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International Journal of Food Microbiology 120 (2007) 51 – 70 www.elsevier.com/locate/ijfoodmicro
Bacteriocin-based strategies for food biopreservation
Antonio Gálvez ⁎, Hikmate Abriouel, Rosario Lucas López, Nabil Ben Omar
Área de Microbiología, Facultad de Ciencias Experimentales, Universidad de Jaén, Spain
Abstract Bacteriocins are ribosomally-synthesized peptides or proteins with antimicrobial activity, produced by different groups of bacteria. Many lactic acid bacteria (LAB) produce bacteriocins with rather broad spectra of inhibition. Several LAB bacteriocins offer potential applications in food preservation, and the use of bacteriocins in the food industry can help to reduce the addition of chemical preservatives as well as the intensity of heat treatments, resulting in foods which are more naturally preserved and richer in organoleptic and nutritional properties. This can be an alternative to satisfy the increasing consumers demands for safe, fresh-tasting, ready-to-eat, minimally-processed foods and also to develop “novel” food products (e.g. less acidic, or with a lower salt content). In addition to the available commercial preparations of nisin and pediocin PA-1/AcH, other bacteriocins (like for example lacticin 3147, enterocin AS-48 or variacin) also offer promising perspectives. Broad-spectrum bacteriocins present potential wider uses, while narrow-spectrum bacteriocins can be used more specifically to selectively inhibit certain high-risk bacteria in foods like Listeria monocytogenes without affecting harmless microbiota. Bacteriocins can be added to foods in the form of concentrated preparations as food preservatives, shelf-life extenders, additives or ingredients, or they can be produced in situ by bacteriocinogenic starters, adjunct or protective cultures. Immobilized bacteriocins can also find application for development of bioactive food packaging. In recent years, application of bacteriocins as part of hurdle technology has gained great attention. Several bacteriocins show additive or synergistic effects when used in combination with other antimicrobial agents, including chemical preservatives, natural phenolic compounds, as well as other antimicrobial proteins. This, as well as the combined use of different bacteriocins may also be an attractive approach to avoid development of resistant strains. The combination of bacteriocins and physical treatments like high pressure processing or pulsed electric fields also offer good opportunities for more effective preservation of foods, providing an additional barrier to more refractile forms like bacterial endospores as well. The effectiveness of bacteriocins is often dictated by environmental factors like pH, temperature, food composition and structure, as well as the food microbiota. Foods must be considered as complex ecosystems in which microbial interactions may have a great influence on the microbial balance and proliferation of beneficial or harmful bacteria. Recent developments in molecular microbial ecology can help to better understand the global effects of bacteriocins in food ecosystems, and the study of bacterial genomes may reveal new sources of bacteriocins. © 2007 Elsevier B.V. All rights reserved.
Keywords: Bacteriocin; Biopreservation; Hurdle technology; Lactic acid bacteria; Food
1. Introduction In spite of modern advances in technology, the preservation of foods is still a debated issue, not only for developing countries (where implementation of food preservation technologies are clearly needed) but also for the industrialized world. Amelioration of economic losses due to food spoilage, lowering the food processing costs and avoiding transmission of microbial pathogens through the food chain while satisfying the growing
⁎ Corresponding author. Área de Microbiología, Departamento de Ciencias de la Salud, Facultad de Ciencias Experimentales, Universidad de Jaén, Campus Las Lagunillas s/n. 23071-Jaén, Spain. Tel.: +34 953 212160; fax: +34 953 212943. E-mail address: firstname.lastname@example.org (A. Gálvez). 0168-1605/$ - see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.ijfoodmicro.2007.06.001
consumers demands for foods that are ready to eat, fresh-tasting, nutrient and vitamin rich, and minimally-processed and preserved are major challenges for the current food industry. The extent of microbiological problems in food safety was clearly reflected in the WHO food strategic planning meeting (WHO, 2002): (i) the emergence of new pathogens and pathogens not previously associated with food consumption is a major concern; (ii) microorganisms have the ability to adapt and change, and changing modes of food production, preservation and packaging have therefore resulted in altered food safety hazards. The empirical use of microorganisms and/or their natural products for the preservation of foods (biopreservation) has been a common practice in the history of mankind (Ross et al., 2002). The lactic acid bacteria (LAB) produce an array of antimicrobial
A. Gálvez et al. / International Journal of Food Microbiology 120 (2007) 51–70
substances (such as organic acids, diacetyl, acetoin, hydrogen peroxide, reuterin, reutericyclin, antifungal peptides, and bacteriocins (Holzapfel et al., 1995; El-Ziney et al., 2000; Holtzel et al., 2000; Magnusson and Schnürer, 2001). Bacteriocins are ribosomally synthesized antimicrobial peptides or proteins (Jack et al., 1995). LAB produce a variety of bacteriocins, most of which can be grouped in one of the classes proposed by Klaenhammer (1993). The structure, biosynthesis, genetics and food application of LAB bacteriocins have been reviewed recently (Cleveland et al., 2001; O'Sullivan et al., 2002; Chen and Hoover, 2003; Cotter et al., 2005; Fimland et al., 2005; Deegan et al., 2006; Drider et al., 2006). The bacteriocins produced by LAB offer several desirable properties that make them suitable for food preservation: (i) are generally recognised as safe substances, (ii) are not active and nontoxic on eukaryotic cells, (iii) become inactivated by digestive proteases, having little influence on the gut microbiota, (iv) are usually pH and heat-tolerant, (v) they have a relatively broad antimicrobial spectrum, against many food-borne pathogenic and spoilage bacteria, (vi) they show a bactericidal mode of action, usually acting on the bacterial cytoplasmic membrane: no cross resistance with antibiotics, and (vii) their genetic determinants are usually plasmid-encoded, facilitating genetic manipulation. The accumulation of studies carried out in recent years clearly indicate that the application of bacteriocins in food preservation can offer several benefits (Thomas et al., 2000): (i), an extended shelf life of foods, (ii) provide extra protection during temperature abuse conditions, (iii) decrease the risk for transmission of foodborne pathogens through the food chain, (iv) ameliorate the economic losses due to food spoilage, (v) reduce the application of chemical preservatives, (vi) permit the application of less severe heat treatments without compromising food safety: better preservation of food nutrients and vitamins, as well as organoleptic properties of foods, (vii), permit the marketing of “novel” foods (less acidic, with a lower salt content, and with a higher water content), and (viii) they may serve to satisfy industrial and consumers demands. In this respect some of the trends of the food industry in Europe, such as the need to eliminate the use of artificial ingredients and additives, the demands for minimally-processed and fresher foods, as well as for ready-to-eat food or the request for functional foods and nutraceuticals (Robertson et al., 2004) could be satisfied, at least in part, by application of bacteriocins. The present review will address different aspects related to food preservation by bacteriocins including factors influencing bacteriocin activity in food systems, hurdle technology, and the impact of recent advances in molecular biology and the analysis of bacterial genomes on bacteriocin studies and application. 2. Bacteriocins and food systems 2.1. Supplementing foods with bacteriocins Foods can be supplemented with ex situ produced bacteriocin preparations, or by inoculation with the bacteriocin-producer strain under conditions that favour production of the bacteriocin in situ (Schillinger et al., 1996; Stiles, 1996). In the first case,
