Critical Reviews in Biotechnology

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Bacteriocins from lactic acid bacteria and their

potential in the preservation of fruit products

Ana Andra Teixeira Barbosa, Hilrio Cuquetto Mantovani & Sona Jain

To cite this article: Ana Andra Teixeira Barbosa, Hilrio Cuquetto Mantovani & Sona Jain
(2017): Bacteriocins from lactic acid bacteria and their potential in the preservation of fruit
products, Critical Reviews in Biotechnology, DOI: 10.1080/07388551.2016.1262323

To link to this article: http://dx.doi.org/10.1080/07388551.2016.1262323

Published online: 03 Jan 2017.

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CRITICAL REVIEWS IN BIOTECHNOLOGY, 2016
http://dx.doi.org/10.1080/07388551.2016.1262323

REVIEW ARTICLE

Bacteriocins from lactic acid bacteria and their potential in the preservation
of fruit products
Ana Andr

ea Teixeira Barbosaa, Hil
ario Cuquetto Mantovanib and Sona Jaina
a
Departamento de Morfologia, Universidade Federal de Sergipe, S~ao Crist
ov~ao, Sergipe, Brazil; bDepartamento de Microbiologia,
Universidade Federal de Vicosa, Vicosa, Minas Gerais, Brazil

ABSTRACT ARTICLE HISTORY

Bacteriocins produced by lactic acid bacteria (LAB) are well-recognized for their potential as nat- Received 19 January 2016
ural food preservatives. These antimicrobial peptides usually do not change the sensorial proper- Revised 25 July 2016
ties of food products and can be used in combination with traditional preservation methods to Accepted 5 August 2016
ensure microbial stability. In recent years, fruit products are increasingly being associated with
food-borne pathogens and spoilage microorganisms, and bacteriocins are important candidates KEYWORDS
to preserve these products. Bacteriocins have been extensively studied to preserve foods of ani- Food preservation;
mal origin. However, little information is available for their use in vegetable products, especially microbial quality; fruit
in minimally processed ready-to-eat fruits. Although, many bacteriocins possess useful characteris- juices; minimally processed
tics that can be used to preserve fruit products, to date, only nisin, enterocin AS-48, bovicin HC5, fruits
enterocin 416K1, pediocin and bificin C6165 have been tested for their activity against spoilage
and pathogenic microorganisms in these products. Among these, only nisin and pediocin are
approved to be commercially used as food additives, and their use in fruit products is still limited
to certain countries. Considering the increasing demand for fresh-tasting fruit products and con-
cern for public safety, the study of other bacteriocins with biochemical characteristics that make
them candidates for the preservation of these products are of great interest. Efforts for their
approval as food additives are also important. In this review, we discuss why the study of bacter-
iocins as an alternative method to preserve fruit products is important; we detail the biotechno-
logical approaches for the use of bacteriocins in fruit products; and describe some bacteriocins
that have been tested and have potential to be tested for the preservation of fruit products.

Introduction intensity of traditional preservation methods, such as

Bacteriocins are ribosomally synthesized and extracellu-
larly release antimicrobial peptides produced by bac-
teria that vary in structure, biochemical properties,
mode of action and spectrum of activity [13]. The bac-
teriocins produced by lactic acid bacteria (LAB) are
more thoroughly characterized on account of their
food grade quality and industrial importance. These
peptides are mainly active against Gram-positive bac-
teria and can inhibit several food-borne spoilage and
pathogenic microorganisms. Several LAB bacteriocins
have been characterized and their potential as natural
food preservatives has been demonstrated [47].
The interest in the use of bacteriocins as an alterna-
tive food preservation method has increased with con-
sumer demand for fresh-tasting and better-preserved
chemical free food products. Bacteriocins generally do
not cause changes in food products and can be used as
an additional hurdle in food processing, reducing the
heat [1]. In this way, the increase in the consumption of
fruit products [8] and consumer demand for food prod-
ucts that maintain their natural characteristics [9] make
bacteriocins as great candidates to be used for the pres-
ervation of fruit products.
The use of bacteriocins as food additives is
widespread, however, little is known about its use in
fruit products, especially in minimally processed fruits
[4,5,10]. In the few last years, fruit products have been
increasingly associated with food-borne pathogens and
spoilage microorganisms [1116].
Although many bacteriocins have characteristics to
be used in the preservation of fruit products, to date,
only nisin [17], enterocin AS-48 [4,5], bovicin HC5 [18],
enterocin 416K1 [19], bificin C6165 [10] and pediocin
[20] have been tested against spoilage and pathogenic
microorganisms in these kinds of products. Among
these, only nisin and pediocin PA-1/AcH are approved

