Membrane-active bacteriocins to control Salmonella in foods

Food Research International 45 (2012) 735–744

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Membrane-active bacteriocins to control Salmonella in foods Are they the definite hurdle? Miriam C. Chalón, Leonardo Acuña, Roberto D. Morero, Carlos J. Minahk, Augusto Bellomio ⁎ INSIBIO, Departamento de Bioquímica de la Nutrición, (CONICET-UNT) and Instituto de Química Biológica “Dr. Bernabé Bloj”, Facultad de Bioquímica, Química y Farmacia, Universidad Nacional de Tucumán, Chacabuco 461, (4000), San Miguel de Tucumán, Argentina

a r t i c l e

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Article history: Received 23 February 2011 Accepted 10 August 2011 Keywords: Microcins Bacteriocins Antimicrobial peptides Food preservation Biopreservation Salmonella

a b s t r a c t According to recent surveys salmonellosis is the main disease caused by foodborne microorganisms in many countries. Although traditional methods to control bacterial contamination in food are effective in controlling Salmonella, a major problem arises with fresh and organic food demanded by the market with little preparation and no chemical additives. Besides the development of new technologies that combine soft physical and chemical treatments in a way that causes minimal changes in food properties, antimicrobial peptides derived from natural sources are presented as an interesting alternative to chemical preservatives. There are many bacteriocins active against Salmonella and they could be used in the food industry alone or in combination with other hurdles to increase the anti-Salmonella effect in the so-called hurdle technology. However, further studies are necessary to demonstrate the safety of new bacteriocins and to improve their activity in different environmental conditions encountered during food processing. Moreover, nisin and pediocin PA-1 already approved as food preservatives by various government agencies, can be used along with other hurdles to control the pathogen in foods. In this paper the use of bacteriocins as hurdles for controlling Salmonella in the future is discussed and analyzed. © 2011 Elsevier Ltd. All rights reserved.

1. Introduction Salmonellosis is an infectious foodborne disease caused by enterobacteria belonging to the genus Salmonella. The pathogenesis includes a set of clinical symptoms mainly manifested as acute gastroenteritis. Not all species, strains or serotypes are recognized as potential pathogens. The current taxonomic classification of Salmonella has simplified the spectrum by grouping all strains (pathogenic or not) in only two species: Salmonella enterica and Salmonella bongori. The latter is not pathogenic for humans. S. enterica is divided into six subspecies, enterica, salamae, arizonae, diarizonae, indica, and houtenae, also known as subspecies I, II, IIIa, IIIb, IV, and VI, respectively (Brenner, Villar, Angulo, Tauxe, & Swaminathan, 2000). Each subspecies consists of different serovars. According to the Kauffman and White serotyping (Kauffman, 1972), Salmonella spp. were classified in more than 2,000 serovars determined by the composition of the O lipopolysaccharide antigens, flagellar H and Vi (Uzzau et al., 2000). S. enterica subsp. enterica is divided into five serogroups: A, B, C, D and E. Each serogroup contains multiple serovars and comprises 99% of the serovars isolated from clinical samples (Old, 1992). The serovars adapted to humans cause infections in humans but rarely affect animals. Salmonella is transmitted from the feces of sick or asymptomatic host through water, food and insects. The ⁎ Corresponding author at: Departamento de Bioquímica de la Nutrición, INSIBIO, Chacabuco 461, T4000ILI, Tucumán, Argentina. Tel./fax: + 54 381 4248921. E-mail address: [email protected] (A. Bellomio). 0963-9969/$ – see front matter © 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.foodres.2011.08.024

most representative serovars are Typhi, Paratyphi A, B, and C and Sendai. Depending on the presence of different serovars and the immunological state of patients Salmonella can induce three types of human disease: bacteremia, typhoid fever and enterocolitis. The latter, which occurs most frequently, is caused mainly by S. enterica serovar Typhimurium (S. Typhimurium), while typhoid fever is caused by S. enterica serovar Typhi (S. Typhi). The infection caused by S. Typhimurium causes typhoid fever in mice. However, in humans it is exclusively associated with enterocolitis (Ukuku & Fett, 2002, 2006; Zhang et al., 2003). There are serovars adapted to animals: pullorum (chickens), abortusovis (sheep), abortus-equi (horses), Dublin (cattle), and Choleraesisus (pigs). Nevertheless, most of them are not adapted to specific hosts and are widely distributed in nature (Valdez, Ferreira, & Finlay, 2009). The aim of the present review is to provide an up-to-date analysis of bacterial ribosomally synthesized antibiotic peptides named bacteriocins (Cotter, Hill, & Ross, 2005) as food biopreservatives for controlling Salmonella. Moreover, the main reports about Salmonella-active bacteriocins will be summarized, stressing on bacteriocins that were already successfully applied in Salmonella contaminated foods. 2. Antibiotic resistance in Salmonella Most of the gastrointestinal tract infections, with the exception of typhoid fever, should not be treated with antibiotics unless affecting patients with underlying illnesses or prolonged and complicated febrile cases. However, the general trend in the last years was the use

