Biopreservation of minimally processed iceberg lettuces using a bacteriocin produced by Lactococcus lactis wild strain

Abstract The industry of minimally processed vegetables (MPV) is constantly searching new technologies for maintaining quality and for inhibiting undesired microbial growth in all steps of production and distribution chain. Among the proposed new technologies, biopreservation, such as bacteriocin-based strategy, is recently considered as a promising perspective in order to reduce the application of chemical preservatives. In the present study the effect of the bacteriocin RUC9 produced by a wild strain of Lactococcus lactis was tested in minimally processed lettuce iceberg samples artificially inoculated with a wild strain of Listeria monocytogenes during storage at 4 °C and compared to that of commercial nisin. Moreover the microbial group dynamics were evaluated by conventional and molecular approaches. Although the treatment did not completely eliminate the pathogen on the produce, the results showed that the bacteriocin reduced the L. monocytogenes viable count of 2.7 log unit in 7 days of storage at 4 °C, suggesting that the treatment can be used as sanitizer to improve microbial safety and to reduce the chemical treatment in MPV processing.

[1]  Lothar Leistner,et al.  Food preservation by hurdle technology , 1995 .

[2]  A. Jones,et al.  Longitudinal microbiological survey of fresh produce grown by farmers in the upper midwest. , 2006, Journal of food protection.

[3]  C. Randazzo,et al.  Listeria innocua growth in fresh cut mixed leafy salads packaged in modified atmosphere , 2009 .

[4]  Aurelio López-Malo,et al.  Minimally processed fruits and vegetables : fundamental aspects and applications , 2000 .

[5]  R. Evans,et al.  Applications of the bacteriocin, nisin , 1996, Antonie van Leeuwenhoek.

[6]  J. Cleveland,et al.  Bacteriocins: safe, natural antimicrobials for food preservation. , 2001, International journal of food microbiology.

[7]  Christophe Nguyen-The,et al.  Influence of Background Microflora on Listeria monocytogenes on Minimally Processed Fresh Broad-Leaved Endive ( Cichorium endivia var. latifolia ). , 1996, Journal of food protection.

[8]  C. Hill,et al.  Bacteriocins: Biological tools for bio-preservation and shelf-life extension , 2006 .

[9]  A. Allende,et al.  Growth and bacteriocin production by lactic acid bacteria in vegetable broth and their effectiveness at reducing Listeria monocytogenes in vitro and in fresh-cut lettuce. , 2007, Food microbiology.

[10]  Chan-Ick Cheigh,et al.  Production of a nisin‐like bacteriocin by Lactococcus lactis subsp. lactis A164 isolated from Kimchi , 2000, Journal of applied microbiology.

[11]  G. Jung,et al.  Lantibiotics and microcins: polypeptides with unusual chemical diversity. , 2000, Current opinion in chemical biology.

[12]  F. Romeo,et al.  Occurrence of Listeria monocytogenes in green table olives. , 2004, Journal of food protection.

[13]  C. Nguyen-the,et al.  The microbiology of minimally processed fresh fruits and vegetables. , 1994, Critical reviews in food science and nutrition.

[14]  Elaine E. Vaughan,et al.  Diversity, Dynamics, and Activity of Bacterial Communities during Production of an Artisanal Sicilian Cheese as Evaluated by 16S rRNA Analysis , 2002, Applied and Environmental Microbiology.

[15]  L. Beuchat.  Ecological factors influencing survival and growth of human pathogens on raw fruits and vegetables. , 2002, Microbes and infection.

[16]  L. Beuchat,et al.  Comparison of chemical treatments to eliminate enterohemorrhagic Escherichia coli O157:H7 on alfalfa seeds. , 1999, Journal of food protection.

[17]  H. Ojamo,et al.  Exopolysaccharide-Producing Bacteria from Sugar Beets , 1999, Applied and Environmental Microbiology.

[18]  J. Kok,et al.  Use of a Genetically Enhanced, Pediocin-Producing Starter Culture, Lactococcus lactis subsp. lactis MM217, To Control Listeria monocytogenes in Cheddar Cheese , 1998, Applied and Environmental Microbiology.

[19]  D. O'beirne,et al.  The microbiological safety of minimally processed vegetables , 1999 .

[20]  S. Scherer,et al.  A Pediocin-Producing Lactobacillus plantarum Strain Inhibits Listeria monocytogenes in a Multispecies Cheese Surface Microbial Ripening Consortium , 2003, Applied and Environmental Microbiology.

[21]  L. Ng,et al.  Isolation and characterization of nisin‐producing Lactococcus lactis subsp. lactis from bean‐sprouts , 1997, Journal of applied microbiology.

[22]  Dike O Ukuku,et al.  Use of hydrogen peroxide in combination with nisin, sodium lactate and citric acid for reducing transfer of bacterial pathogens from whole melon surfaces to fresh-cut pieces. , 2005, International journal of food microbiology.

[23]  Ana Allende,et al.  Minimal processing for healthy traditional foods , 2006 .

[24]  H. Abriouel,et al.  Effect of Immersion Solutions Containing Enterocin AS-48 on Listeria monocytogenes in Vegetable Foods , 2005, Applied and Environmental Microbiology.

[25]  R. Amann,et al.  Sequence heterogeneities of genes encoding 16S rRNAs in Paenibacillus polymyxa detected by temperature gradient gel electrophoresis , 1996, Journal of bacteriology.

[26]  A. Uitterlinden,et al.  Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA , 1993, Applied and environmental microbiology.