bacteriocin preparations obtained by cultivation of the producer strain in a fermentor at industrial scale followed by adequate recovery and processing can be added as partially purified or purified concentrates, which would require specific approval as preservatives from the legislative point of view. So far, nisin is the only bacteriocin licensed as a food preservative (E234). Many preliminary studies on the activity of bacteriocins in vitro or in food systems are carried out with partially-purified preparations obtained from cultured broths. In most cases, a low concentration of bacteriocin is often recovered, which limits the efficacy of such preliminary tests. Ex situ produced bacteriocins can also be added in the form of raw concentrates obtained by cultivation of the producer strain in a food-grade substrate (such as milk or whey). The resulting preparations may be regarded as food additives or ingredients from the legal point of view, since some of their components may play a recognised function in the food (such as increase in protein content, or thickening). They also contain the cell-derived antimicrobial metabolites (such as lactic acid) and bacteriocins, affording an additional bioprotectant function. In addition to already-marketed concentrates such as ALTA™ 2341 or Microgard™, other milk-based preparations have been described recently such as lacticin 3147 (Morgan et al., 1999; Guinane et al., 2005) and variacin (O'Mahony et al., 2001). Ex situ produced bacteriocins can also be applied in the form of immobilized preparations, in which the partially-purified bacteriocin or the concentrated cultured broth is bound to a carrier. The carrier acts as a reservoir and diffuser of the concentrated bacteriocin molecules to the food ensuring a gradient-dependent continuous supply of bacteriocin. The carrier may also protect the bacteriocin from inactivation by interaction with food components and enzymatic inactivation. Moreover, the precise localized application of bacteriocin molecules on the food surface requires much lower amounts of bacteriocin (compared to application in the whole food volume), decreasing the processing costs. A variety of methods have been proposed for bacteriocin immobilization, including adsorption to the producer cells (Yang et al., 1992; Mattila et al., 2003; Ghalfi et al., 2006), silica particles or corn starch powder (Coventry et al., 1996; Dawson et al., 2005), liposome encapsulation (Degnan and Luchansky, 1992), and incorporation on gel coatings and films of different materials such as calcium alginate, gelatin, cellulose, soy protein, corn zein, collagen casings, polysaccharide based films, cellophane, silicon coatings, polyethylene, nylon or other polymer plastic films (Daeschel et al., 1992; Cutter and Siragusa, 1995b; Ming et al., 1997; Siragusa et al., 1999, Natrajan and Sheldon, 2000; Gill and Holley, 2003; Scannell et al., 2000a; Ko et al., 2001; Dawson et al., 2002; Franklin et al., 2004; Luchansky and Call, 2004; Guerra et al., 2005; Lungu and Johnson, 2005). In most cases, immobilized bacteriocin preparations are applied on the surface of the processed food to avoid post-process contamination and surface proliferation of unwanted bacteria. A recent advance in this field is the use of immobilized bacteriocins in the development of antimicrobial packaging. A polyethylene film containing immobilized bacteriocin 32Y from L. curvatus reduced viable counts of L. monocytogenes during storage in the packaged pork steak and ground beef as well as in frankfurters (Mauriello et al.,
2003). as adjunct or co-cultures in combination with a starter culture. by adaptation through repeated subcultivation with increasing bacteriocin concentrations.. growth of the protective cultures must have a neutral impact on the physicochemical and organoleptic properties of the food. For this reason. application of nisin in meat products faces several limitation derived from its interaction with phospholipids emulsifiers and other food constituents (Henning et al. bacteriocin production may also serve to increase the implantation capacity.. Zhou et al.. 2006). precipitation. The strain properties and the amount of bacteriocin produced could be improved by heterologous expression of bacteriocin genes (Rodríguez et al. luteus ATCC 10. Peláez and Requena. or by genetic modification. especially for small economies and developing countries. 1996). 2002). or uneven distribution of bacteriocin molecules in the food matrix. When used as a starter culture. Sometime. a nisin-containing cellophane coating reduced viable counts of total aerobic bacteria in fresh veal meat stored at 8 °C (Guerra et al. but they must not interfere with the primary function of the starter culture.. biofilms. inoculation of milk with an enterocin AS-48 producer enterococcal strain as adjunct culture in combination with a commercial starter culture for cheese manufacture had no effect on growth of the starter or the physicochemical properties of the produced cheese. poor solubility at pH above 6. A protective culture may grow and produce bacteriocin during refrigeration storage of the food. Foulquié Moreno et al. Differences in inoculum density. At the same time.. 2006). Leroy et al. Therefore.. 1992. genus. and the precise moment of bacteriocin production could also be tailored by using inducible production systems (Zhou et al.) –Protection by physico-chemical barriers (microcolonies. 1999). Nevertheless. 2003.. As an illustrative example. The use of bacteriocinogenic cultures requires careful selection of strains that are well-adapted to the particular food environment in which they will be used and able to grow under the food processing and/or storage conditions and to produce enough bacteriocin amounts as to inhibit the target pathogenic or spoilage bacteria. at least ten-fold higher bacteriocin concentrations must be added to foods in order to achieve an equivalent inhibitory effect. 1995). 2. / International Journal of Food Microbiology 120 (2007) 51–70 53 2004.0. Factors influencing the efficacy of bacteriocins in food systems Comparisons of data obtained in culture media with those obtained in food systems reveal that the efficacy of bacteriocins is often much lower in the later (Schillinger et al. In the first case. 2005. Ercolini et al.. Many studies have focused on the selection and development of bacteriocinogenic cultures for food application (Ross et al. bacteriocin resistance of the starter culture may be a key factor. 2005). Bacteriocinogenic strains can be used either directly as starter cultures. 2000. Therefore. 2006). 2006. resting. The efficacy of bacteriocins in foods will greatly depend on a number of food-related factors (Table 1) that in most cases involve interaction with food components. inactivation. and an active package obtained from nisin-treated film reduced viable counts of M. 2004). a faster growth rate of the starter or a delayed bacteriocin production may also permit the starter to grow without interference from the bacteriocinogenic adjunct culture. the use of antimicrobial films containing bacteriocins can improve the quality and safety and prolong the shelf-life of food products. or as protective cultures (especially in the case of nonfermented foods).. while under temperature abuse conditions the protective culture may even act as the predominant spoiler. slime) –Development of resistance/adaptation .. stressed or sub-lethally injured cells. it is necessary to implement the right experimental approaches to select bacteriocin-producing strains that are suitable for use in food production... Similarly. enough bacteriocin was produced in the cheese to ensure inhibition of Bacillus cereus (Muñoz et al. Aasen et al. 2006). the bacteriocinogenic strain must be able to carry out the desired fermentation process optimally besides being able to produce enough bacteriocin amounts to afford protection. Jung et al. endospores..A. and bacteriocin unstability to pH changes –Inactivation by food enzymes –Interaction with food additives/ingredients –Bacteriocin adsorption to food components –Low solubility and uneven distribution in the food matrix –Limited stability of bacteriocin during food shelf life The food microbiota –Microbial load –Microbial diversity –Bacteriocin sensitivity –Microbial interactions in the food system The target bacteria –Microbial load –Bacteriocin sensitivity (Gram-type... and inactivation by formation of a nisinglutathione adduct (Rose et al. This may be achieved by selection of natural resistant mutants. inactivation is Table 1 Bacteriocin efficacy in foods: limiting factors Food-related factors –Food processing conditions –Food storage temperature –Food pH. Bacteriocinogenic protective cultures can be used to inhibit spoilage and pathogenic bacteria during the shelf life period of non-fermented foods. 2003. starving or viable but non-culturable cells.. Työppönen et al. In some cases. 1986. In situ bacteriocin production offers several advantages compared to ex situ production regarding both legal aspects and costs. sometimes this may not be necessary as the bacteriocin may just not be active on the starter culture (as may be the case of many of the bacteriocins that predominantly show antilisterial activity) or this may be much more tolerant to the bacteriocin than the target bacteria in the food system. However.. strains) –Physiological stage (growing.240 cells in broth as well as in raw milk and pasteurized milk during storage (Mauriello et al. where food safety may be seriously compromised (Holzapfel. Adjunct cultures do not need to contribute to the fermentation. Lowering the costs of biopreservation processes may be highly attractive. and/or during temperature abuse conditions.2. competitiveness and stability of the starter (Todorov et al. 2005). As an example. species. Gálvez et al. 2003)... ensuring that pathogenic bacteria do not grow and that the spoiled food is not consumed (Holzapfel et al..