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of antibiotics even for mild Samonella-caused gastroenteritis (Cohen & Tauxe, 1986; Mølbak, 2005). This fact leads to an ever increasing number of multi-resistant isolates of Salmonellae (Carpenter et al., 2008; Folster et al., 2010; Karon, Archer, Sotir, Monson, & Kazmierczak, 2007). Furthermore, since Salmonella are zoonotic, the observed resistance is also due to the use of antibiotics in farm animals (Funk et al., 2007; Scientific Advisory Group on Antimicrobials of the Committee for Medicinal Products for Veterinary Use, 2009). Integrons class I and the so-called Salmonella genomic island 1, a chromosomal multidrug-resistant region play a crucial role in classic antibiotic resistance spread (Boyd, Peters, Ng, & Mulvey, 2000; Fluit & Schmitz, 2004). Even though the high prevalence of multidrug-resistant strains among S. enterica isolates has prompted fluoroquinolones as primary antibiotics in the therapy for invasive salmonellosis, their general use has led to decreased susceptibility (Lynch et al., 2009). Moreover, resistance has been reported among both S. Typhi (Chuang et al., 2009) and S. Paratyphi A (Maskey et al., 2008). Because of this, the use of third-generation cephalosporins, such as ceftriaxone for the management of enteric fever gained acceptance in the last decades. However, resistance cassettes against third-generation cephalosporins had already been found in integron-like structures in other enterobacteriaceae, and resistance to third generation cephalosporins was recently described in Salmonella as well (Majtan, Majtanova, & Majtan, 2010; Ye et al., 2010). Therefore, there is an urgent need for new classes of antimicrobials compounds that can be used in the management of salmonellosis both in humans and farm animals.

of the colicin structural gene, a constitutively expressed immunity gene, which encodes a protein that provides specific protection against the colicin, and a lysis gene, which encodes a protein involved in colicin release from the producer strain. Among the different types of ribosomally synthesized antibacterial molecules, colicins probably have the greatest specificity because many of them only affect strains within the same species (i.e. E. coli colicins). The extremely high specificity of colicins might be particularly advantageous when only one bacterial strain would be targeted without disrupting other microbial populations. In the case of pathogens that colonize the gastrointestinal tract of poultry, cattle and swine, the use of colicin-producing strains would have little effect on most beneficial intestinal bacteria. In poultry, for instance, the use of colicin-producing bacteria has been mainly intended for the control of Salmonella. Colicinogenic E. coli have been actively investigated to inhibit E. coli O157:H7. Several colicins against E. coli O157:H7 have been characterized. As many as 13 different colicins that included colicins E2, E8, E7 among others were reported to inhibit 11 pathogenic strains. Another study demonstrated that Colicin E1 effectively inhibited E. coli O157:H7 growth on beef carcasses and proposed the use of colicin as a potential strategy for controlling E. coli O157:H7 contamination on beef (Patton, Lonergan, Cutler, Stahl, & Dickson, 2008). Although as mentioned before, the colicins are proteins and not peptides, their different functional domains might be exploited in the design of antimicrobial peptides active against Salmonella.

3. Antimicrobial peptides to control Salmonella in foods

As stated above, antibiotic resistance in Salmonella is always a concern and remains as an unsolved problem. Therefore, alternative strategies must be taken into account and antimicrobial peptides generated great expectation (Giamarellou, 2006; Hancock, 2000). Tetracycline, a classical antibiotic, is widely used as growth promoter in livestock (Gaskins, Collier, & Anderson, 2002). This common practice may lead to an increase resistance for this antibiotic in gut flora including Salmonella. However, it was shown that the combination of tetracycline and bacitracin, an antibiotic peptide, reduces the appearance of such resistance not only for Salmonella (Lin, Wolff, Erickson, & Francis, 2009) but also for E. coli (Walton & Wheeler, 1987). Polymyxins represent a group of antimicrobial peptides that has potentially good perspectives for fighting Salmonella infections. Polymyxins are non-ribosomally synthesized peptides (Landman, Georgescu, Martin, & Quale, 2008). The polymyxin family is comprised of at least fifteen chemically different compounds (Martin et al., 2003) that are synthesized by several proteins encoded by a gene cluster (Choi et al., 2009). They exert their antimicrobial effects by interacting with the lipopolysaccharide of Gram-negative bacteria (Storm, Rosenthal, & Swanson, 1977). Polymyxin B and E (colistin) were used as clinical antibiotics till the 1970s. They were abandoned by that time but now they are being used again (Vaara, 2010), proving to be extremely useful against a number of Gram-negative bacteria such as Pseudomonas (El Solh & Alhajhusain, 2009) and Salmonella (Aarestrup et al., 2003). Since the 1950s polymyxins are known to be effective in controlling Salmonella (Manten & de Nooy, 1959). However, resistance against polymyxins in Salmonella is a great challenge. A relatively high mutation rate to colistin resistance of 0.6 × 10 − 6 per cell per generation (Sun, Negrea, Rhen, & Andersson, 2009) was recently reported. Furthermore, Salmonellae have at least three sensor-kinase systems that alter gene expression in the presence of antimicrobial peptides, including polymyxins: PhoP–PhoQ, PmrA–PmrB, and RcsB–RcsC–RcsD, which in turn leads to increasing tolerance towards those peptides (Pilonieta, Erickson, Ernst, & Detweiler, 2009). Other antimicrobial peptides have also been proposed in the last decades such as the bee venom melittin, cecropin, an insect-derived peptide and of hybrids melittin–cecropin. All of them proved to be effective in