CONTACT Ana Andrea Teixeira Barbosa ana.barbosaufs@yahoo.com.br Departamento de Morfologia, Universidade Federal de Sergipe, S~ao
Crist

ov~ao, SE 49100-000, Brazil
2016 Informa UK Limited, trading as Taylor & Francis Group
2 A. A. T. BARBOSA ET AL.
to be used as food additives, but their approval in fruit
products is limited. Considering the increasing demand
for fresh-tasting fruit products and the safety concern,
the study of bacteriocins with biochemical characteris-
tics that make them candidates to preserve these prod-
ucts is of great interest. In this review, we elaborate the
need for the study of bacteriocins as an alternative
method in fruit preservation, discuss the biotechno-
logical approaches for the use of bacteriocins in fruit
products and describe some bacteriocins that have
been tested and have the potential to be tested.
Importance of studying LAB bacteriocins as an
alternative in fruit product preservation
The consumption of fresh foods that maintain their
organoleptic characteristics when preserved has greatly
increased over the past two decades due to the health
benefits, especially for foods of vegetal origin [8,2123].
Most fresh produce receives minimal processing and is
often eaten raw, which has led to the increase in out-
breaks of food-borne illnesses involving these products
[11,21,22,24].
Contamination of fruit products with pathogenic
bacteria may occur by fecal and soil materials from the
farm during growth and harvest, and during transport-
ing and storage [15,25]. When the fruits reach the proc-
essing industry, they may have a microbial load of
104106 cfu g
1 [11]. This external contamination could
reach the interior of the fruit during processing and be
present in the final product. The processing stages of
handling, cutting, shredding, slicing and grating are
also potential sources of contamination that contributes
to the increased microbial load [22].
During minimum processing, washing and sanitiza-
tion are the stages where removal of microorganisms is
accomplished but the effective reduction of microor-
ganisms is difficult to achieve (typically only 100-fold)
[26,27]. In addition, this non-lethal treatment reduces
normal microbiota of fruit and, consequently, can
reduce the competition for space and nutrients among
human pathogenic species [28]. Consequently, out-
breaks of food-borne disease associated with the con-
sumption of fresh and minimally processed fruits and
vegetables, primarily due to Escherichia coli O157:H7,
Salmonella spp. and Listeria monocytogenes, have
increased dramatically [27].
Unlike minimally processed fruits, some fruit prod-
ucts, such as juices and pulps, are heat treated.
Although the heat treatment increases product safety
and shelf-life, it also decreases the nutritional and sen-
sorial properties of the raw materials, but represents
a way to consume fruits outside the harvest period.
These kinds of products are also susceptible to contam-
ination due to the fruits contact with the soil, animals,
insects, or humans during growth or harvesting, reach-
ing the processing industry with a considerable micro-
bial load. During processing, spoilage and pathogenic
microorganisms can gain access to the nutrients inside
the fruit and multiply [27]. Fruit products generally have
acidic pH that, together with heat treatment, eliminates
most of the contaminating microorganisms. However,
these conditions are not sufficient to eliminate thermo
acidophilic spore-forming bacteria. Bacillus, Clostridium
and Alicyclobacillus are among the bacterial genera that
have been most studied and related to spoilage of ther-
mally-processed fruit products [6,7,14,29]. Endospores
from these bacterial groups are generally found in soil
and can contaminate many types of fruits and vegeta-
bles. Alicyclobacillus acidoterrestris has become a major
issue in the pasteurized fruit juice industry [30].
Therefore, both minimally processed fruits and fruit
products that are heat treated are susceptible to the
presence of pathogenic and spoilage microorganisms in
the final product. Many microorganisms have been iso-
lated worldwide from diverse fruit products in recent
years (Table 1). This represents economic losses and a
serious public health problem. Studies have reported
the growth of E. coli O157:H7, Salmonella and Listeria
innocua in minimally processed apple [13,43,44].
Pinheiro et al. [12] also isolated coliforms, Salmonella sp.
and molds from several minimally processed fruits.
Enterotoxigenic Staphylococcus aureus were recently
isolated from fruit salads [33]. Moreover, fresh fruit
and fruit juices have been implicated in outbreaks of
food-borne illnesses caused by human pathogens
such as E. coli O157:H7, Salmonella spp., and
L. monocytogenes [4547].
Due to the increased incidence of food outbreaks
involving fruit products contaminated with pathogenic
microorganisms, it is of most importance to study alter-
native methods to improve the safety of these products.
Bacteriocins from LAB could be used as an additional
hurdle in the preservation of fruit products to prevent
the growth of pathogenic and spoilage microorganisms.
Studies are showing that these antibacterial substances
are effective both in minimally processed fruits and
thermally-processed fruit products, as will be discussed
in the next sections of this review. Many studies have
shown that bacteriocins inhibit vegetative growth and
spore germination and also reduce the thermal resist-
ance of bacterial endospores [6,18,48]. In addition, bac-
teriocins are well-known not to cause changes in
nutritional and sensorial properties of foods.
Settanni and Corsetti [49] raised the importance of
bacteriocins from LAB to promote the microbial safety
 CRITICAL REVIEWS IN BIOTECHNOLOGY 3

Table 1. Incidence of microorganisms in fruit products in diverse countries.

