Skip to main content
SpringerLink
Log in

Assessment of the antifungal activity of Lactobacillus and Pediococcus spp. for use as bioprotective cultures in dairy products

  • Original Paper
  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Fungi are commonly involved in dairy product spoilage and the use of bioprotective cultures can be a complementary approach to reduce food waste and economic losses. In this study, the antifungal activity of 89 Lactobacillus and 23 Pediococcus spp. isolates against three spoilage species, e.g., Yarrowia lipolytica, Rhodotorula mucilaginosa and Penicillium brevicompactum, was first evaluated in milk agar. None of the tested pediococci showed antifungal activity while 3, 23 and 43 lactobacilli isolates showed strong antifungal activity or total inhibition against Y. lipolytica, R. mucilaginosa and P. brevicompactum, respectively. Then, the three most promising strains, Lactobacillus paracasei SYR90, Lactobacillus plantarum OVI9 and Lactobacillus rhamnosus BIOIII28 at initial concentrations of 105 and 107 CFU/ml were tested as bioprotective cultures against the same fungal targets in a yogurt model during a 5-week storage period at 10 °C. While limited effects were observed at 105 CFU/ml inoculum level, L. paracasei SYR90 and L. rhamnosus BIOIII28 at 107 CFU/ml respectively retarded the growth of R. mucilaginosa and P. brevicompactum as compared to a control without selected cultures. In contrast, growth of Y. lipolytica was only slightly affected. In conclusion, these selected strains may be good candidates for bioprotection of fermented dairy products.

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

Similar content being viewed by others

References

  • Axel C, Brosnan B, Zannini E, Peyer LC, Furey A, Coffey A, Arendit EK (2016) Antifungal activities of three different Lactobacillus species and their production of antifungal carboxylic acids in wheat sourdough. Appl Microbiol Biot 100:1701–1711

    Article  CAS  Google Scholar 

  • Belguesmia Y, Rabesona H, Mounier J, Pawtowsky A, Le Blay G, Barbier G, Haertlé T, Chobert JM (2014) Characterization of antifungal organic acids produced by Lactobacillus harbinensis K.V9.3.1.Np immobilized in gellan-xanthan beds during batch fermentation. Food Control 36:205–211

    Article  CAS  Google Scholar 

  • Bernardeau M, Vernoux JP, Herni-Dubernet S, Guéguen M (2008) Safety assessment of dairy microorganisns: the Lactobacillus genus. Int J Food Microbiol 126:278–285

    Article  CAS  Google Scholar 

  • Berthier F, Ehrlich SD (1998) Rapid species identification within two groups of closely related lactobacilli using PCR primers that target the 16S/23S rRNA spacer region. FEMS Microbiol Lett 161:97–106

    Article  CAS  Google Scholar 

  • Caplice E, Fitzgerald GF (1999) Food fermentations: role of microorganisms in food production and preservation. Intl J Food Microbiol 50:131–149

    Article  CAS  Google Scholar 

  • Crowley S, Mahony J, van Sinderen D (2012) Comparative analysis of two antifungal Lactobacillus plantarum isolates and their application as bioprotectants in refrigerated foods. J Appl Microbiol 113:1417–1427

    Article  CAS  Google Scholar 

  • Dalié DKD, Deschamps AM, Richard-Forget F (2010) Lactic acid bacteria – potential for control of mould growth and mycotoxins: a review. Food Control 21:370–380

    Article  Google Scholar 

  • Dallagnol AM, Catalán CAN, Mercado MI, Font de Valdez G, Rollán GC (2011) Effect of biosynthetic intermediates and citrate on the phenyllactic and hydroxyphenyllactic acids production by Lactobacillus plantarum CRL 778. J Appl Microbiol 111:1447–1455

    Article  CAS  Google Scholar 

  • Delavenne E, Mounier J, Déniel F, Barbier G, Le Blay G (2012) Biodiversity of antifungal lactic acid bacteria isolated from raw milk samples from cow, ewe and goat over one-year period. Int J Food Microbiol 155:185–190

    Article  CAS  Google Scholar 

  • Delavenne E, Ismail R, Pawtowski A, Mounier J, Barbier G, Le Blay G (2013) Assessment of lactobacilli strains as yogurt bioprotective cultures. Food Control 30:206–213

    Article  CAS  Google Scholar 

  • Doulgeraki AI, Ercolini D, Villani F, Nychas GJE (2012) Spoilage microbiota associated to the storage of raw meat in different conditions. Int J Food Microbiol 157:130–141