The inner membrane (IM) is the action target of many antimicrobial peptides, which affect its integrity. Many bacteriocins act by dissipating the transmembrane potential and the electrochemical gradient in a manner not yet fully understood triggering events that culminate in cell death (see below). However, a major problem that arises when combating Salmonella is the outer membrane (OM). The OM is a lipid bilayer, in whose external hemilayer the predominant lipid is the lipopolysaccharide (LPS), a very particular lipid whose detailed structure description has been reported elsewhere (Kawasaki, this issue). The OM constitutes a formidable permeability barrier to toxic compounds as antibiotics and antimicrobial peptides (Delcour, 2009; Kawasaki, this issue; Nikaido, 2003; Pagès, James, & Winterhalter, 2008). Even though some antimicrobial peptides are able to kill Salmonella despite the presence of OM, a combination of peptides and OM-disrupting treatments is needed for other bacteriocins as discussed below. 3.1. Colicins Colicins are proteins of molecular mass ranging from 40 to 80 kDa produced by some strains of E. coli that are lethal for related strains of E. coli. All colicins are organized into three domains. The N-terminal domain is involved in translocation through the membrane, and the central domain is involved in binding to the receptor, while the C-terminal domain contains the active part (Cascales et al., 2007). The narrow spectrum of activity of colicins is due to the presence of specific receptors at the surface of sensitive strains that colicins bind before killing. It has been shown that receptors are outer membrane proteins that allow the entry of specific nutrients (Braun, Patzer, & Hantke, 2002; Zihler et al., 2009). Once the colicins enter the cell, they kill it by means of one of several mechanisms: channel formation in cytoplasmic membrane, cellular DNA degradation, protein biosynthesis inhibition by RNA cleaving and murein or LPS biosynthesis inhibition by interfering with the lipid carrier regeneration. Colicin is not active against the producing bacteria due to the presence of a specific antagonist protein called the immunity protein. Colicin genetic clusters are located on plasmids and are usually composed

3.2. Non-ribosomally synthesized and eukaryotic cationic antimicrobial peptides active against Salmonella

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controlling not only S. Typhimurium but also Pseudomonas aeruginosa, E. coli and Enterobacter cloacae. Moreover, melittin–cecropin hybrid also showed an interesting synergistic effect with clinical antibiotics (Piers, Brown, & Hancock, 1994). Shorter hybrid peptides, which retained most of the activity and were potentially more practical due to their small size, were reported as well (Andreu et al., 1992). In the same trend, even better hybrids were designed and produced in Pichia pastoris, with higher antimicrobial activity and no hemolytic activity. Therefore, a potential application was proposed (Cao et al., 2010).

Table 2 Nisin as effective hurdle against Salmonella in foods. Class of hurdle

Synergistic agent applied

Food

Chelator additives

Lactate Trisodium phosphate EDTA, lactate or sorbate Oregano essential oil p-cymene Cinnamon Lysozyme Lysozyme and EDTA Chilling and EDTA PEF and lysozyme

Beefa Chicken skinb Cantaloupec Minced sheep meatd Ready to eat foodse Apple juicef Smoked salmong Cooked ham and bolognah Chicken carcassesi Orange juicej

Other chemical additives

Physical

3.3. Bacteriocins from Gram positive bacteria active against Salmonella a

In the last years, bacteriocins have been considered very promising agents for fighting foodborne pathogens (García, Rodríguez, Rodríguez, & Martínez, 2010; Mills, Stanton, Hill, & Ross, 2011). Even though bacteriocins are produced by either Gram-positive or Gram-negative bacteria, the most accepted peptides for food preservation or even clinical applications are those produced by the former group of bacteria, especially bacteriocins from lactic acid bacteria (LAB) because these species are generally present and they are even intensively used in foods. Moreover, they are generally recognized as safe (Carr, Chill, & Maida, 2002; Pedersen, Iversen, Sørensen, & Johansen, 2005). These peptides were described in detail elsewhere and many applications have been proposed (Acuña, Morero, & Bellomio, 2010; De Vuyst & Leroy, 2007). Although a number of peptides were described in the literature so far, nisin and pediocin PA-1 are better positioned than the other peptides as food preservatives. On one hand, nisin was discovered in 1928 (Rogers, 1928) and it is the best known lanthibiotic (Field, Hill, Cotter, & Ross, 2010). Nisin is the only bacteriocin approved so far as food preservative and it has been used in nearly 40 countries as such for more than sixty years now (Cleveland, Montville, Nes, & Chikindas, 2001). Nisin was recognized as food preservative by FAO/WHO in 1969. For instance, nisin (E 234) was authorized for food preservation in the European Union by Directive 95/2/EC on food additives (EFSA). There are almost 15 known nisin manufacturers worldwide (Jones, Salin, & Williams, 2005). Danisco is the global leader of antimicrobial food preservatives and commercialize nisin as Nisaplin® from 1953. Unfortunately, nisin does not have any activity against Salmonella (Gänzle, Hertel, and; Hammes, 1999), unless it is combined with other agents or procedures in the so-called hurdle technology (see below in section 4.1). It could be used as powder, liquid, dip, spray, coated and impregnated film (Jones et al., 2005). On the other hand, pediocin PA-1 is a nonmodified bacteriocin belonging to the subclass IIa, which is also very

Table 1 Bacteriocins active against Salmonella. Name

Inhibited strain

Reference

From Gram-positive bacteria Enterocin AS-48 BacTN635 Paracin 1.7 Plantaricin MG E 50–52 Enterocin P Lactococcin BZ Enterocin 012 Acidophilin 80

S. enterica S. enterica Salmonella spp S. Typhimurium S. Enteritidis S. Typhimurium Salmonella spp S. Typhimurium S. Panama 1467

Ananou et al. (2010) Smaoui et al. (2010) Ge et al. (2009) Gong et al. (2010) Svetoch et al. (2008) Kang and Lee (2005) Şahingil et al. (2011) Jennes et al. (2000) Zamfir et al. (1999

From Gram-negative bacteria Microcin J25 S. Newport S. Enteritidis Microcin B17 Clinical isolates Microcin 24 Clinical isolates Klebicin K S. enterica Raoultellin L S. enterica

Rintoul et al. (2001) Portrait et al. (1999) Zihler et al. (2009) Zihler et al. (2009) Fleming et al., 2010 Fleming et al. (2010)

