Critical Reviews in Biotechnology

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Trends in utilization of agro-industrial byproducts for production of bacteriocins and their biopreservative applications Vandana Bali, Parmjit S. Panesar & Manab B. Bera To cite this article: Vandana Bali, Parmjit S. Panesar & Manab B. Bera (2016) Trends in utilization of agro-industrial byproducts for production of bacteriocins and their biopreservative applications, Critical Reviews in Biotechnology, 36:2, 204-214, DOI: 10.3109/07388551.2014.947916 To link to this article: http://dx.doi.org/10.3109/07388551.2014.947916

Published online: 28 Nov 2014.

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Date: 15 October 2016, At: 09:15

http://informahealthcare.com/bty ISSN: 0738-8551 (print), 1549-7801 (electronic) Crit Rev Biotechnol, 2016; 36(2): 204–214 ! 2014 Informa Healthcare USA, Inc. DOI: 10.3109/07388551.2014.947916

REVIEW ARTICLE

Trends in utilization of agro-industrial byproducts for production of bacteriocins and their biopreservative applications Vandana Bali, Parmjit S. Panesar, and Manab B. Bera Biotechnology Research Laboratory, Department of Food Engineering and Technology, Sant Longowal Institute of Engineering and Technology, Longowal, Punjab, India Abstract

Keywords

Bacteriocins are proteinaceous, ribosomally synthesized bio-molecules having major roles in food preservation due to their antimicrobial action against food spoilage microorganisms. These have gained importance in the last decades because of increasing interest in natural products and their applications in the field of biopreservation, pharmaceutical, aquaculture, livestock, etc. Their production is quite expensive which includes the cost of synthetic media and downstream processing of which 30% of the total production cost relies on synthetic media and nutritional supplements used for growth of microorganisms. The low cost agroindustrial by-products, rich in nutritional supplements, can act as a good substitute for high valued synthetic media. This review provides comprehensive information on the use of cost effective, renewable agro-industrial by-products as substrates for the production of bacteriocins and their application in food as biopreservatives.

Agro-industrial by-products, antimicrobial packaging, bacteriocin, immobilization, production, whey

Introduction Globally, there is a lot of concern about the preservation and safety of food products among the consumers. A number of methods especially thermal treatment or chemical treatments are commonly used for the purpose. The level of microorganisms that survive in food is affected by the degree of heat treatment and time of exposure. In addition, the composition of food, moisture level and other environmental conditions is determined by the level of killing of microorganisms by heat. Boiling food for a short duration inhibits enzyme activity besides removing surface microorganisms. Pasteurization leads to killing of vegetative forms of food borne vegetative bacteria, yeast and moulds, however heat resistant strains especially Clostridium botulinum and spores remain there. Growth of these survived microorganisms can be further minimized by low temperature, low pH or addition of chemical preservatives. Sterilization at a temperature 4100  C may lead to denaturation of proteins, undesirable browning of food, loss of nutrients especially vitamins and flavoring compounds (Lado & Yousef, 2002). Further addition of more ingredients to heat treated food at later stages may add to microbial load (Stannard, 1997). However, excessive use of chemical preservatives is associated with many drawbacks and side effects such as allergies, Address for correspondence: Parmjit S. Panesar, Biotechnology Research Laboratory, Department of Food Engineering and Technology, Sant Longowal Institute of Engineering and Technology, Longowal 148106, Punjab, India. Tel: +91-1672-253252. Fax: +91-1672-280057. E-mail: [email protected]

History Received 24 September 2012 Revised 19 April 2014 Accepted 1 July 2014 Published online 26 November 2014

indigestibility and headaches (Devlieghere et al., 2004; Ross et al., 2002). Meat and other related products are commonly preserved by adding salt or sodium nitrite. Epidemiology data have shown increased risk of cancer by excessive consumption of these nitrites (Kushi et al., 2012; Norat et al., 2010). Thus, due to thermal denaturation or the harmful effects of chemical preservatives, alternative technologies of biopreservatives are being developed (Altuntas et al., 2010; Gu¨llu¨ce et al., 2013). Bacteriocins are extracellular, ribosomally synthesized, peptides or proteins or peptide complexes that show a bactericidal/static effect against closely related species (Tagg et al., 1976). The bacteriocins produced by lactic acid bacteria are also reported to possess antimicrobial activity against phylogenetically distant species and food spoilage microorganisms such as Campylobacter sp., Clostridium perfringens, Listeria monocytogenes, Bacillus cereus, Staphylococcus aureus etc. (Bali et al., 2013; Mehta et al., 2013; Messaoudi et al., 2012; Omar et al., 2013; Svetoch & Stern, 2010). Based on their various characteristics, bacteriocins have been classified into the following different classes (Rea et al., 2011): (a) Class I: Post translationally modified bacteriocins, which have been further subdivided into four groups: Class Ia (Lantibiotics) having small peptides 55 kDa and 19–28 amino acids and further subdivided into four subclasses I, II, III and IV; Class Ib (Labyrinthopeptins) having carbacyclic modified amino acid labionin; Class Ic (sactibiotics) having sulphur to the a-carbon linkage. Sactibiotics have been further subdivided into single and two peptide bacteriocins. Earlier, a number of authors

