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Antimicrobial Potential of Leuconostoc Species Against E. Coli O157:H7 in Ground Meat

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Antimicrobial Potential of Leuconostoc Species Against E. Coli O157:H7 in Ground Meat J Korean Soc Appl Biol Chem (2015) 58(6):831–838 Online ISSN 2234-344X DOI 10.1007/s13765-015-0112-0 Print ISSN 1738-2203 ARTICLE Antimicrobial potential of Leuconostoc species against E. coli O157:H7 in ground meat Ok Kyung Koo1,2 . Seung Min Kim1 . Sun-Hee Kang3 Received: 12 June 2015 / Accepted: 3 August 2015 / Published online: 12 August 2015 Ó The Korean Society for Applied Biological Chemistry 2015 Abstract Ground beef is risky by foodborne pathogens Keywords Antimicrobial activity Á Escherichia coli such as E. coli O157:H7 due to the cross-contamination O157:H7 Á Ground meat Á Leuconostoc during grinding. The objective of this study was to evaluate the antagonistic activities of Leuconostoc species isolated from ground beef product in order to limit the growth of Introduction E. coli O157:H7. While Leuconostoc has been known as spoilage bacteria, the Leuconostoc isolates showed Pathogenic Escherichia coli has been the most frequent antimicrobial activity on foodborne pathogens such as cause of foodborne illness in Korea since 2003 (MFDS E. coli O157:H7, Salmonella, Staphylococcus aureus, 2015). While enterohemorrhagic E. coli (EHEC) is not the Listeria monocytogenes, and meat-spoilage bacteria Bro- most reported pathogenic E. coli in Korea, it can cause chothrix thermosphacta. Antimicrobial activity of cell-free significant disease such as hemolytic uremic syndrome. supernatant (CFS) was evaluated by heat, enzyme, and pH E. coli O157:H7 is one of the most frequent EHEC by adjustment and antagonistic activity by cell competitive about 30 % of infection in Korea and it was first isolated growth. In addition, CFS concentration was screened for from a patient in 1998 in Korea (Jo et al. 2004). Raw meat the presence of organic acids for the antimicrobial prop- and other meat products contaminated with animal feces erties. Regulation of virulence genes was investigated by have been studied as the major sources of E. coli O157:H7. inhibition of locus of enterocyte effacement expression by Especially, ground meat product which is one of the most CFS. The result showed that Leuconostoc isolates inhibited consumed types of meat, was ranked as the highest risk of the growth of E. coli O157:H7 by active antimicrobial contamination by foodborne pathogens (Mintel Group Ltd agent including organic acids and the growth of back- 2010). In addition, intervention technology on E. coli ground microorganisms, and E. coli O157:H7 in ground O157:H7 control should be continuous regardless of the beef was inhibited with the supplement of the CFS. seasons, since the prevalence was not affected by the seasons (Williams et al. 2010). While food safety regula- tions and HACCP programs reduced the risk of foodborne illness associated with contaminated ground beef, there are & Ok Kyung Koo still pre-consumer interventions that are necessary to [email protected] minimize the risk (Taylor et al. 2012). Although the efforts seemed to control the contamination, there are continuous 1 Food Safety Research Group, Korea Food Research Institute, outbreaks and recalls reported. In addition, there are 1201-62, Anyangpangyo-ro, Bundang-gu, Seongnam-si, Gyeonggi-do 13539, Republic of Korea increasing demands on no additives or chemical residues, minimal processing, convenient preparation, safe, and 2 Department of Food Biotechnology, Korea University of Science & Technology, Daejeon 34113, Republic of Korea economic production by consumers. Various types of natural antimicrobial materials have 3 Traditional Alcoholic Beverages Research Team, Korea Food Research Institute, Seongnam-si, Gyeonggi-do 13539, been tested in ground meat to reduce foodborne pathogens Republic of Korea by researchers. Essential oils have been a great approach 123 832 J Korean Soc Appl Biol Chem (2015) 58(6):831–838 by their antimicrobial efficiency such as clove and Materials and methods lemongrass in bovine ground meat to reduce L. monocy- togenes (de Oliveira et al. 2013) and cinnamon and olive Bacteria extract to reduce S. Typhimurium in ground pork (Chen et al. 2013). However, essential oils have a strong and Staphylococcus aureus ATCC 6538, ATCC 25923, and unique flavor that can limit the practical application in KCCM 40881; Salmonella Typhimurium PTU 302, PT 10, market. Cranberry concentrates in ground beef reduced and ATCC 14028; Listeria monocytogenes ATCC 15315, E. coli O157:H7 growth. Other chemical agents such as ATCC 19114, and ATCC 19115; Escherichia coli O157:H7 lauric arginate with carvacrol showed synergistic effect in ATCC 43895, ATCC 43890, and NCCP 11091; and Bro- ground turkey by reducing Salmonella (Oladunjoye et al. chothrix thermosphacta KCTC 3402 were used in this study. 