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b c d e f g h i j

Cutter and Siragusa (1995b). Carneiro de Melo et al. (1998). Ukuku and Fett (2004). Govaris et al. (2010). Rattanachaikunsopon and Phumkhachorn (2010). Yuste and Fung (2004). Datta et al. (2008). Gill and Holley (2000). Boziaris and Adams (2000). Liang et al. (2002).

promising as preservative. However, even though there are commercial preparations of pediocin PA-1 (e.g. ALTA 2431, Kerry Bioscience. Cork Ireland), it has not been legally approved yet as food additive worldwide (Jeevaratnam, Jamuna, & Bawa, 2005; Settanni & Corsetti, 2008). Pediocin PA-1 is active against foodborne pathogens including Staphylococcus aureus, Clostridium perfringens, Listeria monocytogenes, and other bacteria closely related to the producer strain Pediococcus acidilactici PAC1.0 (Bhunia, Johnson, & Ray, 1988; Gonzalez & Kunka, 1987). As nisin, pediocin PA-1 also failed to kill Salmonella unless combined, for example with high hydrostatic pressures (Kalchayanand, Dunne, Sikes, & Ray, 2004). However, approval and acceptance of bacteriocins produced by microorganisms that are not generally considered as safe is highly unlikely in the near future. Initially, it was thought that bacteriocins isolated from Gram-positive bacteria were only active on the same kind of microorganisms. At present, there are many reports of new bacteriocins produced by Grampositive bacteria with inhibitory activity against Gram-negative bacteria (Table 1). As a result, several peptides were described. Among them, it can be mentioned BacTN635, a peptide produced by Lactobacillus plantarum sp TN635 that was able to kill not only Salmonella but also pathogenic fungus Candida tropicalis R2 CIP203 (Smaoui et al., 2010). Plantaricin MG is another interesting exception that was recently reported (Gong, Meng, & Wang, 2010). This peptide is relatively small as compared to other bacteriocins produced by Lactobacillus. Its mode of action seems to be quite similar to the rest of membrane-active bacteriocins though (Gong et al., 2010). On the other hand, a relatively large bacteriocin called paracin 1.7 was also reported as Salmonella-active peptide (Ge et al., 2009). It is important to note that paracin 1.7, produced by Lactobacillus paracasei HD1.7, is even active against Pseudomonas and yeasts (Ge et al., 2009). Surprisingly, E 50–52 a pediocin-like bacteriocin produced by Enterococcus faecium (NRRL B-30746) was shown to be very effective in controlling S. enteritidis as well as C. jejuni, and E. coli O157:H7 among others. It should be noted that the anti-Salmonella activity was not only demonstrated in vitro but also in therapeutic tests in chickens (Svetoch et al., 2008). Similar to E 50– 52, Kang and Lee (2005) reported some years ago that an enterocin P-like bacteriocin produced by E. faecium GM-1 had a broad antimicrobial spectrum including S. Typhimurium. This finding is in sharp contrast to enterocin P itself, which is unable to kill Gram-negative bacteria (Cintas, Casaus, Håvarstein, Hernández, & Nes, 1997). Another recently reported bacteriocin with broad inhibitory spectrum is the enterocin produced by an Enterococcus faecium isolated from mangrove environment. In particular, it was shown that this enterocin was active against S. Paratyphi (Annamalai, Manivasagan,

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Balasubramanian, & Vijayalakshmi, 2009). Alessandra Ferreira et al., screened 70 strains of Enterococcus mundtii and found that only four of them produced bacteriocins active against Salmonella Enteritidis as well as Listeria innocua, Listeria monocytogenes and Listeria plantarum. These bacteriocins were only partially purified and characterized so far (Ferreira, Canal, Morales, Fuentefria, & Corção, 2007). One of the newest bacteriocins from lactic acid bacteria reported to be active against Salmonella spp. is lactococcin BZ, which is produced by Lactococcus lactis subsp lactis BZ. This peptide is relatively heat labile because its activity is abolished after 15 min at 110 °C. It is also sensitive to beta mercaptoethanol. The anti-Salmonella activity does not seem to be that high, at least as compared to other food pathogens tested (Şahingil, Işlero lu, Yildirim, Akçelik, & Yildirim, 2011). Enterocin 012 and acidophilin 80 are among the few long known bacteriocins able to kill Salmonella. On one hand, acidophilin 80, a bacteriocin with a very narrow inhibitory spectrum, surprisingly inhibits Salmonella Panama 1467 and E. coli Row (Jennes, Dicks, & Verwoerd, 2000; Zamfir et al., 1999). On the other hand, enterocin 012 is a bacteriocin produced by Enterococcus gallinarum 012, a strain isolated from the duodenum of an ostrich. Unlike other bacteriocins from lactic acid bacteria, enterocin 012 is a lytic peptide (Jennes et al., 2000). Although all these peptides are very promising for future applications, none of them are being used to control Salmonella neither in foods nor in animal feeds at present. The cyclic bacteriocin enterocin AS-48 deserves a special mention. It is non-active against Salmonella in vitro unless combined with other treatments (Abriouel, Valdivia, Gálvez, & Maqueda, 1998). However, enterocin AS-48 alone did show a positive effect in lowering Salmonella counts during ripening of fermented sausages (Ananou et al., 2010) and was extensively tested in foods (Gálvez, Abriouel, López, & Ben Omar, 2007). 3.4. Microcins Bacteriocins from Gram-negative bacteria, known as microcins (Asensio, Pérez-Díaz, Martínez, & Baquero, 1976), are less studied as food preservatives, especially because they are produced by coliform bacteria, which are not recognized as safe by regulatory agencies. However, some of them are potential food additives and have antiSalmonella activity (see Table 1). An interesting example is microcin J25 (MccJ25), a peptide with an unusual lasso distinctive structure (Bayro et al., 2003; Rosengren et al., 2003; Wilson et al., 2003). S. Newport and S. Enteritidis were shown to be extremely sensitive to this peptide, (Portrait, Gendron-Gaillard, Cottenceau, & Pons, 1999; Rintoul, de Arcuri, Salomón, Farías, & Morero, 2001) but had no effects on many other serotypes including S. Typhimurium and S. Derby (Vincent, Delgado, Farías, & Salomón, 2004). Because of its structure, MccJ25 is highly resistant to proteases with the only exception of thermolysin (Blond et al., 1999). Because of this, MccJ25 might retain its activity in the intestine and hence alter the gut microbiota. Nonetheless, a microcin variant was recently produced with a cleavage site for chymotrypsin. This analog keeps the full activity but at the same time it is readily hydrolyzed and inactivated in the small intestine. It is therefore a very promising food preservative (Pomares et al., 2009). MccJ25 was also proposed for clinical applications against Salmonella (Lopez, Vincent, Zenoff, Salomón, & Farías, 2007). Other microcins that were shown to be very efficient are microcin B17 and microcin 24 (Zihler et al., 2009). Interestingly, other peptides from coliforms also have great prospective as food additives, especially active against Salmonella. They are Klebicin K and Raoultellin L, produced by Klebsiella ozaenae and Raoultella terrigena respectively (Fleming, Bolzan, & Nascimento, 2010). 3.5. Mechanism of action of bacteriocins Most bacteriocins from LAB and microcins disrupt the cytoplasmic membrane of the target bacteria (Acuña et al., 2010; Cotter et al.,