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proposed different subclasses/types for lantibiotic bacteriocins (Cotter et al., 2005a,b; Heng et al., 2007; Jung, 1991; Pag & Sahl, 2002; Piper et al., 2009; Willey & van der Donk, 2007) e.g. Nisin A, Subtilin, Lacticin. (b) Class II: Unmodified bacteriocins, 510 kDa have heterogeneous groups of peptides, which have been further classified in Class IIa (pediocin like), Class IIb (two peptide unmodified bacteriocins); Class IIc (circular bacteriocins) and Class IId (unmodified, linear, nonpediocin like bacteriocins). These classes have been further subdivided into various subclasses (Rea et al., 2011) e.g. pediocin PA1, enterocin A, circularin A, plantaricin S. (c) Bacteriolysins (Formerly class III bacteriocins) have large heat stable antimicrobial proteins. These are basically non-bacteriocin lytic proteins with a domain type structure e.g. lysostaphin, helveticin J. Products from microbial sources are more useful as compared to animal/plant origin as these can be conveniently produced in large quantities by fermentation (Bali et al., 2011). Wide applications for the bacteriocin including their biopreservative potential have been reported in the literature (Balciunas et al., 2013; Koueta et al., 2014; Kumar et al., 2012; O’Shea et al., 2013). Besides bringing about a reduction in food spoilage organisms and providing fresh tasting foods, bacteriocin applications include decreasing food poisoning, improved shelf life of the product and maintaining food nutritional value (Galvez et al., 2007, 2011; Robertson et al., 2004; Thomas et al., 2000). Bacteriocins have been widely applied in purified and concentrated/immobilized form as preservatives in the dairy and food industries (Faye et al., 2000; Kumar et al., 2012; Molinos et al., 2008; Munoz et al., 2007), alcoholic beverages (Ruiz-Larrea et al., 2010) and the baking industry (Martinez-Viedma et al., 2011). Inhibition of spoilage bacteria by bacteriocin in beer, wine and cider has been reported by Galvez et al. (2011). Contamination and spoilage of fresh cut vegetables, fruits and seed sprouts could be prevented with the application of bacteriocins (Molinos et al., 2005, 2008). Different concentrations of bacteriocin is required for inhibiting growth of single type target bacteria or mixed populations (Grande et al., 2006, 2007). Development of bacteriocin disinfectants in the form of wipes is helpful in prevention and protection against pathogenic microbes (Blackburn & de la Harpe, 1998). The use of bacteriocin in preventing the growth of microbes responsible for gum infection and tooth decay has been reported (McConville & Beecham, 1995). In meat and poultry products, bacteriocin helps in the decontamination of raw meat and inhibition of pathogens in cooked and fermented meat products (Gu¨llu¨ce et al., 2013). Bacteriocin has also found application as alternative antibiotics for medical and veterinary use (Dobson et al., 2011; Klostermann et al., 2010). Hassan et al. (2012) extensively reviewed the potential application of these antimicrobial peptides against antibiotic resistance (Figure 1). Due to narrow spectrum and specificity (inhibit closely related or particular pathogens), the non-inhibitory effect on beneficial bacteria, high potency (pico-nanomolar), bacteriocin is more significant as compared to antibiotics. Further, due to the development of multidrug resistant pathogens against

Packaging

205

Waste treatment

Bio-preservation

Livestock Bacteriocin

Aquaculture

Quorum sensing

Human health

Pharmaceutical

Figure 1. Potential applications of bacteriocins.

different antibiotics, there is extensive need for the discovery of novel antimicrobial agents (Papadimitriou & Alexandraki, 2014). The application of bacteriocin producing L. lactis and P. acidilactici isolated from human feces decreased the intestinal colonization of vancomycin resistant enterococci in a mouse model (Millette et al., 2008). Cost is one of the important factors affecting the production of bacteriocin and, thus, restricts the application of bacteriocin as a food additive or its other applications (Han et al., 2011; Makkar et al., 2011). Addition of various peptides like biopeptone, meat extract, yeast extract in commercial media including MRS, resulted in the high cost of bacteriocin production (Ogunbanwo et al., 2003). To make the fermentation process/product economically viable, various methods can be employed. Overproduction of bacteriocin can be obtained by strain improvement/modification, optimizing various process parameters including media components, temperature, pH etc. (Abbasiliasi et al., 2011; Garsa, et al., 2014; Saeed & Salam, 2013; Vera Pingitore et al., 2009) and cost effective downstream processing. Replacement of yeast extract with beef extract/malt extract resulted in decreased biomass and bacteriocin production in L. sakei CCUG 42687 (Aasen et al., 2000), while tryptone resulted in high bacteriocin levels as compared to peptone/soytone (Lechiancole et al., 2002). As the cost of medium commonly used is quite high, another approach involved in the inexpensive production of bacteriocin is the use of raw substrates (industrial byproducts with least or no value), having appropriate and sufficient amounts of balanced nutrients required for growth and product formation (Guerra et al., 2001). As per report on ‘‘Food Preservative Market: Global trend and forecast to 2018’’, the global food preservative market will be growing at 2.4% of the compound annual growth rate with more demand for natural preservatives due to consumer preferences for safe preservatives (http://www.marketsandmarkets.com/MarketReports/food-preservatives-market-420.html). Further, natural preservatives are cost effective as they are required in very small dosage.

