atienza E, Nahuelquín Y, Poeta P, Igrejas G, Hernandez PE et al (2015) Inhibition of fish pathogens by the microbiota from rainbow trout (Oncorhynchus mykiss, Walbaum) and rearing environment. Anaerobe 32:7–14CrossRefGoogle Scholar
  3. Azhar NS, Noor Zin NHM, Abdul Hamid THTA (2017) Lactococcus Lactis strain a5 producing nisin-like bacteriocin active against gram positive and negative bacteria. Trop Life Sci Res 28(2):107–118CrossRefGoogle Scholar
  4. Behnam S, Mohammad A, Masoud R, Siyavash S, Reza S (2015) Effect of nisin as a biopreservative agent on quality and shelf life of vacuum packaged rainbow trout (Oncorhynchus mykiss) stored at 4C. J Food Sci Technol 52(4):2184–2192CrossRefGoogle Scholar
  5. Ben Omar N, Castro A, Lucas R, Abriouel H, Yousif NMK, Franz CMAP, Holzapfel WH, Rubén P-P, Martínez-Canãmero M, Gálvez A (2004) Functional and safety aspects of enterococci isolated from different Spanish foods. Syst Appl Microbiol 27:118–130CrossRefGoogle Scholar
  6. Biscola V, Todorov SD, Capuano VSC, Abriouel H, Galvez A, Franco BDGM (2013) Isolation and characterization of a nisinlike bacteriocin produced by a Lactococcus lactis strain isolated from charqui, a Brazilian fermented, salted and dried meat product. Meat Sci 93:607–613CrossRefGoogle Scholar
  7. Biscola V, Abriouel H, Todorov SD, Capuano VSC, Galvez A, de Melo Franco BDG (2014) Effect of autochthonous bacteriocin-producing Lactococcus lactis on bacterial population dynamics and growth of halotolerant bacteria in Brazilian charqui. Food Microbiol 44:296–301CrossRefGoogle Scholar
  8. De Barros JR, Kunigk L, Jurkiewicz CH (2010) Incorporation of nisin in natural casing for the control of spoilage microorganisms in vacuum packaged sausage. Braz J Microbiol 43:1001–1008CrossRefGoogle Scholar
  9. de Kwaadsteniet M, ten Doeschate K, Dicks LMT (2008) Characterization of the structural gene encoding nisin F, a new lantibiotic produced by a Lactococcus lactis subsp. lactis isolate from freshwater catfish (Clarias gariepinus). Appl Environ Microbiol 74:547–549CrossRefGoogle Scholar
  10. de las Rivas B, Marcobal A, Muñoz R (2005) Improved multiplex-PCR method for the simultaneous detection of food bacteria producing biogenic amines. FEMS Microbiol Lett 244:367–372CrossRefGoogle Scholar
  11. Dicks LMT, Todorov SD, Franco BDGM (2011) Current status of antibiotic resistance in lactic acid bacteria. In: Bonilla AR, Muniz KP (eds) Antibiotic resistance: causes and risk factors, mechanisms and alternatives. Pharmacology-research, safety testing and regulation. Nova Publisher, New York, pp 379–425Google Scholar
  12. Doern CD, Nguyen ST, Afolabi F, Burnham C-AD (2014) Probiotic-associated aspiration pneumonia due to Lactobacillus rhamnosus. J Clin Microbiol 52:3124–3126CrossRefGoogle Scholar
  13. Domingo L, Nadal M (2017) Carcinogenicity of consumption of red meat and processed meat: a review of scientific news since the IARC decision. Food Chem Toxicol 105:256–261CrossRefGoogle Scholar
  14. Eaton TJ, Gasson MJ (2001) Molecular screening of Enterococcus virulence determinants and potential for genetic exchange between food and medical isolates. Appl Environ Microbiol 67:1628–1635CrossRefGoogle Scholar
  15. EFSA Panel on Additives and Products or Substances used in Animal Feed (FEEDAP) (2011) Scientific opinion on the safety and efficacy of Lactococcus lactis (NCIMB 30160) as silage additive for all species. EFSA J 9(9): 2366. www.efsa.europa.eu/efsajournal
  16. Ekhtiarzadeh H, Basti AA, Misaghi A, Sari A, Khanjari A, Rokni N, Abbaszadeh S, Partovi R (2012) Growth response of Vibrio parahaemolyticus and listeria monocytogenes in salted fish fillets as affected by Zataria multiflora boiss. essential oil, nisin, and their combination. J Food Saf 32(3):263–269CrossRefGoogle Scholar
  17. European Parliament and the Council of European Union (2009) Regulations: regulation (EC) no 1107/2009 of the European parliament and of the council of 21 October 2009 concerning the placing of plant protection products on the market and repealing Council Directives 79/117/EEC and 91/414/EEC. Off J Eur Union L309:1–50Google Scholar
  18. Gevers D, Danielsen M, Huys G, Swings J (2003) Molecular characterization of tet (M) genes in Lactobacillus isolates from different types of fermented dry sausage. Appl Environ Microbiol 69:1270–1275CrossRefGoogle Scholar