2013). Mustard leaf kimchi extract was added to raw All strains were from the culture collection at the Korea ground pork and the total microbial count decreased sig- Food Research Institute. The cultures were maintained in nificantly (Lee et al. 2010). Physical treatments that have 15 % glycerol at -80 °C. S. aureus, S. Typhimurium, and been applied to meat products for the bacterial inactivation E. coli O157:H7 were incubated in tryptic soy broth (TSB, are temperature control, radiation, high pressure process- Merck& Co., USA). L. monocytogenes was incubated in ing, pulsed electric fields and others, or packaging with TSB supplemented with 0.6 % yeast extract (TSB-YE) (BD, modified atmosphere and/or active packaging with modi- USA), and B. thermosphacta was incubated in brain heart fied packaging materials (Mor-Mur and Yuste, 2010). infusion broth (BD). They were incubated at 37 °C for Bacteriophages are another novel antimicrobial agent due 18–20 h, except B. thermosphacta which was incubated at to the high specificity and the examples are L. monocyto- 25 °C before starting the experiment. genes-specific phage (LMP-102) and E. coli O157:H7- specific bacteriophage in ground meat (Abuladze et al. Isolation and identification of antagonistic bacteria 2008). Lactic acid bacteria (LAB) can be used in the food products in the form of fermented food, food biopreser- Ground beef was purchased from local grocery stores in vatives, and functional food. This application is primarily Gyeonggi-do, Korea, and the products were kept under based on their antimicrobial activities and their safe and refrigeration until use. Purchased ground beef was used health benefits to human (Suskovic et al. 2010). within 24 h of purchase. In order to isolate antagonistic Leuconostoc spp. has been known as spoilage bacteria, bacteria from the food product, 25 g of ground meat was while it is also known to have antimicrobial activity by homogenized with 225 mL of 0.1 % peptone water for producing bacteriocin such as leucocin and mesentericin. 2 min using stomacher (Interscience, France). Then, the These bacteriocins were reported to be produced only by homogenized sample was plated on MRS agar and plate Leu. mesenteroides, Leu. gelidum, Leu. carnosum, and Leu. count agar. Once the colonies were grown, TSA 0.8 % agar pseudomesenteroides (Pujato et al. 2014). Lactic acid was poured over the plates with 0.1 % of overnight cul- bacteria produce antimicrobial substances, and bacteriocin tured E. coli O157:H7 ATCC 43895. Any colonies with a has been most studied. Bacteriocin is a small cationic clear zone were isolated for the further identification. Any peptide that can kill target bacteria by pore-forming the colonies showing antimicrobial activity were selected, and cytoplasmic membrane. Nisin (NisaplinÒ), pediocin the genomic DNA was extracted and its 16s rRNA was (ALTA 2341), and enterocin (AS-48, CCM4231, and EJ97) sequenced and identified using the EzTaxon server (http:// are the commercial bacteriocins that can be used in food www.ezbiocloud.net/eztaxon; Kim et al. 2012). products (Yang et al. 2014). However, the range of antimicrobial target of bacteriocins tends to be limited predominantly by gram-positive bacteria, and bacteriocin Antimicrobial activity analysis resistance has been an emerging concern that other types of antimicrobials are in demand (Hartmann et al. 2011). Not Double layer assay was performed by spot-inoculation of only bacteriocins but also other antimicrobial substances colonies of isolates on MRS and incubated at 30 °C for are produced by LAB, such as organic acids, biosurfac- 48 h. Cocktails of the overnight culture of S. aureus, S. tants, hydrogen peroxide, and low molecular mass com- Typhimurium, L. monocytogenes, E. coli, and B. thermo- pounds. Therefore, crude bacterial fermentate application sphacta, respectively, were prepared with equal concen- is another type of antimicrobials to show synergistic effects tration and inoculated in TSA 0.8 % agar with total to the food product (Hartmann et al. 2011). The purpose of concentration of 107 CFU/mL, and the soft agar was this study was to isolate antagonistic bacteria such as poured onto the MRS. The double layer plate was incu- Leuconostoc spp. from food to inhibit the growth of E. coli bated at 37 °C for 24 h, and the diameters of inhibition O157:H7 and to investigate the antimicrobial properties. zone were measured. 123 J Korean Soc Appl Biol Chem (2015) 58(6):831–838 833 Based on double layer assay, isolated Leuconostoc spp. The analysis of derivative organic compounds including were selected and their antimicrobial activity was investi- phenyllactic acid and hydroxyphenyllactic acid, which gated with the culture supernatant and the cells. Overnight have shown the antimicrobial activities by Leuconostoc, culture of Leuconostoc isolates was subcultured at 30 °C was carried out using the filter-sterilized overnight CFS in for 24 h. The culture was centrifuged at 5,3009g for a UPLC system (Agilent 1290 infinity, Agilent). The sys- 10 min, and the supernatant was sterilized using 0.45 lm tem was coupled with an accurate-mass quadrupole-time- filter. The pellet was further used for the competitive of-flight instrument (Agilent 6520 with Jet Stream Tech- growth study. The culture supernatant was treated with nology, Agilent) with an ACE Excel UHPLC column three different methods.
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