Fruit product Microorganisms Country Reference
Unpasteurized fruit juice Escherichia coli Colombia [31]
Fruits Listeria monocytogenes Greece [32]
Fruit salads Staphylococcus aureus Argentina [33]
Mango and passion fruit pulps Listeria monocytogenes Costa Rica [34]
Orange juices Salmonella spp. Spain [35]
Staphylococcus aureus
Fruit juices Escherichia coli O157:H7 Greece [36]
Staphylococcus aureus
Fresh Escherichia coli O157:H United States [37]
Strawberries
Juices Alicyclobacillus spp. United States [38]
High-moisture dried fruits Bacillus spp.; Staphylococcus spp.; Salmonella spp. South Africa [39]
Mango juice and concentrate Alicyclobacillus acidocaldarius South Africa [29]
Melon, bean sprouts Listeria monocytogenes United Kingdom [40]
Escherichia coli
Strawberries Listeria monocytogenes Norway [41]
Staphylococcus spp.
Orange juice Salmonella serotype Muenchen Canada [42]
United States

of vegetable food products. This paper states that bac-
teriocins could be used in this kind of products by using
pure bacteriocins as food additives or by the use of bac-
teriocinogenic strains as starter cultures, protective cul-
tures or co-cultures. Bacteriocins can ensure
microbiological safety and also contribute to maintain
the nutritional properties of fruits. Results have previ-
ously shown that nisin, apart from its antibacterial activ-
ity, also contributes to preserve the vitamin C content
of minimally processed mangoes and fruit juices [48,50].
Biotechnological approaches for the use of
bacteriocins in fruit products
Bacteriocins can be added directly to the fruit products
in purified or semi purified form for their preservation.
Alternatively, these antimicrobial peptides could be pro-
duced in situ by probiotic cultures, or be incorporated
into the surface of the fruit as an edible coating or in
the matrix of plastic films used for packaging [4853].
Some studies have shown the potential of semi or
purified forms of the bacteriocins to preserve fruit juices
and pulps by direct addition [6,7,10,18,50]. These prod-
ucts are generally thermally-processed, therefore, it is
important that the bacteriocins are heat-stable.
The use of bacteriocins to ensure the safety of fresh
or minimally processed fruits or vegetables is receiving
great attention, even though their commercial applica-
tion has not been fully exploited [3,20,48,54]. One
approach to use bacteriocins in the conservation of
minimally processed fruits is by incorporating these
peptides in the packaging material [48]. This is known
as active packaging which, besides protecting the prod-
uct from external environment, inhibits microbial
growth, minimizing direct addition of preservatives. It
also satisfies the demand for healthier foods as it con-
tains fewer additives [55].
Bacteriocin-incorporated films avoid the risks of
negative interaction with the food components and can
provide longer preservation compared with the conven-
tional addition directly into the food [51]. This is a
promising technology, as the majority of solid or semi-
solid foods present high microbial growth on their sur-
face [56]. However, the information available on the use
of active packaging containing bacteriocins for the pres-
ervation of minimally processed fruits is still limited
[48].
Edible coatings added with bacteriocins could also
be a great alternative to preserve minimally processed
fruits. Thin layers of biopolymers (carbohydrate, lipid or
protein) applied directly on the surface of whole or min-
imally processed fruit, prevent water loss and reduce
respiration rates [57] and can be conveniently used as
carriers of bioactive ingredients, such as bacteriocins, to
prolong shelf-life [20].
Biocontrol using LAB can also be a good alternative
for some products [16], but the use of LAB can also
compromise the product quality, as these LAB can fer-
ment or acidify vegetable substrates altering their desir-
able characteristics [24].
LAB bacteriocins with potential in the
preservation of fruit products
This section describes the bacteriocins that have been
tested for the preservation of fruit products (Table 2)
and also lists some that have the potential to be used
in the preservation of these products (Table 3). The sec-
tion is subdivided into individual bacteriocin tested,
where the studies showing effectiveness and the way
4 A. A. T. BARBOSA ET AL.

Table 2. Bacteriocins that have been tested in the preservation of fruit products.
Bacteriocin Class Producer strain Antimicrobial activitya Applied product References
Bificin C6165 I Bifidobacterium animalis subsp. Alicyclobacillus acidoterrestris Fruit juices [58]
animalis CICC 6165
Bovicin HC5 I Streptococcus bovis HC5 A. acidoterrestris, Bacillus cereus, Mango pulp [6,7]
Clostridium tyrobutyricum
Enterocin AS48 II Enterococcus faecalis AS48 acidoterrestris Fruit juices, Raw fruits [5961]
Enterocin 416K1 II Enterococcus casseliflavus IM 416K1 Listeria monocytogenes Ready to eat fruits [19]
Nisin I Lactococcus lactis sup lactis A. acidoterrestris Fruit juices, Mango pulp, [6,7,17,48];
Minimally processed mangoes [83]
Pediocin II Pediococcus pentosaceus Mesophilic bacteria and fungi Minimally processed papaya [20]
a
Antimicrobial activity against spoilage or pathogenic microorganisms in fruit products.