2005; Duquesne, Destoumieux-Garzón, Peduzzi, & Rebuffat, 2007). In the last years, membrane-associated receptors have been characterized for many bacteriocins. The first receptor described was the lipid II for class I bacteriocin nisin (Breukink et al., 1999). Nisin requires lipid II as a receptor to penetrate the membrane and its mechanism of action is dual i.e. it binds to lipid II and inhibits peptidoglycan synthesis. On the other hand, nisin uses lipid II as an anchor, penetrates and disrupts the plasma membrane (Wiedemann et al., 2001). Many of the post-translationally unmodified bacteriocins belonging to class II also need a receptor in the target cell membrane. In this case, it was determined that the mannose-phosphotransferase system (man-PTS) is the receptor for many of them (Héchard, Pelletier, Cenatiempo, & Frère, 2001; Kjos, Nes, & Diep, 2009). Furthermore, a loop in the C-terminal region of man-PTS IIC subunit from L. monocytogenes has already been characterized as responsible for the interaction with class IIa bacteriocins pediocin PA-1, sakacin P, leucocin C, among others (Kjos, Salehian, Nes, & Diep, 2010). Moreover, class IIc bacteriocin lactococcin A requires the presence of both, man-PTS IIC and IID subunits and interacts in a more complex way with the receptor (Kjos et al., 2010). The mechanism of action is basically the same, the bacteriocin would bind to the receptor, anchor and insert into the membrane. In the case of microcins, the mechanism of action is a bit more complex. As previously mentioned, microcins are bacteriocins acting on Gram-negative bacteria. Since their OM is an insurmountable barrier for peptides and proteins, microcins need to be transported into the periplasmic space by an OM protein. The OM transport protein is the first receptor which must be specifically recognized by the microcins. Once in the periplasm, linear class II microcins, the Gram-negative version of LAB bacteriocins belonging to the class IIa, need to be anchored to the IM receptor in order to penetrate the cell membrane. Therefore, they also require the presence of a specific protein in the IM that could act similarly to the membrane receptor required for class II bacteriocins. SdaC is the protein receptor for colicin V also known as microcin V (Gérard, Pradel, & Wu, 2005). For microcin E492 the receptor is the mannose permease (Biéler, Silva, & Belin, 2010; Bieler, Silva, Soto, & Belin, 2006) and for microcin H47 is the F0 proton channel from the ATP synthase complex (Rodríguez & Laviña, 2003; Trujillo, Rodríguez, & Laviña, 2001). On the other hand, class I microcins are posttranslationally modified peptides, which act at the intracellular level by interacting with specific targets (Severinov, Semenova, Kazakov, Kazakov, & Gelfand, 2007). Microcin J25 belongs to the class I microcin, it acts in the IM by inducing the production of superoxide radicals (Bellomio, Vincent, de Arcuri, Farías, & Morero, 2007) and by binding to RNA-polymerase and inhibiting the transcription after crossing the IM (Delgado, Rintoul, Farías, & Salomón, 2001). Microcin C (MccC) acts blocking translation by inhibiting the aspartyl-tRNA synthesis. This microcin is a heptapeptide–nucleotide. Once it is cleaved by intracellular proteases inside the target cell (Kazakov et al., 2008) an aspartyl-adenylate is released, which blocks the aspartyl-tRNA synthetase function (Metlitskaya et al., 2006). Microcin B17 (MccB) inhibits DNA replication by blocking the DNA gyrase (Heddle et al., 2001; Herrero & Moreno, 1986). The Salmonella OM and the need for two specific receptors for microcins significantly limit their spectrum of action. For example, MccJ25 is transported to the periplasm through the transporter of iron chelates FhuA, (Destoumieux-Garzón et al., 2005; Salomón & Farías, 1993). S. Typhimurium is resistant because its FhuA does not recognize the peptide. However, expressing E. coli fhuA in S. Typhimurium the bacteria becomes hypersensitive. Bacteriocins that are currently used as biopreservatives, nisin and pediocin PA-1, cannot pass across the OM of Gram-negative bacteria and, therefore, they are not active on Salmonella. Even if pediocin could pass across the OM, it still needs the presence of a protein in the IM that serves as a receptor. The case of nisin is different: it does not require a receptor protein, but lipid II that is present in Gram-positive and Gram-negative. For that reason, if nisin could

