Probiotics & Antimicro. Prot.
DOI 10.1007/s12602-017-9330-6
Bacteriocinogenic LAB Strains for Fermented Meat Preservation:
Perspectives, Challenges, and Limitations
Lorenzo Favaro 1 & Svetoslav Dimitrov Todorov 2
# Springer Science+Business Media, LLC 2017
Abstract Over the last decades, much research has focused
on lactic acid bacteria (LAB) bacteriocins because of their
potential as biopreservatives and their action against the
growth of spoilage microbes. Meat and fermented meat prod-
ucts are prone to microbial contamination, causing health
risks, as well as economic losses in the meat industry. The
use of bacteriocin-producing LAB starter or protective cul-
tures is suitable for fermented meats. However, although bac-
teriocins can be produced during meat processing, their levels
are usually much lower than those achieved during in vitro
fermentations under optimal environmental conditions. Thus,
the direct addition of a bacteriocin food additive would be
desirable. Moreover, safety and technological characteristics
of the bacteriocinogenic LAB must be considered before their
widespread applications. This review describes the perspec-
tives and challenges toward the complete disclosure of new
bacteriocins as effective preservatives in the production of
safe and Bhealthy^ fermented meat products.
Keywords Lactic acid bacteria . Bacteriocins . Meat .
Preservation . Spoilage
* Lorenzo Favaro
lorenzo.favaro@unipd.it
1
Department of Agronomy Food Natural Resources Animals and
Environment (DAFNAE), University of Padova, Agripolis, Viale
dell’Università 16, 35020 Legnaro, PD, Italy
2
Food Research Center (FoRC), Department of Food and
Experimental Nutrition, Faculty of Pharmaceutical Sciences,
University of São Paulo, 580, Professor Lineu Prestes, 13B, Sao
Paulo, SP 05508-000, Brazil
Introduction
Microbial contaminations often contribute to serious safety
problems and quality defects in meat production. Meat has
appropriate contents of water, proteins, and essential nutri-
ents with favorable pH to support the growth of bacteria,
molds, yeast, and viruses. Safety and quality issues in the
meat industry frequently occur due to microbial prolifera-
tions [1, 2]. The main spoilage bacteria in meat include the
g e n e r a A c i n e t o b a c t e r, B ro c h o t h r i x , M o r a x e l l a ,
Enterobacter, Lactobacillus, Leuconostoc, Proteus, and
Pseudomonas. Moreover, meat contamination by patho-
genic microorganisms could be dangerous. It is the case
of Bacillus cereus, Campylobacter jejuni, Clostridium
botulinum, Clostridium perfringens, Escherichia coli,
Listeria monocytogenes, Salmonella spp., Staphylococcus
aureus, and Yersinia enterocolitica [1, 3]. Propagation of
spoilage organisms qualitatively changes texture and sen-
sory properties of meat and fermented meat products.
However, meat spoilage microbes usually do not affect
public safety, except through typical gastrointestinal disor-
ders [4]. On the contrary, pathogens could cause illness or
even death in humans. Many disease outbreaks are occur-
ring annually because of harmful microbes contaminating
fermented meat products. For instance, the presence of
entero-hemorrhagic E. coli O157:H7 in beef, veal, and bi-
son products resulted in recent foodborne disease out-
breaks in the USA. Eleven infected persons were reported
in five states and seven were hospitalized. One person de-
veloped hemolytic uremic syndrome, a type of kidney fail-
ure, but no deaths were reported. The same consequences
with high volumes of product recalls due to Li.
monocytogenes and Salmonella spp. in pork, chicken, and
beef have recently been recorded (Center of Disease
Control and Prevention, http://www.cdc.gov/).

To avoid both spoilage and pathogenic microbes in meat
processing, specific physical and chemical technologies have
been adopted [5, 6]. The use of natural antimicrobial agents
has received much attention [7]. Although they can be detect-
ed elsewhere, antimicrobial proteins of bacterial origin, com-
monly referred as bacteriocins, have become the focus of
many food research groups. Bacteriocins from lactic acid bac-
teria (LAB) have attracted much attention from various indus-
tries due to their potential applications as biopreservatives [8,
9]. Moreover, they are a new trend in food packaging, as they
can be incorporated into the extruder when the antimicrobial
film or co-extruded film is produced [10]. The Bgenerally
regarded as safe^ (GRAS) distinction of LAB and their by-
products given by the U.S. Food and Drug Administration
(FDA) emphasized the applicability of bacteriocins as safe
food preservatives [11]. Nevertheless, despite the great efforts
applied so far, only few bacteriocin preparations (mainly
nisin) reached the market to be used in the processing of meat
commodities [7]. Moreover, although extensively utilized in
meat preservation, nisin clearly demonstrated low applicabil-
ity in meat matrices compared to dairy products [12]. This
calls for additional research activities tailored to search for
novel bacteriocins and/or bacteriocin LAB producers to be
efficiently used in fermented meat products. This review over-
views the latest outcomes on LAB-secreting bacteriocins with
promise in terms of meat processing applications, focusing
mostly on fermented meat products. Moreover, limitations
and challenges will be discussed and included. The final aim
is to give for the first time a clear picture of the traits (i.e.,
antimicrobial activity, safety, and cytotoxicity) that should be
considered to select and further improve bacteriocins and/or
bacteriocin producers with great potential in biopreservation
of fermented meat products.
Brief Overview on Bacteriocins
In microbial ecosystems, some microorganisms produce anti-
microbial compounds, such as bacteriocins, that limit the
growth of other microbes. It has been proposed that more than
half to almost all bacterial species produce bacteriocins [13,
14]. They belong to a huge family of ribosomally synthesized
peptides that usually show antimicrobial activity to strains that
are closely related to the producer strain (narrow-spectrum
activity) and sometimes to strains across genera (broad-
spectrum activity) [15].
Although bacteriocins can be believed as antibiotics, they
diverge from conventional antibiotics in numerous features
[16]. Bacteriocins are inherently tolerant to higher thermal
levels and are more active at a wider pH range than traditional
antibiotics. The development of resistant microbial strains
among their target bacteria is improbable since bacteriocins
ensure fast-acting antimicrobial mechanisms that are highly
Probiotics & Antimicro. Prot.
effective even at very low concentrations. Moreover, their
proteinaceous nature minimizes resistance development as
they are easily degraded by proteases, thus lowering the
chances of target strains developing any resistance machinery.
Finally, the most promising advantage of bacteriocins over
conventional antibiotics is their primary metabolite nature that
renders them easily suitable for bioengineering to increase
their bioactivity against selected pathogens [17].
With the discovery of new bacteriocins having unique
traits, it has become evident that they are a very assorted and
heterogeneous group of compounds. Over the years, many
classification schemes of LAB bacteriocins have been sug-
gested [13, 18–22]. The classification outlined by Cotter and
colleagues is the most extensively recognized, limiting the
grouping in just two classes: the lantibiotics (class I) and
nonlantibiotics-containing bacteriocins (class II) [13]. The
most notable change in this new scheme is the recommended
exclusion of class III bacteriocins and renaming them as
bacteriolysins since they are lytic enzymes rather than pep-
tides. A further class for circular bacteriocins has been pro-
posed [20].
Class I bacteriocins are small peptides (< 5 kDa) with un-
usual posttranslationally modified amino acid residues such as
lanthionine or 3-methyllanthionine [23]. These rare residues
form covalent bridges between amino acids resulting in the
formation of an internal Bring^ or cyclic structure which gives
stability to the whole molecule. Nisin A, the first reported and
most comprehensively studied bacteriocin, belongs to this
class. Class II bacteriocins are the most abundant. They are
relatively small (< 10 kDa), heat-stable, nonlanthionine-
containing peptides, which, unlike lantibiotics, do not undergo
extensive posttranslational modification. This group was fur-
ther divided into four subclasses: Bpediocin-like^ bacteriocins
(class IIa); two-peptide bacteriocins (class IIb); circular bacte-
riocins (class IIc); and unmodified, linear, nonpediocin-like
bacteriocins (class IId).
Class IIa bacteriocins are distinguished by a conserved se-
quence in the N-terminal region (YGNGV) providing these
group a very strong inhibitory activity against Li.
monocytogenes [24]. This group is called pediocin-like be-
cause pediocin PA-1/AcH (both bacteriocins refer to the same
structure) was the first discovered bacteriocin belonging to
this group. While class IIb bacteriocins are two-peptide bac-
teriocins which require both peptides to be fully active [22,
25], class IIc bacteriocins are clustered based on the circular
configuration of their structure. The N- and C-termini of class
IIc bacteriocins are covalently linked, thus resulting in a very
stable molecular structure [26]. Although previously thought
as being rare, the discovery of circular bacteriocins has recent-
ly become more common. This is noteworthy as their high
stability and activity could open the next generation of
biopreservatives. Definitely, garvicin ML, gassericin A,
lactocyclin Q, and leucocyclin Q hinder a range of Gram-
Probiotics & Antimicro. Prot.
positive bacteria including food spoilage bacteria and food
pathogens. Their outstanding bioactivity and stability is attrib-
uted to their head to tail cyclization which results in increased
protease and heat resistance [27, 28].
Class IId bacteriocins comprise the remaining bacteriocins
that are combined as miscellaneous or one-peptide
nonpediocin linear group [13]. Sec-dependent bacteriocins
and the increasing number of bacteriocins without leader pep-
tide belong to this class [29].
Microbes Involved in Fermented Meat Products
Meat and fermented meat products are extremely sensitive to
microbial spoilage mainly because of their ecological proper-
ties (water activity, pH, and nutrients). The microorganisms
that are primarily involved in meat fermentation include spe-
cies of LAB, molds, and yeasts.
LAB constitute a part of the initial microflora which de-
velops easily after meat is processed, chilled, stored, or packed
under vacuum or modified atmosphere. LAB play a signifi-
cant role in meat fermentations causing flavor and texture
changes together with a preservative effect resulting in an
increase in the shelf life of the transformed product. LAB in
fresh meat bring about a mild fermentation process without
producing variations in the organoleptic characteristics be-
cause of the low carbohydrate content and the strong buffering
capacity of meat. In the same way, the growth of LAB in
naturally fermented meats after the addition of sugar trans-
forms the products mainly through the production of lactic
acid by the LAB and the subsequent pH decrease which de-
natures the meat proteins. This process usually ends up in a
microbial stabilization of the product.
LAB isolated from fermented meats are well adapted to the
ecology of meat fermentation. The identification and techno-
logical characterization of LAB involved in meat fermentation
are crucial to select the best strains to use as starters [30, 31].