monocytogenes show the same degree of sensitivity to antilisterial bacteriocins (Martínez et al. the efficacy of the bacteriocin will depend more directly on the microbial load of the contaminant.. the bacteriocin may not always target the desired bacterial group (for example. the bacteriocin and the environmental conditions (Gravesen et al. factors influencing bacteriocin production are of most importance when using bacteriocinogenic cultures (Fig. the most important. In processed foods. In addition. and of 10− 3 to 10− 4 for mesenterocin 52. Therefore. In raw foods. Most probably. the efficacy of bacteriocins in food will greatly depend on the food microbial composition and microbial physiological stage (Table 1). and changes of the target organisms in response to environmental stress factors may also result in decreased bacteriocin sensitivity. Mazzotta and Montville. of 10− 4 to 10− 6 for the class IIa bacteriocins leucocins A. 1998). microorganisms from post-process contamination may easily proliferate because of the lack of competitors. or grow in the form of slime-covered biofilms on food surfaces. depending on the strain (Ming and Daeschel. a complex food microbiota may frequently cause a lower efficacy of bacteriocins due to the presence of resistant bacteria (such as Gram-negatives) and/or the higher chances for production of inactivating enzymes (such as proteases). they will tend to form microcolonies in a solid or particulate food. and may clearly limit the efficacy of bacteriocins as well. not all strains of L. the autochthonous microbiota may counteract development of potential pathogens. Influence of different factors on the efficacy of in situ bacteriocin production for biopreservation.. — Fig. or the induction of bacteriocin production). 2002a). (vi) a low capacity for bacteriocin production in the food system (which will depend greatly on the food storage conditions.. However. Bacteriocin-resistant L. redox potential. The protective effect of biofilms against antimicrobial substances in the food industry is well documented (Kumar and Anand. The fitness costs of bacteriocin resistance may vary greatly depending on the strain.. Variations in strain sensitivities and development of strain resistance/adaptation are also of major concern for application of bacteriocins. In situ bacteriocin production may also depend greatly on physicochemical factors (such as pH.. time of incubation…) as well as food-related factors (such as the food structure — fluidity. aw. which may greatly influence bacteriocin sensitivity. 2006). CO2. Gálvez et al. increasing bacteriocin sensitivity. although processing treatments may trigger spore germination and outgrowth. 1. In commercially sterile foods. Most worrying. 1994). 1998). O2. 1994. Davies and Adams.54 A. monocytogenes have been reported to appear at frequencies of 10− 3 to 10− 9 for nisin. the developed resistance to one bacteriocin may also afford protection against other bacteriocins. (v) difficulties for genetic manipulation and transfer of bacteriocinogenic trait to suitable starters. (ii) the susceptibility of the producer strain to infection by bacteriophages. . Martínez et al. (iv) inadequacy of producer strain as a starter. 2005). 2005). (iii) antagonism of other bacteria towards the producer strain. In addition to the factors influencing the effectiveness of bacteriocins as antimicrobials in food systems. 2002b). E and sakacin A (Dykes and Hastings. / International Journal of Food Microbiology 120 (2007) 51–70 lower in cooked meats due to the loss of free sulphydryl groups during cooking as a result of the reaction of glutathione with proteins (Stergiou et al. 1993.. B. Foods are complex ecosystems with a range of microbial compositions. and. These vary from (commercially) sterile foods to raw or fermented foods. For example. the capacity of the producer strain for implantation and proliferation. emulsions…. temperature. 1997. Under these conditions. curvaticin 13 and plantaricin C19 (Rekhif et al. It should also be considered that microorganisms are seldom distributed homogeneously as planktonic cells in the food matrix. particulate matter. cells that are not actively growing may be more resistant to bacteriocins. bacteriocin inactivation of the LAB responsible for food fermentation would be clearly undesirable). The use of bacteriocinogenic cultures faces several limitations directly related to the producer strain such as (i) the spontaneous loss of the bacteriocinogenic trait. The needs to find novel bacteriocins showing no cross resistance with existing ones are clearly patent. 1). and the observed cross-resistance between pediocin-like bacteriocins has been attributed to a general mechanism of resistance (Gravesen et al. and a higher bacteriocin concentration will always be required in order to inactivate a higher number of target cells. Inactive bacterial forms (endospores) may also be resistant to bacteriocins. As an example. microorganisms can also be found in a variety of physiological stages.
leading to energy exhaustion and cell death. stationary phase cells. while cells were still growing (Larsen et al.. and the physiological state of the bacteria (Holzapfel et al. 1998). Since bacteriocin production is linked to cell growth.. The interactions of the induction factor with the food matrix (such as adsorption or inactivation) may have a great influence on bacteriocin production. 2003. it may also depend on factors affecting this parameter (such as inhibitory substances like salt or nitrite) or the lack of available nutrients (such as manganese in the case of many LAB). On the other hand. the intensity of damage may be higher since some of the antimicrobial factors may act on the same cellular target. or cells already stressed in response to other unfavourable environmental conditions)..g. 2003. and NaCl was shown to interfere with bacteriocin induction (Verluyten et al. 2004a).. 1995. The application of bacteriocins as part of hurdle technology has received great attention in recent years (Chen and Hoover. 1994) or divercin (Sip et al. 1993). 2004). 2005).5 of initial pH (Aymerich et al. pressure homogeneization or other procedures that may indirectly damage bacterial cells. the production of enterocins A and B by Enterococcus faecium CTC492 was significantly inhibited by sausage ingredients and additives. composition — available nutrients. Bavaricin A production was negatively affected at NaCl concentrations of 3% or higher. competing microbiota. 2000). . In addition. 2005). 1978. Similarly. when cells are exposed to a combination of antimicrobial factors.) may also stimulate bacteriocin production.0 to 7. a minimum concentration of inoculum is often required. Over 60 potential hurdles have been described to improve food stability and/or quality (Leistner. 2003. After exposure of a bacterial population to a single antimicrobial factor there is often a heterogeneous response. Rodríguez et al. and also by sodium chloride (Verluyten et al. Ross et al. The effect on bacteriocin production was even detected at low NaCl concentrations where there was no growth inhibition. The repair of multiple damages may also require much higher energy costs. bacteriocin production may also depend greatly on microbial-related factors such as the microbial load and diversity.. The addition of sodium chloride and pepper de- creased production by 16-fold. etc. as well as thermal treatments and other treatments intended to reduce the microbial load). oxygen.. (ii) showing an increased resistance because of its physiological state (e. A fraction of the population may receive a lethal dose of the antimicrobial factor. 2005). 1).. 2005). A suboptimal temperature (22 °C) and a moderate NaCl stress (0. The remaining fraction may survive due to several reasons: (i) receiving a sub-lethal dose. As an example.A. having a good opportunity to develop mechanisms of resistance or adaptation that would make them immune to further challenges with the particular antimicrobial factor. bacteriocin production in food must be understood as a dynamic process where the different interactions change over time. and how optimum production may require a certain combination of influencing factors (Leal-Sánchez et al. Since the bacteriocinogenic strain will thrive within a (more or less complex) microbial population in the food ecosystem. 2002). with optima between 25 and 35 °C. Sub-lethally injured cells as well as cells with increased resistance may repair the damage caused by the antimicrobial agent and survive. specific Gram-positive bacteria activate both plantaricin NC8 (PLNC8) production by Lactobacillus plantarum NC8 and the PLNC8-autoinducing activity (Maldonado et al. 2000). leading to cell death. will also have a direct influence on the food environment through the consumption of and competition for nutrients. Similarly.. 2004a). dictating the ultimate result as far as food preservation (Fig. Amylovorin production by Lactobacillus amylovorus DCE 471 was stimulated by NaCl (Neysens et al. 1999.. / International Journal of Food Microbiology 120 (2007) 51–70 55 buffering capacity.65 M) stimulated bacteriocin production by Lactobacillus pentosus B96 (Delgado et al. Bacteriocin production is often an inducible trait that depends on cell density and concentration of the inducer (which may be the bacteriocin itself). and (iii) cells naturally resistant to the antimicrobial agent. and from 6.. 1995. 2000). with the exception of nitrate (Aymerich et al. growth and curvacin A production by Lactobacillus curvatus LTH 1174 were negatively affected by nitrite (even by a concentration as low as 10 ppm). production of metabolites and modification of the food microbial balance through the produced bacteriocin. The presence of competing microorganisms can be an environmental factor stimulating production of LAB bacteriocins such as lactacin B (Barefoot et al. antimicrobials… — and processing conditions — freezing and thawing. 1999). additives. Therefore. 2003.. Gálvez et al. 2003) as well as carbon dioxide (Neysens and De Vuyst. Growth and sakacin production in meat sausages by Lactobacillus sakei CTC 494 was affected negatively by salting and curing with nitrite as well as manganese limitation (Leroy and De Vuyst. Leistner and Gorris.. Several other stress factors (such as ethanol. Bacteriocins and hurdle technology The concept of hurdle technology began to apply in the food industry in a rational way after the observation that survival of microorganisms greatly decreased when they were confronted with multiple antimicrobial factors (Leistner. in turn. All these factors will be sensed by the bacteriocinogenic strain which.. Devlieghere et al... the probabilities for survival and proliferation for cells confronted with multiple hurdles are very low. Therefore. 2004). depending on the intensity of treatment as well as many other factors. Leistner. A model was proposed to illustrate the influence of environmental factors on sakacin production in a meat system (Leroy and De Vuyst. the microbial interactions occurring in the food during storage (such as the competition for nutrients or the production of other antagonistic substances). Therefore. the food matrix may also facilitate the concentration of the induction factor around cells or microcolonies formed by the bacteriocinogenic culture in the food. The temperature and pH influenced enterocin production.. 3. the synergy between different antimicrobial factors may allow the use of lower doses compared to their individual application. 2004b). Growth and curvacin A production were also negatively affected by some species (especially by nutmeg) in a meat system (Verluyten et al. By contrast. Several illustrative examples may explain how bacteriocin production can change dramatically by altering environmental conditions.
