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Journal of Food Science and Technology logoLink to Journal of Food Science and Technology
. 2015 Feb 11;52(9):5408–5417. doi: 10.1007/s13197-014-1666-2

Strategies for the use of bacteriocins in Gram-negative bacteria: relevance in food microbiology

Cláudia Vieira Prudêncio 1, Miriam Teresinha dos Santos 1, Maria Cristina Dantas Vanetti 1,✉
PMCID: PMC4554667  PMID: 26344957

Abstract

Bacteriocins are ribosomally synthesized peptides that have bacteriostatic or bactericidal effects on other bacteria. The use of bacteriocins has emerged as an important strategy to increase food security and to minimize the incidence of foodborne diseases, due to its minimal impact on the nutritional and sensory properties of food products. Gram-negative bacteria are naturally resistant to the action of bacteriocins produced by Gram-positive bacteria, which are widely explored in foods. However, these microorganisms can be sensitized by mild treatments, such as the use of chelating agents, by treatment with plant essential oils or by physical treatments such as heating, freezing or high pressure processing. This sensitization is important in food microbiology, because most pathogens that cause foodborne diseases are Gram-negative bacteria. However, the effectiveness of these treatments is influenced by several factors, such as pH, temperature, the composition of the food and target microbiota. In this review, we comment on the main methods used for the sensitization of Gram-negative bacteria, especially Salmonella, to improve the action of bacteriocins produced by Gram-positive bacteria.

Keywords: Bacteriocins, Biocontrol, Gram-negative bacteria, Outer membrane

Introduction

Bacteriocins are antimicrobial peptides that are ribosomally synthesized by Gram-negative and Gram-positive bacteria that have bacteriostatic or bactericidal effects on other bacteria (Héchard and Sahl 2002; Meghrous et al. 1999). These peptides show great potential for use in foods as a strategy for control of foodborne pathogens and spoilage microorganisms (Allende et al. 2007; Deegan et al. 2006). The use of bacteriocins has minimal impact on the nutritional and sensory properties of foods, thus satisfying consumer demand for products with a lower amount of chemical additives (Gálvez et al. 2007; Settanni and Corsetti 2008). In addition, bacteriocins have several desirable characteristics, such as low toxicity and stability against proteases and temperature (Dischinger et al. 2014; Garcia et al. 2010).

Usually, Gram-negative bacteria are naturally resistant to the bacteriocins produced by Gram-positive bacteria, due to their outer membrane, which acts as an effective barrier (Cao-Hoang et al. 2008; Gyawali and Ibrahim 2014). Nevertheless, agents or treatments that destabilize the outer membrane enable these peptides to affect Gram-negative bacteria (Gálvez et al. 2014; Chalón et al. 2012; Martin-Visscher et al. 2011). This sensitization is relevant in food microbiology, because most pathogens related to foodborne diseases are Gram-negative bacteria (Boziaris and Adams 1999). This strategy has been demonstrated with food additives, such as chelating agents or plant essential oils; with sanitization treatments using other antimicrobial compounds, such as sodium hypochlorite; and with conservation and food processing treatments, such as freezing, high pressure processing and pulsed electric fields, on several Gram-negative bacteria, including Aeromonas hydrophila, Arcobacter butzleri, Citrobacter freudii, Enterobacter aerogenes, Escherichia coli, Salmonella, Shigella flexneri, Shigella sonnei, Pseudomonas aeruginosa, Pseudomonas fluorescens, Pseudomonas putida and Yersinia enterocolitica (Tables 1 and 2).

Table 1.