Table 3. Bacteriocins that have potential to be used in the preservation of fruit products.a
Bacteriocin Class Producer strain Producer strain isolated from: References
Bacteriocin EF2019 II Enterococcus faecium Rabbits feces [62]
BacPPK34 Pediococcus pentosaceus strain K34 Alheira [63]
Bacteriocin BacJ1 Weissella paramesenteroides J1 Chicken gizzard [64]
Bacteriocin KU24 Lactococcus lactis KU24 Kimchi [65]
Bacteriocin ST16Pa Lactobacillus plantarum ST16Pa Papaya [66]
Bacteriocin ST5Ha II Enterococcus faecium Smoked salmon [67]
Bovicin HJ50 I Streptococcus bovis HJ50 Raw milk [68]
Enterocin A5-11 II Enterococcus durans Mongolian airag [69]
Gassericin A V Lactobacillus gasseri LA39 Feces of a 4-month-old male infant [70]
Lacticin LC14 I Lactococcus lactis BMG6.14 Tunisian white cheese [71]
Lactocin 705 II Lactobacillus curvatus CRL705 Dry fermented sausages. [7274]
Pentocin TV35b Lactobacillus pentosus Vaginal secretions [75]
Plantaricin ASM1 I Lactobacillus plantarum A-1 Tortilla [76]
Salivaricin 9 I Streptococcus salivarius NU10 Oral microbiota of humans [77]
Sakacin LSJ618 II Lactobacillus sakei LSJ618 Fermented radish [78]
Suicin 3908 I Streptococcus suis Healthy carrier pig [79]
Thermophilin 1277 I Streptococcus thermophyllus BT1277 Raw milk [80]
a
Bacteriocins that have activity at acidic pH and are thermostable.
() Not determined.

bacteriocins have been tested are described.
These include a bacteriocin not yet tested but with the
potential to be used for fruit products and a biocontrol
using LAB to preserve fruit products.
Nisin
Nisin is the most studied and best characterized bacteri-
ocin for the preservation of fruit products. It is a class I
bacteriocin produced by strains of Lactococcus lactis
subspecies lactic and consists of a 34-residue peptide.
Nisin has been approved to be used in foods since 1988
by the US Food and Drug Agency (FDA) [2]. It has been
used in processed cheeses, dairy products and canned
foods [81], but its approval in fruit products is limited to
certain countries. This bacteriocin is thermostable and
its activity is increased at acidic pH [82]. Nisin is active
against S. aureus, L. monocytogenes, A. acidoterrestris,
Clostridium and Bacillus spores and even inhibits some
Gram-negative bacteria [1,48,83].
Nisin has been tested alone and in combination with
thermal and non-thermal technologies in the preserva-
tion of fruit products such as juices, pulps and minim-
ally processed fruits. Nearly two decades of studies
have shown the effectiveness of this bacteriocin for the
preservation of fruit products.
This bacteriocin inhibited vegetative growth and
spore outgrowth of A. acidoterrestris in apple, grape and
orange juices [17,84]. Komitopoulou et al. [17] showed
that addition of nisin in fruit juices (100 AU/ml) inhibited
A. acidoterrestris under all temperatures and time of
storage conditions. Nisin decreased the decimal reduc-
tion time up to 40% and its minimal inhibition concen-
tration against A. acidoterrestris spores was only 5 AU/ml
at 25  C [83]. Also showed that nisin decreased the
D90 C value of spores from this microorganism by 75%.
Pathanibul et al. [85] showed that nisin, in combin-
ation with high-pressure homogenization, helped in the
control of E. coli and L. innocua in apple and carrot jui-
ces. Saldan~ a et al. [86] also demonstrated that the appli-
cation of pulsed electric fields at moderate
temperatures in the presence of nisin has the potential
to control the growth of S. aureus and L. monocytogenes
in fruit juices. Earlier, nisin has also shown bactericidal
activity against strains of Bacillus cereus, Bacillus thurin-
giensis [6] and Clostridium tyrobutyricum in acidic mango
pulp [7].
In 2013, Yu et al. [87] tested the effect of dimethyl
dicarbonate (DMDC), nisin and mild heat on the