.. lactocin 705 (at 5–7%. Also. 2004). Chumchalová et al. Ukuku and Fett.. (1995) found that the sensitivity of L. The combination of hurdles to be applied will depend greatly on the type of food and its microbial composition. Hornbæk et al. For example. Thomas and Wimpenny. 2002) and Carnobacterium piscicola A9b bacteriocin (at 2–4% NaCl.. 1981.. elimination of some members of the population may provide a more favourable environment for others. 2003. due to the lack of competition.5% NaCl. pediocin (at 6...b) and enterocin AS-48 against B. Buncic et al.. Gálvez et al. leucocin F10.. / International Journal of Food Microbiology 120 (2007) 51–70 2003. The combinations of nisin and nitrite delayed botulinal toxin formation in meat systems and showed increased activity on clostridial endospores outgrowth (Rayman et al. 1991. 2004). 2004). 2000. 1997). Further reports have confirmed the increased antibacterial activity of nisin in combination with sodium lactate in several food systems (Scannell et al. 2006). cereus in Fig. Combination of bacteriocins with chemical substances and natural antimicrobials Previous studies have shown that the presence of NaCl enhanced the antimicrobial action of bacteriocins such as nisin. food acidification may select for aciduric bacteria while heat treatment may select for endospore formers. 2000). monocytogenes to nisin (400 IU/ml) increased in combination with lactate.56 A. 1996). The interaction of different antimicrobial factors may also modify their individual antimicrobial spectra. 1997. leucocins 4010 (at 2. The solubility of bacteriocins may also increase at lower pH. 1991).. curvacin (Verluyten et al. The protective effect of sodium chloride may be due to interference with ionic interactions between bacteriocin molecules and charged groups involved in bacteriocin binding to target cells (Bhunia et al. monocytogenes. as well as did pediocin AcH activity in combination with sodium diacetate and sodium lactate (Uhart et al. 1996) and the activities of enterocin EJ97 against L.. Taylor et al.. the combination of nisin with acetic acid and sorbate controlled L. Gram-negative bacteria may become sensitized to bacteriocins and other molecules upon exposure to hurdles that destabilise the bacterial outer membrane.. 1983. Application of bacteriocins as part of hurdle technology. Sodium chloride may also induce conformational changes of bacter- iocins (Lee et al. Deegan et al. 1998. 2003). . monocytogenes contamination over a long period storage (70 days) at 6–8 °C (Davies et al.. 2000). Nykänen et al. A nisinsorbate combination showed increased activity against Listeria (Avery and Buncic..5% NaCl. 3. nisin activity was also antagonized by low concentration of NaCl (Bouttefroy et al. while acidification enhances the antibacterial activity of both organic acids and bacteriocins (Jack et al.1. 1997). As an example. Jydegaard et al. Bacillus coagulans and Bacillus macroides (García et al. 1993) or changes in the cell envelope of the target organisms (Jydegaard et al. and B. Reduction of nitrite content by addition of bacteriocins may be beneficial in the food industry. licheniformis (Mansour et al. 1995. Vignolo et al. 1997. Mazzotta et al. Addition of nitrite also increased the anti-listeria activity of bacteriocinogenic lactobacilli in meat (Hugas et al.. This must be carefully considered. 1998).. Parente et al. enterocin AS-48 and others (Harris et al. 2003. Ananou et al. 2004). since bacteriocins can be used purposely in combination with selected hurdles in order to increase microbial inactivation (Fig. 2). The increase in net charge of bacteriocins at low pH might facilitate translocation of bacteriocin molecules through the cell wall.. cereus (Abriouel et al. Himmelbloom et al.... 1998).. 1996. since different hurdles usually have different effects on the members of a microbial community. 2002). Activity of enterocin AS-48 against B. as will be discussed further on. 2001). Sodium chloride also decreased the antilisterial activity of acidocin CH5 (at 1–2%. monocytogenes (Gill and Holley.. 1998). 2000b). facilitating diffusion of bacteriocin molecules.. Long and Phillips. 2000). Lacticin 3147 activity also increased in combination with sodium lactate or sodium citrate (Scannell et al... In the production of Ricotta-type cheeses. However. Organic acids and their salts can potentiate the activity of bacteriocins greatly.. 1985) and also on Leuconostoc mesenteroides and L. 2. Stiles. 2004a.
An increased antibacterial activity can also be achieved by combination of bacteriocins with other (non-bacteriocin) antimicrobial proteins or peptides. 1991. subtilis (Ettayebi et al. 1995a. The spectrum of the nisin-lysozyme combination could be extended to Gram-negative bacteria by addition of chelating agents (Gill and Holley. innocua. against L. Nisin and lysozyme acted synergistically against Gram-positive bacteria.. 1997). 2005).. disodium pyrophosphate.. aureus cell in vegetable sauces was potentiated significantly in combination with the phenolic compounds carvacrol. Lactic acid. Vaara. terpineol. cereus in milk (Pol et al. 1998. However. Chelating agents can also enhance the activity of bacteriocins on Gram-positive bacteria. Periago et al. B.b). eugenol. sodium lactate and peracetic acid (as well as several other chemical compounds) increased AS-48 activity for decontamination of L. 1993) or with leucocin F10 (Parente et al. an increased activity of chrisin (a commercial nisin preparation) in combination with EDTA has been reported against several Gram-positive bacteria (Gill and Holley. Ananou et al. Sensitization of Gram-negative bacteria to bacteriocins by other chelators such as maltol or ethyl maltol has been reported (Schved et al. 1999. hexametaphosphate or citrate and bacteriocins against Gram-negative bacteria has been demonstrated for nisin both under laboratory conditions and in foods (Stevens et al. 2003. 1994). development of cross-resistance should be carefully considered. 2004). plantarum and Staphylococcus aureus. 2000) The combined addition of nisin and the lactoperoxidase system (LPS) had a strong antimicrobial effect against L.. 2003). monocytogenes (Brewer et al. 2003). but also to avoid regrowth of bacteriocin-resistant/adapted cells.. 2004). 2004). 2001a.. monocytogenes ATCC 15313 in skim milk at 25 °C for at least 15 days (Boussouel et al. coagulans and B. 2002).. 1998) provides a greater antibacterial activity than each bacteriocin separately. Cutter and Siragusa. Other antimicrobial compounds such as ethanol can act synergistically with nisin to reduce the survival of L.. 1999... 1998) as well as lactacin B or lactacin F with nisin or pediocin AcH. 2004a). as it has been shown that a general mechanism may account for high-level resistance to class IIa bacteriocins in L. caffeic acid. L. trisodium phosphate.. monocytogenes and B. best results were obtained for nisin with phytic acid (Bari et al. 2002a. 1991. 1995).. subtilis (Olasupo et al. cereus (cells and spores). the phenolic compounds are also attractive natural preservatives (Burt. The simultaneous use of nisin with pediocin AcH (Hanlin et al. Reuterin also showed a significant synergistic effect on L. especially for the combinations of bacteriocins belonging to the same class. 2000). monocytogenes in sprouts (Cobo Molinos et al.. licheniformis vegetative cells and spore outgrowth in milk (Mansour et al. Gao et al.b). eugenol. The simultaneous use of two or more bacteriocins could be useful not only to lower the added bacteriocin doses. monocytogenes (Pol and Smid. 2005).. 2006). The combination of nisin and cinnamon accelerates death of Salmonella Typhimurium and Escherichia coli O157:H7 in apple juice (Yuste and Fung. allowing bacteriocins to reach the cytoplasmic membrane (Stevens et al.A. Chelating agents permeate the outer membrane (OM) of Gram-negative bacteria by extracting Ca2+ and Mg2+ cations that stabilize lipopolysaccharide of this structure. Synergism was also observed for the sucrose fatty acid esters sucrose palmitate and sucrose stearate and nisin against several strains of L. aureus after in combination with nisin (100 IU/ml). monocytogenes Scott A in skim milk after 24 h at 30 °C (Zapico et al. cereus and/or L. citral and hydrocinnamic acid (Grande et al. Boziaris and Adams. Essential oils and their active components. monocytogenes in fresh produce..5 mM) was used to enhance the synergy found between nisin and a pulsed electric field treatment (PEF) against vegetative cells of B. although the antimicrobial effect of reuterin against Gram-negative pathogens was not enhanced.... the dose of added phenolic compounds could be lowered thereby decreasing their impact on the food flavour and taste.. 2003).b. Combinations of bacteriocins have also been tested in order to increase their antimicrobial activities. and also against fish spoilage flora (Elotmani and Assobhei. 1998). A combination of nisin and sodium polyphosphate showed an increased activity against L. The enhanced effect of chelators such as EDTA. eugenol or thymol against B. Nattress and Baker. monocytogenes Ohio and (to a lesser extent) L.. The antimicrobial activity of enterocin AS-48 against S. 2005). 1998). 2001. 2000). Carneiro De Melo et al. 1994. aureus (Chung and Hancock. Helander et al... The combination of sodium tripolyphosphate and enterocin EJ97 showed increased activity against B. 2000). The combination of nisin and lactoferrin showed . 2004). Combinations of nisin with carvacrol. Carvacrol (0. 1999. but not against Gram-negative bacteria (Thomas et al. When nisin and pediocin were used in combination with chemical compounds to combat L. p-coumaric acid. 2004). monocytogenes (Gravesen et al. Gálvez et al. 1999).. 2007). The natural variant nisin Z also acted synergistically with thymol against L. monocytogenes than each bacteriocin individually (Bouttefroy and Millière. and lactacin 481/pediocin AcH (MuletPowell et al.. 2004). monocytogenes (Buncic et al. When used in combination with bacteriocins.. Nisin acted synergistically with carvacrol.. Brochrocin C and enterocin AS-48 also showed increased antimicrobial activity on EDTA-treated Gram-negative bacteria (Abriouel et al. monocytogenes. Sub-lethal concentrations of nisin (30 IU/ml) and monolaurin (100 μg/ml) in combination acted synergistically on B. Fang and Tsai. Lactoferrin (and its partialhydrolysis derivative lactoferricin) is another natural protein (which is found in milk and other secretions) with antimicrobial activity due to its iron-binding capacity and polycationic nature (Ellison. 1992. / International Journal of Food Microbiology 120 (2007) 51–70 57 rice gruel was also potentiated by sodium lactate (Grande et al.. 1996). macroides (García et al. or thymol resulted in synergistic action against Bacillus subtilis and Listeria innocua. including spoilage lactobacilli and S. Simultaneous or sequential additions of nisin (50 IU/ml) and curvaticin 13 (160 AU/ml) also induced a greater inhibitory effect against L.. though (Arqués et al.. More recently. Sodium lactate or sodium citrate in combination with nisin showed increased antimicrobial activity against Arcobacter butzleri in chicken due to their chelating effect (Long and Phillips.. geraniol. Yamazaki et al. but only additive against B. 2000. monocytogenes and a slight additive effect on S. while nisin and cinnamic acid had synergistic activity against L. 1998. Schved et al. 2003).