The main LAB players belong to the following genera
Carnobacterium, Lactobacillus, Pediococcus, Leuconostoc,
Weissella, and Enterococcus [30–32]. The dominant species
are usually members of Lactobacillus, while in certain slightly
acidified sausages, Lactobacillus and Enterococcus popula-
tions reach similar sizes [33]. Although Lactobacillus
curvatus and Lactobacillus plantarum are commonly isolated
from fermented sausages, Lactobacillus sakei remains the pre-
dominant LAB in southern European sausages [2, 6]. In many
fermented sausages systems, Lb. sakei has more fitness than
other lactobacilli, showing a shorter lag phase, a higher max-
imum growth rate, and a higher final cell density [1, 2, 31]. As
a result, in spontaneously fermented sausages, facultative
heterofermentative lactobacilli are the predominant bacteria
during ripening. Lb. curvatus and/or Lb. sakei generally dom-
inate the fermentation process. Lb. sakei is specially adapted
to the meat environment and has been widely used as a starter
culture for the production of a variety of meat-based
fermented products [34, 35]. Chaillou and coworkers deter-
mined the complete genome sequence of the French sausage
isolate Lb. sakei 23K, demonstrating that this strain has a
specialized metabolic repertoire that may contribute to its
competitive ability in these ecosystems [36].
As a result, Lb. sakei appears to be the most competitive,
frequently representing half to two thirds of all LAB isolates
from spontaneously fermented sausage, whereas Lb. curvatus
is often found in amounts up to one fourth of all LAB isolates.
Other lactobacilli that may be found, albeit generally at minor
levels, include Lb. plantarum, Lb. bavaricus, Lactobacillus
brevis, Lactobacillus buchneri, and Lactobacillus paracasei.
However, talking about application of Lb. curvatus, Lb. sakei,
and Lactobacillus garvieae, it is noteworthy to acknowledge
that these species have been distinguished only at the begin-
ning of the twenty-first century and, as a result, some reports
described the reclassification of many strains belonging to
these newly classified species [37].
Pediococci are less frequently isolated from European
fermented sausages but occasionally occur in limited shares
[38]. They are more common in fermented sausages from the
USA where they are deliberately added as starter cultures to
speed up meat acidification.
Enterococci are sometimes associated with fermented meat
products, in particular artisan ones from Southern Europe,
where they increase during early fermentation stages and can
be detected in the end-product at low levels [38–40].
Molds, such as Penicillium nalgiovense and Penicillium
chrysogenum, are efficiently applied during the ripening of
sausages, particularly in Southern Europe [41]. Yeast pop-
ulations, dominated by Debaryomyces hansenii, may also
be found on the sausage surface with additional potential
benefits in terms of organoleptic traits of fermented meat
products [42, 43].
Bacteriocin-Producing LAB Isolated
from Fermented Meat Products
Many LAB strains have been isolated from fermented meat
products and described for their potential applications as
biopreservatives (Table 1), with lactococci, lactobacilli,
pediococci, and enterococci the most frequent ones.
Bacteriocin-producing Lactococcus spp. and Leuconostoc
mesenteroides [45] have been isolated from fermented meat.
Lactobacillus spp. isolated from sausages frequently produce
bacteriocins or bacteriocin-like compounds, as has been prov-
en for Lb. sakei, Lb. curvatus, Lb. plantarum, Lb. brevis, and
Lactobacillus casei. Several nisin-producing Lactococcus
lactis strains, isolated from Spanish [44] and traditional Thai
fermented sausage [45], were effective in inhibiting closely
Table 1 Examples of bacteriocinogenic LAB strains isolated from fermented meat products

Producer strain Bacteriocin Class Source Other Ba. Br. Cl. Cl. En. Li. Propionibacterium S. aureus References
LAB cereus thermosphacta botulinum perfringes faecalis/ monocytogenes sp.
faecium

Lc. lactis BB24 Nisin Ia Spanish sausages X X X X [44]

Lc. lactis WNC20 Nisin Z Ia Thai sausages X X X X X [45]
Lc. lactis 69 Nisin Z Ia Brazilian dry X X X X [46]
meat
Lb. sakei 148 Lactocin S Ia Spanish sausages X X X X [47]
Lb. sakei L45 Lactocin S Norwegian X X X X [48]
salami dry
sausages
Lb. sakei Lb706 Sakacin A IIa Beef, meat X X X [49]
products
Lb. sakei LS5 IIa Italian sausages X X X [50]
Lb. sakei CTC494 Sakacin K IIa Spanish sausages X X X [49]
Lb. sakei ST154Ch Sakacin IIa Pork product X X X X [51]
ST154Ch
Lb. sakei MN Bavaricin MN IIa Retail cuts of X [52]
beef
Lb. brevis SB27 Brevicin 27 IId Semidry X X [53]
sausages
Lb. curvatus Lactocin 705 IIb Argentine X X X X [54]
CRL705 sausages
Lb. curvatus L442 Curvaticin L442 IIa Greek sausages X X [55]
Lb. curvatus 54M16 Sakacin A,C,K IIa Italian sausages X X X X [56]
Lb. plantarum N014 Plantaricin A IId Thai pork X X [57]
Le. mesenteroides Leucocin A IIa Greek sausages X [58]
E131
Le. carnosum 4010 Leucocin B IId Vacuum-packed X X X [59]
meat
Pe. acidilactici L50 Pediocin L50 IId Spanish sausages X X X X X X X [60]
Pe. pentosaceous Pediocin PA-1 IIa Spanish sausages X X X X X X [61]
Z102
C. piscicola LV17A Carnobacteriocin IId Processed meat X X [62]
A
Enterococcus Enterocin Portuguese meat X X X [40]
faecium
ST211Ch
Enterococcus Enterocin P IId Spanish dry X X X X [63]
faecium P13 sausages
Enterococcus Enterocin 416K1 IIa Italian sausages X [64]
casseliflavus
IM416K1
Enterococcus Enterocin Sausages X X X X X [65]
faecalisCEC-
T7121
Probiotics & Antimicro. Prot.
Probiotics & Antimicro. Prot.
related LAB, Li. monocytogenes, Cl. perfringens, Ba. cereus,
and S. aureus. Moreover, Lb. sakei L45 isolated from
Norwegian dry sausages and Lb. sakei L48 from Spanish
fermented sausages produce lactocin S, a lantibiotic active
against LAB and Clostridium spp. strains. Finally, lactocin
705 secreted by Lb. curvatus CRL705, isolated from
Argentine fermented sausages, is the first two-peptide
bacteriocin reported from a meat-associated strain. This
bacteriocin was effective in the inhibition of other LAB
and Brochothrix thermosphacta when assayed in experi-
mental meat systems [66].
Few Pediococcus spp. strains isolated from fermented meat
have been reported to be bacteriocinogenic. This is the case of
Pediococcus acidilactici isolated from American-style sau-
sages and Pediococcus pentosaceus from Spanish-style sau-
sages. Many enterococci from fermented meat are known to
produce bacteriocins with high antilisterial activity [41].
Enterocin A and B produced by Enterococcus faecium
CTC492 isolated from Spanish dry fermented sausages were
described for their ability to inhibit the growth of many LAB,
Li. monocytogenes, and Clostridium spp. [67].
Bacteriocins Applied in Meat Biopreservation
For fermented meat preservation, nitrates are traditionally
used: their partial conversion into nitrites by microbial nitrate
reductases can prevent growth of Clostridium spp. and other
spoilage bacteria. Direct addition of nitrites has also been pro-
posed. The reaction of nitrites with secondary amines in
fermented meat products can produce, under certain condi-
tions, significant levels of carcinogenic nitrosamines [1].
Today, the application of chemical preservatives is question-
able because of their carcinogenic and toxic effects [7, 68]. To
look for other alternatives, a number of plant-derived antimi-
crobial extracts have been tested [9, 69]. However, few chal-
lenging aspects have to be addressed before the widespread
application of phytochemicals into meat processing. Meat
characteristics and process conditions can greatly hamper the
antimicrobial effects of plant-derived extracts. Moreover,
Table 2 Recent nisin
applications in meat processing Meat product
Raw buffalo minced meat
Cooked sausage
Sous vide cooked seasoned beef
Meat emulsions
Raw meat
Vacuum-packed cooked ham
Round steak
Natural sausage casings
toxicological information on phytochemicals is still limited
and must be significantly increased [9, 69].
On the other hand, bacteriocins have technological proper-
ties better than those of plant extracts: antimicrobial peptides
of microbial origin can tolerate higher thermal stress, be active
within a wide pH range, and could be effective also at low
concentration. Moreover, bacteriocin applications do not usu-
ally result in the alteration of sensory and organoleptic atti-
tudes of fermented meat products.
Nisin and Other Commercial Bacteriocin-Containing
Products
For meat processing and preservation, in addition to nisin,
which is the only bacteriocin licensed as a food preservative
in over 50 countries, concentrated supernatants of bacteriocin
producer cultures such as ALTA 2341 (Quest) and Microgard
(Danisco) are also on the market [1, 70, 71]. For instance, the
surface of frankfurters inoculated with a five-strain mixture of
Li. monocytogenes was treated with different dosages of
ALTA 2341 [70]. The authors demonstrated that ALTA 2341
supplementation in combination with postpackaging thermal
treatment offers an effective treatment combination for the
control of Li. monocytogenes [70].
Nevertheless, nisin is the most applied product as meat
preservative (Table 2).
Nisin preparations in fermented meat products manufactur-
ing have been mainly adopted as powder, solution, and more
recently, as biofilm component. In the case of powder supple-
mentation, different dosages have been applied to control Li.
monocytogenes (Table 2). Paik and colleagues used 2.5 to
12.5 mg kg−1 nisin in vacuum-cooked seasoned beef meat to
inhibit Ba. cereus and Cl. perfringens [74].
Moreover, nisin supplementation in round steak effectively
inhibited Br. thermosphacta [78] and, once formulated in meat
emulsions, was efficient in inhibiting Li. monocytogenes [75].
Nisin addition was also applied to natural sausage casings
(Table 2).
More recently, to control Li. monocytogenes in sausage
model, the combined formulation of nisin (12.5–25 ppm),
Nisin levels Target microbes References
10–20 mg/kg Li. monocytogenes [72]
11.25 mg/kg – [73]
2.5–12.5 mg/kg Ba. cereus, Cl. perfringens [74]
0.25–2.5 mg/kg Li. monocytogenes [75]
25 mg/kg Li. monocytogenes [76]
10–130 mg/kg LAB [77]
125 mg/l Br. thermosphacta [78]
50 mg/l Cl. sporogenes [79]

nitrite (100–200 ppm), organic acid salts (1.55–3.1%), and the
mixture of Chinese cinnamon and Cinnamon bark essential
oils (EOs) (0.025–0.05%) has been proposed. The authors
reported positive effects without affecting sensorial character-
istics of the fermented sausages [80].