inactivation of indigenous microorganisms (bacteria,
molds and yeasts) in litchi juice. The authors confirmed
that addition of nisin can enhance the inactivation of
bacteria by DMDC, and that nisin and DMDC work in
synergism to inactivate the bacteria. No microorganisms
were detected in the litchi juice added with 200 IU/mL
nisin as compared with the addition of 250 mg/L of
DMDC at 45  C for 3 h. Functional drinks based on fruit
and vegetable juices were stabilized at room tempera-
ture for 90 days by the use of nisin and low pH circum-
venting the need for any chemical preservatives [88].
More recently, our results have shown that nisin
remained stable in cashew, soursop, peach, passion
fruit, orange, guava, and cupuassu juices for at least
30 days at room temperature (26  C) or at 4  C and did
not cause any negative effect on the physico-chemical
properties of fruit juices [50]. Besides, nisin favored the
preservation of vitamin C content in juices. Nisin was
also efficient in controlling L. monocytogenes, A. acido-
terrestris, B. cereus and S. aureus in cashew, soursop,
peach and mango juices [50].
Beside fruit juice and pulps, nisin has also shown
potential to preserve minimally processed fruits [89].
Showed the effectiveness of chlorine and nisinEDTA
treatments on whole melons and freshly cut pieces in
reducing native micro flora and the same authors in
2004 described the combined effect of nisin, EDTA,
sodium lactate and potassium sorbate in reducing
Salmonella from fresh-cut cantaloupe [90]. Ukuku et al.
[91] also indicated that the use of hydrogen peroxide in
combination with nisin, sodium lactate and citric acid
was effective to reduce the transfer of bacterial patho-
gens from whole melon surfaces to fresh-cut pieces.
In a more recent study, we also tested the effect of
nisin-incorporated films on the control of L. monocyto-
genes and S. aureus in minimally processed mangoes
[48]. Our results showed that the viable cell number of
these food-borne pathogens was reduced during the
storage time when samples were packed with anti-
microbial films. The physico-chemical quality of minim-
ally processed mangoes was not affected by the
bacteriocin and the antibacterial activity of nisin-
incorporated films remained stable for at least 70 days
[48].
Bovicin HC5
Bovicin HC5 is a bacteriocin produced by strains of
Streptococcus bovis HC5, a rapidly growing Gram-
positive ruminal bacterium that has few nutritional
requirements [92]. Bovicin HC5 has a molecular mass of
2440 Da and its amino acid sequence shows structural
similarities with the lantibiotics [92,93]. Although this
CRITICAL REVIEWS IN BIOTECHNOLOGY 5
bacteriocin is not currently approved for commercial
use, studies suggest that it can be produced at lower
costs compared with other bacteriocins produced by
LAB [94,95].
The histological and immunostimulatory effects of
bovicin HC5 in animal models showed minor effects on
intestinal permeability and did not elicit an allergenic
response [96]. When this bacteriocin was tested against
mammalian cells, cytotoxic effects were observed only
at concentrations that were higher than the concentra-
tion needed for its biological activity [97]. These results
suggest that bovicin HC5 could be safely used as a food
preservative.
Bovicin HC5 exhibits stability at high temperatures
and acidic pH and has inhibitory activity against
several strains of food-borne pathogens and spoilage
microorganisms, including L. monocytogenes,
Clostridium tyrobutyricum, B. cereus, B. thuringiensis
and A. acidoterrestris. It also inhibits strains of LAB,
such as Streptococcus, Lactococcus, Enterococcus and
Lactobacillus [6,7,18,92,98]. A patent solicitation (num-
ber PI1001695-3A2) for the use of this bacteriocin in the
preservation of fruit juices was deposited by this
laboratory.
This bacteriocin showed effectiveness in preserving
fruit juices and pulps. Carvalho et al. [6,7] demonstrated
that bovicin HC5 was bactericidal against B. cereus,
B. thuringiensis and C. tyrobutyricum and reduced the
outgrowth of endospores from Bacillus strains in acidic
mango pulp. These latter results indicated that bovicin
HC5 was as effective as nisin to control Bacillus and
Clostridium strains in mango pulp. When bovicin HC5
was tested in mango pulp against A. acidoterrestris, the
bacteriocin showed bactericidal effect against vegeta-
tive cells and sporicidal activity [18]. The D-values of
A. acidoterrestris spores that had been heat treated in
acidic mango pulp decreased more than 90% in the
presence of bovicin HC5, compared with untreated con-
trols [18].
Enterocin as-48
Enterocin AS-48 is a 70-residue cyclic peptide produced
by Enterococcus faecalis subsp. liquefaciens S-48, and
consists of a globular arrangement of five a-helices
enclosing a compact hydrophobic core [99]. This bac-
teriocin is the first enterocin which was purified to
homogeneity and characterized [100]. Enterocin AS-48
shows a broad antimicrobial spectrum against both
Gram-positive and Gram-negative bacteria and is also
stable at high temperatures and active at acidic pH [99].
This bacteriocin is not currently approved for com-
mercial use. However, preliminary studies indicate that
6 A. A. T. BARBOSA ET AL.
it could be safe for use. The bacteriocin concentration
necessary to induce partial morphological changes in a