Bacteriocin production from industrial by-products Various industrial byproducts from the food processing industries, rich in carbon and nitrogen sources, like whey, molasses, marine byproducts, etc. (Table 1) have been explored as low cost nutritional medium for the production of bacteriocin. Utilization of waste material for the production of bio-molecules is favorable due to low cost and reduction in environmental pollution (Makkar et al., 2011).

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Table 1. Various food industry by-products used for bacteriocin production. Industrial by-product Whey

Whey permeate Mussel processing waste Cheese whey Octopus peptone Cull potatoes Visceral and fish muscle residues Condensed distillers solubles Skimmed milk Soybean meal Fermented barley extract Sweet whey Molasses

Microorganism

Bacteriocin

References

Lactococcus lactis subsp. lactis CECT 539 Pediococcus acidilactici NRRL B-5627 Enterococcus faecalis A-48-32 Lactobacillus casei subsp. casei CECT 4043 Lactococcus lactis subsp. lactis ATCC 7962 Pediococcus acidilactici C20 Lactococcus lactis subsp. lactis CECT 539 Pediococcus acidilactici NRRL B-5627 Bacillus licheniformis P40 Lactococcus lactis subsp. lactis ATCC 11454 Lactococcus lactis Pediococcus acidilactici Lactococcus lactis subsp. lactis ATCC 11454 L. lactis CECT 539 P. acidilactici NRRL B-5627 Lactococcus lactis subsp. lactis ATCC 11454 Lactococcus lactis subsp. lactis ATCC 11454 Bacillus sp. P34 Bacillus sp. P11 Lactococcus lactis subsp. lactis ATCC 11454 Lactococcus lactis UQ2 Leuconostoc mesenteroides E131

Nisin Pediocin Enterocin AS-48 Nisin Nisin Pediocin C20 Nisin Pediocin NA Nisin Nisin Pediocin Nisin Nisin Pediocin Nisin Nisin NA NA Nisin Nisin Bacteriocin

Guerra et al. (2001) Guerra et al. (2005a) Ananou et al. (2008) Berna´rdez et al. (2008) Flores & Alegre (2001) Halami & Chandrashekar (2005) Guerra & Castro (2002) Guerra & Castro (2002) Cladera-Olivera et al. (2004) Liu et al. (2004) Va´zquez et al. (2004c) Va´zquez et al. (2004c) Liu et al. (2005b) Va´zquez et al. (2006) Liu et al. (2007) Jozala et al. (2007) Motta & Brandelli (2007) Lea˜es et al. (2011) Furuta et al. (2008) Gonza´lez-Toledo et al. (2010) Metsoviti et al. (2011)

NA, Not available.

Bacteriocin production from whey Whey, a byproduct of the dairy industry, is produced during cheese production constituting lactose (75% of dry matter) and protein (12–14%). Of the total whey produced, only 50% is recycled into useful products such as animal feed and food ingredients. Disposal of whey is problematic due to its high biological oxygen demand (BOD) value. Thus, processes have been developed for the utilization of whey in the production of bacteriocin (Cladera-Olivera et al., 2004; Liu et al., 2004, 2005a). Although differences in production rate was observed, whey supported the production of both biomass and bacteriocins as compared to other media (de Man et al., 1964; Guerra & Pastrana, 2002a; Halami & Chandrashekar, 2005; Jozala et al., 2007; Mirhosseini & Emtiazi, 2011). Diluted whey resulted in higher titer of nisin and pediocin from Lactococcus lactis subsp. lactis CECT 539 and P. acidilactici NRRL B-5627, respectively, as compared to concentrated whey in batch fermentation (Guerra et al., 2001). Nisin activity of 5280 IU mL 1 has been achieved during batch fermentation of L. lactis subsp. lactis ATCC 7962 on supplemented cheese whey permeate after 9 h incubation (Flores & Alegre, 2001). The recombinant strains of L. lactis ssp. lactis, Streptococcus thermophilus and E. faecalis have been successfully used for the pediocin production in skim milk and cheese whey (Somkuti & Steinberg, 2003). The re-alkalized fed-batch culture was characterized by higher biomass and pediocin concentrations by P. acidilactici NRRL B-5627 on whey as compared with batch processes (Guerra & Castro, 2003; Guerra et al., 2005b). Statistical analysis of response surface methodology showed maximum bacteriocin production at an initial pH and temperature between 6.5–7.5 and 26–37  C, respectively, with 70 g L 1 whey concentration. Simultaneous production of nisin (92.9 mg L 1) and lactic acid (19.3 g L 1) by L. lactis subsp. lactis ATCC 11454 has