Use of bacteriocins on Gram-negative bacteria associated to different treatments

Bacteriocin Target microorganism Concentration Associated treatment Reference
Nisin Several serovars of Salmonella, E. coli, E. aerogenes, S. flexneri, C. freudii 50 μg.mL−1 EDTA (20 mM) Stevens et al. (1991)
E. coli 200 to 1000 AU.mL−1 EDTA (10 mM), phosphate (20 mM), citric acid (20 mM) and pyrophosphate (20 mM) Boziaris and Adams (1999)
P. fluorescens, S. sonnei, S. enterica Enteritidis 100 AU.mL−1 High pressure processing (155 to 400 MPa, 15 min) Masschalck et al. (2001)
A. butzleri 500 AU.mL−1 EDTA (20 mM) and phosphate trisodium (10 %) Phillips and Duggan (2001)
E. coli O157:H7 1066 AU.mL−1 EDTA (500 and 1000 mM) and sodium lactate (800 mM) Belfiore et al. (2007)
E. coli 25 to 1000 AU.mL−1 Fast freezing Cao-Hoang et al. (2008)
E. coli DH5α, P. aeruginosa, S. enterica Typhimurium 50 μM EDTA (20 mM) Martin-Visscher et al. (2011)
E. coli, S. enterica Typhimurium 100 AU.mL−1 Low temperature (6.5 °C) Elliason and Tatini (1999)
S. enterica Enteritidis 500 to 2500 AU.mL−1 Heating (55 °C, 15 min) Boziaris et al. (1998)
A. butzleri 500 AU.mL−1 Heating (50 °C) Phillips and Duggan (2002)
S. enterica Typhimurium, Y. enterocolitica, A. hydrophila, P. putida 4000 AU.mL−1 Heating (55 °C, 10 min) or frozen (− 20 °C, 2 h) Kalchayanand et al. (1992)
S. enterica Typhimurium 200 AU.mL−1 EDTA (1.5 mM) Prudêncio et al. (2015)
Gallidermin E. coli, P. aeruginosa, S. enterica Typhimurium 50 μM EDTA (20 mM) Martin-Visscher et al. (2011)
Bovicin HC5 S. enterica Typhimurium 50–200 AU.mL−1 EDTA (1.6 mM), citric acid (7 mM), gluconic acid (100 mM) sodium citrate (100 mM), nitrile-tri-acetic acid (6.25 mM) and diethanolamine (50 mM); Tween 80 and Ramnolipid (5X CMC) Prudêncio et al. (2014)
Lactocin 705 E. coli O157:H7 2133 AU.mL−1 EDTA (500 and 1000 mM) and sodium lactate (800 mM) Belfiore et al. (2007)
Cerein 8A S. enterica Enteritidis, 3200 AU.mL−1 EDTA (20 to 100 mM) and sodium lactate (200 mM) Lappe et al. (2009)
Carnocyclin A E. coli DH5α, P. aeruginosa 25 μM EDTA (20 mM) Martin-Visscher et al. (2011)
Carnobacteriocin BM1 P. aeruginosa
Piscicolin 126
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Table 2.

Use of bacteriocins on Gram-negative bacteria in foods associated to different treatments

Bacteriocin Target microorganism Concentration Associated treatment Food matrix Reference
Nisin E. coli 1280 AU.g−1 High pressure processing (400 MPa, 10 min) Ham Garrida et al. (2002)
A. butzleri 500 AU.mL−1 Sodium lactate (2 %), sodium citrate (1.5 %) Chicken Long and Phillips (2003)
E. coli, P. fluorescens 500 AU.mL−1 High pressure processing (200 to 500 MPa, 5 min) Milk Black et al. (2005)
S. enterica Typhimurium 0.25 to 0.5 μg.mL−1 Essential oil (5 to 30 μL.100 mL−1) Barley soup Moosavy et al. (2008)
Pseudomonas sp. 500 to 1500 AU.g−1 EDTA (10 mM) Chicken Economou et al. (2009)
S. enterica Stanley, E. coli, S. enterica Newport 300 AU.mL−1 EDTA (20 mM) Apple juice Ukuku et al. (2009)
S. enterica Enteritidis 500 or 1000 AU.g−1 Oregano essential oil (0.6 or 0.9 %) Sheep meat Govaris et al. (2010)
Pseudomonas sp. 500 AU.mL−1 EDTA (20 mM), potassium sorbate, sodium benzoate, sodium diacetate (3 %) Shrimps Norhana et al. (2012)
S. enterica Enteritidis 500 to 2500 AU.mL−1 Heating (55 °C) Egg white Boziaris et al. (1998)
Enterocin AS-48 E. coli O157:H7 50, 100 or 200 μg.mL−1 EDTA (20 mM), sodium polyphosphate (0.3 or 0.5 %) Apple juice Ananou et al. (2005)
S. enterica Choleraesuis 30 μg.mL−1 Pulsed electric field (35 kV, 150 Hz) Viedma et al. (2008)
S. enterica 25 μg.mL−1 Lactic acid (1.5 %) and polyphosphoric acid (0.1 %), tri-sodium phosphate (1.5 %), sodium hypochlorite (100 ppm) Soybean sprouts Cobo Molinos et al. (2008)
E. coli, S. sonnei, S. flexneri, E. aerogenes, Y. enterocolitica and A. hydrophila 25 μg.mL−1 Polyphosphoric acid (different concentrations for each species between 0.2 and 2 %)
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The efficacy of these strategies has already been demonstrated in several tests both in vitro and in food models. Most such tests have used nisin (Tables 1 and 2), because of its approval for use in foods by the Food and Drug Administration (FDA) as a “Generally recognized as Safe” (GRAS) additive (Federal Register 1988). Bacteriocins can be used in several products foods, such as meat, chicken, dairy, eggs, seafoods, fruit and vegetables products (Gálvez et al. 2014). Its use increases the food security and the shelf life of foods (Allende et al. 2007; Deegan et al. 2006). They are produced in foods, by activity of bacteriocin-producing strains or are added in foods, as food preservatives (Settanni and Corsetti 2008). Its activity can be influenced by several factors, such as environmental conditions of storage of food, food components, solubility and food additives (Settanni and Corsetti 2008). The sensibility of target cell can be also altered due to changes in cell composition in response to environmental conditions (Kawasaki 2012).

