Skip to main content
Log in

Broad-spectrum antifungal-producing lactic acid bacteria and their application in fruit models

  • Published:
Folia Microbiologica Aims and scope Submit manuscript

Abstract

A large-scale screen of some 7,000 presumptive lactic acid bacteria (LAB), isolated from animal, human, or plant origin, identified 1,149 isolates with inhibitory activity against the food-spoilage mould Penicillium expansum. In excess of 500 LAB isolates were subsequently identified to produce a broad spectrum of activity against P. expansum, Penicillium digitatum, Penicillium notatum, Penicillium roqueforti, Rhizopus stolonifer, Fusarium culmorum, Aspergillus fumigatus and Rhodotorula mucilaginosa. Partial 16S rRNA sequencing of 94 broad spectrum isolates revealed that the majority of antifungal producers were strains of Lactobacillus plantarum. The remaining population was composed of Weissella confusa and Pediococcus pentosaceous isolates. Characterization of six selected broad-spectrum antifungal LAB isolates revealed that antifungal activity is maximal at a temperature of 30 °C, a pH of 4.0 and is stable across a variety of salt concentrations. The antifungal compound(s) was shown to be neither proteinaceous nor volatile in nature. P. pentosaceous 54 was shown to have protective properties against P. expansum spoilage when applied in pear, plum and grape models, therefore representing an excellent candidate for food-related applications.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Adebayo CO, Aderiye BI (2011) Suspected mode of antimycotic action of brevicin SG1 against Candida albicans and Penicillium citrinum. Food Control 22:1814–1820

    Article  CAS  Google Scholar 

  • Broberg A, Jacobsson K, Strom K, Schnurer J (2007) Metabolite profiles of lactic acid bacteria in grass silage. Appl Environ Microbiol 73:5547–5552

    Article  PubMed  CAS  Google Scholar 

  • Bryden LW (2007) Mycotoxins in the food chain: human health implications. Asia Pac J Clin Nut 16:95–101

    CAS  Google Scholar 

  • Chung TC, Axelsson L, Lindgren SE, Dobrogosz WJ (1989) In vitro studies on reuterin synthesis by Lactobacillus reuteri. Microb Eco Health Dis 2:137–144

    Article  Google Scholar 

  • Corsetti A, Settanni L, van Sinderen D (2004) Characterization of bacteriocin-like inhibitory substances (BLIS) from sourdough lactic acid bacteria and evaluation of their in vitro and in situ activity. J Appl Microbiol 96:521–534

    Article  PubMed  CAS  Google Scholar 

  • Corsetti A, Settanni L, van Sinderen D, Felis GE, Dellaglio F, Gobbetti M (2005) Lactobacillus rossii sp. nov., isolated from wheat sourdough. Int J Sys Evo Microbiol 55:34–40

    Google Scholar 

  • Dal Bello F, Clarke CI, Ryan LAM, Ulmer H, Schober TJ, Ström K, Sjögren J, van Sinderen D, Schnürer J, Arendt EK (2007) Improvement of the quality and shelf life of wheat bread by fermentation with the antifungal strain Lactobacillus plantarum FST 1.7. J Cereal Sci 45:309–318

    Article  CAS  Google Scholar 

  • Dalie DK, Deschamps AM, Atanasova-Penichon V, Richard-Forget F (2010) Potential of Pediococcus pentosaceus (L006) isolated from maize leaf to suppress fumonisin-producing fungal growth. J Food Prot 73:1129–1137

    PubMed  CAS  Google Scholar 

  • Djossou O, Perraud-Gaime I, Mirleau FL, Rodriguez-Serrano G, Karou G, Niamke S, Ouzari I, Boudabous A, Roussos S (2011) Lactobacillus plantarum sp. as potential antagonist of Aspergillus carbonarius. Anaerobe 17:267–272

    Article  PubMed  Google Scholar 

  • Falguni P, Shilpa VIJ, Mann B (2010) Production of proteinaceous antifungal substances from Lactobacillus brevis NCDC 02. Int J Dairy Technol 63:70–76

    Article  CAS  Google Scholar 

  • Filtenborg O, Frisvad JC, Thrane U (1996) Moulds in food spoilage. Int J Food Microbiol 33:85–102

    Article  PubMed  CAS  Google Scholar 

  • Gerez CL, Torino MI, Rollan G, de Valdez G (2009) Prevention of bread mould spoilage by using lactic acid bacteria with antifungal properties. Food Control 20:144–148

    Article  CAS  Google Scholar 

  • Gerez CL, Carbajo MS, Rollan G, Torres Leal G, de Valdez G (2010a) Inhibition of citrus fungal pathogens by using lactic acid bacteria. J Food Sci 75:354–359

    Article  Google Scholar 

  • Gerez CL, Torino MI, Obregozo MD, de Valdez G (2010b) A ready-to-use antifungal starter culture improves the shelf life of packaged bread. J Food Prot 73:758–762

    PubMed  CAS  Google Scholar 

  • Guo J, Mauch A, Galle S, Murphy P, Arendt EK, Coffey A (2011) Inhibition of growth of Trichophyton tonsurans by Lactobacillus reuteri. J Appl Microbiol 111:474–483

    Article  PubMed  CAS  Google Scholar 

  • Hassan YI, Bullerman LB (2008) Antifungal activity of Lactobacillus paracasei ssp. tolerans isolated from a sourdough bread culture. Int J Food Microbiol 121:112–115