been achieved using a cheese whey based medium (Liu et al., 2004). The effect of the extremely low-frequency (ELF) magnetic field on nisin production by L. lactis subsp. lactis using cheese whey permeate was studied during batch fermentation (Alvarez et al., 2006). With respect to substrate consumption and biomass formed, nisin yield was reported to be three and five times higher, respectively, as compared to the control under magnetic field treatment (4 h, 1.50 m s 1 and 5 mT). Mixed cultures of Saccharomyces cerevisiae with L. lactis subsp. lactis ATCC 11454 were cultured to stimulate the production of nisin (0.85 times) on whey based medium (Liu et al., 2006). S. cerevisiae utilized the lactic acid and maintained the pH at 6.0, thus increasing nisin production. Pediocin production by P. acidilactici NRRL B-5627 was followed in both batch and re-alkalized fed-batch fermentations on diluted whey (DW) supplemented with 2% (w/v) yeast extract (DWYE2) medium (Guerra et al., 2007). The studies indicated that the use of feeding substrates containing glucose instead of lactose could be an appropriate alternative for increasing fed-batch production of pediocin. The whey derived substrate Esprion-300 has been used for the production of bacteriocin AS-48 by Enterococcus faecalis A-48-32 (Ananou et al., 2008). Optimized parameters, i.e. 5% (w/v) Esprion-300 and 1% (w/v) glucose with 8% (v/v) inoculum level at 28  C, pH 6.5 for 18 h gave maximum activity of 360 AU mL 1. Maximum Lactobacillus casei CECT 4043 biomass (0.33 g L 1) with antibacterial activity (3.42 AU mL 1) was reported using diluted whey based media with batch fermentation after 12 h of incubation (Bernardez et al., 2008). Dried semi-purified nisin produced in a bioreactor by L. lactis UQ2 on supplemented whey medium showed activity of 102 150 IU g 1 (Gonzalez-Toledo et al., 2010). Bacteriocin producing microorganisms have also been immobilized on different matrices for increasing the

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Table 2. Production of bacteriocin using various microorganisms immobilized on different material.

Microorganism

Immobilization matrix

Bacteriocin produced

Lactococcus lactis subsp. lactis NZ1 Pediococcus acidilactici P02

Calcium alginate

Nisin

Entrapment in the void volume within the fibrous matrix

Pediocin

Carnobacterium divergens V41

Calcium alginate

Divercin

Enterococcus faecium A 2000

Calcium alginate

Enterocin

Lactococcus lactis subsp. lactis DPC 3147 Lactococcus lactis IO-1

Calcium alginate

Lacticin 3147

Porous chitosan beads, Chitopearl SH-2510 Photo-crosslinked resin gel beads, ENTG-3800 -Carrageenan/locust bean gum gel

Nisin Z

Lactococcus lactis IO-1 Lactococcus lactis subsp. lactis biovar diacetylactis UL719 Lactococcus lactis

Calcium alginate

Pediococcus acidilactici UL5

-Carrageenan/locust bean gum gel

Lactobacillus paracasei HD1.7

Calcium alginate

Nisin Z Nisin Z Nisin

Remarks Comparable production achieved as with batch culture Pediocin activity of 6400 AU mL 1 at dilution rates of 1.19 day 1 at pH 4.5; 1.0  107 AU L 1 day 1 at dilution rate of 1.58 day l at pH 4.5. Activity increased to 105 AU L 1 h 1 from 2.8  103 AU L 1 h 1 in batch fermentation. Production increased by 50%; immobilized cells reused up to three times. Stable and long term production of 5120 AU mL 1. Productivity about 1.7 times greater than the free cells. Improved productivity at higher dilution rates. Stable and high nisin-Z production (8200 IU mL 1).