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cross the OM with a “gimmick” it should be active against Gram-negative bacteria such as Salmonella. Even though the interaction of nisin with the lipid II of Gram-negative bacteria was not demonstrated, treatments of Salmonella and other enterobacteriae with chelating agents that alter the permeability of the outer membrane combined with nisin proved to be useful (see below) (Stevens, Sheldon, Klapes, & Klaenhammer, 1991). In fact, S. Typhimurium deep rough LPS mutants who have an increased permeability and therefore an increased sensitivity to antibiotics are sensitive to nisin (Stevens, Klapes, Sheldon, & Klaenhammer, 1992).

pulsed electric fields (Toepfl, Heinz, & Knorr, 2005) and ultrasonication (Chemat, Zill-E-Huma, & Khan, 2010). In general, application of bacteriocins is more feasible than the use of either bacteriophages or colicins because of their physical properties. As a matter of fact, since bacteriocins are peptides, they do not easily lose activity. Furthermore, they are able to tolerate high temperatures as well as extreme pHs. Many of them can be autoclaved without changes in antibacterial activity.

4. Hurdle technology

4.1.1. Use of chelating agents in combination with bacteriocins Nisin was proposed for controlling Salmonella as a hurdle in association with chelating agents (Table 2). The first report using this approach conclusively showed that at least 20 Salmonella serovars were inhibited with simultaneous treatment of 50 μg/ml nisin and 20 mM EDTA. In fact, the population was reduced up to 5.3 log units after an hour of treatment. Neither EDTA nor nisin alone were able to inhibit the growth of Salmonella (Stevens et al., 1991). Later, Cutter and Siragusa (1995a) showed a positive effect by combining 50 μg/ml nisin with different chelators such as 500 mM lactate, 100 mM citrate, 50 mM EDTA or 1% (w/v) sodium hexametaphosphate in buffer. S. Typhimurium population was reduced up to 5.5 cfu log units. On the other hand, the combination of 1 μM nisin (~3.35 μg/ml) with 0.5– 5 mM trisodium phosphate was successfully used in controlling S. Enteritidis. Cell counts were dropped over 6 cfu log units after only 30 min of treatment (Carneiro de Melo, Cassar, & Miles, 1998). The main flaw of these reports though, is that experiments were performed under cell starvation conditions, which seem to constitute a different model from food products and hence the conclusions may not be accurate. Actually, Cutter and Siragusa (1995b) only got 0.4-log unit reduction of Salmonella upon nisin-lactate treatment when experiments were carried out in beef instead of buffer. In the same trend, Carneiro de Melo et al. (1998) only found over 1 log unit reduction when nisin– trisodium phosphate was applied in chicken skins instead of buffer. Furthermore, although Branen and Davidson (2004) working with trypticase soy broth instead of buffer still observed synergistic effect with nisin–EDTA combination on two pathogenic E. coli strains, the effect on S. Enteritidis was not synergistic at all. However, they did observe some bactericidal activity with a minimal bactericidal concentration of 46.9 μg/ml nisin and 1.25 mg/ml EDTA (~3.4 mM). It is important to

Hurdle technology (Leistner, 1978) is the combined use of various preservatives factors (called hurdles) in order to maximize the benefits that can be obtained from each one individually. Therefore, safer and more stable foods can be elaborated even without refrigeration (Leistner, 1992; Leistner, 2000). Thus, hurdle technologies are the rational combinations of hurdles in order to improve the total quality of foods as well as their nutritional and economic properties. The most important hurdles are high and low temperature, water activity, pH changes, redox potential, competitive microorganisms and chemical preservatives such as EDTA, lactic acid and the like (Leistner, 2000). Among over 200 hurdles currently available (Leistner & Grahame, 2005), the application of LAB is undoubtedly one of the most promising hurdles (Stiles, 1996; Stiles & Hastings, 1991). LAB may introduce several hurdles at a time i.e. acidify the medium, use essential nutrients and secrete antagonistic substances. In fact, a particular hurdle related to LAB, that will turn out to be of unquestionable importance, is the application of bacteriocins (Calo-Mata et al., 2008; Gálvez et al., 2007), especially when used in combination with hurdles that alter OM (see Fig. 1). In fact, an even transient modification of bacterial permeability might allow peptides cross OM and reach IM where they can exert their bactericidal action. The OM barrier disruption can be achieved by chemical treatments with chelating agents such as EDTA (Schved, Pierson, & Juven, 1996; Vaara, 1992), cationic compounds e.g. polymyxin (Vaara & Vaara, 1983) or cationic detergents such as benzalkonium chloride and cetyltrimethylammonium chloride (Hancock & Wong, 1984). On the other hand, physical treatments can also desestabilize the OM: high hydrostatic pressure (HHP) (Kato & Hayashi, 1999; Klotz, Mañas, & Mackey, 2010), cold stress, high-intensity

4.1. Antimicrobial peptides as hurdle against Salmonella

B)

A) Nisin

Pediocin

Class I Microcin

Class II Microcin

OM OMR

PG

IMR

IMT

IMR

IMT

IM Lipid II

IT

IT

Fig. 1. Salmonella biocontrol using bacteriocins on intact cells (A) and after permeabilization of the outer membrane (B). Some microcins are able to enter the periplasm through a transporter and then exert their effect. Bacteriocins of Gram (+) bacteria do not have a specific OM transporter, and therefore they have no activity against Salmonella. However, after OM permeabilization, some bacteriocins such as nisin can pass through this membrane and exert its antimicrobial action. On the other hand, pediocin-like peptides do not have antimicrobial activity at low concentrations after permeabilization due to the absence of a specific receptor. PG: peptidoglycan, OMR: outer membrane receptor, IMR: inner membrane receptor, IT: intracellular target.