The use of 125 μg/ml of nisin and 30 mM of disodium
ethylenediamine tetra acetate (EDTA), immobilized on the
surface of the nanocrystal (CNC)/chitosan nanocomposite
films by means of genipin as a cross-linking agent, was
efficiently proposed [81]. In addition, the effect of low-
dose gamma irradiation on the antimicrobial activity of the
films was tested. The genipin cross-linked films prepared
by irradiating at 1.5 kGy demonstrated the highest antimi-
crobial activity against E. coli and Li. monocytogenes. As
a result, the authors suggested that the development of
antimicrobial packaging containing natural antimicrobials
can be considered as a novel technology to assure food
safety [81].
A combination of food-grade compounds with edible films,
used to control foodborne pathogens associated with fresh or
further processed meat food products, is attracting scientific
attention. The use of pullulan films containing lauricarginate
(LAE) and nisin Z, alone or in combination, to inhibit E. coli,
Salmonella spp., S. aureus, and Li. monocytogenes Scott A,
was lately applied in fresh and further processed meat food
products after long-term refrigerated storage [82].
Although extensively used also in meat processing, nisin
has particular physicochemical properties influencing espe-
cially its stability and biological activity. Thus, when nisin is
applied to meat matrix, the resulting antimicrobial activity will
heavily depend on the product characteristics. The efficacy of
nisin in meat is mainly faced by the presence of glutathione, a
molecule capable of inactivating nisin by a glutathione S-
transferase catalyzed reaction [83]. This glutathione inactiva-
tion is lower in cooked meat due to the loss of free sulfydryl
groups, which catalyze the reaction between glutathione and
proteins, during heating process. Nisin can also be deactivated
by proteases generally found in fresh meat. In addition to
glutathione and the presence of proteolytic enzymes, nisin
can easily interact with the meat fats, further reducing its an-
timicrobial efficacy. In this context, nisin has been proven to
be more effective in dairy than in fermented meat products
in terms of interactions between nisin and phospholipids
[84]. Davies and colleagues investigated the effects of
phospholipids and fat on its activity, demonstrating that
with lower fat level, a higher antimicrobial ability of nisin
was detected [85]. As a general rule, nisin stability in meat
during storage depends mainly on temperature, pH, pres-
ence or absence of intact glutathione and/or active prote-
ases, and storing period [12]. The above considerations
clearly call for novel and effective bacteriocins to be pro-
posed as efficient biopreservatives for meat processing and
conservation.
Probiotics & Antimicro. Prot.
The Application of LAB Strains
In fermented meat products, nisin is apparently not the bacte-
riocin of choice. Therefore, bacteriocinogenic LAB may be
better in introducing inhibitory compounds into meat
fermented products, providing a bacteriocin source over a lon-
ger period of time. However, in situ production of bacteriocins
is sometimes hampered by many environmental and techno-
logical factors [86]. It seems important to apply strains from
the same environment, naturally adapted to the characteristics
of the product and the technology used.
Novel bacteriocins can be supplemented by means of three
main approaches including the direct (a) inoculation of bacte-
riocin producing starter or protective cultures; (b) application
of cell-free supernatant, purified or partially purified bacterio-
cins; and (c) use of partially purified or purified bacteriocins in
the formulation of antimicrobial packaging. This review will
focus mainly on the first two options.
Starter LAB
Direct utilization of bacteriocin-producing LAB could be one
of the most useful ways to obtain healthy, improved, and even
novel fermented meat products. In the case of starter cultures,
inoculated LAB should support (a) the production of acids and
bacteriocins and (b) the hydrolysis of proteins, thus changing
the properties and organoleptic traits of meat food products.
Ideally, a protective bacteriocinogenic LAB culture should
be able to suppress the growth of spoilage bacteria without
changing sensorial and organoleptic texture of meat foods.
Despite considerable work on both research strategies, con-
cerns remain in relation to the use of bacteriocin-producing
LAB as inoculum for fermented meat processing [7, 16]. The
major drawbacks are mainly related to the low compatibility
between bacteriocinogenic and other starter cultures in multi-
ple starter systems [16, 33, 41]. Moreover, other problems are
caused by incomplete fermentation using bacteriocin-
producing LAB single-strain starter cultures [2, 41, 87].
Furthermore, food matrix interference and nonoptimized con-
ditions of bacterial growth and antibacterial production may
reduce the protective effects of LAB [88]. As amphiphilic
peptides, bacteriocins are susceptible to adsorption to food
macromolecules and proteolytic degradation, which may limit
their use as preservation agents. As a consequence, a large
fraction (up to 80%) of bacteriocins produced or added to
fermented meat products could be sequestered or adsorbed
by food constituents, resulting in low or inadequate protective
function [12, 89].
A multiple strain starter system has been recently proposed
for the production of ostrich meat salami [90]: Lb. plantarum
423 and Lb. curvatus DF126, plantaricin and curvacin pro-
ducers, respectively, were utilized together with Micrococcus
spp. MC50. Both bacteriocinogenic strains were compatible
Probiotics & Antimicro. Prot.
with Micrococcus spp. MC50 and effectively inhibited the
growth of Li. monocytogenes in salami.
Lb. plantarum 423 has been shown to be an effective starter
culture in the production of salami from a number of meat
types, including horse, beef, mutton, springbok, and blesbok,
producing good sensorial and organoleptic properties [91].
The same authors evaluated also the effectiveness of commer-
cial starter culture of Lb. curvatus DF38 in salami production,
reporting more anti-Listeria activity than Lb. plantarum 423
in all meat salami.
Another recent and potential starter culture has been pro-
posed: Pe. pentosaceus BCC 3772, able to produce pediocin
PA-1/AcH, was applied for Nham, a Thai traditional
fermented pork sausage. This strain efficiently inhibited Li.
monocytogenes growth without significant changes in sensory
attributes and consumer acceptance of the final product [92].
A Lb. curvatus strain, namely 54M16, producing at least
three different sakacins, was lately described to improve the
quality and safety of traditional fermented sausages [56]. The
selected strains exhibited relevant technological properties
and antimicrobial activities against S. aureus and
Enterobacteriaceae.
One more bacteriocin-producing LAB was found to be
effective as starter: Lc. lactis subsp. lactis 69, during the fer-
mentation of charqui, a Brazilian fermented and sun-dried
meat product [46]. This nisin Z-producing strain showed a
potential for application as an additional hurdle in the preser-
vation of salted fermented meat products. Moreover, the au-
thors carefully assessed the absence of virulence genes, further
supporting the perspective of using Lc. lactis subsp. lactis 69
as safe starter LAB for meat and other food applications.
Protective LAB
In the last decades, few protective LAB cultures have been
applied for meat processing. These include Le. carnosum
4010, Lb. curvatus CRL705, and CWBI-B28-wt [93–95].
Addition of Le. carnosum 4010 to vacuum-packed slices of
cooked meat instantaneously reduced the population numbers
of Li. monocytogenes to a level below the detection limit [93].
Interestingly, the authors clearly demonstrated that the use of
the living protective culture was more effective in preventing
growth of Li. monocytogenes than the addition of the partially
purified leucocins 4010 or bacteriocin produced during fer-
mentation before heat treatment of the meat [96].
The inoculum of Lb. curvatus CRL705 on vacuum-
packaged fresh beef suppressed for 60 days the growth of
Li. monocytogenes and Br. thermosphacta [66]. This strain
was found to be active also at low temperature, without any
sensorial damages to the final product. Therefore, inocula-
tion with this bacteriocin-producing strain would provide
an additional hurdle to improve storage life of refrigerated
vacuum-packaged beef without affecting its sensory and
structural traits [94].
Finally, Lb. curvatus CWBI-B28wt was able to inhibit Li.
monocytogenes proliferation in raw and cooked pork meat
[95]. The entrapment of protective culture was also proposed
to protect them from the adverse conditions in food environ-
ments [16, 97, 98]. The bacteriocinogenic Lb. curvatus
MBSa2 isolated from salami was entrapped in calcium algi-
nate and tested for functionality in salami experimentally con-
taminated with Li. monocytogenes, simulating manufacture
process conditions, including fermentation and maturation
steps [99]. The authors demonstrated for the first time that
the encapsulation of bacteriocin-producing LAB in calcium
alginate could be a promising technological way to control
Li. monocytogenes growth in fermented meat goods.
Bacteriocin Supplementation as Food Additive
During the last decades, the incorporation of novel bacterio-
cins as additive in fermented meat products received great
attention. This approach is desirable when living LAB are
not able to produce or ensure sufficient bacteriocin levels in
the real meat systems. Bacteriocin preparations can be vari-
ous: purified, partly purified, or cell-free supernatant.
Application of En. faecium CTC492 was not successful as
starter or protective culture for fermented meat products, but
the supplementation of its enterocins A and B resulted to be
very effective in the inhibition of Listeria innocua in different
types of meat foods, including minced pork, deboned chicken
breasts, cooked ham, pâté and fermented sausages [100].
Purified lactocin AL705 and its producer, Lb. curvatus
CRL705, were reported to be both effective in the control of
Li. innocua throughout the storage period of vacuum-
packaged raw meat [94]. The application of partially purified
bacteriocin from Pe. acidilactici was bactericidal against Li.
monocytogenes and bacteriostatic against Cl. perfringens on
raw meat stored at 15 °C [101]. The bacteriostatic application
of semipurified pediocin AcH (pediocin PA-1) against Li.
monocytogenes and spoilage LAB on sliced cooked sausage
was also demonstrated [102].
The antilisterial activity of nisin A and pediocin AcH
(pediocin PA-1) was considered for the decontamination of
artificially polluted raw pork. Nisin A was considerably more
proficient than pediocin AcH [103].
Addition of pentocin 31-1, an antimicrobial peptide pro-
duced by Lb. pentosus 31-1, to chilled pork suppressed the
gro wth of L i . mo nocy to gene s a nd Ps eudo mo nas
fluorescens, improved physicochemical properties and or-
ganoleptic characteristics, and extended product shelf life
by up to 15 days [104].
The partly purified enterocin AS-48, bacteriocin produced
by Enterococcus faecalis A-48-32, was applied to control the
growth of Salmonella spp. and Li. monocytogenes during

ripening of slightly acidic fermented sausage. It is notable that
a substantial improvement of Salmonella inhibition was ob-
served when enterocin AS-48 was applied together with high
hydrostatic pressure treatment [105] shedding light on new
combinations to increase antimicrobial activity of
bacteriocins.
Two bacteriocins produced by En. faecium strains, consid-
erably reduced the growth of Li. monocytogenes on raw meat
sausage after 5 days of storage at 4 °C [106]. More recently,
sakacin Q produced by Lb. curvatus ACU-1 was applied to
control the growth of Li. innocua artificially inoculated on
cooked meat surface during chilled storage [107]. Partially
purified sakacins P and X from Lb. curvatus MBSa2, when
supplemented to salami, caused great reduction of Li.
monocytogenes. The same bacteriocins have been successful-
ly tested also on other salami and fermented meat products,
further supporting their high potential as biopreservatives
against Li. monocytogenes [108].