but not under 100% N2. Prolongation of the shelf life of food by MAP is based on retardation of intrinsic food changes and inhibition of spoilage microbiota. 2001. 3. Moreover. 2000). the combined application of bacteriocins and PEF is expected to elicit increased bactericidal effects.. Nisin and heat act synergistically against L. Bendicho et al. Bacteriocins and pulsed electric fields Pulsed electric field (PEF) technology is a non-thermal process where microbial inactivation is achieved by application of high-voltage pulses between a set of electrodes (Vega-Mercado et al. such as sub-lethally injured cells or bacterial endospores (Fig.... innocua to nisin in liquid whole egg following PEF treatment exhibited an additive effect on inactivation of the microorganism (Calderón-Miranda et al.b). In a modified atmosphere. 2003). 1999). monocytogenes by enhancing membrane permeabilization (Nilsson et al. reducing the heat resistance of L. Bacteriocins can also provide an additional protection during food storage against proliferation of endospores surviving heat treatments. The effects of PEF resemble bacterial electroporation. 2004). 2002.. monocytogenes also increased in cold smoked salmon packaged under vacuum as well as under a 100% CO2 atmosphere (Nilsson et al.58 A. the added bacteriocin. Nisin-resistant L. 1998). 2000). The efficacy of the combined treatments of PEF and bactericiocins in food preservation depends on several factors related to the PEF treatment (such as field strength. It has been reported that nisin and CO2 atmosphere acted synergistically on the cytoplasmic membrane of L. MAP and bacteriocins are therefore two complementary hurdles of advantage to food spoilage. Activity of nisin as well as ALTA™ 2341 against L. Gram-negative bacteria are generally more sensitive to CO2. 1999a. Several investigations have thrown light on the effectiveness of combined treatments of bacteriocins and PEF treatments in food systems (Table 2). Fang and Lin (1994a.. particular applications of bacteriocins and PEF must be studied in detail for each type of food and target bacteria. 1997). 1998). 1998). 1994.b) found that growth of L. monocytogenes was completely inhibited on pork immersed in 10 IU/ml nisin and packed in 80% CO2/20% air during 30 days of storage at 4 °C. Boziaris et al. bacteriocins could also provide an additional hurdle against survivors from PEF treatments. 1991. 2004)... plantarum and L. the food microbial load. extending their spectrum of action. 1999).2. coli was greatly enhanced by pediocin PA-1. Since most bacteriocins act on the bacterial cytoplasmic membrane. 2005). 2004). Church. Although this technology can only be applied to pumpable food products.. enterocin AS-48 (Abriouel et al. sakacin P. since PEF disrupts the bacterial outer membrane allowing bacteriocin molecules to reach the bacterial cytoplasmic membrane target (Fig. aureus cells sub-lethally injured by heat due to the lower concentration of remaining viable cells and to the cell damage induced by the heat treatment (Ananou et al... All of these may have an influence on the numbers and types of bacteria surviving the combined treatment and.. Moreover.. 1992. 1994). A cocktail of seven L. Ueckert et al.3. most important.. Although no potential application has been proposed for the observed synergy. or jenseniin G (Bakes et al.. 1988). The antimicrobial activity of pleurocidin (an antimicrobial peptide from fish) against E. Szabo and Cahill. PEF could also be applied to extend the antimicrobial spectrum of bacteriocins. Since Gram-negative bacteria are usually not sensitive to bacteriocins. 2006). Wandling et al. Grande et al. Gálvez et al. and other environmental factors (Wouters et al. Synergy between eukaryotic antimicrobial peptides and bacteriocins has also been investigated. it has gained attraction in recent years as an individual treatment or in combination with other hurdles such as bacteriocins. 1998. Ananou et al. A synergistic effect was observed as the electric field intensity. heat and a chelating agent (Abriouel et al. it has been demonstrated that the intensity of heat treatments against bacterial endospores can be lowered in combination with nisin as well as with enterocin AS-48 (Beard et al. 1998. or 40% CO2/60% N2 (Szabo and Cahill. Heinz et al. Bacteriocins and modified atmosphere packaging Modified atmosphere packaging (MAP) is frequently used in the food industry to prolong the shelf life of perishable food products. innocua treated by PEF-nisin in skimmed milk exhibited an increase in the cell wall . 2005). monocytogenes cells grown in the presence of nisin were more sensitive to heat at 55 °C than wild-type cells (Modi et al... 2002).. Bacteriocins and heat treatments Bacteriocins can be used to reduce the intensity of heat treatments in foods without compromising microbial inactivation. the dissolved CO2 will determine growth inhibition of microorganisms (Devlieghere et al. 3). monocytogenes in milk (Maisnier-Patin et al. their proliferation during the shelf life period of the processed food. Sub-lethal heat has been shown to sensitize Gram-negative bacteria to several bacteriocins such as nisin or pediocin AcH (Kalchayanand et al. but the higher intensity of this treatment causes severe damage to the bacterial cell membrane. For this reason... the available synthetic pleurocidin could probably be used in combination with bacteriocins for selective inhibition of Gram-negative bacteria in fish.. number of pulses and nisin concentration increased both in liquid whole egg and in skim milk (Calderón-Miranda et al. MAP may be defined as “the enclosure of food products in gas-barrier materials. Highest sensitization was reported for combined treatments of bacteriocins. number of pulses.. 1995) and in cold-pack lobster meat (Budu-Amoako et al. Exposure of L. while lactic acid bacteria are much more resistant (Farber. monocytogenes (Mahadeo and Tatini. L. The efficacy of enterocin AS-48 was higher on S. composition and physiological stage. / International Journal of Food Microbiology 120 (2007) 51–70 increased antilisterial activity when tested in culture media (Branen and Davidson. 1999.. in which the gaseous environment has been changed” (Young et al. monocytogenes isolates was inhibited by nisin as well as by ALTA™ 2341 under a 100% CO2 atmosphere. 3). and curvacin A (Lüders et al. saving costs in the heat treatment and decreasing the impact of heat on the food. 3.4. 1999.... 1999a). wave form or pulse duration). Ananou et al. 3. 1997. 1998).