[27]  M L Bari,et al.  Combined efficacy of nisin and pediocin with sodium lactate, citric acid, phytic acid, and potassium sorbate and EDTA in reducing the Listeria monocytogenes population of inoculated fresh-cut produce. , 2005, Journal of food protection.

[28]  R. Paull,et al.  Fruit temperature and crown removal on the occurrence of pineapple fruit translucency , 2001 .

[29]  O. Lamikanra,et al.  Fresh-Cut Fruits and Vegetables : Science, Technology, and Market , 2002 .

[30]  H. Nissen,et al.  Development and Evaluation of a 16S Ribosomal DNA Array-Based Approach for Describing Complex Microbial Communities in Ready-To-Eat Vegetable Salads Packed in a Modified Atmosphere , 2002, Applied and Environmental Microbiology.

[31]  A. Allende,et al.  Microbial and sensory quality of commercial fresh processed red lettuce throughout the production chain and shelf life. , 2004, International journal of food microbiology.

[32]  H. Abriouel,et al.  Bacteriocin-based strategies for food biopreservation. , 2007, International journal of food microbiology.

[33]  Danilo Ercolini,et al.  PCR-DGGE fingerprinting: novel strategies for detection of microbes in food. , 2004, Journal of microbiological methods.

[34]  S. Maisnier-Patin,et al.  Inhibition of Listeria monocytogenes in Camembert cheese made with a nisin-producing starter , 2006 .

[35]  G. López‐Gálvez,et al.  Quality changes in packaged salad products during storage , 1997 .

[36]  R. Bennett,et al.  Microbial evaluation of selected fresh produce obtained at retail markets. , 2002, Journal of food protection.

[37]  L. Beuchat,et al.  Efficacy of spray application of chlorinated water in killing pathogenic bacteria on raw apples, tomatoes, and lettuce. , 1998, Journal of food protection.

[38]  L. Cocolin,et al.  Direct Identification in Food Samples of Listeria spp. and Listeria monocytogenes by Molecular Methods , 2002, Applied and Environmental Microbiology.

[39]  William F. Fett,et al.  Effectiveness of chlorine and nisin-edta treatments of whole melons and fresh-cut pieces for reducing native microflora and extending shelf-life , 2002 .

[40]  D. O'beirne,et al.  Effects of process severity on survival and growth of Escherichia coli and Listeria innocua on minimally processed vegetables , 2005 .

[41]  S. Ennahar,et al.  Inhibition of Listeria monocytogenes in a smear-surface soft cheese by Lactobacillus plantarum WHE 92, a pediocin AcH producer. , 1998, Journal of food protection.

[42]  L. Leistner,et al.  Basic aspects of food preservation by hurdle technology. , 2000, International journal of food microbiology.

[43]  M. Harrison,et al.  Microbial antagonists of foodborne pathogens on fresh, minimally processed vegetables. , 2002, Journal of food protection.

[44]  J. Usall,et al.  Microbiological quality of fresh, minimally-processed fruit and vegetables, and sprouts from retail establishments. , 2008, International journal of food microbiology.

[45]  L. A. Rogers,et al.  LIMITING FACTORS IN THE LACTIC FERMENTATION , 1928, Journal of bacteriology.

[46]  R. Brackett,et al.  Shelf Stability and Safety of Fresh Produce as Influenced by Sanitation and Disinfection. , 1992, Journal of food protection.

[47]  Ming Yang,et al.  Biocontrol of Listeria monocytogenes on Fresh-Cut Produce by Treatment with Lytic Bacteriophages and a Bacteriocin , 2003, Applied and Environmental Microbiology.

[48]  R. Peixoto,et al.  Use of rpoB and 16S rRNA genes to analyse bacterial diversity of a tropical soil using PCR and DGGE , 2002, Letters in applied microbiology.

[49]  J. R. Gorny,et al.  Microbiological Safety of Fresh and Fresh-Cut Produce: Description of the Situation and Economic Impact , 2003 .

[50]  A. Simpson,et al.  Rapid silver staining and recovery of PCR products separated on polyacrylamide gels. , 1994, BioTechniques.

[51]  J. Farber,et al.  Changes in populations of Listeria monocytogenes inoculated on packaged fresh-cut vegetables. , 1998, Journal of food protection.

[52]  R. P. Ross,et al.  Inhibition of Listeria monocytogenes in cottage cheese manufactured with a lacticin 3147‐producing starter culture , 1999, Journal of applied microbiology.

[53]  F. Tomás-Barberán,et al.  Modified-atmosphere packaging of minimally processed “Lollo Rosso” (Lactuca sativa) Phenolic metabolites and quality changes , 1998 .

[54]  R. P. Ross,et al.  Lantibiotics: structure, biosynthesis and mode of action. , 2001, FEMS microbiology reviews.

[55]  Rosalia Trias,et al.  Bioprotection of Golden Delicious apples and Iceberg lettuce against foodborne bacterial pathogens by lactic acid bacteria. , 2008, International journal of food microbiology.

[56]  L. Settanni,et al.  Application of bacteriocins in vegetable food biopreservation. , 2008, International journal of food microbiology.

[57]  L. Cocolin,et al.  The rpoB gene as a target for PCR-DGGE analysis to follow lactic acid bacterial population dynamics during food fermentations , 2004 .

[58]  Martin R. Adams,et al.  Factors affecting the efficacy of washing procedures used in the production of prepared salads , 1989 .