  19. Ghrairi T, Manai M, Berjeaud JM, Frère J (2004) Antilisterial activity of lactic acid bacteria isolated from rigouta, a traditional Tunisian cheese. J Appl Microbiol 97:621–628CrossRefGoogle Scholar
  20. Goldstein EJC, Tyrrell KL, Citron DM (2015) Lactobacillus species: taxonomic complexity and controversial susceptibilities. Clin Infect Dis 60:S98–S107CrossRefGoogle Scholar
  21. Grosu-Tudor SS, Stancu M-M, Pelinescu D, Zamfir M (2014) Characterisation of some bacteriocins produced by lactic acid bacteria isolated from fermented foods. World J Microbiol Biotechnol 30:2459–2469CrossRefGoogle Scholar
  22. Hanan TAH (2010) lactic acid bacteria and their antimicrobial peptides: induction, detection, partial characterization, and their potential applications. Division of Microbiology Department of Food and Environmental Sciences Faculty of Agriculture and Forestry University of HelsinkiGoogle Scholar
  23. Hwanhlem N, Biscola V, El-Ghaish S, Jaffrès E, Dousset X, Haertlé T, Chobert J-M (2013) Bacteriocin-producing lactic acid bacteria isolated from mangrove forests in southern Thailand as potential bio-control agents: Purification and characterization of bacteriocin produced by Lactococcus lactis subsp. lactis KT2W2L. Probiotics Antimicro Prot 5(4):264–278CrossRefGoogle Scholar
  24. Hwanhlem N, Jaffres E, Dousset X, Pillot G, Choiset Y, Haertle T, Kittikun A, Chobert JM (2015) Application of a nisin Z-producing Lactococcus lactis subsp. lactis KT2W2L isolated from brackish water for biopreservation in cooked, peeled and ionized tropical shrimps during storage at 8 °C under modified atmosphere packaging. Eur Food Res Technol 240(6):1259–1269CrossRefGoogle Scholar
  25. Kaktcham PM, Temgoua J-B, Zambou NF, Diaz-Ruiz G, Wacher C, Perez-Chabela ML (2017) Quantitative analyses of the bacterial microbiota of rearing environment, tilapia and common carp cultured in earthen ponds and inhibitory activity of its lactic acid bacteria on fish spoilage and pathogenic bacteria. World J Microbiol Biotechnol 33(2):1–12CrossRefGoogle Scholar
  26. Kaktcham PM, Foko Kouam EM, Tchabou Tientcheu ML, Wacher C, Zambou Ngoufack F, Pérez-Chabela ML (2019) Nisin-producing Lactococcus lactis subsp. lactis 2MT isolated from freshwater Nile tilapia in Cameroon: bacteriocin screening, characterization, and optimization in a low-cost medium. LWT-Food Sci Technol 107:272–279CrossRefGoogle Scholar
  27. Klaenhammer TR (1993) Genetics of bacteriocins produced by lactic acid bacteria. FEMS Microbiol Rev 12:39–86CrossRefGoogle Scholar
  28. Loh JY, Lim YY, Ting ASY (2017) Bacteriocin-like substances produced by Lactococcus lactis subsp. lactis CF4MRS isolated from fish intestine: antimicrobial activities and inhibitory properties. Int Food Res J 24(1):394–400Google Scholar
  29. Martin-Platero AM, Valdivia E, Maqueda M, Martinez-Bueno M (2009) Characterization and safety evaluation of enterococci isolated from Spanish goats’ milk cheeses. Int J Food Microbiol 132:24–32CrossRefGoogle Scholar
  30. Matsusaki H, Sonomoto K, Ishizaki A (1998) Some characteristics of nisin Z, a peptide antibiotic produced by Lactococcus lactis IO-1. Food Sci Technol Int 4(4):290–294Google Scholar
  31. McAfee A, Emier M, McSorley A, Geraldine J, Cuskelly B, Bruce W, Moss C, Julie M, Wallace A, Bonham P, Fearon M (2010) Red meat consumption: an overview of the risks and benefits. Meat Sci 84:1–13CrossRefGoogle Scholar
  32. Migaw S, Ghrairi T, Belguesmia Y, Choiset Y, Berjeaud J-M, Chobert J-M, Hani K, Haertle T (2014) Diversity of bacteriocinogenic lactic acid bacteria isolated from Mediterranean fish viscera. World J Microbiol Biotechnol 30:1207–1217CrossRefGoogle Scholar
  33. Moraes PM, Perin LM, Todorov SD, Silva AJR, Franco BDGM, Nero LA (2012) Bacteriocinogenic and virulence potential of Enterococcus isolates obtained from raw milk and cheese. J App Microbiol 113:318–328CrossRefGoogle Scholar
  34. Nga Ombede SN, Kaktcham PM, Malang S, Zambou NF (2018) Changes in sensory, physicochemical, and microbiological properties of fresh captured tropical pink shrimps (Penaeus duorarum notialis) inoculated with Lactobacillusplantarum Lp6SH, Lactobacillus rhamnosus Yoba, and their cell-free culture supernatants during storage at 4 °C. J Food Saf.  https://doi.org/10.1111/jfs.12579 Google Scholar
