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foods
Review
Lactic Acid Bacteria as Antimicrobial Agents: Food Safety and
Microbial Food Spoilage Prevention
Salam A. Ibrahim 1, * , Raphael D. Ayivi 1, Tahl Zimmerman 1, Shahida Anusha Siddiqui 2,3 ,
Ammar B. Altemimi 4, Hafize Fidan 5, Tuba Esatbeyoglu 6and Reza Vaseghi Bakhshayesh 7,8
Citation: Ibrahim, S.A.; Ayivi, R.D.;
Zimmerman, T.; Siddiqui, S.A.;
Altemimi, A.B.; Fidan, H.;
Esatbeyoglu, T.; Bakhshayesh, R.V.
Lactic Acid Bacteria as Antimicrobial
Agents: Food Safety and Microbial
Food Spoilage Prevention. Foods 2021,
10, 3131. https://doi.org/10.3390/
foods10123131
Academic Editors: Marios Mataragas,
Loulouda Bosnea and Eugenio Parente
Received: 28 October 2021
Accepted: 14 December 2021
Published: 17 December 2021
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Copyright: © 2021 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
1Food and Nutritional Sciences Program, North Carolina A&T State University, Greensboro, NC 27411, USA;
rdayivi@aggies.ncat.edu (R.D.A.); tzimmerman@ncat.edu (T.Z.)
2Department of Biotechnology and Sustainability, Technical University of Munich (TUM),
94315 Straubing, Germany; s.siddiqui@dil-ev.de
3DIL e.V.—German Institute of Food Technologies, 49610 D-Quakenbrück, Germany
4Department of Food Science, College of Agriculture, University of Basrah, Basrah 61004, Iraq;
ammaragr@siu.edu
5Department of Nutrition and Tourism, University of Food Technologies, 26 Maritza Blvd.,
40002 Plovdiv, Bulgaria; hfidan@abv.bg
6Institute of Food Science and Human Nutrition, Gottfried Wilhelm Leibniz University Hannover,
Am Kleinen Felde 30, 30167 Hannover, Germany; esatbeyoglu@lw.uni-hannover.de
7Department of Food Biotechnology, Branch for Northwest & West Region, Agricultural Biotechnology
Research Institute of Iran, Agricultural Research, Education and Extension Organization (AREEO),
Tabriz 5355179854, Iran; reza.vaseghi68@gmail.com
8Department of Food Science and Technology, University of Tabriz, Tabriz 5166616471, Iran
*Correspondence: ibrah001@ncat.edu
Abstract:
In the wake of continual foodborne disease outbreaks in recent years, it is critical to
focus on strategies that protect public health and reduce the incidence of foodborne pathogens and
spoilage microorganisms. Currently, there are limitations associated with conventional microbial
control methods, such as the use of chemical preservatives and heat treatments. For example, such
conventional treatments adversely impact the sensorial properties of food, resulting in undesirable
organoleptic characteristics. Moreover, the growing consumer advocacy for safe and healthy food
products, and the resultant paradigm shift toward clean labels, have caused an increased interest
in natural and effective antimicrobial alternatives. For instance, natural antimicrobial elements
synthesized by lactic acid bacteria (LAB) are generally inhibitory to pathogens and significantly
impede the action of food spoilage organisms. Bacteriocins and other LAB metabolites have been
commercially exploited for their antimicrobial properties and used in many applications in the dairy
industry to prevent the growth of undesirable microorganisms. In this review, we summarized the
natural antimicrobial compounds produced by LAB, with a specific focus on the mechanisms of action
and applications for microbial food spoilage prevention and disease control. In addition, we provide
support in the review for our recommendation for the application of LAB as a potential alternative
antimicrobial strategy for addressing the challenges posed by antibiotic resistance among pathogens.
Keywords:
antimicrobial; lactic acid bacteria (LAB); bacteriocin; biopreservation; foodborne pathogens
1. Introduction
Foodborne diseases and food spoilage organisms continue to exert negative impacts
on public health and the food industry. Foodborne disease outbreaks have resulted in a
high rate of mortality, along with the high financial burden stemming from healthcare costs.
Moreover, the soaring numbers of confirmed cases of foodborne illnesses are very alarming,
despite the availability of the hazard analysis and critical control point (HACCP) system.