E. coli O157:H7, a foodborne pathogen reported from dif-
ferent cases related to consumption of food products, has been
subject of study for inhibition by different bacteriocins on
cooked pork meat [109] and ground beef [110].
Limitation of the Application
Since the discovery of nisin in 1933, more than 7000 papers
have been published on bacteriocins (www.scopus.com,
accessed on 05 May 2017), with almost 3100 manuscripts
about nisin and nearly 550 ones on pediocin PA-1.
Meanwhile, nisin and pediocin PA-1 are extensively
adopted for the biopreservation of different dairy products
[97], and only few applications have been reported for
fermented meat products. The main issues to be addressed
toward the widespread utilization of bacteriocins in meat pro-
cessing could be summarized in technological and safety
challenges.
Technological Aspects
Application of bacteriocins or bacteriocin producers as agents
for biopreservation is a promising but complex process. It
needs a deep knowledge of biochemical properties of bacte-
riocin(s) from one side and specific physiological properties
of bacteriocin(s) producer from the other. The effectiveness of
bacteriocins in fermented meat products will depend on many
factors including the interaction with the food matrix and/or
with the target bacteria and the action of the indigenous meat
microbiota [111]. As an example, supplementation of divalent
ions such as Mg2+ or Ca2+ led to a reduction of nisin activity.
The cations were bounded to anionic phospholipids making
the cytoplasmic membrane more rigid, thus reducing the af-
finity of the bacteriocin toward the cytoplasmic membrane
Probiotics & Antimicro. Prot.
[111]. Regarding the action of indigenous microbial popula-
tions, the occurrence of competing microorganisms can be an
environmental factor stimulating antimicrobial compound
production. In other cases, microbiota can compete for nutri-
ents with the bacteriocinogenic strain inhibiting growth and,
therefore, bacteriocin secretion [97, 111].
In meat biopreservation processes, application of bacte-
riocins can be influenced by the presence of traditionally
used nitrates. The use of nisin in fermented meat products
with nitrate addition gave conflicting results: nisin, in com-
bination with lower levels of nitrate, can prevent the
growth of Clostridia. However, some researchers conclud-
ed that it is not effective in meat applications together with
nitrate addition in fermented or dry cured fermented meat
products [112, 113].
In pork meat, nitrite has only a slight negative effect on the
growth of Li. monocytogenes [114]. It is therefore necessary to
take additional preventive measures such as the use of a starter
culture having the ability to grow and produce bacteriocin in
situ. The anti-Listeria action and the pH modification of Lb.
curvatus strains in meat systems during storage at 4 °C have
been extensively studied [95]. This noteworthy research led to
the following remarks: (a) Lb. curvatus strains grew better in
fat-rich than in lean meat, probably due to the differences in
water activity of the meat; (b) there was no significant varia-
tion in the pH in any inoculated product; (c) the protection
obtained by the bacteriocinogenic strains was not complete
and proteolytic degradation of bacteriocin was detected [95];
and (d) nitrite negatively affected the antimicrobial activity by
means of various mechanisms.
The decreased production of bacteriocins by LAB in the
presence of sodium chloride has been also described [115].
The reduction in bacteriocin production in the presence of
salt is due to interference of sodium chloride molecules
with binding of the induction factor, which is essential
for bacteriocin production, to its receptor [116]. The high
concentration of fat significantly limited the anti-Listeria
effect of bacteriocinogenic Lb. curvatus [95]. Sakacin P
could adsorb to fat particles, thus resulting in inactivation
[117]. Some bacteriocins have a stabilizing effect on the
fat-water interface: their association with fat is readily re-
versible and does not prevent their action [111].
Concerning practical applications of bacteriocins, the
essential issue is on their activity rather than their bind-
ing to meat components. So far, few studies have ad-
dressed this topic. More than 80% of the added bacteri-
ocin was adsorbed to the muscle protein, but the activity
of the protein-bound bacteriocin could not be assessed
[89]. Protease caused inactivation of the sakacin P, and
probably other bacteriocins in unheated food products
could be a problem as well, but these authors suggested
that losses could be compensated by increased dosages
of bacteriocins [118].
Probiotics & Antimicro. Prot.
Moreover, application of bacteriocins in meat biopreserva-
tion faces other serious problems. As discussed above [13],
several bacteriocins, including nisin (class I, lantibioitcs) and
pediocin PA-1 (class IIa, anti-listerial bacteriocins), interfere
with the target cells via lipid II receptor. Furthermore, most
bacteriocins can have affinity to other lipids as well and can
form complexes. Based on these observations, the presence of
different lipids can reduce the biological activity of several
bacteriocins. Another limitation of the application of bacteri-
ocin in meat biopreservation is the fact that some proteases are
frequently present in these fermented meat products.
An additional concern on the application of bacteriocinogenic
LAB strains in biopreservation is related to the lines of evidence
that bacteriocin production is not always strictly linked to bac-
terial growth. Several reports demonstrated that bacteriocin pro-
duction is dependent on cultivation temperatures, pH, water ac-
tivity, and availability of nutrients, including quantity and variety
of carbohydrates and organic nitrogen sources [88, 119–121].
Meat extract, peptone, or yeast extract can influence bacteriocin/
s production [120, 121]. However, all these reports are per-
formed in well-controlled laboratory conditions.
Bacteriocin productions in Breal^ fermentation conditions
are even more complex. Moreover, bacteriocin production
is not equal in liquid medium and in solid medium. As a
result, bacteriocin(s) can be produced and expressed on
meat substrates in different levels, compared to the labora-
tory commercial media [120].
Bacteriocinogenic LAB can be even more Bbeneficial^ if
they can exhibit also technological properties. However, it is
very important for applied LAB to have the ability to express
their bacteriocin/s into the food matrix in the context of the
physiological and biochemical characteristics of the fermented
food product. LAB can normally ferment glucose and several
other carbohydrates as well as grow at temperatures from 15 to
45 °C both in the presence or absence of oxygen. Another
technological problem is that very frequently, fermentation
time in the preparation of some fermented food products is
reasonably short, and after that, products are stored at refrig-
eration condition. In this scenario, production and expression
of the bacteriocin/s can be compromised because LAB strains
can struggle to grow. LAB will probably survive at the refrig-
eration and freezing conditions but definitely cannot ensure
the production of bacteriocin(s). Finally, bacteriocin(s) pro-
duction can be also regulated by the level of pH, temperature,
and presence of different proteins and be a part of quorum
senses [13, 97, 122]. Taking into consideration all these fac-
tors, bacteriocin production in meat ecosystems is still a key
aspect to be extensively addressed. Another option will be the
application of the semipurified or purified bacteriocin/s and/or
to look for technological and environmental balance consid-
ering both the growth of beneficial microbes and quality of
meat processing. In the first case, the cost-effective production
of bacteriocins would be crucial toward their wide utilization
in meat processing. One of the main costs (about 30% of the
total) in bacteriocin production is the substrate [123, 124], and
cheap substrates should be used to support high levels of bac-
teriocins secreted by the desired microbes.
Despite that the great availability of waste streams from
agricultural, industrial, and food processing sectors has been
already explored for the production of many commodities
such as biofuels, biopolymers, and enzymes [125–132], only
few research papers focused on bacteriocin production from
waste materials, mainly cheese whey and molasses [119, 121,
124]. As such, there is a lot of room to reduce production cost
of purified and semipurified bacteriocins ready to use in meat
and food processing.
Besides the search for cheap feedstock, what will be the
next challenge and perspective? The applied science already
faced the problems with the application of bacteriocins in food
preservation. Bacteriocin performance in the fermented food
meat systems can be improved and protected from proteolytic
enzymes by engineering of derivates with increased resistance
[133, 134]. Specific delivery modifications of bacteriocins can
be related not only to the protection/encapsulation of the ac-
tive molecules [135–137] but can also be approached by im-
proving the delivery systems [135] or by the modification of
amino acid sequence [138]. Such modification could influ-
ence (i) the stability, resistance, and performance of the bac-
teriocins in the fermented food systems and (ii) the spectrum
of activity [139].
This perspective calls for a link between fermented food
products and the health of humans and other animals. This is
the dream of Hippocrates: that our food can be medicine and
medicine our food. In such a scenario, bacteriocins produced
by LAB and bacteriocin producers used in biopreservation not
only can have positive effects on biopreservation of food com-
modities but also can actively improve the health status of
humans and other animals by repressing the pathogens.
Cytotoxicity of Bacteriocins
Toward the application of specific bacteriocins in meat pro-
cesses, their cytotoxicity traits must be carefully characterized.
Most of the studies proved that nisin can be considered as safe,
and even the use of nisin was stated by FDA as GRAS since
1988 based on its long-term application as food preservative
(E234) without being involved in health problems. However,
the cytotoxicity of bacteriocins is a key aspect which deserves
more attention.
Toxicological studies demonstrated that nisin intake does
not cause toxic effects with an estimated lethal dose (LD50) of
6950 mg kg−1, which is similar to that of salt, when adminis-
tered orally [140]. In general, some authors have associated
LD50 of bacteriocins with digestive enzymes capable of rap-
idly inactivating these substances such as trypsin and chymo-
trypsin produced in the pancreas [84]. Moreover, different

bacteriocins can have a high variation in molecular mass and
amino acid structure, including even the presence of some
nonprotein subunits involved in their activity. These features
can interfere with their cytotoxicity. Therefore, specific eval-
uation of each bacteriocin needs to be performed. A literature
research on this topic reveals that the analysis of cytotoxicity
of bacteriocins is not routine and only a few studies are avail-
able. The toxicity profile of nisin on epithelial monkey kidney
cells (Vero) was assessed, and at 1.04 μg/ml, nisin reduced the
cell viability by 50% [141]. Two bacteriocins (ST202Ch and
ST216Ch), produced by LAB isolated from fermented sau-
sages from Portugal, showed high cytotoxicity levels on
Huh7.5 cells [142].
Suwandecha and colleagues mentioned that majority of
antimicrobial peptides (including bacteriocins as well) have
low cytotoxicity and enhanced stability [143]. They per-
formed in vitro cytotoxicity tests of the antimicrobial protein
called BPep-7^ in order to consider their study for clinical use.
Nevertheless, in our opinion, bacteriocins destined to be used
in the food industry should be tested for cytotoxicity. Another
critical and disputable point is the choice of an appropriate cell
line for worldwide and interlaboratory cytotoxicity experi-
ments. Brogden proposed the use of erythrocyte cells as model
arguing that erythrocyte plasma membrane is a natural mem-
brane in the body containing anionic surface charge and a lipid
monolayer. Thus, it could be considered a good analogue of a
prokaryote negatively charged cell containing a lipid bilayer
[144]. Moreover, a standardized procedure is needed in order
to compare results of cytotoxicity levels from different
bacteriocins.