plantarum in model beer (Ulmer et al. cereus (Pol et al.c.400 U/ml). (2000) buffer –Increased inactivation of P. Several studies have shown that the efficacy of PEF against Gram-negative bacteria can be enhanced by nisin.5 U/ml) and lysozyme (690 U/ml). germinating spores were found to be sensitive to PEF treatment. innocua in liquid Calderón-Miranda whole egg.. the inhibitory effect of nisin increased with the number of pulses applied (Santi et al..37 log cycles) than either nisin or lysozyme alone (Liang et al. S. cell viability loss was increased by an additional 0. aureus in skim milk (Sobrino-Lopez and Martin Belloso. In conclusion. When PEF treatment was applied to Salmonella cells in orange juice in the presence of nisin (100 U/ml).. coli cells was accomplished with nisin (ca. plantarum in model beer Ulmer et al. innocua inactivation. cytoplasmic clumping. 2003). cereus vegetative Pol et al. 2006). PEF treatment combined with cinnamon or nisin triggered cell death of E. addition of nisin can improve the efficacy of PEF treatments against vegetative cells of foodborne Table 2 Reported effects on the application of nisin and pulsed-electic fields for bacterial inactivation Observed effects References –Increased inactivation of M. since exposure to nisin after PEF produced a lower effect on L.A. In contrast. L.. Observed synergism with carvacrol –Inactivation of Salmonella in orange juice.000 IU/ml) and three pulses of 11. At high PEF intensities (i. Nisin-PEF inactivation of E.. Nisin also increased PEF effectiveness against Pseudomonas aeruginosa. 2001b). coli O157:H7 in fresh apple Iu et al.. and rupture of the cell walls and cell membranes (CalderónMiranda et al. Observed synergism with cinnamon –Inactivation of L. 2000). and incorporation of bacteriocins into the food may provide an additional hurdle against surviving endospores. Treatment of B. or a mixture of nisin (27. 2007 –Increased inactivation of E.04 to 2.. Similarly..b cells (more efficient in buffer than in skim milk). 2001a..95 with NaCl and applying PEF at 5 kV/cm (a non-lethal intensity when no other hurdle is used) with the further addition of nisin (1200 IU/ml) resulted in a 5-log cycle reduction of the bacterial population (Terebiznik et al. 11 kV/cm). The synergy between nisin and PEF treatment against resting vegetative cells of B..b. 2000. cereus was enhanced by carvacrol (0. Observed synergism 2002 with reduced water activity –Increased inactivation of B. provided that bacteriocin molecules remain active in the treated food. lysozyme (2. This behaviour was mainly attributed to changes in the cell envelope and to modifications of the medium caused by PEF application (Gallo et al. milk ultrafiltrate media. 2002). Gallo protein concentrate et al. cereus spores with nisin and/or PEF treatment did not lead to direct inactivation of the spores or increased heat sensitivity as a result of sub-lethal damage. 2001a).. leakage of cellular material. 2002). It has been reported recently that the efficiency of the combined treatment of nisin and PEF in liquid whey protein concentrate was strongly dependent on the sequence of application. (2001) cider. Nisin treatment was more efficient than PEF treatment for inactivating germinating spores (Pol et al. 1.75 log cycles. Gálvez et al. 2007). aureus in skim milk Sobrino-Lopez and Martin Belloso (2006) –Increased inactivation of L. and liquid whey et al.25 kV/cm or 500 IU/ml for five pulses of the same intensity (Terebiznik et al. 1999a. The combination of nisin and lysozyme had a more pronounced bactericidal effect (by at least 1. bacteriocins could be applied as an additional hurdle against endospores surviving PEF treatment. roughness. 2000). a 4-log cycle reduction of inoculated E. Effects of pulsed electric fields in combination with bacteriocins on microbial populations. 2000). (2003) –Increased inactivation of S. / International Journal of Food Microbiology 120 (2007) 51–70 59 Fig. The application of nisin clearly enhanced the lethal effect of PEF treatment on other Gram-positive bacteria such as Micrococcus luteus cells in phosphate buffer (Dutreux et al. Accordingly.. (2002) . coli in simulated Terebiznik et al. 2001). Although nisin was totally inactivated by PEF treatment in simulated milk ultrafiltrate media. 3. (2002) Observed synergism with lysozyme –Inactivation of E... skim milk. resulting in a reduction in viable counts of 6 to 8 log cycles (Iu et al. Bacterial endospores are refractile to PEF treatments. Nisin showed less activity against B. aeruginosa Santi et al.. cereus in milk compared to buffer (Pol et al. and vegetative cells of B. coli O157:H7 in fresh apple cider. 2000. coli in simulated milk ultrafiltrate media was enhanced by water activity reduction.. 1999c). Decreasing water activity to 0. 2002). luteus in phosphate Dutreux et al. Liang et al.5 mM)..e.
1998) and L.. bacteriocin-HHP treatments could serve to decrease the intensity of HHP treatment without compromising microbial inactivation. monocytogenes (Karatzas and Bennik. 1999). 1998). The food pH is also an influencing factor. A combination of nisin/ pediocin AcH added to the plating medium was also effective on killing Clostridium spores induced to germinate by HHP treatment (Kalchayanand et al... and increased cell lysis in L. Bacterial endospores are resistant to HHP treatments currently applied to foods (Smelt. 2000). Farkas et al. Nisin in combination with HHP showed strong synergistic effects against L. Since HHP may have unwanted effects on milk components (Trujillo et al. HHP also induces a more persistent sensitisation of Gram-negative bacteria to small dif- fusible antimicrobial molecules (García-Graells et al. 2002). A key issue in the efficacy of HHP treatments is the protective effect afforded by the food. coli and L. Since most bacteriocins act on the bacterial cytoplasmic membrane it can be hypothesized that the observed synergy between bacteriocins and HHP results from cumulative damage to this structure. 1993). Farkas and Hoover. 2000). providing an additional hurdle against selection of pressure-resistant vegetative cells.. Although bacteriocins are generally inactive on Gram-negative bacteria.. Survival of L. Sub-lethally injured vegetative cells surviving HHP treatment may develop pressure resistance... However. 1999. the disruption of H-bonds. 2002). 2000. 2005). since remaining bacteriocin activity may provide an important hurdle against survivors (such as bacterial endospores) after PEF treatment. Similarly. inactivating and preventing growth of sub-lethally injured cells. eg. Masschalck et al. followed by a vegetative cells destruction cycle of 300 or 400 MPa at .. HHP transiently sensitized Gramnegative bacteria to nisin. Combining HHP and nisin (500 IU/ml) also increased inactivation of bacteria associated with milk (Black et al. indicating that cell death occurs as a consequence of multiple events or cumulative cell damage. mesenteroides through cell wall degradation (Kalchayanand et al. 40 °C). / International Journal of Food Microbiology 120 (2007) 51–70 pathogenic and spoilage Gram-positive and Gram-negative bacteria.. Stewart et al. 2001). bacteriocin–membrane interaction during phase transition at high pressure has never been studied. Nisin-HHP has also shown to increase inactivation of Bacillus and Clostridium endospores (Roberts and Hoover.60 A.5. HHP transiently sensitizes Gram-negative bacteria through outer membrane damage. Combined bacteriocin-HHP treatments have successfully applied for inhibition of foodborne pathogens in cheese. 2001. 5 °C). HPP-assisted pasteurisation (ca. Cell death caused by HHP increases with pressure and so does the synergism with bacteriocins. coli MG1655 was reduced from 7 logs at 400 MPa in phosphate buffer to only 3 logs at 700 MPa in milk. 3. 1994. Bacteriocins and high hydrostatic pressure (HHP) High hydrostatic pressure (HHP) is an innovative food processing and preservation method that causes injury and killing of microbial cells (Kalchayanand et al.. but addition of lysozyme (400 μg/ml) and nisin (400 IU/ml) to the milk increased the lethality of treatment (Garcia-Graells et al.. E. 2002). In model cheeses submitted to a germination cycle of 60 MPa at 30 °C for 210 min. as has been previously reported for E. 1998b). and bacteria are usually more resistant to HHP in low acid foods. Several studies have described the combined effects of bacteriocins and HHP on bacteria (Table 3). the combination of lacticin 3147 and HHP increased the viability loss of S.. 2002). and guacamole. During pressurization. 2000. cold HHP pasteurisation (ca. jams. and residual lacticin still showed inhibitory effect in the food. Inactivation of E. 1994. 2004b).. increasing the possibilities for application of bacteriocins in food preservation (Kalchayanand et al. 2005). ionic bonds and hydrophobic interactions of the macromolecules adversely affects their structures and functions (Hoover. combining nisin with high pressure improved the biocidal effect on spores and aerobic mesophilic bacteria (Capellas et al. Ray. 1998a. 2003). 2004a). affecting mainly ATP-generating and transport proteins. 2005). 2000). 90 °C). are now commercially available. Black et al. monocytogenes (ter Steeg et al.g. Patterson. 1998.. coli (GarcíaGraells et al. plantarum.. The increased cell damage caused by combined treatments of HHP and bacteriocins could prevent the tailing effect. such as ready-to-to eat chicken meat.. similar effects are to be expected for other bacteriocins...b.. A tailing effect is often observed after application of HHP treatments (Kalchayanand et al. Pediocin AcH also increased decimal reductions caused by HHP on food spoilage and pathogenic bacteria in peptone solution (Kalchayanand et al. sliced ham.. milk and meat (having a complex composition as well as a pH closer to neutrality) exert a grater protection against HHP. The stability of bacteriocins to PEF treatments is another issue to be addressed. 2006). which determines the different modalities of treatment. Gálvez et al. fruit juices. A variety of pressure-treated products. compensating for the required increase in pressure or temperature. 2000). monocytogenes Scott A in cheeses made from raw milk that were previously inoculated with nisin and other bacteriocin-producer strains decreased as the intensity of HHP treatment increased (Arqués et al. fresh whole oysters. 1996.. or HHP-assisted sterilisation (ca. 1996. In Mato' cheese. The synergistic activity of pediocin AcH in combination with nisin was greatly enhanced during pressurization (Kalchayanand et al. Hauben et al.. monocytogenes in milk and in whey (Morgan et al. aureus and L. Addition of bacteriocins as a second hurdle against surviving endospores could also improve the safety and shelf life of HHP-processed foods (Shearer et al. 2000). although experimental data are needed to support this conclusion. 1998a). and a mechanism of pressure-promoted uptake of antimicrobial proteins and peptides was proposed to explain this sensitisation (Masschalck et al. For example. Presumably. The sub-lethal damage is initiated by membrane phase transitions (Kato and Hayashi. which may act synergistically with other hurdles as well. vegetive cells or endospores) may have great influence on HHP efficacy (Chen et al.. The bacterial type and physiological stage (e. 1999).. The bactericidal effect of HHP (as well as its negative effects on food constituents) increases along with the temperature. Addition of bacteriocins could improve the efficacy of HHP treatments in foods. although HHP treatments can induce endospore germination.