Nisin activity increased 2.1-fold in batch, and 2.9-fold in fed batch system. Pediocin PA-1 Increased pediocin productivity (4096 AU mL 1) activity for over 12 fermentation cycles. Paracin 1.7 Increased productivity up to (19%).

bacteriocin productivity (Table 2). Maximum pediocin activity and productivity of 6400 AU mL 1 and 1.0  107 AU L 1 day 1 has been achieved with dilution rates 1.19 and 1.58 day 1 with controlled pH at 4.5. The effect of aeration and dilution rate on continuous production of nisin Z by L. lactis UL719 was also studied in both free cell and immobilized cells in supplemented whey media (Desjardins et al., 2001). The results showed maximum production of 1090 IU mL 1 at dilution rate of 0.5 h 1 and increased to 2560 IU mL 1 with an increase in aeration rate. L. lactis subsp. lactis biovar. diacetylactis UL719 was immobilized in k-carrageenan/locust bean gum gel beads in supplemented whey permeate medium for the production of nisin (Bertrand et al., 2001). The highest levels of nisin production was obtained by repeated cycle pH controlled batch process as compared to free cell batch or free cell/immobilized cell continuous culture process. The immobilized L. lactis subsp. lactis ATCC 11454 has been employed in a packed bed bioreactor for the continuous production of nisin in laboratory media and whey permeate (Liu et al., 2005a). The bioreactor can be operated continuously for 6 months without encountering any clogging, degeneration or contamination problems. Using whey permeate supplemented medium, repeated cycle batch system has been developed for pediocin PA-1/AcH production by immobilized P. acidilactici UL5 cells (Naghmouchi et al., 2008). Similarly, Gassericin A has been produced from L. gasseri LA39 using cheese whey based medium (Nakamura et al., 2013). Jozala et al. (2013) studied the production of nisin from L. lactis using different concentrations of milk whey (10–100 gL 1). Supplementation

References Zezza et al. (1993) Cho et al. (1996)

Bhugaloo-Vial et al. (1997) Ivanova et al. (2000) Scannell et al. (2000) Sonomoto et al., 2000 Sonomoto et al. (2000) Bertrand et al, (2001) Miserendino et al. (2008) Naghmouchi et al. (2008) Chen et al. (2009)

of this medium with yeast extract and tomato extract resulted in increased bacteriocin production. Entrapped and surface entrapped lactobacilli in calcium alginate beads have been used as a delivery system with preserved viability and antimicrobial activity (Brachkova et al., 2010). This study has opened the possibility of utilization of whey for continuous production of high levels of bacteriocin by lactic acid bacteria for possible application as a food biopreservative. Bacteriocin production from marine byproduct waste Mussel processing waste, being rich in glycogen, has been used for the production of bacteriocin. Various media components and process parameters influence the bacteriocin productivity, therefore, different models have also been studied for bacteriocin production and its optimization. Guerra & Castro (2002) used modified Luedeking and Piret expression for modeling the production of nisin and pediocin using L. lactis subsp. lactis CECT 539 and P. acidilactici NRRL B-5627 respectively, on mussel-processing wastes. The influence of different process parameters like total sugars, nitrogen, phosphorus and buffer concentration on the production of bacteriocin were also studied using response surface methodology. Enhanced nisin production (33 BU mL 1) and pediocin (368 BU mL 1) production was achieved in optimized media. The hydrolyzed medium containing (per L) glucose (5.33 g), protein (1.8 g), total nitrogen (0.65 g) and total phosphorus (0.14 g) with pH 6.3 was prepared after

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treatment of mussel processing waste for bacteriocin production. Addition of carbon (glucose), nitrogen (glycine), phosphorous (KH2PO4) and buffer on the hydrolyzed medium was studied. Increased production of nisin was observed in buffered media, while high pediocin levels were obtained in non-buffered media. Further, the supplementation of glucose and nitrogen (Yeast extract, bacto casitone, ammonium chloride, glycine and glutamic acid) sources were conducted to increase the production of nisin and pediocin using second order orthogonal factorial design (Guerra & Pastrana, 2002b). A three-fold increase was observed in the production of both nisin (from 32 to 100 BU mL 1) and pediocin (from 322 to 934 BU mL 1) as compared to the unsupplemented medium. Applying the mathematical model, it was concluded that mussel-processing waste with two re-alkalinized cycles yielded the highest biomass and pediocin from P. acidilactici NRRL B-5627 in fed-batch fermentation as compared to batch fermentation (Guerra et al., 2005a). Factorial experiments and empirical modeling have been applied to optimize the composition of mussel-processing waste and whey media for the production of pediocin from P. acidilactici NRRL B5627 and nisin from L. lactis subsp. lactis CECT 539 (Pastrana et al., 2005). Further supplementation of yeast extract or casitone increased the production of pediocin or nisin as compared to De Man, Rogosa and Sharpe (MRS) media (De Man et al., 1964). Comparable production of bacteriocin and promoting growth of lactic acid bacteria was reported by utilizing marine by-products as waste protein sources like octopus peptone from food processing industries waste water and fishery residues with that of commercial media or bactopeptones (Vazquez et al., 2004a,c). Pediocin was produced by P. acidilactici using waste material by solid-state fermentation (Vazquez et al., 2004b). Visceral and fish muscle residues have also been used for the increased production of bacteriocin (pediocin, 4500%) as compared to commercially available media (Vazquez et al., 2006). Autohydrolysis of visceral residues at 20  C produced more bacterial growth as compared to fish muscles treated with pepsin. Media supplemented with snow crab hepatopancreas have been used for the production of divergicin M35 resulting in enhanced activity of 3.7  104 AU mL 1. achieved after 10 h batch fermentation at 25 and 30  C and pH 7.0 using Carnobacterium divergens M35 (Tahiri et al., 2009). Bacteriocin production from molasses Molasses, a byproduct of the sugar industry, by weight constitutes of 50–55% fermentable sugar, 9–12% non-sugar organic matter, proteins, vitamins and inorganic components (Maneerat, 2005). A waste molasses based medium has been used for the industrial production of solvents by Clostridium acetobutylicum and release of bacteriocin was reported during the fermentation process (Barber et al., 1979). The potential of bacteriocins produced by Lactobacillus plantarum BN as biopreservative for raw meat was analyzed and the production was achieved in enriched sugarcane molasses medium (3%, w/v) which extended the shelf life of raw meat from 3 to 9 days (Fiorentini et al., 2001). Comparable growth of bacteriocin producing Lactobacillus plantarum AMA-K was observed in molasses-based (10%, w/v) media as compared