Das and Goyal reported on cytotoxicity analysis of
plantaricin DM5 on two different cell lines: human embryonic
kidney 293 (HEK 293) and human cervical cancer (HeLa).
The bacteriocin revealed to be nontoxic and with biocompat-
ible nature. As a result, the authors claimed that plantaricin
DM5 was without any cytotoxic effect on mammalian cells,
and can contribute to the food industry as a novel
biopreservant [145].
The active supernatants containing putative mundticin KS-
like bacteriocins, produced by three different Enterococcus
mundtii strains, did not show cytotoxicity against human
erythrocytes. Hemolysis of human erythrocytes was negative
in PBS and En. mundtii supernatants, showing that the metab-
olites of the tested strains were not hemolytic [146].
A recent review on different aspects on two staphylococcal
lantibiotics, epidermin and gallidermin, focused also on cyto-
toxicity [147]. The traits of gallidermin, nisin A, magainin
peptides, vancomycin, and melittin were investigated and
compared in two gastrointestinal cell models (HT29 and
Caco-2), and the hemolytic activities in sheep erythrocytes
was also determined [147]. Gallidermin was assessed to be
the least cytotoxic, followed by nisin A, magainin I, magainin
II, and melittin [148]. Moreover, melittin and nisin were the
Probiotics & Antimicro. Prot.
only ones exhibiting significant hemolysis. Once compared to
the abovementioned antimicrobial peptides, gallidermin was
the most promising candidate as a therapeutic agent [148].
Various studies showed different levels of cytotoxicity for
bacteriocins using similar approaches and the Vero cell model:
bacteriocins produced by Lb. plantarum [149], En. faecium
[122], and En. mundtii [150] have been deeply investigated.
Overall, the cytotoxicity of bacteriocins needs to be seri-
ously considered as a key trait in future characterization stud-
ies of new bacteriocins. As previously discussed, the results of
cytotoxicity assays could vary upon the type of cell lines used
and the research approaches carried out. Therefore, standard-
ized procedures and cell lines need to be internationally
established. Indeed, the fact that nisin has been granted
GRAS status and applied for decades without serious cases
of toxicity is not enough to ignore the need for the cytotoxicity
assessment of newly described bacteriocins before their appli-
cations in food systems.
Safety of Bacteriocinogenic LAB
As discussed in the previous part, properly selected
bacteriocinogenic LAB could serve as starter or protective
culture. However, with the introduction of additional bacteria
into meat production, special attention needs to be given to the
presence of possible genetic determinants of virulence factors.
Some of them can most probably not be expressed in specific
conditions; however, the presence of genes on the genome of
LAB could be alarming and considered as a hazard.
When we talk about virulence factors, we normally refer to
pathogenic or opportunistic pathogenic bacteria. Moreover,
Enterococcus spp. are frequently examples of high virulence
potential [151, 152]. However, on other side, several
fermented food and fermented meat products have been
enriched with beneficial Enterococcus spp. strains [31, 61,
153].
Where is the truth? Are LAB and particularly Enterococcus
spp. safe or not? Most of the LAB have well-accepted GRAS
status, based on historically long safe application.
Nevertheless, reports from the last decades clearly demon-
strate that we cannot draw equivalence between the LAB
group and even the same species, as safety issues have to be
examined at the strain level. To this aim, it is important to
investigate the presence of virulence factors in LAB by both
molecular and phenotypic procedures [39]. Virulence factors
reported on some Enterococcus spp., and even other LAB
occurring in fermented meat, may be colonization factors
which promote the adhesion of bacteria to host cells; invasion
factors that promote the invasion of epithelial cells disordering
the immune system as well as cell wall-anchored surface pro-
teins; and related to enterococcal pathogenicity, including ag-
gregation substance, enterococcal surface protein, and
collagen-binding components [154].
Probiotics & Antimicro. Prot.
The presence of genes related to antibiotic resistance in
bacteriocinogenic LAB applied in biopreservation can be con-
sidered as a potential reservoir for undesirable antibiotic resis-
tance, that may be transferred via horizontal gene transfer to
(a) other bacteria presented in the fermented meat products or
(b) the GIT microbiota of the consumers [39].
The safety aspects of bacteriocinogenic LAB (Lb.
plantarum, En. faecium, and Lb. sakei) isolated from
fermented meat products from Portugal have been studied
[155]. According to the results of the diffusion method, the
strains demonstrated susceptibility to several antibiotics and
nonantibiotic commercial medicaments. Moreover, their viru-
lence factors profile was limited.
A newly isolated En. faecium strain collection obtained
from artisanal Tunisian fermented meat has been described
also for safety aspects and functional properties [153].
Investigation of virulence factors by PCR amplification re-
vealed the presence of genes encoding for gelatinase (gelE),
enterococcal antigen (efaAfm), sex pheromone (cpd and ccf),
and expression of cytolysin (the hemolytic component cylB),
whereas other presumed virulence genes encoding for agg,
esp, cylM, cylA, and cob were not detected. The isolates were
mostly resistant to a number of antibiotics, further supporting
the need of deep and internationally defined screening on
safety traits of bacteriocinogenic LAB.
Conclusions
Today, consumers are critically concerned about the relation-
ship between food, safety, and quality. The use of functional
starter cultures could be a great way to drive the fermentation
of fermented meat products, allowing high standards of qual-
ity as well as novel and safer productions. Despite the abun-
dant efforts of basic and applied research on the identification,
characterization, and development of bacteriocinogenic LAB
in meat over the past four decades, very few formulations
reached the market. The choice of starter should be drawn in
the context of its application, since functionality is strictly
dependent on the type of product, ingredients, raw materials
used, and technology applied. Moreover, the use of competi-
tive bacteriocinogenic LAB as bioprotective cultures should
be considered only as an additional hurdle to good
manufacturing platforms. The huge amount of information
derived from genetic and genomic analyses offers new pow-
erful tools to make a scientifically sound selection of new
tailored functional cultures with desired physiological traits.
The microbiota of traditional fermented meat could be a pre-
cious trove for the search of well-adapted strains able to com-
pete with indigenous contaminant bacteria. In the selection of
a starter culture, safety features, such as cytotoxicity, antibiotic
resistance, virulence genes, and formation of undesirable me-
tabolites, should not be disregarded.
Compliance with Ethical Standards
Conflict of Interest The authors declare that they have no conflict of
interest.
References
1. Hui Y, Astiasaran I, Sebranek J, Talon R, Toldrá F (2014)
Handbook of fermented meat and poultry. Wiley
2. Lücke F-K (2000) Utilization of microbes to process and preserve
meat. Meat Sci 56(2):105–115
3. Ninios RL, Ahomaa MF, Korkeala H (2014) Enteropathogenic
Yersinia in the pork production chain: challenges for control.
Compr Rev Food Sci Food Saf 13(6):1165–1191
4. Gram L, Ravn L, Rasch M, Bruhn JB, Christensen AB, Givskov
M (2002) Food spoilage—interactions between food spoilage bac-
teria. Int J Food Microbiol 78(1):79–97
5. Chen J, Ren Y, Seow J, Liu T, Bang W, Yuk H (2012) Intervention
technologies for ensuring microbiological safety of meat: current
and future trends. Compr Rev Food Sci Food Saf 11(2):119–132
6. Ojha KS, Kerry JP, Duffy G, Beresford T, Tiwari BK (2015)
Technological advances for enhancing quality and safety of
fermented meat products. Trends Food Sci Technol 44(1):105–
116
7. Woraprayote W, Malila Y, Sorapukdee S, Swetwiwathana A,
Benjakul S, Visessanguan W (2016) Bacteriocins from lactic acid
bacteria and their applications in meat and meat products. Meat
Sci 120:118–132
8. Chen H, Hoover D (2003) Bacteriocins and their food applica-
tions. Compr Rev Food Sci Food Saf 2(3):82–100
9. Lucera A, Costa C, Conte A, Del Nobile MA (2012) Food appli-
cations of natural antimicrobial compounds. Front Microbiol 3:
287
10. Deshmukh P, Thorat P (2013) Bacteriocins: a new trend in anti-
microbial food packaging. Int J Advanced Res Engineering Appl
Sci 1:1–12
11. Food, Administration D (1988) Nisin preparation: affirmation of
GRAS status as a direct human food ingredient. Fed Regist 53:
11247–11251
12. Gharsallaoui A, Oulahal N, Joly C, Degraeve P (2016) Nisin as a
food preservative: part 1: physicochemical properties, antimicro-
bial activity, and main uses. Crit Rev Food Sci Nutr 56(8):1262–
1274
13. Cotter PD, Hill C, Ross RP (2005) Bacteriocins: developing innate
immunity for food. Nat Rev Microbiol 3(10):777–788
14. Riley MA, Wertz JE (2002) Bacteriocins: evolution, ecology, and
application. Ann Rev Microbiol 56(1):117–137
15. Perez RH, Zendo T, Sonomoto K (2014) Novel bacteriocins from
lactic acid bacteria (LAB): various structures and applications.
Microb Cell Factories 13(1):1
16. Balciunas EM, Martinez FAC, Todorov SD, Franco BDGM,
Converti A, Oliveira RPS (2013) Novel biotechnological applica-
tions of bacteriocins: a review. Food Control 32(1):134–142
17. O’Connor PM, Ross RP, Hill C, Cotter PD (2015) Antimicrobial
antagonists against food pathogens: a bacteriocin perspective.
Curr Opin Food Sci 2:51–57
18. Diep DB, Nes IF (2002) Ribosomally synthesized antibacterial
peptides in Gram positive bacteria. Curr Drug Targets 3(2):107–
122
19. Gillor O, Etzion A, Riley M (2008) The dual role of bacteriocins
as anti- and probiotics. Appl Microbiol Biotechnol 81(4):591–606

20. Heng NC, Wescombe PA, Burton JP, Jack RW, Tagg JR (2007)
The diversity of bacteriocins in Gram-positive bacteria. In: Riley
MA, Chavan MA (eds) Bacteriocins. Springer, Berlin, pp 45–92
21. Klaenhammer TR (1993) Genetics of bacteriocins produced by
lactic acid bacteria. FEMS Microbiol Rev 12(1–3):39–85
22. Rea MC, Ross RP, Cotter PD, Hill C (2011) Classification of
bacteriocins from Gram-positive bacteria. In: Prokaryotic antimi-
crobial peptides. Springer, pp 29–53
23. McAuliffe O, Ross RP, Hill C (2001) Lantibiotics: structure, bio-
synthesis and mode of action. FEMS Microbiol Rev 25(3):285–
308
24. Drider D, Fimland G, Héchard Y, McMullen LM, Prévost H
(2006) The continuing story of class IIa bacteriocins. Microbiol
Mol Biol Rev 70(2):564–582
25. Nissen-Meyer J, Oppegård C, Rogne P, Haugen HS, Kristiansen
PE (2010) Structure and mode-of-action of the two-peptide (class-
IIb) bacteriocins. Probiotics Antimicrobial Proteins 2(1):52–60
26. Maqueda M, Sánchez-Hidalgo M, Fernández M, Montalbán-
López M, Valdivia E, Martínez-Bueno M (2008) Genetic features
of circular bacteriocins produced by Gram-positive bacteria.