Vero cell line was higher than the inhibitory concentra-
tions required for most bacteria. Besides, eukaryotic
cells are resistant to this bacteriocin and enterocin AS-
48 can be degraded by proteases from the intestinal
tract (trypsin, pepsin), decreasing its possible impact on
gut microbiota [101,102]. Many studies have shown that
enterocin AS-48 is a safe, natural antimicrobial that
offers a good alternative to conventional preservatives
to prevent the risk of food-borne outbreaks [102,101].
In addition, the efficacy of enterocin AS-48 in food sys-
tems increases greatly in combination with chemical
preservatives, essential oils, phenolic compounds and
physico-chemical treatments such as sublethal heat,
high-intensity pulsed-electric fields or high hydrostatic
pressure [102].
Spoilage and pathogenic microorganisms related to
fruit products, such as S. aureus, L. monocytogenes,
B. cereus and Alicyclobacillus sp., were efficiently inhib-
ited by enterocin AS-48 [4,5,59,103106]. Because of its
stability and broad antimicrobial spectrum, this bacteri-
ocin is a good candidate to be a natural food preserva-
tive and has shown satisfactory results in fruit juices
[60]. Studies have shown that enterocin AS-48 can be
produced using inexpensive food by-products such as
whey permeate, which opens the way for industrial-
scale production of bacteriocin preparations [107].
Enterocin AS-48 was tested in canned pineapple
juice, apple cider and several fruit juices. Grande et al.
[4] showed that this bacteriocin remained stable for at
least 30 days in apple, grapefruit, kiwi, orange, pear and
pineapple and mixed juices. The results obtained by
these researchers also indicated compatibility of the
bacteriocin with food-grade dyes and thickening
agents, making it suitable for food bioprotection [4].
The bacteriocin was found to be bactericidal against
Bacillus coagulans in canned pineapple juice and its
combined use with heat (8095  C for 5 min) signifi-
cantly increased the effect of thermal treatments on B.
coagulans spores [59]. Grande et al. [60] also showed
that enterocin AS-48 inhibited the growth of ropy-form-
ing Bacillus licheniformis and reduced the time required
to achieve complete heat inactivation of intact spores
in apple cider.
The bactericidal and sporicidal activity of enterocin
AS-48 was demonstrated against A. acidoterrestris in
several fruit juices by Grande et al. [5]. These authors
showed that the vegetative cells of this microorganism
were inactivated by this bacteriocin in natural orange
and apple juices for at least 15 days. Commercial
orange, apple, pineapple, peach and grapefruit juices
were added with enterocin, and inoculated with
vegetative cells or endospores from A. acidoterrestris
and incubated at different incubation temperatures (4,
15 and 37  C) for three months. No viable cells were
observed during the incubation period, except for
apple, peach and grape fruit juices at 37  C containing
vegetative cells which, however, were stable for up to
60 days. Electron microscopy analysis showed that
enterocin AS-48 caused cell damage and bacterial lysis
and disorganization of endospore structure from
A. acidoterrestris in all fruit juices.
Molinos et al. [61] also showed that this bacteriocin
could serve as an additional hurdle against L. monocyto-
genes in raw fruits and fruit juices. Enterocin AS-48 was
also effective to control Salmonella enterica in apple
juice in combination with high-intensity pulsed-electric
field [105]. The authors concluded that these combined
treatments could improve the safety of freshly-made
apple juice against S. enterica. This bacteriocin in com-
bination with high-intensity pulsed-electric field also
proved to be useful for inactivation of exopolysacchar-
ide-producing spoilage microorganisms in apple juice
[106,108].
Recently, P
erez Pulido et al. [109] tested the effect of
enterocin AS-48 in combination with high hydrostatic
pressure to control bacterial communities in cherimoya
pulp. They tested the treatments alone and in combin-
ation and concluded that the combined treatment was
the most effective, keeping bacterial cell densities at
1.5 log CFU/g for up to 15 days.
Enterocin 416K1
Enterocin 416K1 is a 5 kDa bacteriocin produced by
strains of Enterococcus casseliflavus IM 416K1 isolated
from Italian sausages. This bacteriocin is stable upon
heating at 90  C for 120 min and storage at 4  C for 6
months, and has demonstrated strong anti-listerial
activity [110]. Studies have shown that this bacteriocin
has potential to be used in food preservation by direct
inoculums or entrapped in an organicinorganic hybrid
coating applied to an LDPE (low density polyethylene)
film used in active food packaging [111,112,19].
Anacarso et al. [19] investigated the anti-listerial
activity of chitosan and Enterocin 416K1 alone or in
association with artificially contaminated L. monocyto-
genes NCTC 10888 ready-to-eat vegetables and fruit.
Their results showed that in apples and grapes, Listeria
viable count in the controls decreased to about 2 log
cfu g
1 within 24 h and remained unchanged until the
end of the experiment. In treated samples, complete
inhibition of Listeria spp. was obtained in the first hour
when chitosan and enterocin were used together, in
the 8 h for enterocin alone samples and in the 72 h for