Classification and mechanism of action of the bacteriocins

Bacteriocins can be subdivided into classes that reflect the similarities and differences of the molecules (Cleveland et al. 2001; Garcia et al. 2010). Class I, also known as lantibiotics, contains small peptides, of 19 to 50 amino acids and a molecular mass of less than 5 kDa (Table 3) (Cleveland et al. 2001). This group is characterized by the presence of unusual amino acids residues, such as lanthionine (Lan) and methyl lanthionine (MeLan), that result from post-translational modifications (Cleveland et al. 2001; Guder et al. 2000; Sahl and Bierbaum 1998). Lantibiotics are subdivided into subclasses or subtypes according to their chemical structure and activity (Kraaij et al. 1999). Subclass A is composed of amphipathic peptides that are elongated and flexible, with capacity to form pores, such as nisin, galidermin and bovicin HC5. Lantibiotics grouped in subclass B are smaller and globular, such as mesarcidin and cinnamicin, and can inhibit specific enzymes (Kraaij et al. 1999).

Table 3.

General characteristics of bacteriocins used against Gram-negative bacteria

Classification Bacteriocin Producer strain Biochemical characteristics Mode of action Reference
Lantibiotic Nisin Lactococcus lactis subsp lactis Amphipathic peptide, elongated, positively charged, of 34 amino acid residues and molecular mass of 3.3 kDa. Contains unusual amino acids (lanthionine and methyl-lanthionine), derived from post-translational modifications. Stable to heat and to pH (between 2.0 and 7.0). Formation of pores in the cytoplasmic membrane and inhibition of cell wall synthesis. Liu and Hansen (1990), Delves-Broughton et al. (1996), Breukink and Kruijff (1999)
Gallidermin Staphylococcus gallinarum Peptide of 22 amino acid residues, similar to epidermin Kellner et al. (1988), Gotz et al. (2014)
Bovicin HC5 Streptococus bovis HC5 Peptide of 2.4 kDa, about 22 amino acid residues. Stable to heat and acidic pH. Mantovani et al. (2002)
-a Cerein 8A Bacillus cereus 8A Peptide with molecular mass of 26 kDa. Stable at temperatures below 80 °C and pH between 2.0 and 11.0 Possible formation of pores in the cytoplasmic membrane. Bizani and Brandelli (2002)
Class II IIc Carnocyclin A Carnobacterium maltaromaticum Circular peptide of 60 amino acid residues and molecular mass of 5.9 kDa. Stable to heat and pH between 2.0 and 12.0. Formation of pores in the cytoplasmic membrane. Martin-Visscher et al. (2008; 2011)
IIa Carnobacteriocin BM1 C. maltaromaticum Peptide of 43 amino acids residues and molecular mass of 4.5 kDa. Quadri et al. (1994)
IIc Enterocin AS-48 Enterococcus faecalis subsp. liquefaciens A 48–32 Circular cationic peptide of 70 amino acids residues, molecular mass of 7.2 kDa. Presents globular structure, formed by five helices (α1 a α5), with pI 10.5. Stable to heat and acidic pH. Samyn et al. (1994), Gonzalez et al. (2000), Cobos et al. (2001)
IIb Lactocin 705 Lactobacillus casei CRL705 Its activity depends of complementation of two peptides, called 705α and 705β, of 33 amino acids residues each. Castellano et al. (2003)
IIa Piscicolin 126 C. maltaromaticum Peptide of 44 amino acids residues and molecular mass of 4.4 kDa. Stable to heat and acidic pH, but inactivated at neutral and alkaline pH. Jack et al. (1996)
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aNot determined