The Council for Agricultural Science and Technology reported that 6.5–33 million cases
of human ailments were associated with food, with a reported fatality rate of 9000 cases
Foods 2021,10, 3131. https://doi.org/10.3390/foods10123131 https://www.mdpi.com/journal/foods
Foods 2021,10, 3131 2 of 13
annually in the U.S. (Food and Agriculture Organization) [
1
]. In the European Union,
the most common causes of foodborne infections are associated with the following bacte-
ria: Campylobacter jejuni,Listeria monocytogenes,Salmonella enterica,Escherichia coli,Listeria
monocytogenes, and Staphylococcus aureus, as well as viral pathogens, such as noroviruses
and rotaviruses [
2
]. Interestingly, most food groups, such as eggs, meat, dairy products,
fruits, vegetables, seafood, and poultry, cause outbreaks of foodborne diseases. According
to the World Health Organization (WHO), if drastic measures are not taken by 2050, the
global death rate from foodborne illnesses will increase to an estimated 10 million people
annually. Such global, prevailing foodborne infection rates thus warrant a systematic
approach for the elimination, prevention, and reduction in pathogenic bacteria in foods via
the application of novel antimicrobial agents [2].
Due to their high nutritional content, moisture, and neutral pH, animal-derived foods
are highly perishable. The processing of food using appropriate methods is critical to
preserving food quality and maintaining safety. Applicable preservation methods for
foods include low-temperature preservation methods, such as refrigeration and freezing
techniques, and high-temperature preservation methods, such as pasteurization, steril-
ization, and chemical preservation [
3
–
6
]. However, because chemical preservatives are
either proscribed or not accepted by consumers, there has been an increase in usage of
biological preservatives for the enhancement of food safety and food quality. For exam-
ple, biopreservation using natural microflora, such as lactic acid bacteria (LAB), has been
recommended in lieu of the conventional use of chemical preservatives. Microbiota are
safer, promote nutritional enhancement, and are considered to be clean label additives [
7
].
Biopreservation has received special attention among alternative food storage technolo-
gies. Biopreservation promotes shelf-life extension and consequently improving hygienic
consistency, without negatively impacting the organoleptic characteristics and nutritional
properties of perishable foods [7].
Numerous fermented foods naturally contain lactic acid bacteria (LAB) and bacte-
riocins, with LAB acting as a natural, vital biopreservative agent. Moreover, some LAB
have produce important metabolites, such as reuterin, bacteriocins, diacetyl, reutericyclin,
organic acids, acetoin, and hydrogen peroxide, which are highly potent biopreservative
agents [
8
]. Most LAB inhibit the growth of some foodborne pathogens and spoilage mi-
croorganisms. Bacteriocins constitute a diverse group of antimicrobial peptides that are
ribosomally synthesised and can destroy closely related microbial strains. Bacteriocins to
inhibit a variety of pathogenic bacteria in several food matrices, such as in vegetables, meat,
and cheese [
2
,
9
]. Ye et al. (2021) [
2
] demonstrated that a novel bacteriocin produced by
Lacticaseibacillus paracasei ZFM54 had a broad-spectrum inhibitory action against targeted
foodborne pathogens, such as Listeria monocytogenes,Micrococcus luteus, and Salmonella
typhimurium, through pore formation in the cell membrane. The 1–3.3 KDa bacteriocin
produced by Lacticaseibacillus rhamnosus 1.0320 demonstrated antimicrobial action against
Gram-negative and Gram-positive bacteria by several mechanisms. These antimicrobial
mechanisms include an increase in cell membrane permeability, pore formation on the
surface of cell membranes, a change in transmembrane pH gradient, dissipation of the
cytoplasmic membrane potential, and the destruction of cell membrane integrity. The
consequence of these processes is cell content loss and eventually cell death. However, the
mechanisms of the actions of other bacteriocins are still unclear [2].
This review thus aims to enhance the current knowledge about the antibacterial
activity of LAB strains and potential use of bacteriocins for future applications, primarily in
the dairy industry. The methodology employed in this review included literature searches
conducted in PubMed, Web of Science, Web of Knowledge, Scopus, and Google Scholar
that were relevant to the subject of antimicrobial properties of LAB. No range of years was
specified; however, only peer-reviewed papers were considered for inclusion in this review.
Foods 2021,10, 3131 3 of 13
2. The Microbial Ecosystem
The microbial ecosystem is uniquely balanced with diverse microorganisms interact-
ing with each other, which ultimately influences other microorganisms in the population.
The ecological system of microbes includes several host–pathogen interactions, namely
predation, commensalism, synergism, parasitism, inhibition, and competition with food [
3
].
In recent decades, the meat and dairy industries have employed LAB as starter cultures in
many applications. In the food industry, strains of both homofermentative and heterofer-
mentative bacteria are used with strictly defined properties and cultivation conditions for
the production of yogurt, sour cream butter, various types of cheese, and fermented bever-
ages. Mixed cultures in food typically comprise of a consortium of microorganisms that
interact with one another, thereby enhancing their metabolic activity to produce desirable
outcomes on product quality and safety.