  35. Raju CV, Shamasundar BA, Udupa KS (2003) The use of nisin as a preservative in fish sausage stored at ambient (28 ± 2 C) and refrigerated (6 ± 2 C) temperatures. Int J Food Sci Technol 38:171–185CrossRefGoogle Scholar
  36. Rattanachaikunsopon P, Phumkhachorn P (2008) Incidence of nisin Z production in Lactococcus lactis subsp. lactis TFF 221 isolated from Thai fermented foods. J Food Prot 71:2024–2029CrossRefGoogle Scholar
  37. Saelao S, Maneerat S, Kaewsuwan S, Rabesona H, Choiset Y, Thomas Haertlé T, Chobert J-M (2017) Inhibition of Staphylococcus aureus in vitro by bacteriocinogenic Lactococcus lactis KTH0-1S isolated from Thai fermented shrimp (Kung-som) and safety evaluation. Arch Microbiol 199(4):551–562CrossRefGoogle Scholar
  38. Sahnouni F (2013) Isolement, identification biochimique et technologique des bactéries lactiques isolées de poissons marins (Sardina pilchardus et Boops boops) pêchés dans la côte occidentale algérienne et mise en évidence de leur pouvoir bioconservateur: cas de la crevette rose (Ariteus antennatus). Thèse PhD en Biologie: Oran (Faculté des Sciences; Département de Biologie-Université d’Oran. Algérie), p 321Google Scholar
  39. Sahnouni F, Boutiba-Maatallah A, Bouhadi D, Boutiba Z (2014) Characterisation of bacteriocin produced by Lactococcus lactis ssp. lactis strains isolated from marine fish caught in the Algerian west coast. Turkish J Agric Natl Sci 2:1838–1843Google Scholar
  40. Sarvamangala RP, Amena S, Sharmila J, Shilpa K, Dheeraj K (2013) Extraction, partial purification and characterization of bacteriocin from Lactobacillus casei NCIM no.2732. J Recent Adv Appl Sci 28:90–95Google Scholar
  41. Schillinger U, Lücke F (1989) Antibacterial activity of Lactobacillus sake isolated from meat. Appl Environ Microbiol 55:1901–1906Google Scholar
  42. Schwendicke F, Dörfer C, Kneist S, Meyer-Lueckel H, Paris S (2014) Cariogenic effects of probiotic Lactobacillus rhamnosus GG in a dental biofilm model. Caries Res 48:186–192CrossRefGoogle Scholar
  43. Sequeiros C, Vallejo M, Marguet ER, Olivera NL (2010) Inhibitory activity against the fish pathogen Lactococcus garvieae produced by Lactococcus lactis TW34, a lactic acid bacterium isolated from the intestinal tract of a Patagonian fish. Arch Microbiol 192:237–245CrossRefGoogle Scholar
  44. The Japan Food Chemical Research Foundation (2018) Standards for use of food additives 24Google Scholar
  45. Van Reenen CA, Dicks LMT, Chikindas ML (1998) Isolation, purification and partial characterization of plantaricin 423, a bacteriocin produced by Lactobacillus plantarum. J Appl Microbiol 84:1131–1137CrossRefGoogle Scholar
  46. 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 42:4473–4479CrossRefGoogle Scholar
  47. Vermeiren L, Devlieghere F, Debevere J (2004) Evaluation of meat born lactic acid bacteria as protective cultures for the biopréservation of cooked meat products. Int J Food Microbiol 96(2):149–164CrossRefGoogle Scholar
  48. Zaukuu J-L, Oduro I, Otoo WE (2016) Processing methods and microbial assessment of pito (an African indigenous beer), at selected production sites in Ghana. J I Brewing 122:736–744CrossRefGoogle Scholar
  49. Zycka-Krzesinska J, Boguslawska J, Aleksandrzak-Piekarczyk T, Jopek J, Bardowski JK (2015) Identification and characterization of tetracycline resistance in Lactococcus lactis isolated from Polish raw milk and fermented artisanal products. Int J Food Microbiol 211:134–141CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Pierre Marie Kaktcham
    • 1
    • 2
    Email author
  • Laverdure Tchamani Piame
    • 1
  • Guy Merlin Sandjong Sileu
    • 1
  • Edith Marius Foko Kouam
    • 1
  • Jules-Bocamdé Temgoua
    • 1
  • François Zambou Ngoufack
    • 1
  • María de Lourdes Pérez-Chabela
    • 2
  1. 1.Research Unit of Biochemistry, Food Science and Nutrition (URBPMAN), Department of Biochemistry, Faculty of ScienceUniversity of DschangDschangCameroon
  2. 2.Departamento de BiotecnologíaUniversidad Autónoma Metropolitana‐Iztapalapa (UAM-I)Mexico CityMexico

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