chitosan alone samples. The authors concluded that the
use of chitosan and enterocin 416K1, alone or in com-
bination, could be a feasible solution to extend the
shelf-life and to obtain the microbiological safety of
ready-to-eat vegetable and fruits [19].
Bificin C6165
Bificin C6165 is produced by strains of Bifidobacterium
animalis subsp. animalis CICC 6165 and has shown
higher activity at acidic pH and elevated temperatures.
These are important characteristics for a bacteriocin to
be used in the preservation of fruit products [10,58].
Bificin C6165 showed antimicrobial activity against sev-
eral strains of A. acidoterrestris, LAB strains and Gram-
positive bacteria including S. aureus and Enterococcus
faecium [58]. Toxicological data about this bacteriocin
are not yet available, but studies with bificin C6165
have been carried out to analyze if this bacteriocin is
safe to be used in food preservation [10,58].
Bificin C6165 was tested against sixteen strains of
A. acidoterrestris in apple juices and showed bactericidal
activity that was better at lower pH (pH 3.5) and at a
higher temperature of 45  C [10]. This bacteriocin also
contributed in the reduction of the thermal resistance
of spores from this microorganism, causing a reduction
of up to 40% [10]. Electron microscopy examination of
the vegetative cells treated with bificin revealed cell
damage and bacterial lysis [10].
Considering their results and the fact that bificin is
relatively heat-stable at acidic pH, Pei et al. [10] indi-
cated a strategy to control A. acidoterrestris in acidic
drinks with the addition of bificin C6165. Bificin could
be added in the juices prior to heat treatment increas-
ing the heat sensitivity of microorganisms and thereby
increasing the lethality of pasteurization [10]. Bificin
could also be tested to be used in edible coating or in
the matrix of plastic films used for packaging minimally
processed fruits.
Pediocin
The antibacterial peptide pediocin is a class II anti-liste-
rial polypeptide that has 44 amino acid residues and, as
with nisin, is commercially available to be used in food
preservation [2,113]. This bacteriocin has stability over a
wide pH range (39) and heat-processing temperatures
(65121  C) [113]. Pediocin exhibits antibacterial activity
against a wide spectrum of food-borne pathogens and
food spoilage Gram-positive bacteria [114]. This bacteri-
ocin has been extensively studied for its use in food
preservation, mainly for foods of animal origin
CRITICAL REVIEWS IN BIOTECHNOLOGY 7
[114116], but recent results show that pediocin can
also be used for fruit products [20].
Recently, Narsaiah et al. [20] reported on the effects
of alginate coatings incorporated with pediocin in pres-
ervation of minimally processed papaya. Their results
showed that alginate (2% (w/w)), added with pediocin,
could be used to store minimally processed papaya
for 3 weeks without compromising physico-chemical
qualities or microbial safety.
Several studies are showing the potential of pediocin
incorporated in antimicrobial films to package foods
from animal origin [56,117,118]. Pediocin could also be
used to produce antimicrobial films to package minim-
ally processed fruits. This strategy could be employed
to improve the effectiveness of pediocin, as studies
have shown that the direct addition of pediocin in food
is effective only for a limited time duration [113].
When pediocin is incorporated in films, the release of
the bacteriocin in the food is controlled or slow, which
prolongs its effectiveness.
Other bacteriocins
In addition to the above-mentioned bacteriocins, many
other LAB bacteriocins have characteristics that make
them ideal candidates for the preservation of fruit-
based products (Table 3). Bacteriocins that are thermo-
stable, active at acidic pH and potential candidates
for preservation of these products. Some examples of
bacteriocins with these characteristics are pentocin
TV35b [75], enterocin A5-11 [69], bacteriocin EF2019
[62], bacteriocins produced by strains of Pediococcus
and Lactococcus from the human intestine [119]. Apart
from heat stability and activity at acidic pH, these bac-
teriocins have also to be tested for stability in the pres-
ence of fruit products. The fruits have proteolytic
enzymes that can eliminate the biological activity of
bacteriocins.
Bacteriocin BacJ1, produced by strains of Weissella
paramesenteroides J1 isolated from the chicken gizzard,
has a molecular mass of 1881.036 Da and is promising
for the prevention of contamination and growth of
pathogenic bacteria, particularly S. typhimurium [64].
This bacteriocin also demonstrated stability at acidic pH
(2.0) and high temperatures (121  C/15 min) [64].
Lactocin 705 incorporated in bioactive films has
shown promising results, enhancing quality and food
safety [73,74]. This is a class IIb bacteriocin produced by
strains of Lactobacillus curvatus CRL705 isolated from
dry fermented sausages. Its activity depends upon the
complementation of two peptides with 33 amino acid
residues each [120,73]. This bacteriocin has shown
effective results in the preservation of meat products
8 A. A. T. BARBOSA ET AL.
and could also be tested for the preservation of minim-
ally processed fruits by incorporating it into films used
for product packaging. As lactocin is stable at high tem-
peratures [72], it could also be used in the preservation
of fruit juices and canned fruit products that are heat
treated.
Bacteriocin ST16Pa produced by strains of
Lactobacillus plantarum ST16Pa isolated from papaya,
remained active after incubation for 2 h at pHs ranging
from 2.0 to 12.0 and no decrease in its activity was
recorded after heat treatment at 121  C for 20 min
[67,66]. This bacteriocin has shown antimicrobial activity
against several food-borne pathogens and spoilage
microorganisms, including L. monocytogenes and S. aur-
eus. The bacteriocin could be tested to be directly
added in fruit products or, considering that this strain
was isolated from papaya and studies are showing its
potential probiotic characteristics [67,66,121], it could
be potentially used as a probiotic bacteriocin producing
strain to ensure microbial quality of some fruit products
that are fermented.
A great number of potential LAB strains were iso-
lated from various fresh and fermented fruits and they
could also produce bacteriocins that could have appli-
cation in food preservation [53,122126]. Considering
that the natural environment of these strains is fruit, the
bacteriocin produced could be useful in the preserva-
tion of fruit products [53,122]. Trias et al. [122] isolated
bacteriocinogenic Leuconostoc mesenteroides strains
from fresh fruits. The bacteriocins produced by some
strains showed high resistance of their antibacterial
activity to temperature and pH, and also bactericidal
activity against L. monocytogenes [122]. Recently,
Liao et al. [53] also isolated strains of L. mesenteroides,
P. pentosaceus and Lactobacillus brevis from mango.
Not all bacteriocins that have the potential for use in
fruit product preservation are mentioned here because
it is not possible to describe all of them in one single
review paper. Our intention here was to show that it is
necessary to find and utilize alternative ways to conven-
tional methods in the preservation of fruit products and
that bacteriocins are excellent choices. In addition, as
reported, a number of options are available when it
comes to choosing a bacteriocin.
Biocontrol using LAB
Besides the purified peptide, bacteriocins could also
preserve some fruit products by being produced in situ
by the producer strain as was demonstrated by Siroli
et al. [16]. These authors showed that Lactobacillus
plantarum strains increased both the safety and shelf-
life of minimally processed apples. The combination of
the selected strains with natural antimicrobials pro-
duced a further increase in the shelf-life of these prod-
ucts without detrimental effects on their organoleptic
properties [16]. L. plantarum strains are known to pro-
duce bacteriocins [127,128] and this could be respon-
sible for preserving the minimally processed apples
described above.
Russo et al. [125] tested fresh-cut pineapple as a car-
rier of probiotic LAB. These authors showed that the
L. plantarum and L. fermentum population on pineap-
ples pieces ranged between 7.3 and 6.3 log cfu g
1,
respectively, without affecting the final quality of the
fruit. Besides, these strains were able to inhibit patho-
genic microorganisms such as L. monocytogenes. Trias
et al. [122] analyzed the effect of LAB on the control of
L. monocytogenes in wounds of Golden Delicious apples
and concluded that the bacteriocinogenic strain offers
potential application for the prevention of L. monocyto-
genes in fresh fruit and vegetables.
Liao et al. [53] isolated strains of L. mesenteroides,
P. pentosaceus and L. brevis from mango and used these
strains as starter culture in fermented mango juice.
Harima-Mizusawa et al. [129] also used strains of L. plan-
tarum as a probiotic and starter culture in fermented
citrus juice. As stated by Di Cagno et al. [124] and by
Swain et al. [130], lactic acid fermentation is expected
to become an important tool in preserving fresh vege-
tables, fruits and other food items. Fermentation,
besides increasing the shelf-life of fruits and vegetables,
enhances nutritive value and flavors, reduces toxicity,
and the fermented product can be used as a potential
source of probiotics as they harbor several LAB [130]. In
addition to lactic acid, these strains also produce several
bacteriocins that also contribute to the microbial stabil-
ity of the fermented product.
Concluding remarks
Currently, one of the major challenges of the food
industry is to satisfy consumers demand for better pre-
served and fresh-tasting foods, and this scenario is par-
ticularly relevant in fruit processing industries [22,131].
This review shows the potential of some LAB bacterio-
cins to ensure the safety of fruit products. These pepti-
des are demonstrating antimicrobial activity against
several spoilage and pathogenic microorganisms
related to these products. Studies have also shown that
bacteriocin exerts their antimicrobial activity without
changing the organoleptic and/or sensorial characteris-
tics of fruit [48,50].
To date, only five antimicrobial peptides have been
tested in fruit products, among these, only nisin and
pediocin are approved for use in foods, but their