    Article  Google Scholar 

  • Dubernet S, Desmasures N, Guéguen MA (2002) PCR-based method for identification of lactobacilli at the genus level. FEMS Microbiol Lett 214:271–275

    Article  CAS  Google Scholar 

  • Garnier L, Valence F, Pawtowski A, Auhustsinava-Galerne L, Frotte N, Baroncelli R, Deniel F, Coton E, Mounier J (2017) Diversity of spoilage fungi associated with varius French dairy products. Int J Food Microbiol 241:191–197

    Article  CAS  Google Scholar 

  • Giraffa G, Chanishvili N, Widyastuti Y (2010) Importance of lactobacilli in food and feed biotechnology. Res Microbiol 161:480–487

    Article  Google Scholar 

  • Guarneri T, Rossetti L, Giraffa G (2001) Rapid identification of Lactobacillus brevis using the polymerase chain reaction. Lett Appl Microbiol 33:377–381

    Article  CAS  Google Scholar 

  • ISO 6887-1:1999 (1999) Microbiology of food and animal feeding stuffs - preparation of tests samples, initial suspension and decimal dilutions for microbiological examination - Part 1: general rules for the preparation of the initial suspension and decimal dilutions

  • ISO 7218:2008 (2008) Microbiology of food and animal feeding stuffs - General requirements and guidance for microbiological examinations

  • Khurana H, Kanawjia S (2007) Recent trends in development of fermented milks. Curr Nutr Food Sci 3:91–108

    Article  CAS  Google Scholar 

  • König H, Fröhlich J (2009) Chap. 1: lactic acid bacteria. In: König H, Uden G, Fröhlich J (eds) Biology of microorganisms on grapes, in must and in wine, 1st edn. Springer, Berlin, pp 3–5

    Chapter  Google Scholar 

  • Le Lay C, Mounier J, Vasseur V, Weill A, Le Blay G, Barbier G, Coton E (2016) In vitro and in situ screening of lactic acid bacteria and propionibacteria antifungal activities against bakery product spoilage molds. Food Control 60:247–255

    Article  Google Scholar 

  • Li H, Liu L, Zhang S, Uluko H, Cui W, Lv J (2013) Potential use of Lactobacillus casei AST18 as bioprotective culture in yogurt. Food Control 34:675–680

    Article  CAS  Google Scholar 

  • Limsowtin GKY, Broome MC, Powell IB (2002) Lactic acid bacteria, taxonomy. In: Roginski H, Fuquay JW, Fox PF (eds) Encyclopedia of dairy science. 1st edn. Elsevier, pp 1470–1478

  • LPSN – List of prokaryotic names with standing in nomenclature (2017) http://www.bacterio.net/index.html. Accessed 6 February 2017

  • Mayoral MB, Martín R, Sanz A, Hernández PE, González I, García T (2005) Detection of Kluyveromyces marxianus and other spoilage yeasts in yoghurt using a PCR-culture technique. Int J Food Microbiol 105:27–34

    Article  CAS  Google Scholar 

  • Muhialdin BJ, Hassan Z, Abu Bakar F, Saari N (2016) Identification of antifungal peptides produced by Lactobacillus plantarum IS10 grown in the MRS broth. Food Control 59:27–30

    Article  CAS  Google Scholar 

  • Nawaz M, Wang J, Zhou A, Ma C, Wu X, Moore JE, Millar BC, Xu J (2011) Characterization and transfer of antibiotic resistance in lactic acid bacteria from fermented food products. Curr Microbiol 62:1081–1089

    Article  CAS  Google Scholar 

  • Ndagijimana M, Chaves-López C, Corsetti A, Tofalo R, Serge M, Paparella A, Guerzoni ME, Suzzi G (2008) Growth and metabolites production by Penicillium brevicompactum in yogurt. Int J Food Microbiol 127:276–283

    Article  CAS  Google Scholar 

  • Pfannebecker J, Fröhlich J (2008) Use of species-specific multiplex PCR for the identification of pediococci. Int J Food Microbiol 128:288–296

    Article  CAS  Google Scholar 

  • Pot B, Tsakalidou E (2009) Taxonomy and metabolism of Lactobacillus. In: Ljungh Å, Wadström T (eds) Lactobacillus molecular biology. Academic Press, Norfolk, pp 3–58

    Google Scholar 

  • Praphailong W, Fleet GH (1997) The effect of pH, sodium chloride, sucrose, sorbate and benzoate on the growth of food spoilage yeasts. Food Microbiol 14:459–468

    Article  CAS  Google Scholar 

  • Rouse S, Harnett D, Vaughan A, Sinderen D (2008) Lactic acid bacteria with potential to eliminate fungal spoilage in foods. J Appl Microbiol 104:915–923