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to MRS (Todorov, 2008). Low-cost carbon sources like waste molasses and sugar refinery plant waste were utilized for the production of bacteriocin from Leuconostoc mesenteroides E131 in submerged shake flasks (Metsoviti et al., 2011). Waste molasses proved to be the best carbon source for the production of both biomass and bacteriocin (with activity 320 AU mL 1) with the accumulation of mannitol in the medium. Bacteriocin production from soy waste Increased health awareness of consumers have focused the interest of the food industry towards soy based foods and drinks. Soy byproduct constituting 30% (w/v) fermentable carbohydrates and nearly 60% (w/v) solid carbohydrates can serve as a good source of carbon for supporting the growth of microorganisms. Studies have indicated that soy waste and its supplementation with other nutrients (waste or commercial media) can effectively increase bacteriocin productivity (Lea˜es et al., 2011; Mitra et al., 2010). Soya-bean protein based medium gave the maximum activity with bacteriocin production from Bacillus sp. P 34 as compared to no activity in other waste substrates such as fish meal, feather meal, whey and grape waste (Motta & Brandelli, 2007). The soy waste and its supplementation can be utilized as potential substitute for the commercially available media for bacteriocin production under optimized conditions, thereby, reducing the production cost. Both peptide powder obtained from soya-bean fermentation and soybean meal, a byproduct of soybean oil extraction, at concentration of 10 g/L resulted in maximum production of bacteriocin. Approximately 40.6% cost reduction was obtained in bacteriocin production by Lactobacillus plantarum YJG as compared to MRS media (Han et al., 2011). Bacteriocin production from other industrial wastes Waste from the agro-industry and food processing industry, such as potato liquor, grape waste, fish meal, have been utilized as the nutritional supplementation of microorganisms for the production of bacteriocin (Baranova et al., 1993; Lea˜es et al., 2011). Cull potatoes, waste potato tubers, along with peptone from soy and corn steep solid (as nutritional supplements) have been used as a nutrient medium for the simultaneous production of nisin and lactic acid by L. lactis subsp. lactis ATCC 11454 (Liu et al., 2005b). Condensed distillers soluble (CDS)-based medium, co-product of ethanol industry, was also optimized through RSM for the production of nisin and lactic acid by L. lactis subsp. lactis ATCC 11454 (Liu et al., 2007). Two-fold increases in nisin were observed with the addition of 5% CDS. However, at higher concentrations (5–15%), production inhibition was observed due to the presence of lactate and acetate in the medium. Addition of auxiliary nutrients like yeast extract for further improvement in production was carried out. CDS (37 g/L) and Yeast extract (7.5 g/L) were optimized for maximum production. Broad spectrum bacteriocin (bacST4SA) with 12 800 AU mL 1 activity was produced on corn steep liquor and production was increased to 102 400 AU mL 1 under optimized conditions (Coetzee et al., 2007). Yields comparable to a basal medium of nisin A by L. lactis subsp. lactis ATCC 11454 was reported from a glucose-supplemented ethanol insoluble fraction of fermented barley extract from shochu kasu, a by-

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product of barley shochu (Furuta et al., 2008). More than 2 million tons of dates are discarded every year due to its improper texture. Dates are rich in carbohydrate, protein and number of minerals such as iron, potassium, calcium and can be used for the production of various bioactive compounds including bacteriocins (Khiyami et al., 2008; Tang et al., 2014).