Class II bacteriocins are composed of thermostable peptides, containing 20 to 60 amino acids, without post-translational modifications and molecular mass lower than 10 kDa (Table 3) (Deegan et al. 2006; Héchard and Sahl 2002). Generally, this class is subdivided into subclasses: subclass IIa is composed of peptides that demonstrate activity against Listeria and exhibit a common N-terminal domain (Tyr-Gly-Asn-Gly-Val-X-Cys). Examples of this group include the carnobacteriocin BM1 and the piscicolin 126 (Cintas et al. 2001; Ennahar et al. 2000; Héchard and Sahl 2002). Subclass IIb is composed of bacteriocins that are formed by two peptides that act synergistically, such as lactocin 705, in which the active molecule is formed by the interaction of two peptides, of 33 amino acids residues each, called 705α and 705β (Castellano et al. 2003). Subclass IIc includes circular peptides that are dependent on the Sec system, such as carnocyclin A and enterocin AS-48 (Cintas et al. 2001; Héchard and Sahl 2002).

Generally, bacteriocins act in sensitive cells by forming pores in the cytoplasmic membrane, which causes an efflux of intracellular metabolites, such as potassium and amino acids, resulting in the depolarization of the membrane and, consequently, cellular death (Helander and Mattila-Sandholm 2000; Nes et al. 2006). During the anchoring in the cytoplasmic membrane, the bacteriocins can use a specific receptor, which explain the high efficiency in vivo. Nisin, gallidermin and bovicin HC5 appear to use the same receptor molecule, lipid II (Bonelli et al. 2006; Hasper et al. 2004; McAuliffe et al. 2001; Paiva et al. 2011; Wiedemann et al. 2001). Thus, these bacteriocins also interfere with the biosynthesis of peptidoglycan (Guder et al. 2000). Because the lipid II is a molecule that is highly conserved among prokaryotes, if these peptides have access to the cytoplasmic membrane, they will act more efficiently than those peptides that require specific receptors for anchoring to the membrane, such as carnobacteriocin BM1 and piscicolin 126 that use the mannose phosphotransferase system (Martin-Visscher et al. 2011). In this case, the amino acid sequence of the receptor may vary among different bacterial species, which can lead to differences in the sensitivity of target cells (Martin-Visscher et al. 2011).

Despite some similarities among the bacteriocin molecules of the same class, the sensitivity of target cells varies. These variations are not only due to changes in the bacteriocin molecule but also to differences in the lipid composition of the target cell membrane (Nissen-Meyer and Nes 1997).

Bacteriocins combined with food preservatives

Food preservatives are substances added to products to extend the storage life, by prevent or retard the deterioration of odor, color, texture, flavor, appearance, safety and nutritive value (Richter et al. 1993). Examples including the ethylenediaminetetraacetic acid (EDTA), which is widely used as a chelating agent to minimize reactions catalyzed by metals and acids and their salts, which used to minimize the growth of microorganism and with technologic function (Beales 2004; Branen and Davidson 2004; Chalón et al. 2012). These preservatives may act in destabilize of the outer membrane, by release of components of the structure or by intercalate in the membrane, permitting the bacteriocin action (Alakomi et al. 2000).