Microbial growth is also impacted by several environmental factors. Some microorgan-
isms have symbiotic interactions with each other. For example, one type of microorganism
could synthesize chemical compounds that serve as an important primary resource for
another microorganism to metabolize. This relationship is generally termed as a symbiotic
interaction. This growth is usually found in food matrices that contain two or more mi-
crobes. Another example of an interaction between microorganisms is observed when two
or more microbial types have hindered growth as a result of their interaction [
4
]. Microor-
ganisms do not exist as pure cultures. Their physiological structures are determine by a
complex interaction of ecological and environmental factors that exist between members in
a diverse taxonomical community. Mixed cultures are fundamentally used for studying
microbial interactions. A classic example uses mixed microbial isolates for population
dynamic studies, such as mutualism and competition. Recently, synthetically mixed cul-
tures were verified for specific characteristics and functions, such as biofuel generation
and bioremediation, and these are useful for industrial applications. Mixed culture studies,
which offer much evidence-based information linked to cultivation of microbial mixtures,
are an excellent focal point for studying various biochemical interactions and ecological
transformations looking for, and globally cultivating, these untreated microorganisms [
4
,
5
].
Sieuwerts et al. (2018) [
6
] studied the presence of mutualistic symbiotic interactions be-
tween Lactiplantibacillus plantarum,Lactobacillus sanfranciscensis, and Saccharomyces cerevisiae
in sourdough fermentation, hypothesizing that the consumption of lactic acid by S. cere-
visiae, or the growth stimulatory action of yeast, resulted in de-acidification of the growth
medium, thereby leading to the growth of L. sanfranciscensis. As a result of their analysis,
it was evident during the pre-fermentation stages that the carbon dioxide produced by S.
cerevisiae and the use of oxygen led to an increase in the activity of L. sanfranciscensis in
MRS (De Man, Rogosa, and Sharpe) agar. Another important indicator was the stimulation
of L. sanfranciscensis, that was also observed in the process of dough fermentation. The
stimulation was not explained by the deacidification of the agar plate, so it must have been
a result of the vitamins provided by S. cerevisiae. The co-culturing of L. sanfranciscensis
and S. cerevisiae was shown to enhance fermentation due to the consumption of lactic acid
by yeast in the dough environment, which ultimately stimulated the growth of LAB in
the sourdough, thereby drastically slowing down the rate of acidification. On the other
hand, S. cerevisiae could only stimulate L. plantarum only when specific carbon sources,
such as lactose, glucose, and fructose, but not sucrose, galactose, starch, and maltose, were
available [6].
3. LAB Affect the Growth of Microorganisms
The overall objective of shelf-life extension is to keep food products safe and stable,
and this could generally be achieved by controlling the growth of spoilage microorganisms
and pathogenic bacteria. In addressing and controlling pathogenic growth, an antimicrobial
agent, such as nisin, or two or more antimicrobial agents could be employed synergistically
against the target organism. This concerted action is effective, as an individual agent may
fail to completely prevent the growth of the target microorganism. It is noteworthy that
Foods 2021,10, 3131 4 of 13
the action of these antimicrobial agents does not negatively impact the nutritional and
sensorial qualities of foods, thereby preserving their physicochemical structure. LAB are
beneficial when added to food because they are able to: (1) prevent the growth of harmful
enteric pathogens, (2) supply enzymes, (3) eliminate toxic food elements in the intestine,
(4) promote immunomodulatory action stimulate the immune system, and (5) enhance the
peristaltic action of the gastrointestinal tract [5].
Antagonistic activity against intestinal and food pathogens is an essential part of
the probiotic properties of LAB, and antimicrobial activity is a sought after quality in
selecting strains. LAB possess antimicrobial properties that target fungi and several Gram-
negative and Gram-positive bacteria [
6
], and are therefore important for the fermentation,
preservation, and storage of food. The antimicrobial properties of LAB strains are mediated
by the antimicrobial molecules produced by these strains. These antimicrobials can be
divided into three primary groups: (a) peptidic or proteinacious bacteriocins; (b) organic
acids (butyric acetic acids and lactic acid); (c) other small molecules, for example diacetyl,
hydrogen peroxide, acetaldehyde, acetoine, reuterin, and reutericyclin [
7
]. These are
elaborated as follows:
(a) Bacteriocins are antimicrobial peptides generated from various types of bacteria,
including LAB [
8
]. Bacteriocins are generally active against strains closely related to the
producing strain although there are examples of broader spectrum bacteriocins [
9
]. LAB-
produced bacteriocins are considered ideal for use with food for the following reasons:
(1) LAB byproducts are categorized by the FDA as GRAS (generally recognized as safe) [
10
];
(2) they are odorless and colorless; (3) they do not impact the organoleptic and sensorial
characteristics of food; (4) unlike traditional antibiotics, bacteriocins are cleared by the
digestive system by proteolytic enzymes [
11
]. In addition, bacteriocins have the potential
to be bioengineered for improved performance [11].