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note that Branen and Davidson used a low concentration of the chelator as compared to the papers commented above, which does not allow direct comparisons between them. Besides, it was shown that S. Typhimurium OM was stabilized by nisin pre-treatment when cells were suspended in 0.1 mM EDTA. Therefore, nisin should not be used in combination with chelating agents at low concentrations. On the other hand, high concentrations of these agents would be able to completely disrupt OM and therefore, nisin would reach IM and exert its bactericidal effect (Helander & Mattila-Sandholm, 2000). Even though most of the reports on hurdle technology with chemical agents for controlling Salmonella in food involve nisin, enterocin AS-48 proved to be a useful tool as well. This bacteriocin was evaluated on S. Choleraesuis LT2 in combination with EDTA and Tris. The cell survival was reduced proportionally to the enterocin concentration. This positive effect could be enhanced either by using acidic (pH b 4) or alkaline conditions (pH N 9) or mild heat treatment (Abriouel et al., 1998). Both nisin and enterocin AS-48 were successfully used for surface decontamination of fruits and vegetables. In this regard, a positive effect of nisin-chelating agents treatment in foods was reported by Ukuku and Fett (2004). They combined 50 μg/ml nisin with 20 mM EDTA, 3% sodium lactate or 2% potassium sorbate as sanitizer treatments on whole and fresh-cut cantaloupe. All the combinations reduced 3 log units/cm 2 at day 0 of treatment and 2 log units/cm 2 after 3–7 days of treatment. On the other hand, enterocin AS-48 was used in order to get rid of S. enterica from soybean sprouts (Cobo Molinos et al., 2008). However, this bacteriocin was combined with several chemical and physical agents (see below). 4.1.2. Association of bacteriocins with other chemical treatments Nisin was successfully combined with several spices, displaying a remarkable effect controlling Salmonella. On one hand, 500–1000 international units of nisin/g combined with 0.6–0.9% oregano essential oil showed bactericidal activity in minced sheep meat. Salmonella population was reduced 1–2 log unit/g after two days of treatment and remained constant for the rest of the storage (Govaris, Solomakos, Pexara, & Chatzopoulou, 2010). In this report, the authors stressed that the predominant components of oregano essential oil were carvacrol and thymol. However, the involvement of other components in the synergistic combination with nisin cannot be ruled out. In fact, nisin also showed positive effect in association with other important oregano essential oil constituent such as p-cymene in ready-to-eat food (Rattanachaikunsopon & Phumkhachorn, 2010). Alternatively, the use of nisin and cinnamon in apple juice accelerates death of S. Typhimurium, being undetectable by direct plating in 3 days (Yuste & Fung, 2004). Moreover, nisin was used in combination with lysozyme added to calcium alginate coated on the surface of ready-to-eat smoked salmon samples at low temperature (Datta, Janes, Xue, Losso, & La Peyre, 2008). Moreover, 2-log unit reduction of S. Enteritidis in liquid egg white at 24 °C was achieved by nisin coated onto biodegradable polylactic acid polymer (Jin & Zhang, 2008). The S-layer from Lactobacillus acidophilus ATCC 4356 has murein hydrolase activity. Thus, in combination with nisin, S-layer acts synergistically to inhibit the growth of S. Newport (Prado-Acosta, Ruzal, Allievi, Palomino, & Sanchez Rivas, 2010). A similar effect was observed when cooked ham and bologna were coated with gelatin gel containing 25.5 g/l of lysozyme-nisin (1:3) plus 25.5 g/l of EDTA (Gill & Holley, 2000). An interesting approach was used by Cobo Molinos et al. (2008), who developed a combined treatment for the washing and storage of soybean sprouts. Enterocin AS-48 was associated to a number of chemical preservative compounds from which lactic, polyphosphoric and peracetic acids, hexadecyl pyridinium chloride and hydrocinnamic acid showed positive interaction. In fact, they significantly reduced the viable cells, enhancing the bactericidal effect of enterocin AS-48 even during storage. The best combinations were 1.5% lactic

acid-enterocin and 0.1% polyphosphoric acid-enterocin with a total reduction of around 4 log units for both treatments. In this report, the authors also combined enterocin AS-48 with some physical hurdles such as an initial washing at 65 °C containing enterocin in alkaline solution in order to reduce the initial pathogen load. Microcin J25 deserves a paragraph of its own because MccJ25 and its chymotrypsin-sensitive mutant were the only microcins tested in food so far (see above). Moreover, the use of the membrane-permeabilizing peptide (KFF)3K applied alongside MccJ25 allowed the inhibition of some S. Typhimurium strains that were naturally resistant to microcin (Pomares, Delgado, Corbalán, Farías, & Vincent, 2010). A pioneering work from Styles' group sub-cloned the gene of microcin V in a Grampositive expression vector downstream divergicin A signal peptide, which allowed its expression in lactic acid bacteria. This strategy might set the basis for controlling Gram-negative pathogens in foods using safe and beneficial bacteria without adding chemical preservatives (McCormick, Klaenhammer, & Stiles, 1999).