approval in fruit products is still limited [2,132]. Nisin is
available in its commercial form as: NisaplinV, NovasinTM
R
(Gillco) and Chrisin CV (CHR Hansen), among others and
R
pediocin PA-1/AcH as ALTA 2341. However, the legisla-
tion of many countries does not currently permit the
use of purified bacteriocins other than nisin.
Considering the fact that some food-borne patho-
genic and spoilage microorganisms are not sensitive to
nisin, the purification and characterization of novel bac-
teriocins are of great relevance in order to develop
novel products and applications [133]. The use of puri-
fied or semi purified preparations of bacteriocins as
food preservatives have legal implications. In order to
be approved for commercial and industrial applications,
studies must be performed to provide detailed safety
information supported by toxicological data.
Additionally, proof of efficacy in foods, description of
manufacturing process, as well as the safety levels
should be investigated [1,3]. Many research groups are
dedicated to solve these aspects and in a few decades
one can envision that other bacteriocins will be
approved for commercial use, especially in the preserva-
tion of fruit products, following the expansion of its
market worldwide.
Acknowledgements
The authors would like to thank the Conselho de
Desenvolvimento Cient
fico e Tecnolo
gico (CNPq), Bras
lia,
Brazil, the Fundac~ao de Apoio a Pesquisa e a inovac~ao
Tecnolo
gica do Estado de Sergipe (FAPITEC), Sergipe, Brazil,
for providing fellowships and financial support which sup-
ports the research with bacteriocins in our laboratory.
Disclosure statement
The authors report no conflict of interest.
Funding
The authors would like to thank the Conselho de
Desenvolvimento Cient
fico e Tecnolo
gico (CNPq), Bras
lia,
Brazil, the Fundac~ao de Apoio a Pesquisa e a inovac~ao
Tecnolo
gica do Estado de Sergipe (FAPITEC), Sergipe, Brazil,
for providing fellowships and financial support which sup-
ports the research with bacteriocins in our laboratory.
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