FEMS Microbiol Rev 32(1):2–22
27. Gabrielsen C, Brede DA, Nes IF, Diep DB (2014) Circular bacte-
riocins: biosynthesis and mode of action. Appl Environ Microbiol
80(22):6854–6862
28. Sivonen K, Leikoski N, Fewer DP, Jokela J (2010)
Cyanobactins—ribosomal cyclic peptides produced by
cyanobacteria. Appl Microbiol Biotechnol 86(5):1213–1225
29. Alvarez-Sieiro P, Montalbán-López M, Mu D, Kuipers OP (2016)
Bacteriocins of lactic acid bacteria: extending the family. Appl
Microbiol Biotechnol 100(7):2939–2951
30. Ammor S, Dufour E, Zagorec M, Chaillou S, Chevallier I (2005)
Characterization and selection of Lactobacillus sakei strains iso-
lated from traditional dry sausage for their potential use as starter
cultures. Food Microbiol 22(6):529–538
31. Hugas M, Garriga M, Aymerich M (2003) Functionalty of entero-
cocci in meat products. Int J Food Microbiol 88(2):223–233
32. Hugo CJ, Hugo A (2015) Current trends in natural preservatives
for fresh sausage products. Trends Food Sci Technol 45(1):12–23
33. Ammor MS, Mayo B (2007) Selection criteria for lactic acid bac-
teria to be used as functional starter cultures in dry sausage pro-
duction: an update. Meat Sci 76(1):138–146
34. Hugas M, Monfort JM (1997) Bacterial starter cultures for meat
fermentation. Food Chem 59(4):547–554
35. Rahman U, Khan MI, Sohaib M, Sahar A, Ishaq A (2017)
Exploiting microorganisms to develop improved functional meat
sausages: a review. Food Reviews Inter 33(2):195–215
36. Chaillou S, Champomier-Vergès M-C, Cornet M, Crutz-Le Coq
A-M, Dudez A-M, Martin V, Beaufils S, Darbon-Rongère E,
Bossy R, Loux V (2005) The complete genome sequence of the
meat-borne lactic acid bacterium Lactobacillus sakei 23K. Nat
Biotechnol 23(12):1527–1533
37. Koort J, Vandamme P, Schillinger U, Holzapfel W, Björkroth J
(2004) Lactobacillus curvatus subsp. melibiosus is a later syno-
nym of Lactobacillus sakei subsp. carnosus. Int J Syst Evol
Microbiol 54(5):1621–1626
38. Papamanoli E, Tzanetakis N, Litopoulou-Tzanetaki E,
Kotzekidou P (2003) Characterization of lactic acid bacteria iso-
lated from a Greek dry-fermented sausage in respect of their tech-
nological and probiotic properties. Meat Sci 65(2):859–867
39. Franz CM, Stiles ME, Schleifer KH, Holzapfel WH (2003)
Enterococci in foods-a conundrum for food safety. Int J Food
Microbiol 88(2):105–122
40. Todorov SD, Favaro L, Gibbs P, Vaz-Velho M (2012)
Enterococcus faecium isolated from Lombo, a Portuguese tradi-
tional meat product: characterisation of antibacterial compounds
Probiotics & Antimicro. Prot.
and factors affecting bacteriocin production. Benefic Microbes
3(4):319–330
41. Leroy F, Verluyten J, De Vuyst L (2006) Functional meat starter
cultures for improved sausage fermentation. Int J Food Microbiol
106(3):270–285
42. Andrade MJ, Córdoba JJ, Casado EM, Córdoba MG, Rodríguez
M (2010) Effect of selected strains of Debaryomyces hansenii on
the volatile compound production of dry fermented sausage
Bsalchichón^. Meat Sci 85(2):256–264
43. Cano-García L, Flores M, Belloch C (2013) Molecular character-
ization and aromatic potential of Debaryomyces hansenii strains
isolated from naturally fermented sausages. Food Res Int 52(1):
42–49
44. Rodriguez J, Cintas L, Casaus P, Horn N, Dodd H, Hernandez P,
Gasson M (1995) Isolation of nisin-producing Lactococcus lactis
strains from dry fermented sausages. J Appl Bacteriol 78(2):109–
115
45. Noonpakdee W, Santivarangkna C, Jumriangrit P, Sonomoto K,
Panyim S (2003) Isolation of nisin-producing Lactococcus lactis
WNC 20 strain from nham, a traditional Thai fermented sausage.
Int J Food Microbiol 81(2):137–145
46. Biscola V, Todorov SD, Capuano V, Abriouel H, Gálvez A,
Franco BDGM (2013) Isolation and characterization of a nisin-
like bacteriocin produced by a Lactococcus lactis strain isolated
from charqui, a Brazilian fermented, salted and dried meat prod-
uct. Meat Sci 93(3):607–613
47. Sobrino OJ, Rodríguez JM, Moreira WL, Cintas LM, Fernández
MF, Sanz B, Hernández PE (1992) Sakacin M, a bacteriocin-like
substance from Lactobacillus sake 148. Int J Food Microbiol
16(3):215–225
48. Nes IF, Mørtvedt CI, Nissen-Meyer J, Skaugen M (1994) Lactocin
S, a lanthionine-containing bacteriocin isolated from
Lactobacillus sake L45. In: Vuyst LD, Vandamme EJ (eds)
Bacteriocins of lactic acid bacteria. Springer, Heidelberg, pp
435–449
49. Aymerich M, Garriga M, Monfort J, Nes I, Hugas M (2000)
Bacteriocin-producing lactobacilli in Spanish-style fermented sau-
sages: characterization of bacteriocins. Food Microbiol 17(1):33–
45
50. Amadoro C, Rossi F, Piccirilli M, Colavita G (2015) Features of
Lactobacillus sakei isolated from Italian sausages: focus on strains
from Ventricina del Vastese. Italian J Food Safety 4(4):5449
51. Todorov SD, Vaz-Velho M, Franco BDGM, Holzapfel WH (2013)
Partial characterization of bacteriocins produced by three strains of
Lactobacillus sakei, isolated from salpicao, a fermented meat
product from north-west of Portugal. Food Control 30(1):111–121
52. Lewus CB, Kaiser A, Montville TJ (1991) Inhibition of food-
borne bacterial pathogens by bacteriocins from lactic acid bacteria
isolated from meat. Appl Environ Microbiol 57(6):1683–1688
53. Benoit V, Mathis R, Lefebvre G (1994) Characterization of
brevicin 27, a bacteriocin synthetized byLactobacillus brevis
SB27. Curr Microbiol 28(1):53–61
54. Vignolo GM, Suriani F, APdR H, Oliver G (1993) Antibacterial
activity of Lactobacillus strains isolated from dry fermented sau-
sages. J Appl Bacteriol 75(4):344–349
55. Xiraphi N, Georgalaki M, Van Driessche G, Devreese B, Van
Beeumen J, Tsakalidou E, Metaxopoulos J, Drosinos EH (2006)
Purification and characterization of curvaticin L442, a bacteriocin
produced by Lactobacillus curvatus L442. Antonie Van
Leeuwenhoek 89(1):19–26
56. Casaburi A, Di Martino V, Ferranti P, Picariello L, Villani F (2016)
Technological properties and bacteriocins production by
Lactobacillus curvatus 54M16 and its use as starter culture for
fermented sausage manufacture. Food Control 59:31–45
57. Rattanachaikunsopon P, Phumkhachorn P (2006) Isolation and
preliminary characterization of a bacteriocin produced by
Probiotics & Antimicro. Prot.
Lactobacillus plantarum N014 isolated from nham, a traditional
Thai fermented pork. J Food Prot 69(8):1937–1943
58. Xiraphi N, Georgalaki M, Rantsiou K, Cocolin L, Tsakalidou E,
Drosinos E (2008) Purification and characterization of a bacterio-
cin produced by Leuconostoc mesenteroides E131. Meat Sci
80(2):194–203
59. Wan X, Saris PE, Takala TM (2015) Genetic characterization and
expression of leucocin B, a class IId bacteriocin from Leuconostoc
carnosum 4010. Res Microbiol 166(6):494–503
60. Cintas LM, Rodriguez JM, Fernandez MF, Sletten K, Nes IF,
Hernandez PE, Holo H (1995) Isolation and characterization of
pediocin L50, a new bacteriocin from Pediococcus acidilactici
with a broad inhibitory spectrum. Appl Environ Microbiol
61(7):2643–2648
61. Castellano P, Belfiore C, Fadda S, Vignolo G (2008) A review of
bacteriocinogenic lactic acid bacteria used as bioprotective cul-
tures in fresh meat produced in Argentina. Meat Sci 79(3):483–
499
62. Quadri L, Sailer M, Roy KL, Vederas JC, Stiles ME (1994)
Chemical and genetic characterization of bacteriocins produced
by Carnobacterium piscicola LV17B. J Biol Chem 269(16):
12204–12211
63. Cintas LM, Casaus P, Håvarstein LS, Hernandez PE, Nes IF
(1997) Biochemical and genetic characterization of enterocin P,
a novel sec-dependent bacteriocin from Enterococcus faecium
P13 with a broad antimicrobial spectrum. Appl Environ
Microbiol 63(11):4321–4330
64. Sabia C, Manicardi G, Messi P, De Niederhäusern S, Bondi M
(2002) Enterocin 416K1, an antilisterial bacteriocin produced by
Enterococcus casseliflavus IM 416K1 isolated from Italian sau-
sages. Int J Food Microbiol 75(1):163–170
65. Sparo M, Nuñez G, Castro M, Calcagno M, Allende MG, Ceci M,
Najle R, Manghi M (2008) Characteristics of an environmental
strain, Enterococcus faecalis CECT7121, and its effects as addi-
tive on craft dry-fermented sausages. Food Microbiol 25(4):607–
615
66. Castellano P, Vignolo G (2006) Inhibition of Listeria innocua and
Brochothrix thermosphacta in vacuum-packaged meat by addition
of bacteriocinogenic Lactobacillus curvatus CRL705 and its bac-
teriocins. Lett Appl Microbiol 43(2):194–199
67. Aymerich T, Artigas M, Garriga M, Monfort J, Hugas M (2000)
Effect of sausage ingredients and additives on the production of
enterocin A and B by Enterococcus faecium CTC492.