Bacteriocins and other non-thermal treatments In spite of the many other non-thermal treatments currently under study for food processing application. The spectrum of applications of food irradiation could be expanded in combination with bacteriocins.. innocua in liquid whole egg Ponce et al. a greater inactivation of E. monocytogenes Scott A in cheese inoculated with a nisin-producing strain Arqués et al.. 1999. L. 2005). coli and L. fluorescens) suspended in peptone water Increased cell lysis through cell wall degradation in L. coli at reduced temperature ter Steeg et al. (2001) P. innocua improved significantly with nisin addition. enteritidis. pediocin AcH or nisin) had no influence on killing and survival of Salmonella enterica. 2002). S. especially if the radiation dose can be lowered. S.6. coli. monocytogenes viable counts and inhibition of proliferation during storage in meat model Garriga et al. S. 1998a..3 kGy) had an increased antimicrobial effect on L. coli became sensitive to lysozyme and nisin during homogeneisation at pressures above 150 MPa when these compounds were added before the HPH treatment. (2005) Increased inactivation of E. Nisin also kept staphylococci at significant low levels during storage and reduced slime-producing LAB below the detection limit. aureus) Increased inactivation of bacteria associated with milk (E. 2003). (2002) Reduction of L. aureus. cereus spores and inhibition of the surviving fraction in cheese López-Pedemonte et al. HHP inactivation of E. . typhimurium.. innocua was reported at 450 MPa and 5 mg/l of nisin. It was observed that E. coli Kalchayanand et al. plantarum and E. aureus. (1998b) S. monocytogenes. 2005 Increased sensitivity of pressure-resistant E. (2003) Increased inactivation of L. Bacteriocin addition could improve the efficacy of HHP treatments at lower pressure without adverse effects on meat (Hugas et al.. (2000) 30 °C for 15 min the presence of nisin significantly increased inactivation of B. monocytogenes during storage in the case of nisin. but cells treated by HPH remained insensitive for lysozyme and nisin added after that treatment (Diels et al. Kalchayanand et al. flexneri. L. fluorescens. mesenteroides. L. 3. / International Journal of Food Microbiology 120 (2007) 51–70 Table 3 Reported effects on the application of bacteriocins and high tydrostatic pressure (HHP) for bacterial inactivation Bacteriocin Nisin Observed effects Increased inactivation of B. enterocins A Reduction of L. 2002). monocytogenes viable counts and inhibition of proliferation during storage in meat model Garriga et al. sakacin K. High pressure homogeneisation (HPH) is another processing treatment applied to certain types of food. It was reported that the combined application of pediocin (as ALTA™ 2341) and low-dose irradiation (2. cereus spores and reduced proliferation of the surviving fraction measured 24 h and 15 d after HHP treatment (López-Pedemonte et al.A.. aureus.. nisin reduced viable counts of E. (2002) system Pediocin AcH + nisin Increased inactivation of S. Gálvez et al... coli O157:H7. and Garriga et al. reduced growth of S.. mesenteroides Kalchayanand et al. coli. Salmonella Thyphimurium and E. 1998).. S. HPH may sensitise E. P. viridescens) Black et al. 2002). Stewart et al. E. O157:H7 2004a Killing of Clostridium spores induced to germinate Kalchayanand et al. liquefaciens. coli (N6 logs) was reported in the presence of nisin (Garriga et al. innocua. coli Garcia-Graells et al. and sometimes the products may develop a rubbery consistency (Murano et al. (1998) In a meat model system. (1999) Strong synergistic effects against L. enterocins A and B as well as pediocin AcH (Garriga et al. and the two microorganisms were not detectable after one month of storage at 4 °C (Ponce et al. and P. In liquid whole egg.. A reduction of almost 5 log units in E. sonnei. These results clearly indicate that each particular bacteriocin may show different effects in HHP-combined treatments depending on the target bacteria. while added bacteriocins (enterocins A and B. B. the risks of foodborne pathogens in HPH-treated foods could be lowered by an optimised incorporation of bacteriocins in foods before HPH treatment. subtilis and Clostridium spores References 61 Roberts and Hoover. coli to lysozyme and nisin by inducing a transient permeabilisation of the outer membrane that does not involve a physical disruption and that is immediately repaired after the process. monocytogenes Scott A. 1998. coagulans. L. only a few reports have been published on their combination with bacteriocins. Presumably. L. Irradiation offers a great potential for application in food preservation (Farkas. The application of HHP to fresh meat products may result in a cooked-like aspect. Similarly to HHP. sakei. 2006). monocytogenes and S. fluorescens and S. monocytogenes on frankfurters (Chen et al. the combination of more than one bacteriocin and HHP could provide better results when the target consists of a mixture of different bacteria with varying sensitivities to bacteriocins. 2000 Increased bactericidal activity and spectrum (E. since low-dose gamma irradiation has less unwanted effects on food and may also have better acceptance among consumers. S. and Garcia-Graells et al. (1999) Improved bactericidal effect on spores and aerobic mesophilic bacteria in cheese Capellas et al. 2002). coli and L. In a meat model system. (2000) Increased inactivation of B. typhimurium. (2002) suppressed slime-producing bacteria Pediocin AcH Increased inactivation of food spoilage and pathogenic bacteria (S. 1996. L. (2002) and B system Lacticin 3147 Increased inactivation of L. coli. Although the bacteriocin-HHP treatment failed to inhibit proliferation of L. Accordingly. coli counts and more than 6 log units for L. counts of listeria remained below detection levels in samples treated with sakacin K. Masschalck et al.b. aureus in milk and in whey Morgan et al. (2004b) Sakacin K.
In other cases. Abriouel H. The use of fluorescence-based technology (such as fluorescence in-situ hybridisation—FISH—. or the response to stress factors. Grattepanche et al. the inducible character of many bacteriocins. Similarly.. Other non-thermal treatments such as pulsed magnetic fields (PMF) have also been tested in combination with bacteriocins. One of the main limitations of gamma irradiation is the increased resistance of bacterial endospores (Farkas. This approach could provide additional data independent of the biases introduced by sample preparation procedures and the pressure of selective media currently used for enumeration of microorganisms. 2007). requiring the application of combined treatments for a higher effectiveness.. Bacteriocins and recent advances in molecular biology and genome studies Advances in molecular biology and molecular microbial ecology have provided new valuable tools to study microorganisms in food ecosystems. 2002). Swings J. 2002)..62 A.. faecium by PCR amplification. Similarly.. (2005) used this method to evaluate the impact of the nisin Z-producing L. 2007). as well as the influence of environmental conditions on gene expression and the stress response of target bacteria to the produced or added bacteriocin in food. lactis subsp. PCR amplification with specific primers for bacteriocin genes may be used to follow the predominance of an inoculated strain in food fermentation. a combined treatment of nisin. multiplex PCR targeting both bacteriocin genes and species-specific genes can serve for precise identification of bacteriocinogenic strains in a single analysis.. These techniques may facilitate the study of the effects of bacteriocins in food systems at the level of single cells. a class II bacteriocin (Altermann et al. 4.. on the distribution of bacteriocinogenic strains within the food matrix (Fernández de Palencia et al. Vancanneyt M. 10 min) and gamma irradiation (5 kGy) markedly reduced the number of survivors for at least 42 days at an abuse temperature of 10 °C (Farkas et al. Ben Omar et al.R. Connil et al.. Maldonado et al. As an example. Real-time PCR could also provide more precise information on cells sub-lethally injured by bacteriocin molecules. A recent study addressed the use of DGGE to evaluate simultaneously the impact of a bacteriocinogenic LAB on foodborne pathogens inoculated in a fermented food as well as on the overall microbiological profile of the fermentation (Díaz G. sakei strain I151 in sausages was studied in order to determine the influence of the production procedure for fermented sausages on bacteriocin production (Urso et al. 2005). Verluyten J. such as the determination of their bacteriocinogenic potential. confocal laser microscopy. Leroy F. divergens V41 were identified rapidly by this procedure (Moschetti et al. Similarly.. As an example. diacetylactis strain UL719 on Lactococcus cremoris in milk fermented with mixed cultures. providing a completely new scenario picture of bacteriocin effects. 2004). 1998). 2004) or the heterogeneous response of bacterial populations to bacteriocins (Hornbæk et al.. and Galvez A. Gálvez et al. a combined treatment of PMF with EDTA and nisin had no effect on E. (2002) established that the plantaricin S operon is widely distributed among wild-type L. 2006b). gasseri K7 in semi-hard cheese (Matijašiæ et al. as shown for sakacin-P producing L. sakei during production of fermented sausages (Urso et al.. in silico analyses of the probiotic strain Lactobacillus acidophilus NCFM predicted a chromosomal locus for lactacin B. Adriany T. Multiplex PCR was also used successfully to follow implantation of V41 strain in cold smoked salmon (Connil et al. Lucas R. coli (San Martín et al. unpublished) or PFGE analysis (Moschetti et al... plantarum strains from olive fermentations by PCR amplification and hybridization with specific probes. cereus. In a recent work. the capacity for proliferation and inhibition of unwanted bacteria... (2004) studied the distribution of propionicin T1 genes among propionibacteria in a similar way.. it could solve the problems of differentiation of closely related bacteria in mixed populations. and the loss of the production capacity (which may be caused by gene mutation.. This alternative method could overcome the biases introduced by the currently used extraction procedures on the determination of the amounts of bacteriocin produced in the food. / International Journal of Food Microbiology 120 (2007) 51–70 2004). 