The use combined of the bacteriocins with EDTA is one of most common strategies in the sensitization of Gram-negative bacteria (Tables 1 and 2). EDTA acted promotes the release of the LPS layer (Alakomi et al. 2003). Details of the action mechanism are not yet understood, but it is known that there is at least partial disruption of the lipopolysaccharide layer (LPS), possibly due to binding to calcium and magnesium ions, which would establish a cross-link with sugar residues and phosphate radicals, inside the core polysaccharide, reinforcing the structure of the outer membrane (Alakomi et al. 2003; Branen and Davidson 2004). Thus, EDTA acts to enhance the bacterial activity of other antimicrobials, in addition to expanding the spectrum of action of bacteriocins, particularly against Gram-negative bacteria, such as Salmonella, E. aerogenes, S. flexneri, C. freudii, E. coli, P. aeruginosa and A. butzleri (Table 1) (Branen and Davidson 2004). Usually, low concentrations of EDTA (10 to 20 mM) are sufficient to produce sensitization for bacteriocin activity (Tables 1 and 2).

However, several factors can alter the sensibility of target cells, including the manner of administration of the chelating agent, the time of treatment and the environmental conditions of treatment (Boziaris and Adams 1999; Phillips and Duggan 2001; Prudêncio et al. 2015). The inhibition of microbial growth appears to be a time-dependent process, and the method of application can be a critical factor in obtaining the desired effect, it is recommended the simultaneous use of the bacteriocin and the chelating agent (Boziaris and Adams 1999; Phillips and Duggan 2001; Stevens et al. 1991). The activity of the chelating agent is also influenced by pH: at low pH, a large proportion of the carboxylate group is in its non-ionized form, which is not a particularly effective electron donor and the EDTA-metal complex is less stable. Therefore, the combination of EDTA with bacteriocins is more effective at near-neutral pH, although several peptides, such as nisin and bovicin HC5, are more efficient to low pH value (Ananou et al. 2005; Boziaris and Adams 1999; Houlihan et al. 2004; Lappe et al. 2009; Norhana et al. 2012; Prudêncio et al. 2015).

The sensitivity to the combination of bacteriocins and EDTA varies between different species of Gram-negative bacteria, and even between different strains of the same species. The concentration of chelating agent necessary for sensitization is also variable, possibly because of the differences in the structure of the LPS layer, which interfere with the permeability (Boziaris and Adams 1999). For use in foods, large quantities of the chelating agent may be required for the removal of exogenous divalent cations that are associated with the food system and for the effective sensitization of Gram-negative cells (Boziaris and Adams 1999; Lappe et al. 2009).

Other chemical compounds can also be used for the disruption of the outer membrane, such as acids and salts (Tables 1 and 2). Lactic, citric and polyphosphoric acids and their salts, as well as tri-sodium phosphate, act as disintegrating agents of the outer membrane and have demonstrated activity in the sensitization of Gram-negative bacteria, including E. coli, S. sonnei, S. flexneri, E. aerogenes, Y. enterocolitica, A. hydrophila, Salmonella and A. butzleri (Tables 1 and 2) (Alakomi et al. 2000; Belfiore et al. 2007; Cobo Molinos et al. 2008; Long and Phillips 2003; Phillips and Duggan 2001). These associations are efficient in foods, and different methods of application can be employed, such as in a washing solution for sanitization or addition of bacteriocin with compounds, similar to food additives (Table 2) (Belfiore et al. 2007; Cobo Molinos et al. 2008).

Bacteriocins combined with plant essential oils

Plant essential oils are volatile complex natural substances, characterized by the presence of phenolic compounds with a strong odor that are produced by aromatic plants as secondary metabolites. Essential oils may have bactericidal, fungicidal, virucidal activities and medicinal properties, and have practical applications, such as analgesics, perfumes, anti-inflammatory agents, local anesthetics and food preservatives (Bakkali et al. 2008; Burt 2004).

Components of plant essential oils such as thymol and carvacrol, act on the bacterial membrane, resulting in important morphological alterations and in the depletion of the intracellular content (Govaris et al. 2010; Moosavy et al. 2008). The mechanism of action of such agents is still poorly understood, but it is known that thymol and carvacrol act to disintegrate the outer membrane, and their activity does not involve the chelation of divalent cations from the outer membrane, because compounds such as magnesium chloride do not interfere with their activity, in contrast to the action of EDTA (Helander et al. 1998).