Optimization of in vitro production and anti-listerial effect in dry
fermented sausages. J Appl Microbiol 88(4):686–694
68. Alahakoon AU, Jayasena DD, Ramachandra S, Jo C (2015)
Alternatives to nitrite in processed meat: up to date. Trends
Food Sci Technol 45(1):37–49
69. Jayasena DD, Jo C (2013) Essential oils as potential antimicrobial
agents in meat and meat products: a review. Trends Food Sci
Technol 34(2):96–108
70. Chen C-M, Sebranek J, Dickson J, Mendonca A (2004)
Combining pediocin (ALTA 2341) with postpackaging thermal
pasteurization for control of Listeria monocytogenes on frank-
furters. J Food Prot 67(9):1855–1865
71. O’Connor E, Roos R, Hill C (2007) Application of bacteriocins in
food industry. Norfolk: Bacteriocins current research and applica-
tions:153–176
72. Pawar D, Malik S, Bhilegaonkar K, Barbuddhe S (2000) Effect of
nisin and its combination with sodium chloride on the survival of
Listeria monocytogenes added to raw buffalo meat mince. Meat
Sci 56(3):215–219
73. Reunanen J, Saris P (2004) Bioassay for nisin in sausage; a shelf
life study of nisin in cooked sausage. Meat Sci 66(3):515–518
74. Paik H-D, Kim H-J, Nam K-J, Kim C-J, Lee S-E, Lee D-S (2006)
Effect of nisin on the storage of sous vide processed Korean sea-
soned beef. Food Control 17(12):994–1000
75. Karina P, Julio C, Leda G, Noemi Z (2011) Behavior of Listeria
monocytogenes type1 355/98 (85) in meat emulsions as affected
by temperature, pH, water activity, fat and microbial preservatives.
Food Control 22(10):1573–1581
76. Mohamed HM, Elnawawi FA, Yousef AE (2011) Nisin treatment
to enhance the efficacy of gamma radiation against Listeria
monocytogenes on meat. J Food Prot 74(2):193–199
77. Kalschne DL, Geitenes S, Veit MR, Sarmento CM, Colla E (2014)
Growth inhibition of lactic acid bacteria in ham by nisin: a model
approach. Meat Sci 98(4):744–752
78. Tu L, Mustapha A (2002) Reduction of Brochothrix
thermosphacta and Salmonella serotype Typhimurium on
vacuum-packaged fresh beef treated with nisin and nisin com-
bined with EDTA. J Food Sci 67(1):302–306
79. Wijnker J, Weerts E, Breukink E, Houben J, Lipman L (2011)
Reduction of Clostridium sporogenes spore outgrowth in natural
sausage casings using nisin. Food Microbiol 28(5):974–979
80. Ghabraie M, Vu KD, Tnani S, Lacroix M (2016) Antibacterial
effects of 16 formulations and irradiation against Clostridium
sporogenes in a sausage model. Food Control 63:21–27
81. Khan A, Gallah H, Riedl B, Bouchard J, Safrany A, Lacroix M
(2016) Genipin cross-linked antimicrobial nanocomposite films
and gamma irradiation to prevent the surface growth of bacteria
in fresh meats. Innovative Food Sci Emerg Technol 35:96–102
82. Pattanayaiying R, Aran H, Cutter CN (2015) Incorporation of
nisin Z and lauric arginate into pullulan films to inhibit foodborne
pathogens associated with fresh and ready-to-eat muscle foods. Int
J Food Microbiol 207:77–82
83. Rose N, Sporns P, Stiles M, McMullen L (1999) Inactivation of
nisin by glutathione in fresh meat. J Food Sci 64(5):759–762
84. Deegan LH, Cotter PD, Hill C, Ross P (2006) Bacteriocins: bio-
logical tools for bio-preservation and shelf-life extension. Int
Dairy J 16(9):1058–1071
85. Davies EA, Milne CF, Bevis HE, Potter RW, Harris JM, Williams
GC, Thomas LV, Delves-Broughton J (1999) Effective use of nisin
to control lactic acid bacterial spoilage in vacuum-packed bolo-
gna-type sausage. J Food Prot 62(9):1004–1010
86. Ravyts F, Barbuti S, Frustoli MA, Parolari G, Saccani G, De Vuyst
L, Leroy F (2008) Competitiveness and antibacterial potential of
bacteriocin-producing starter cultures in different types of
fermented sausages. J Food Prot 71(9):1817–1827
87. Van Wezemael L, Verbeke W, Kügler JO, Scholderer J (2011)
European consumer acceptance of safety—improving interven-
tions in the beef chain. Food Control 22(11):1776–1784
88. Gálvez A, Abriouel H, López RL, Omar NB (2007) Bacteriocin-
based strategies for food biopreservation. Int J Food Microbiol
120(1):51–70
89. Aasen IM, Markussen S, Møretrø T, Katla T, Axelsson L,
Naterstad K (2003) Interactions of the bacteriocins sakacin P
and nisin with food constituents. Int J Food Microbiol 87(1):35–
43
90. Dicks LMT, Mellett F, Hoffman L (2004) Use of bacteriocin-
producing starter cultures of Lactobacillus plantarum and
Lactobacillus curvatus in production of ostrich meat salami.
Meat Sci 66(3):703–708
91. Todorov SD, Koep K, Van Reenen C, Hoffman L, Slinde E, Dicks
LMT (2007) Production of salami from beef, horse, mutton,
Blesbok (Damaliscus dorcas phillipsi) and Springbok
(Antidorcas marsupialis) with bacteriocinogenic strains of
Lactobacillus plantarum and Lactobacillus curvatus. Meat Sci
77(3):405–412
92. Kingcha Y, Tosukhowong A, Zendo T, Roytrakul S, Luxananil P,
Chareonpornsook K, Valyasevi R, Sonomoto K, Visessanguan W

(2012) Anti-listeria activity of Pediococcus pentosaceus BCC
3772 and application as starter culture for Nham, a traditional
fermented pork sausage. Food Control 25(1):190–196
93. Budde BB, Hornbæk T, Jacobsen T, Barkholt V, Koch AG (2003)
Leuconostoc carnosum 4010 has the potential for use as a protec-
tive culture for vacuum-packed meats: culture isolation, bacterio-
cin identification, and meat application experiments. Int J Food
Microbiol 83(2):171–184
94. Castellano P, González C, Carduza F, Vignolo G (2010) Protective
action of Lactobacillus curvatus CRL705 on vacuum-packaged
raw beef. Effect on sensory and structural characteristics. Meat
Sci 85(3):394–401
95. Kouakou P, Ghalfi H, Destain J, Duboisdauphin R, Evrard P,
Thonart P (2008) Enhancing the antilisterial effect of
Lactobacillus curvatus CWBI-B28 in pork meat and cocultures
by limiting bacteriocin degradation. Meat Sci 80(3):640–648
96. Jacobsen T, Budde B, Koch A (2003) Application of Leuconostoc
carnosum for biopreservation of cooked meat products. J Appl
Microbiol 95(2):242–249
97. Favaro L, Penna ALB, Todorov SD (2015) Bacteriocinogenic
LAB from cheeses—application in biopreservation? Trends
Food Sci Technol 41(1):37–48
98. Muthukumarasamy P, Holley RA (2006) Microbiological and sen-
sory quality of dry fermented sausages containing alginate-
microencapsulated Lactobacillus reuteri. Int J Food Microbiol
111(2):164–169
99. Barbosa MS, Todorov SD, Jurkiewicz CH, Franco BDGM (2015)
Bacteriocin production by Lactobacillus curvatus MBSa2
entrapped in calcium alginate during ripening of salami for control
of Listeria monocytogenes. Food Control 47:147–153
100. Aymerich T, Garriga M, Ylla J, Vallier J, Monfort J, Hugas M
(2000) Application of enterocins as biopreservatives against
Listeria innocua in meat products. J Food Prot 63(6):721–726
101. Nieto-Lozano JC, Reguera-Useros JI, Peláez-Martínez MC, de la
Torre AH (2006) Effect of a bacteriocin produced by Pediococcus
acidilactici against Listeria monocytogenes and Clostridium
perfringens on Spanish raw meat. Meat Sci 72(1):57–61
102. Mattila K, Saris P, Työppönen S (2003) Survival of Listeria
monocytogenes on sliced cooked sausage after treatment with
pediocin AcH. Int J Food Microbiol 89(2):281–286
103. Murray M, Richard JA (1997) Comparative study of the
antilisterial activity of nisin A and pediocin AcH in fresh ground
pork stored aerobically at 5°C. J Food Prot 60(12):1534–1540
104. Zhang J, Liu G, Li P, Qu Y (2010) Pentocin 31-1, a novel meat-
borne bacteriocin and its application as biopreservative in chill-
stored tray-packaged pork meat. Food Control 21(2):198–202
105. Ananou S, Garriga M, Jofré A, Aymerich T, Gálvez A, Maqueda
M, Martínez-Bueno M, Valdivia E (2010) Combined effect of
enterocin AS-48 and high hydrostatic pressure to control food-
borne pathogens inoculated in low acid fermented sausages.
Meat Sci 84(4):594–600
106. Turgis M, Stotz V, Dupont C, Salmieri S, Khan RA, Lacroix M
(2012) Elimination of Listeria monocytogenes in sausage meat by
combination treatment: radiation and radiation-resistant bacterio-
cins. Radiat Phys Chem 81(8):1185–1188
107. Rivas FP, Castro MP, Vallejo M, Marguet E, Campos CA (2014)
Sakacin Q produced by Lactobacillus curvatus ACU-1: function-
ality characterization and antilisterial activity on cooked meat sur-
face. Meat Sci 97(4):475–479
108. Barbosa M, Todorov SD, Ivanova I, Chobert J-M, Haertlé T,
Franco BDGM (2015) Improving safety of salami by application
of bacteriocins produced by an autochthonous Lactobacillus
curvatus isolate. Food Microbiol 46:254–262
109. El-Ziney M, Van Den Tempel T, Debevere J, Jakobsen M (1999)
Application of reuterin produced by Lactobacillus reuteri 12002
Probiotics & Antimicro. Prot.
for meat decontamination and preservation. J Food Prot 62(3):
257–261
110. Koo OK, Kim SM, Kang S-H (2015) Antimicrobial potential of
Leuconostoc species against E. coli O157: H7 in ground meat. J
Korean Soc Appl Biological Chem 58(6):831–838
111. Campos C, Castro M, Rivas F, Schelegueda L (2013) Bacteriocins
in food: evaluation of the factors affecting their effectiveness. In:
Méndez-Vilas A (ed) Microbial pathogens and strategies for com-
bating them: sciences, technology and education. Formatex,
Badajoz, pp 994–1004
112. Chung K-T, Dickson JS, Crouse JD (1989) Effects of nisin on
growth of bacteria attached to meat. Appl Environ Microbiol
55(6):1329–1333
113. Rayman K, Malik N, Hurst A (1983) Failure of nisin to inhibit
outgrowth of Clostridium botulinum in a model cured meat sys-
tem. Appl Environ Microbiol 46(6):1450–1452
114. Junttila J, Hirn J, Hill P, Nurmi E (1989) Effect of different levels
of nitrite and nitrate on the survival of Listeria monocytogenes
during the manufacture of fermented sausage. J Food Prot 52(3):
158–161
115. Chumchalová J, Josephsen J, Plocková M (1998) The antimicro-
bial activity of acidocin CH5 in MRS broth and milk with added
NaCl, NaNO3 and lysozyme. Int J Food Microbiol 43(1):33–38
116. Nilsen T, Nes IF, Holo H (1998) An exported inducer peptide
regulates bacteriocin production in Enterococcus faecium
CTC492. J Bacteriol 180(7):1848–1854
117. Schillinger U, Kaya M, Lücke FK (1991) Behaviour of Listeria
monocytogenes in meat and its control by a bacteriocin-producing
strain of Lactobacillus sake. J Appl Bacteriol 70(6):473–478
118. Zhu M, Du M, Cordray J, Ahn DU (2005) Control of Listeria
monocytogenes contamination in ready-to-eat meat products.