2001).. avoiding the problem to distinguish the two bacterial populations in differential media when they were in the same order of magnitude. Matijašiæ et al. or fluorescence ratio imaging microscopy—FRIM—) could also provide valuable information. expression of sakacin P structural gene sspA by the L. However. Ben Omar N. lactis biovar.. 2006a) and L. 2006). the analysis of complete genomes may reveal the presence of potential bacteriocin genes and new bacteriocins independently of the producer capacity of strains (Nes and Johnsborg. Nisin-producing lactococci and divercin 41 producing C. Martínez Cañamero M..... (2004) analyzed the incidence of structural genes for several known bacteriocins among food isolates of Enterococcus faecalis and E. REP-PCR (Foulquié-Moreno M. 2001) have also been used to evaluate strain implantation in food systems and the impact of bacteriocinogenic starters on the food quality from the microbiological point of view. for example. heat (90 °C. unpublished). and Faye et al. Another line of research on bacteriocin application may rise from genomic studies. In sous vide meals inoculated with spores of psychrotrophic B. gene loss or genetic rearrangements). and De Vuyst L.. Classical methods for detection of produced bacteriocins may underestimate the bacteriocinogenic potential of LAB due to several factors such as the influence of environmental conditions on bacteriocin production. 2002).. Other suggested applications could be to study the distribution of target bacteria in the food both in the absence and in the presence of bacteriocin pressure and the generation of gradients and protected niches as a function of bacteriocin concentration. Similarly. However. 2001. The distribution of bacteriocin-encoding genes among food isolates is a common issue that can be easily be resolved by molecular techniques. Real-time PCR could be used to follow survival of target bacteria in the presence of added or in situ produced bacteriocin while simultaneously determining the growth of bacteriocinogenic strains. while a limited number of bacteriocins have been described in .. Other procedures such as analysis of RAPD-PCR profiles (Ryan et al. 2001. DNA-based technology could be used to follow the expression of bacteriocin genes in food systems.
as has been demonstrated for PEF and HHP. (vi) stress. and (iv) possibly transporting nisin across the membrane or extruding nisin out of the membrane (Kramer et al. termed penocin A (Diep et al. The antimicrobial effects of bacteriocins and bacteriocinogenic cultures in food ecosystems must be understood in terms of microbial interactions.. (iii) phospholipid. 2006)... 2005). sakei strains (Møretrø et al. (iii) preventing the insertion of nisin into the membrane. BAGEL is freely accessible at: http://bioinformatics.. it will be possible to develop adequate methodologies (such as microarray technology) to study the global response of bacteria to bacteriocins. thermophilus could be exploited by genetic engineering in order to develop new bacteriocinogenic strains of technological interest. 2006). sakei host that contains the complete apparatus for gene activation. blpU. the set of methodologies that have emerged in recent years provide an arsenal of barely unexplored tools that could expand the potential of bacteriocinogenic strains for food application and improve our understanding on the global effects of bacteriocins in food ecosystems. The comparative transcriptome analysis of nisin-sensitive and nisin-resistant L. sakei. Transcriptome analysis can also reveal new and relevant data on the biology of bacteriocins such as the mechanisms of resistance/adaptation. mainly (i) preventing nisin from reaching the cytoplasmic membrane. knowledgebased bacteriocin databases and motif databases has been recently created (De Jong et al. The application of a microbial ecology approach may provide a more realistic portrait of the complex interactions . The data available suggest that bacteriocin loci in S. (ii) reducing the acidity of the extracellular medium. nonsense mutations detected in some of the regulatory genes indicate that this locus is not functional at least in some strains. lactis concluded that nisin resistance is a complex phenotype. which makes this bacterium a poor bacteriocin-producer.. 2006). irradiation. The first locus (lab. Cloning of penA and peiA in a L. pneumoniae and displays the typical characteristics of a Class II bacteriocin locus. Hopefully. for lantibiotic) contains genes that are similar to genes generally found in lantibiotic production loci. However.rug. blpU. lactis mediated by the two-component system KinD/LlrD (Martínez et al. thermophilus strains also contain genes encoding bacteriocinlike peptides (i.and fatty acid metabolism. 2006). a potential immunity gene (termed peiA) as well as genetic determinants involved in bacteriocin transport and regulation. 2006). The blp loci of the S. Bacteriocinogenic cells may also act as living factories in foods. lpD. (v) transport. Many bacteriocins are encoded by small genes that are often omitted in the annotation process of bacterial genomes (De Jong et al. sakei 23 K has revealed that this strain carries a 6. The use of novel preservation technologies offers new opportunities for application of bacteriocins as part of hurdle technology. blpK in strain LMG18311. (iv) gene regulation. there is a need to determine more precisely the most effective conditions for application of each particular bacteriocin. Bacteriocins are a diverse group of antimicrobial proteins/peptides. Overall. maturation and externalization of bacteriocins confirmed the production of this new and potent bacteriocin. the combined application of many other technologies (such as ultrasonication. The identification of genes that are functionally similar but have limited or no sequence homology is often a problem in genome data mining. However. lactis that are naturally adapted or transiently resistant to nisin can be readily obtained by subcultivation with sub-lethal nisin amounts.A. by using microarrays for global analysis of gene expression. it is not clear whether this locus is really involved in lantibiotic production. Based on the genome sequences and gene identification. thereby stimulating the binding of nisin to the cell wall.. it has been shown that lactococcin 972 induces a cell-envelope stress response in L.. The adaptation is lost upon subcultivation without nisin. Since spp homologue genes (mainly sppK and sppR homologues) seem to be widely distributed among L. 1996). and (vii) miscellaneous or unknown functions (Kok et al. 2005 and references cited therein).. Studies similar to these are clearly needed in order to elucidate the mechanisms that may be involved in adaptation of foodborne pathogens upon exposure to bacteriocin pressure in food systems. Similarly. the accessory gene involved in transport and the inducer gene involved in regulation are missing.. involving various different mechanisms. sakei Lb674 (Hühne et al. this software will help researchers to identify novel bacteriocin-related genes in the upcoming LAB genome sequences. Strains of L..e. blpE. 2005) described previously in L. Nevertheless. it has been suggested that these genes could be used as a fingerprinting region in typing methods and/or as a marker for L. The second locus is similar to the bacteriocin-like peptide (blp) locus described in S. 2005). Gálvez et al. Transcriptome analysis of adapted strains revealed a significant up/down regulation of 95 genes belonging to several main functional categories: (i) cell wall synthesis. A recent data mining study demonstrated that the genome of Pediococcus pentosaceus ATCC 25745 contains a gene cluster that resembles a regulated bacteriocin system (Diep et al. genome sequencing of L. 2005).biol. microwave and ohmic heating. or pulsed light) still remains unexplored. Conclusions A large number of bacteriocins from LAB have been characterized to date.5 kb region containing part of the spp gene cluster responsible for sakacin P production (Møretrø et al. analysis of the genome sequences available revealed two loci predicted to be related to bacteriocin production (Hols et al. The gene cluster has an operon-like structure consisting of a putative pediocin-like bacteriocin gene (termed penA). However.. A web server (BAGEL) that identifies putative bacteriocin ORFs in a DNA sequence using novel.nl/websoftware/bagel. bacteriocins and their accessory proteins are often encoded by poorly conserved ORFs. (ii) central and energy metabolism. 2005). blpF in strain LMD9. 5. / International Journal of Food Microbiology 120 (2007) 51–70 63 Streptococcus thermophilus (Gilbreth and Somkuti. and blpK in strain CNRZ1066 (Hols et al. In one example. 2006). and many different studies have indicated the potential usefulness of bacteriocins in food preservation. and therefore are expected to behave differently on different target bacteria and under different environmental conditions. Since the efficacy of bacteriocins in foods is dictated by environmental factors. allowing a more rational application of these natural antimicrobial hurdles in foods... In addition.
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