Application of bacteriocins in food preservation Bacteriocins have a wide range of applications in food preservation, health care and pharmaceuticals, especially in treating infectious diseases and as therapeutic agents. Biopreservation of the food products can be carried out by supplementing with bacteriocins or by inoculation of the bacteriocin producing strain under conditions favoring in situ production of bacteriocin. Application of bacteriocins by in situ method In situ production of bacteriocins is a comparatively favorable method than its application ex situ. It bears the additional advantage that both fermentation and bacteriocin production will take place during product formation, thereby, increasing the shelf life of food products. The applications of various bacteriocins in the preservation of red meat carcasses, raw pork and fresh pork sausages has been reported, although wide variations in the degree of inhibition were observed (Cutter & Siragusa, 1998; Pawar et al., 2000; Zhang et al., 2010). Bacteriocin producing starter cultures or co-starter cultures has been used in various fermentation processes (Hurtado et al., 2011; Leal-Sanchez et al., 2002). Lactic acid bacteria producing bacteriocin have been used as starter cultures to control and inactivate pathogenic microorganisms such as L. monocytogenes in various food items (Galvez et al., 2008). Further, such microorganisms have been isolated from various food sources to be used as starter cultures. Lactobacillus lactis 40FEL3LAB isolated from fermented Italian food can be used as starter cultures in cottage cheese and have the ability to control Listeria monocytogenes (Bello et al., 2011). Staphylococcus xylosus S03/1M/1/2 survived efficiently in salamis, a traditional dry-fermented Slovakian meat product and produces heat stable bacteriocin with inhibitory activity in pH 5–7. Therefore, it can be helpful in handling or meat processing. Similarly, pediocin LB-B1 from Lactobacillus plantarum LB-B1 from fermented dairy beverages, inhibited the growth of both Gram-positive and Gramnegative bacteria, including species of Listeria, Lactobacillus, Streptococcus, Shigella, Bacillus, Enterococcus and Escherichia contamination. Hence, contributing to the safety of the food products (Laukova et al., 2010; Xie et al., 2011). It has been reported that the addition of L. lactis subsp. lactis INIA 415 as starter cultures helped in preventing late blowing defects (caused by Clostridium beijerinckii INIA 63) in cheese leading to spoilage in semi hard and hard ripened cheeses, without effecting its sensory (in terms of odor, flavor) and other characteristics (Garde et al., 2011).

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combination with other preservation methods, such as heat treatment, high pressures, hurdle technology or modified atmosphere packaging (Allende et al., 2006). Preservation of food items by ex situ methods can be conducted either by directly adding bacteriocin to food products in the form of raw concentrates/by soaking food items into a bacteriocin solution or by adsorption/immobilization of concentrated bacteriocin molecules on different packing surfaces/carriers obtained by growth of producer strains in food grade substrates in fermenters followed by its adequate recovery. These molecules are released slowly and continuously from the reservoir ensuring the safety of the food product. In some cases, the carrier prevents the enzymatic inactivation of the bacteriocin by interaction with food components (Galvez et al., 2007). Adsorption/Immobilization on packaging materials Bioactive packaging has additional advantages over traditional methods of food preservation. During storage, microbial spoilage begins on the surface of the food products. Thus, application of bacteriocin on the packaging material can inhibit the growth of microbes on the food surface. Therefore, different matrices such as polyethylene, polypropylene, polyamide, polyester, acrylics and polyvinyl chloride (Table 3) have been used as packaging materials for bacteriocin adsorption/immobilization (Appendini & Hotchkiss, 2002). Immobilized bacteriocin peptides on films have been used as packaging materials to increase the shelf life of the food products inhibiting the growth of food pathogenic/spoilage bacteria. Application of nisin in edible cellulosic films inhibited the growth of Listeria innocua and Staphylococcus aureus (Coma et al., 2001). In case of packaged pork steak, ground beef and frankfurters, growth of L. monocytogenes has also been reduced by the application of immobilized bacteriocin 32Y (L. curvatus) on polyethylene films (Ercolini et al., 2006; Mauriello et al., 2004). The reduction in the viable count of total aerobic bacteria was observed during storage of fresh veal meat in cellophase-coated nisin (Guerra et al., 2005c). Similarly, immobilized nisin into palmitoylated alginate-based films or in activated alginate beads could assist decreasing growth of pathogenic Staphylococcus aureus responsible for spoilage at the surface of round beef or other meat products (Millette et al., 2007). Chen & Williams discussed the application of bacteriocin in food packaging safety to actively control microbial growth and extend product shelf life (http://www.silliker.com/html/eResearch/vol1issue2.php). Silicates (zeosil and expanded perlite), inert inorganic compounds commonly used as food grade anticaking, clarifying or filtering agents have been used as carrier of anti-listerial bacteriocin, produced by E. faecium CRL1385 and thus offer a promising alternative to incorporate this compound into food products (Ibarguren et al., 2010). The use of immobilized bacteriocins containing antimicrobial films can prolong the shelf life of food products, ensuring the quality and safety of food products. Micro and nanoencapsulation

Applications of bacteriocin by ex situ method The role of bacteriocin in the preservation of food has been reported widely in the literature, individually or in

Microencapsulation deals with a controlled release system of contents over prolonged periods of time. Besides having a major role in pharmaceutical sector, this approach also has

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Table 3. Packaging materials used for ex situ applications of bacteriocins in food products.