4.1.3. Physical hurdles in combination with bacteriocins It has been long known that a rapid chilling of S. Enteritidis suspended in either nutrient broth or phosphate-buffered saline leads to a transient cellular permeabilization. Boziaris and Adams (2000) took advantage of this effect and combined it with nisin. Interestingly, there was no effect in the absence of nisin but a dose-dependent increase in lethality was observed when this bacteriocin was present. This mild treatment was also tested in combination with EDTA in chicken carcasses, with a modest reduction of 0.7 log units of Salmonella. This poor result could be attributed to a buffering of the temperature shock by adherent bacteria and binding of the nisin to food particles. Therefore, the authors suggested that this approach should be improved in order to get a faster chilling. They also suggested that it might be combined with storage at low temperature in liquid medium since this treatment sensitizes bacteria against nisin (Elliason & Tatini, 1999). Kalchayanand, Hanlin, and Ray (1992) studied the effect of heating samples at 55 °C for 10 min followed by rapid cooling at 4 °C and final freezing at −20 °C in combination with rather high concentrations of either nisin or pediocin AcH (4000 AU/ml) on the survival of S. Typhimurium. The best effect was obtained with nisin (4 log unit reduction) as compared to pediocin AcH (1.9 log unit reduction). Control cells treated with no antimicrobial peptides dropped 1.2 log units. The same group studied the effect of the same bacteriocins at high concentration (5000 AU/ml) in combination with ultrahigh hydrostatic pressure (UHP) and pulsed electric field. The physical hurdles alone used in this paper affect the survival of S. Typhimurium (6.3 log units at 50,000 lb/in. for UHP). However, the reduction is even more pronounced i.e. 9.9 log units at 50,000 lb/in. when UHP is combined with nisin (Kalchayanand, Sikes, Dunne, & Ray, 1994). In a later study, the same group performed a series of studies in order to analyze cellular morphology upon use of high pressure to control Salmonella. It was concluded that bacteriocins enhanced cell morphology changes after HP treatment. In fact, extensive changes in cell envelope were observed (Kalchayanand et al., 2004). High hydrostatic pressure (HHP) was also combined with nisin with positive results. In fact, lower levels of pressure were needed when nisin was used for reducing S. Enteritidis counts (Lee & Kaletunç, 2010). Another example of successful combination of nisin and HPP was recently reported by Ogihara et al., who showed that 1% nisin alongside 250 MPa for 30 min completely inactivated S. Enteritidis (Ogihara, Yatuzuka, Horie, Furukawa, & Yamasaki, 2009). In addition, HHP was applied to control S. enterica in combination with the cyclic bacteriocin enterocin AS-48 in low acid fermented sausages. HHP treatment reduced Salmonella counts in control fuets by 2.08 log units and when combined with enterocin AS-48 there was a 2.72 log unit reduction of Salmonella population (Ananou et al., 2010).

M.C. Chalón et al. / Food Research International 45 (2012) 735–744

Pulsed-electric field (PEF) was chosen as a means of reducing Salmonella from fruit juices in association with nisin, lysozyme and enterocin AS-48. On the one hand, enterocin AS-48 in combination with high intensity PEF was successfully used to eliminate S. enterica in apple juice (Martínez Viedma et al., 2008). The authors obtained an important reduction of 4.5 log units of Salmonella by choosing the right temperature (40 °C) and time of treatment (1000 μs) as well as the right order of treatment i.e. bacteriocin first, electric pulse afterward. On the other hand, PEF also proved to be an interesting approach for controlling S. Typhimurium in orange juice (Liang, Mittal, & Griffiths, 2002). The electric pulses alone were effective in reducing Salmonella (5.9 log units) but combination with nisin did not improve the efficiency (just 5.94 log unit reduction). Lysozyme reduced 8.65 log units when associated with PEF and the combination of PEF, nisin and lysozyme got an impressive 10 log unit reduction.

5. Conclusions According to the Centers for Disease Control and Prevention (CDC) estimates, foodborne diseases have reduced 25% in the last 15 years, except Salmonella infections (CDC, 2011). Moreover, nontyphoidal Salmonella spp. represent the most important bacterial food pathogen in the USA in the last decade causing hospitalization and death (Scallan et al., 2011). Even though the usage of antibiotics for human and animal treatment is sometimes unavoidable, it should always be considered as the last choice because of the resistance problems discussed above. Therefore, preventive measures have to be taken beforehand alongside strict screening programs and rapid detection analysis for preventing food poisoning. Chemical preservatives are also being questioned nowadays because there is a growing demand for minimally processed foods. For that reason, the current tendency is to use a combination of different mild treatments in the so-called hurdle technology. Interestingly, bacteriocins seem to be a useful hurdle that urges to be taken into account. However, from all the bacteriocins described so far, only a few bacteriocins were studied in some detail in food preservation against Salmonella always in combination with OM disruptive methods as it was discussed in this review. At present, there is an intensive search for bacteriocins active on Salmonella, which do not need permeabilizing treatments in order to kill this pathogen. These bacteriocins are going to be of extraordinary help in keeping foods and animal feeds free of Salmonella without interfering with organoleptic properties of the products. The implementation of bacteriocins as a hurdle is just starting to arise and it definitely has an enormous potential in the near future. Furthermore, by knowing the structure–function relationship of both bacteriocins from Gram-negative and Gram-positive bacteria as well as colicins, in conjunction with the full understanding of their mechanism of actions, improved bacteriocins with enhanced activity against Salmonella or other pathogens could be designed. Bacteriocins could be developed with different physical–chemical properties i.e. hydrophobicity, electric charge, solubility, resistance to proteases, optimal temperature of work and resistance to diverse environmental conditions such as pH, temperature and water activity. Therefore, they might be used in a variety of food systems depending on the requirements imposed for their processing. Thus they may constitute the definitive hurdle against Salmonella.

Acknowledgments Financial support was provided by CONICET (Grants PIP 4996 and 2852), CIUNT (Grant 26/D439-4), and the Agencia Nacional de Promoción Científica y Técnica (PICT 2107, PAE 22642). M.C.C and L.A. is recipient of a CONICET fellowship. R.D.M., C.J.M. and A.B. are researchers of CONICET.

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