However, the use of essential oils and their derivatives in foods is limited by sensory changes, because high concentrations are needed to exert antimicrobial activity (Govaris et al. 2010; Gutierrez et al. 2008; Nazer et al. 2005). Furthermore, food composition may influence the action of essential oils: high protein concentrations and moderately acidic pH result in an increase in the antimicrobial activity of oregano and thyme essential oils, while concentrations of potato starch or sunflower oil greater than 5 % reduce their efficiency (Gutierrez et al. 2008).

Thus, one alternative has been an association with other antimicrobial agents, such as bacteriocins. The effectiveness of this strategy has already been demonstrated with carvacrol and pediocin on E. coli O157:H7 (Turgis et al. 2012), and carvacrol and thymol and nisin on S. enterica Enteritidis, and others (Table 2) (Govaris et al. 2010). This strategy is viable, because of the consequent reduction of the amount of antimicrobial added to foods, and such a dual application prevents possible undesirable sensory changes due to the presence of large amounts of essential oils (Govaris et al. 2010; Nazer et al. 2005; Turgis et al. 2012). This was demonstrated on S. enterica Typhimurium and S. aureus, in which the presence of nisin considerably reduced the concentration of essential oil for the inhibition of both bacteria (Moosavy et al. 2008).

Bacteriocins combined with high pressure processing (HPP)

High pressure processing has been evaluated as a food pasteurization technique for inactivating microorganisms at room temperature, and thus minimizing the loss of sensory and nutritional components of the food (Huang et al. 2014; Masschalck et al. 2001). Under normal conditions, the process preserves the original color, flavor and nutritional content because smaller molecules such as pigments, vitamins, volatile compounds and others are less affected by high pressure (Huang et al. 2014).

The mode of action of HPP depends on the level of pressure. Pressures between 30 and 50 MPa can influence gene expression, protein synthesis and reduce the number of ribosomes. A pressure of 100 MPa induces partial protein denaturation, while 200 MPa causes damage to the cytoplasmic membrane and the internal cell structure. An increase of 300 MPa or more induces irreversible damage, such as the denaturation of enzymes and proteins and the rupture of the membrane (Garrida et al. 2002; Huang et al. 2014).

Microorganisms demonstrate differences in their resistance to pressure, depending on the species, strain, physiological state, processing temperature and substrate (Huang et al. 2014; Patterson 2005). As the different levels of pressure exert distinct effects, it is necessary to evaluate the response of each microorganism in each food system (Huang et al. 2014). In low-acid foods, vegetative cells exhibit great resistance to this process, requiring high pressure for the inactivation of microorganisms, which is not economically feasible and furthermore may causes changes in the sensory characteristics of foods, such as texture and color (Black et al. 2005; Garrida et al. 2002; Masschalck et al. 2001).

Generally, HPP treatment does not completely inactivate microorganisms, allowing the recovery of injured cells, but such recovery is dependent upon the treatment conditions and of the presence of other antimicrobial compounds (Patterson 2005). Food constituents may protect microbial cells against the increase in hydrostatic pressure or facilitate their recovery after treatment. Thus, to prevent the emergence of resistant cells, this technology has been used in conjunction with other antimicrobial compounds to ensure food safety. One of the alternatives is the use of bacteriocins, because high pressure destabilizes the outer membrane, increasing the activity of bacteriocins in Gram-negative cells. Furthermore, Gram-negative bacteria are more sensitive to HPP, whereas Gram-positive bacteria are more sensitive to bacteriocins. Thus, combined use is complementary (Garrida et al. 2002; Masschalck et al. 2001; Patterson 2005).

Several works have demonstrated the efficacy of this strategy and report an increase in bactericidal activity against important pathogens, such as Salmonella and E. coli, in addition to the spoilage microorganisms that are measured by the total plate count (Tables 1 and 2) (Ponce et al. 1998; Rodriguez et al. 2005; Zhao et al. 2013). Moreover, pressure-resistant strains of E. coli have also demonstrated sensitivity to nisin, when treated under high pressure (Masschalck et al. 2000).