    Article  PubMed  CAS  Google Scholar 

  • Laitila A, Alakomi HL, Raaska L, Mattila-Sandholm T, Haikara A (2002) Antifungal activities of two Lactobacillus plantarum strains against Fusarium moulds in vitro and in malting of barley. J Appl Microbiol 93:566–576

    Article  PubMed  CAS  Google Scholar 

  • Lan W, Chen Y, Wu H, Yanagida F (2012) Bio-protective potential of lactic acid bacteria isolated from fermented wax gourd. Folia Microbiol 57:99–105. doi:10.1007/s12223-012-0101-1

    Article  CAS  Google Scholar 

  • Lavermicocca P, Valerio F, Evidente A, Lazzaroni S, Corsetti A, Gobbetti M (2000) Purification and characterization of novel antifungal compounds from the sourdough Lactobacillus plantarum strain 21B. Appl Environ Microbiol 66:4084–4090

    Article  PubMed  CAS  Google Scholar 

  • Legan JD (1993) Mould spoilage of bread: the problem and some solutions. Int Biodeter Biodeg 32:33–53

    Article  Google Scholar 

  • Magnusson J, Schnurer J (2001) Lactobacillus coryniformis subsp. coryniformis strain Si3 produces a broad-spectrum proteinaceous antifungal compound. Appl Environ Microbiol 67:1–5

    Article  PubMed  CAS  Google Scholar 

  • Magnusson J, Strom K, Roos S, Sjoren J, Schnurer J (2003) Broad and complex antifungal activity among environmental isolates of lactic acid bacteria. FEMS Microbiol Lett 219:129–135

    Article  PubMed  CAS  Google Scholar 

  • Mauch A, Dal Bello F, Coffey A, Arendt EK (2010) The use of Lactobacillus brevis PS1 to in vitro inhibit the outgrowth of Fusarium culmorum and other common Fusarium species found on barley. Int J Food Microbiol 141:116–121

    Article  PubMed  CAS  Google Scholar 

  • Pitt JI, Hocking AD (1999) Fungi and food spoilage, 2nd edn. Aspen, Gaithersburg

    Google Scholar 

  • Prema P, Smila D, Palavesam A, Immanuel G (2010) Production and characterization of an antifungal compound (3-phenyllactic acid) produced by Lactobacillus plantarum strain. Food Bioprocess Technol 3:379–386

    Article  CAS  Google Scholar 

  • Rouse S, Canchaya C, van Sinderen D (2008a) Lactobacillus hordei sp. nov., a bacteriocinogenic strain isolated from malted barley. Int J Syst Evol Microbiol 58:2013–2017

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Ryan LAM, Dal Bello F, Arendt EK (2008) The use of sourdough fermented by antifungal LAB to reduce the amount of calcium propionate in bread. Int J Food Microbiol 125:274–278

    Article  PubMed  CAS  Google Scholar 

  • Sathe SJ, Nawani NN, Dhakephalkar PK, Kapadnis BP (2007) Antifungal lactic acid bacteria with potential to prolong shelf-life of fresh vegetables. J Appl Microbiol 103:2622–2628

    Article  PubMed  CAS  Google Scholar 

  • Schillinger U, Villarreal JV (2010) Inhibition of Penicillium nordicum in MRS medium by lactic acid bacteria isolated from foods. Food Control 21:107–111

    Article  CAS  Google Scholar 

  • Sjogren J, Magnusson J, Broberg A, Schnurer J, Kenne L (2003) Antifungal 3-hydroxy fatty acids from Lactobacillus plantarum MiLAB 14. Appl Environ Microbiol 69:7554–7557

    Article  PubMed  Google Scholar 

  • Strom K, Sjogren J, Broberg A, Schnurer J (2002) Lactobacillus plantarum MiLAB 393 produces the antifungal cyclic dipeptides cyclo(L-Phe-L-Pro) and cyclo(L-Phe-trans-4-OH-L-Pro) and 3-phenyllactic acid. Appl Environ Microbiol 68:4322–4327

    Article  PubMed  CAS  Google Scholar 

  • Valerio F, Favilla M, De Bellis P, Sisto A, de Candia S, Lavermicocca P (2009) Antifungal activity of strains of lactic acid bacteria isolated from a semolina ecosystem against Penicillium roqueforti, Aspergillus niger and Endomyces fibuliger contaminating bakery products. Syst Appl Microbiol 32:438–448

    Article  PubMed  CAS  Google Scholar 

  • Voulgari K, Hatzikamari M, Delepoglou A, Georgakopoulos P, Litopoulou-Tzanetaki E, Tzanetakis N (2010) Antifungal activity of non-starter lactic acid bacteria isolates from dairy products. Food Control 21:136–142

    Article  CAS  Google Scholar 

  • Wang H, Yan Y, Wang J, Zhang H, Qi W (2012) Production and characterization of antifungal compounds produced by Lactobacillus plantarum IMAU10014. PLoS One 7:e29452

    Article  PubMed  CAS  Google Scholar 

  • Yang EJ, Chang HC (2010) Purification of a new antifungal compound produced by Lactobacillus plantarum AF1 isolated from kimchi. Int J Food Microbiol 139:56–63

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

S. Crowley is the recipient of a Lauritzson Foundation scholarship. D. van Sinderen is a recipient of a Science Foundation Ireland (SFI) Principal Investigatorship award (ref. no. 08/IN.1/B1909).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Douwe van Sinderen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Crowley, S., Mahony, J. & van Sinderen, D. Broad-spectrum antifungal-producing lactic acid bacteria and their application in fruit models. Folia Microbiol 58, 291–299 (2013). https://doi.org/10.1007/s12223-012-0209-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12223-012-0209-3

Keywords

Navigation