Compr Rev Food Sci Food Saf 4(2):34–42
119. Schirru S, Favaro L, Mangia NP, Basaglia M, Casella S,
Comunian R, Fancello F, Franco BDGM, de Souza Oliveira RP,
Todorov SD (2014) Comparison of bacteriocins production from
Enterococcus faecium strains in cheese whey and optimised com-
mercial MRS medium. Ann Microbiol 64(1):321–331
120. Todorov SD (2008) Bacteriocin production by Lactobacillus
plantarum AMA-K isolated from Amasi, a Zimbabwean
fermented milk product and study of the adsorption of bacteriocin
AMA-K to Listeria sp. Braz J Microbiol 39(1):178–187
121. Ünlü G, Nielsen B, Ionita C (2015) Production of antilisterial
bacteriocins from lactic acid bacteria in dairy-based media: a com-
parative study. Probiotics Antimicrobial Proteins 7(4):259–274
122. Todorov SD, Wachsman M, Tomé E, Dousset X, Destro MT,
Dicks LMT, Franco BDGM, Vaz-Velho M, Drider D (2010)
Characterisation of an antiviral pediocin-like bacteriocin produced
by Enterococcus faecium. Food Microbiol 27(7):869–879
123. Jones E, Salin V, Williams GW (2005) Nisin and the market for
commercial bacteriocins. Consumer and Product Research CP-01-
05, Texas Agribusiness Market Research Center, Texas A&M
University, College Station, Tex, USA
124. Bali V, Panesar PS, Bera MB (2016) Trends in utilization of agro-
industrial byproducts for production of bacteriocins and their
biopreservative applications. Crit Rev Biotechnol 36(2):204–214
125. Romanelli MG, Povolo S, Favaro L, Fontana F, Basaglia M,
Casella S (2014) Engineering Delftia acidovorans DSM39 to pro-
duce polyhydroxyalkanoates from slaughterhouse waste. Int J
Biol Macromol 71:21–27
126. Koutinas AA, Vlysidis A, Pleissner D, Kopsahelis N, Garcia IL,
Kookos IK, Papanikolaou S, Kwan TH, Lin CSK (2014)
Valorization of industrial waste and by-product streams via fer-
mentation for the production of chemicals and biopolymers.
Chem Soc Rev 43(8):2587–2627
127. Cripwell R, Favaro L, Rose SH, Basaglia M, Cagnin L, Casella S,
van Zyl W (2015) Utilisation of wheat bran as a substrate for
Probiotics & Antimicro. Prot.
bioethanol production using recombinant cellulases and amylolyt-
ic yeast. Appl Energy 160:610–617
128. Shah A, Favaro L, Alibardi L, Cagnin L, Sandon A, Cossu R,
Casella S, Basaglia M (2016) Bacillus sp. strains to produce bio-
hydrogen from the organic fraction of municipal solid waste. Appl
Energy 176:116–124
129. Tsapekos P, Kougias P, Treu L, Campanaro S, Angelidaki I (2017)
Process performance and comparative metagenomic analysis dur-
ing co-digestion of manure and lignocellulosic biomass for biogas
production. Appl Energy 185:126–135
130. Alibardi L, Favaro L, Lavagnolo MC, Basaglia M, Casella S
(2012) Effects of heat treatment on microbial communities of
granular sludge for biological hydrogen production. Water Sci
Technol 66(7):1483–1490
131. Alibardi L, Green K, Favaro L, Vale P, Soares A, Cartmell E,
Bajon Fernandez Y (2017) Performance and stability of sewage
sludge digestion under CO2 enrichment: a pilot study. Bioresour
Technol. https://doi.org/10.1016/j.biortech.2017.08.071
132. Favaro L, Cagnin L, Basaglia M, Pizzocchero V, van Zyl WH,
Casella S (2017) Production of bioethanol from multiple waste
streams of rice milling. Bioresour Technol 244:151–159
133. Chikindas ML, Weeks R, Drider D, Chistyakov VA, Dicks LM
(2018) Functions and emerging applications of bacteriocins. Curr
Opin Biotechnol 49:23–28
134. O’Shea EF, O’Connor PM, Cotter PD, Ross RP, Hill C (2010)
Synthesis of trypsin-resistant variants of the Listeria-active bacte-
riocin salivaricin P. Appl Environ Microbiol 76(16):5356–5362
135. Carmona-Ribeiro AM, de Melo Carrasco LD (2014) Novel for-
mulations for antimicrobial peptides. Int J Mol Sci 15(10):18040–
18083
136. de Abreu LCL, Todaro V, Sathler PC, da Silva LCRP, do Carmo
FA, Costa CM, Toma HK, Castro HC, Rodrigues CR, de Sousa
VP (2016) Development and characterization of nisin nanoparti-
cles as potential alternative for the recurrent vaginal candidiasis
treatment. AAPS PharmSciTech 17(6):1421–1427
137. Torres NI, Noll KS, Xu S, Li J, Huang Q, Sinko PJ, Wachsman
MB, Chikindas ML (2013) Safety, formulation and in vitro antivi-
ral activity of the antimicrobial peptide subtilosin against herpes
simplex virus type 1. Probiotics Antimicrobial Proteins 5(1):26–35
138. Healy B, Field D, O’Connor PM, Hill C, Cotter PD, Ross RP
(2013) Intensive mutagenesis of the nisin hinge leads to the ratio-
nal design of enhanced derivatives. PLoS One 8(11):e79563
139. Carroll J, Field D, O'connor PM, Cotter PD, Coffey A, Hill C,
O’Mahony J (2010) The gene encoded antimicrobial peptides, a
template for the design of novel anti-mycobacterial drugs.
Bioengineered Bugs 1(6):408–412
140. Jozala AF, De Andrade MS, De Arauz LJ, Pessoa A, Penna TCV
(2007) Nisin production utilizing skimmed milk aiming to reduce
process cost. Appl Biochem Biotechnol 137(1–12):515–528
141. Vaucher RA, Motta SA, Brandelli A (2010) Evaluation of the
in vitro cytotoxicity of the antimicrobial peptide P34. Cell Biol
Int 34(3):317–323
142. Carneiro B, Braga A, Batista M, Rahal P, Favaro L, Penna A,
Todorov S (2014) Lactobacillus plantarum ST202Ch and
Lactobacillus plantarum ST216Ch-what are the limitations for
application. J Nutritional Health Food Engineering 1(2):00010
143. Suwandecha T, Srichana T, Balekar N, Nakpheng T,
Pangsomboon K (2015) Novel antimicrobial peptide specifically
active against Porphyromonas gingivalis. Arch Microbiol 197(7):
899–909
144. Brogden KA (2005) Antimicrobial peptides: pore formers or met-
abolic inhibitors in bacteria? Nat Rev Microbiol 3(3):238–250
145. Das D, Goyal A (2014) Characterization of a noncytotoxic bacte-
riocin from probiotic Lactobacillus plantarum DM5 with potential
as a food preservative. Food Funct 5(10):2453–2462
146. Settanni L, Guarcello R, Gaglio R, Francesca N, Aleo A, Felis GE,
Moschetti G (2014) Production, stability, gene sequencing and in
situ anti-Listeria activity of mundticin KS expressed by three
Enterococcus mundtii strains. Food Control 35(1):311–322
147. Götz F, Perconti S, Popella P, Werner R, Schlag M (2014)
Epidermin and gallidermin: staphylococcal lantibiotics. Int J
Med Microbiol 304(1):63–71
148. Maher S, McClean S (2006) Investigation of the cytotoxicity of
eukaryotic and prokaryotic antimicrobial peptides in intestinal ep-
ithelial cells in vitro. Biochem Pharmacol 71(9):1289–1298
149. Martinez RCR, Wachsman M, Torres NI, LeBlanc JG, Todorov SD, de
Melo Franco BDG (2013) Biochemical, antimicrobial and molecular
characterization of a noncytotoxic bacteriocin produced by Lactobacillus
plantarum ST71KS. Food Microbiol 34(2):376–381
150. Todorov SD, Wachsman MB, Knoetze H, Meincken M, Dicks LM
(2005) An antibacterial and antiviral peptide produced by
Enterococcus mundtii ST4V isolated from soya beans. Int J
Antimicrob Agents 25(6):508–513
151. Fisher K, Phillips C (2009) The ecology, epidemiology and viru-
lence of Enterococcus. Microbiology 155(6):1749–1757
152. Rathnayake I, Hargreaves M, Huygens F (2012) Antibiotic resis-
tance and virulence traits in clinical and environmental
Enterococcus faecalis and Enterococcus faecium isolates. Syst
Appl Microbiol 35(5):326–333
153. Belgacem ZB, Abriouel H, Omar NB, Lucas R, Martínez-
Canamero M, Gálvez A, Manai M (2010) Antimicrobial activity,
safety aspects, and some technological properties of
bacteriocinogenic Enterococcus faecium from artisanal Tunisian
fermented meat. Food Control 21(4):462–470
154. Hendrickx AP, Willems RJ, Bonten MJ, van Schaik W (2009)
LPxTG surface proteins of enterococci. Trends Microbiol 17(9):
423–430
155. Todorov S, Franco B, Wiid I (2014) In vitro study of beneficial
properties and safety of lactic acid bacteria isolated from
Portuguese fermented meat products. Benefic Microbes 5(3):
351–366