However, the process of sensitization can be transient, this is occurs only during the period in which the Gram-negative cells are subjected to high pressure. Therefore, the simultaneous administration of bacteriocin with high pressure is recommended (Black et al. 2005; Masschalck et al. 2001). The sensitivity of different species is variable and P. fluorescens demonstrated more sensitivity than E. coli, in milk (Black et al. 2005).

Bacteriocins combined with a pulsed electric field

The application of a pulsed electric field is considered a non-thermal technology that acts by forming reversible or irreversible pores in the cell membrane. This process improves the sensitization of Gram-negative bacteria to the action of bacteriocins, which work synergistically, increasing the damage to the cytoplasmic membrane (Table 2) (Viedma et al. 2008).

There is little information available about the effect of this strategy in Gram-negative bacteria. However, it is known that the efficiency of the treatment increases with temperature, possibly due to the increase in cell membrane fluidity, which facilitates the process of disorganization promoted by these treatments. However, this parameter can be maintained in mild temperatures. For example: for apple juice, a temperature of 40 °C is adequate, and such a temperature ensures sensory and nutritional qualities and reduces the costs of the process, which is of great interest for the food processing industry (Viedma et al. 2008).

As with other treatments, the method of application is an important parameter, with the simultaneous use of pulsed electric fields with bacteriocins being more efficient. This is primarily due to the high resistance of Gram-negative bacteria to treatments with pulsed electric fields, particularly at acidic pH, a condition under which bacteriocins demonstrate greater efficiency (Boziaris and Adams 1999; Houlihan et al. 2004; Viedma et al. 2008).

Bacteriocins combined with temperature treatments

Temperature treatments may promote perturbations in the outer membrane, either at low or high temperatures, favoring the action of bacteriocins.

A reduction in temperature promotes a change in the structure of the outer membrane. These alterations may permeabilize the cell to bacteriocin, allowing the nisin to act on S. Typhimurium and E. coli at refrigeration temperatures (Elliason and Tatini 1999; Prudêncio et al. 2015). The chilling process only allows the effective sensitization of Gram-negative bacteria to the action of bacteriocins, when the temperature drops rapidly, because there is not enough time for the reorganization of the outer membrane, altering its permeability. It has been demonstrated that the growth phase of E. coli influences the concentration of bacteriocin required for inhibition. Thus, cells in stationary phase under rapid chilling require higher concentrations of nisin (Cao-Hoang et al. 2008). As observed with other strategies, simultaneous treatment with bacteriocins has a more significant result than the sequential use (Cao-Hoang et al. 2008).

The bactericidal effect varies depending on the strains, bacteriocins and methodologies used, as demonstrated by the results of Kalchayanand et al. (1992), wherein S. enterica Typhimurium and Y. enterocolitica were more sensitive to nisin, while A. hydrophila and Pseudomonas putida were more sensitive to pediocin during freezing.

Heat also sensitizes Gram-negative bacteria to the action of bacteriocins (Boziaris et al. 1998; Phillips and Duggan 2002). The application of bacteriocin after heat treatment resulted in a synergistic effect, and unlike other treatments, simultaneous use only slightly increases the reduction in viability (Ueckert et al. 1998). Differences related to strains and bacteriocins were also observed with the use of heat, and pediocin was generally more efficient than nisin (Kalchayanand et al. 1992).

Conclusions

Currently, there is a large number of characterized bacteriocins with potential use in food. However, the effectiveness of this strategy depends on several factors, such as pH, temperature, food composition and target microbiota. Therefore, it is necessary to establish effective conditions for the use of each bacteriocin in each food matrix.

Although several agents and/or treatments used in combination with bacteriocins inhibit bacterial growth alone, the presence of these peptides provides an additional level of protection by preventing the growth of cells affected by sublethal damage, thus ensuring greater safety for the food product.

The use of bacteriocins in association with chemical compounds or physical treatments allows us to extend the spectrum of action of these peptides on Gram-negative bacteria, in addition to minimizing the emergence of resistant cells. However, for effective application of this technology, more studies are necessary, with different food matrices and in mixed cultures, to understand how bacteria can survive and adapt in a complex environment.

Acknowledgments

The authors thank to the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), and the Fundação de Amparo à Pesquisa do Estado de Minas Gerais for financial support.

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