    Article  CAS  Google Scholar 

  • Schnürer J, Magnusson J (2005) Antifungal lactic acid bacteria as biopreservatives. Trends Food Sci Tech 16:70–78

    Article  Google Scholar 

  • Schwenninger SM, Meile L (2004) A mixed culture of Propionibacterium jensenii and Lactobacillus paracasei subsp. paracasei inhibits food spoilage yeasts. Syst Appl Microbiol 27:229–237

    Article  Google Scholar 

  • Schwenninger SM, Lacroix C, Truttmann S, Jans C, Spörndli C, Bigler L, Meile L (2008) Characterization of low-molecular-weight antiyeast metabolites produced by a food-protective Lactobacillus-Propionibacterium coculture. J Food Protect 71:2481–2487

    Article  CAS  Google Scholar 

  • Song YL, Kato N, Liu CX, Matsumiya Y, Kato H, Watanabe K (2000) Rapid identification of 11 human intestinal Lactobacillus species by multiplex PCR assays using group - and species-specific primers derived from the 16S-23S rRNA intergenic spacer region and its flanking 23S rRNA. FEMS Microbiol Lett 187:167–173

    CAS  Google Scholar 

  • Standarová E, Vorlová L, Kordiovská P, Janštová B, Dračková M, Borkovcová I (2010) Biogenic amine production in Olomouc curd cheese (Olomoucké tvarůžky) at various storage conditions. Acta Veta Brno 79:147–156

    Article  Google Scholar 

  • Suomalainen TH, Mäyrä-Makinen AM (1999) Propionic acid bacteria as protective cultures in fermented milks and breads. Le Lait 79:165–174

    Article  CAS  Google Scholar 

  • Valerio F, Di Biase M, Lattanzio VMT, Lavermicocca P (2016) Improvement of the antifungal activity of lactic acid bacteria by addition to the growth medium of phenylpyruvic acid, a precursor of phenyllactic acid. Int J Food Microbiol 222:1–7

    Article  CAS  Google Scholar 

  • Varsha KK, Nampoothiri KM (2016) Appraisal of lactic acid bacteria as protective cultures. Food Control 69:61–64

    Article  CAS  Google Scholar 

  • Walter J, Tannock GW, Tilsava-Timisjarvi A, Rodtong S, Loach DM, Munro K, Alatossava T (2000) Detection and identification of gastrointestinal Lactobacillus species by using denaturing gradient gel electrophoresis and species-specific PCR primers. Appl Environ Microbiol 66:297–303

    Article  CAS  Google Scholar 

  • Ward LJH, Timmins MJ (1999) Differentiation of Lactobacillus casei, Lactobacillus paracasei and Lactobacillus rhamnosus by polymerase chain reaction. Lett Appl Microbiol 29:90–92

    Article  CAS  Google Scholar 

  • Zhang Y, Liu Y, Bao Y, Zhang H (2010) Influence of pH, heat and enzymatic treatments on the activity of antibacterial substance in MRS and milk media produced by Lactobacillus fermentum F6. Agri Sci in China 9:911–920

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the project IMA 2015-FVHE-19 of the University of Veterinary and Pharmaceutical Sciences Brno.

Author information

Authors and Affiliations

  1. Department of Milk Hygiene and Technology, Faculty of Veterinary Hygiene and Ecology, University of Veterinary and Pharmaceutical Sciences Brno, Palackého tř. 1946/1, 612 42, Brno, Czech Republic

    Ines Lačanin, Marta Dušková, Josef Kameník & Renáta Karpíšková

  2. Laboratoire Universitaire de Biodiversité et Ecologie Microbienne, IBSAM, ESIAB, Université de Brest, EA3882, Technopôle Brest – Iroise, 29280, Plouzané, France

    Jérôme Mounier & Audrey Pawtowski

  3. Veterinary Research Institute, Hudcova 296/70, 621 00, Brno, Czech Republic

    Marta Dušková & Renáta Karpíšková

Authors
  1. Ines Lačanin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jérôme Mounier
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Audrey Pawtowski
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marta Dušková
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Josef Kameník
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Renáta Karpíšková
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jérôme Mounier.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 77 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lačanin, I., Mounier, J., Pawtowski, A. et al. Assessment of the antifungal activity of Lactobacillus and Pediococcus spp. for use as bioprotective cultures in dairy products. World J Microbiol Biotechnol 33, 188 (2017). https://doi.org/10.1007/s11274-017-2354-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11274-017-2354-y

Keywords

Search

Navigation