Packaging material Silicon coating

Legend/coating solution used Ethylene acrylic acid

Corn zein film Polyethylene Hydroxypropyl methylcellulose (HPMC) films Corn-zein films

– –

Bacteriocin Nisin Nisin Nisin

Lipid

Nisin Nisin

Polyethylene films Coupled polythene-oriented polyamide films Cellophane ‘‘P’’ films Polythene films Cellulose acetate film

Lauric acid and EDTA-impregnated Cellulosic solution 70% isopropanol – – Cellulose base emulsion

NisaplinÕ Bacteriocin 32Y Pediocin (ALTAÕ 2351)

Pectin

Lipid

Enterocin

Nisin Bacteriocin 32Y

significant applications in the food sector for encapsulation of bacteriocins. Entrapped and surface adsorbed lactobacilli in calcium alginate beads have been widely used as a delivery system with preserved viability and antimicrobial activity of the producer strain (Brachkova et al., 2010). Liposome encapsulated nisin Z retained 90% (280 ± 14 IU/g) activity against Listeria innocua as compared to 12% with a nisinogenic starter culture after 6 months during cheese storage (Benech et al., 2002). Purified and microencapsulated bacteriocin (B602 and OR 7) in polyvinylpyrrolidone was administered in the feed at concentrations of 250 mg/kg which resulted in the reduced cecal Campylobacter jejuni colonization in infected broiler chickens (Cole et al., 2006). Similarly, microencapsulation of enterocin through ionic gelation of pectin with calcium ions and addition of lipids (for gradual liberation of bacteriocin) was observed to be a simple and low cost delivery system with anti-listerial activity in food stored at 18  C up to 1 year (Ibarguren et al., 2012). On the other hand, a new hybrid system of nisin-loaded chitosan/alginate nanoparticles have been developed and found to be more effective against Listeria monocytogenes ATCC 25923 and Staphylococcus aureus ATCC 19117 in ultrafiltered (UF) Feta cheese as compared to nisin alone besides improving physicochemical and sensory properties of product (Zohri et al., 2013). Thus, it can be concluded that encapsulation is effective to increase the stability of bacteriocins, thereby, increasing the shelf life of food products. Soaking/raw concentrates Bacteriocin in food grade medium/substrate can be added in food products as raw concentrates. Various commercially available bacteriocins include raw concentrates such as ALTAÔ 2341, MicrogardÔ and milk based preparations such as lacticin 3147, variacin (Guinane et al., 2005; Morgan et al., 1999; O’Mahony et al., 2001). Both nisin and pediocin PA-1 have effectively increased the shelf life and reduced the count of food spoilage bacteria in cottage cheese, cream, canned foods, fish etc. (Pucci et al., 1988; Ross et al., 2002).

Inhibitory microorganism

References

Lactobacillus leichmannii ATCC 4797 Escherichia coli Lactobacillus helveticus and Brochothrix thermosphacta Listeria innocua and Staphylococcus aureus Listeria monocytogenes and Salmonella enteritidis Listeria monocytogenes Listeria monocytogenes

Daeschel & Mc Guire (1992) Padgett et al. (1998) Siragusa et al. (1999)

Total aerobic bacteria Listeria monocytogenes V7 Listeria innocua and Salmonella sp. Listeria monocytogenes

Guerra et al. (2005c) Ercolini et al. (2006) Santiago-Silva et al. (2009) Ibarguren et al. (2012)

Coma et al. (2001) Hoffman et al. (2001) Cha et al. (2003) Mauriello et al. (2004)

Addition of nisin (2000 IU/g) in cheese resulted in a 1000-fold decrease in L. monocytogenes counts after 7-day storage under refrigerated conditions, thereby, preventing food spoilage (Ferreira & Lund, 1996). Similarly, pediocin AcH/PA-1 (2400 AU/g) resulted in a significant decrease in the L. monocytogenes count as compared to the control sample (Goff et al., 1996).

Conclusions Bacteriocins can act as potential biological preservatives and have various applications, however, low cost production of these molecules at the industrial scale is the area of concern for research and industry. Various agro-industrial wastes such as whey, molasses, marine byproducts, soy waste etc. can be utilized as efficient low cost substrate contributing to process economics. Recent techniques like micro and nano-encapsulation, antimicrobial packaging can be helpful to increase the stability of the bacteriocins along with targeted delivery and gradual release of bacteriocins, thereby, solving the problem of food industries in terms of quality, freshness by preventing surface spoilage of food products. Hence, cost effective production of bacteriocins and development of suitable food packaging systems for their ex situ application is an upcoming area of food safety and preservation.

Declaration of interest The authors report no declarations of interest. Vandana Bali is thankful to Department of Science and Technology, New Delhi, for providing INSPIRE fellowship.

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