There are two major classes of bacteriocins. Class I bacteriocins, such as lactoccocin,
function primarily by inhibiting peptidoglycan synthesis. Class II bacteriocins, such as nisin,
function by destabilizing the cytoplasmic membrane, via the creation of pores [
12
]. With
the latter, bacteriocin molecules are absorbed on the membrane surface and form transient
pores. This leads to the loss of proton motive force, which alters the permeability of the
membrane causing leakage of small nutrient molecules into the surrounding environment,
a process which kills the cells. In addition, some bacteriocins function as lysin [
13
], which
degrades the bacterial cell wall, typically composed of peptidoglycan, thus leading to
cell lysis.
Many studies reported the inhibitory effects of diverse LAB bacteriocins against a
wide variety of food pathogens. For example, the lactobacillin bacteriocin XH1 inhibits
the proliferation of Staphylococcus aureus and Escherichia coli [
14
], and plantaricin P1053
(produced by L. plantarum PBS067) demonstrates a broad-spectrum antimicrobial activity
against Gram-negative bacteria, such as E. coli, and the Gram-positive S. aureus. Bacteriocins
are powerful and promising antimicrobials. Therefore, bacteriocin-producing LAB are
promising strains for use in food safety applications. Nevertheless, despite their promise,
the only LAB bacteriocin that has been approved for use in food by the FDA is nisin [
15
].
However, many other bacteriocins are being developed for use in food (Table 1).
(b) LAB produce different organic acids that have non-specific antimicrobial effects
(Table 2). For example, organic acids, such as acetic acid, propionic acid, and lactic acid,
are synthesized by some species of Acetobacter aceti,Propionibacterium, and Lactobacillus,
respectively. Other typical organic acids produced by LAB are formate and succinate.
Organic acids are attractive because they impede the growth of Gram-negative and Gram-
positive bacteria, as well as yeast and molds in several food products. Furthermore, organic
acids are generally regarded as safe for human use. Organic acids have antimicrobial
properties, and this property has been attributed to dissociated molecules that are depro-
tonated upon entry into cellular membranes. Another cause of the antimicrobial action
of LAB is generally organic acids and this could be due to the concerted effect of both
dissociated ions and undissociated molecules, that result in cellular injury. LAB strains are
Foods 2021,10, 3131 5 of 13
very promising for several food applications due to the synthesis of important metabolites,
such as organic acids.
Table 1. LAB bacteriocins and their food applications.
Bacteriocin Strain Food Applications Reference
Nisin Lactococcus lactis
Milk [16]
Lobster [17]
Trout [18]
Apple Cider [19]
Liquid Whey [20]
Lacticin Lactococcus lactis Milk [21]
Pork sausage [22]
Reuterin Limosilactobacillus reuteri Skim milk [23]
Gassericin Lactobacillus gasseri Custard Cream [24]
Lactococcin Lactococcus lactis Milk [25]
Enterocin Enteroccocus spp. Apple juice [19]
Ready to eat salad [26]
Table 2. Organic acids and their applications in foods.
Organic Acid Example of Prominent LAB Producer Example Food Pathogen
Application Application in Food
Lactic acid Lactobacillus delbrueckii subsp. bulgaricus [27]Pseudomonas spp. [28] Sliced Salmon [28]
Formic acid Lactococcus lactis subsp. cremoris [29]
Esherichia coli [30]
Listeria spp. [30]
Salmonella spp. [30]
Clostridium perfringens [31]
Poultry [30]
Animal Feed [30]
Pork [31]
Succinic acid Lactococcus lactis subsp. lactis [29]Salmonella spp. [30] Chicken meat [32]
Malic acid Limosilactobacillus reuteri [33]Staphylococcus [27,33] Meat products [33]
Propionic acid Lactococcus lactis subsp. lactis [29]Campylobacter spp. [34] Poultry Food [35]
Acetic acid Lactobacillus acidophilus [29]Pseudomonas spp. [28] Sliced Salmon [28]
Butyric Acid Lactobacillus acidophilus [29]Salmonella spp. [36] Poultry [36]
(c) Many other small molecules exhibiting antimicrobial effects, such as diacetyl,
hydrogen peroxide (H
2
O
2
), and reuterin, are produced by LAB (Table 3). For example,
Gram-positive and Gram-negative bacteria have been controlled by diacetyl. A highly
effective antimicrobial agent used synergistically with heat is hydrogen peroxide (H
2
O
2
).
The bactericidal action is more pronounce when it is combined with heat. The antimicrobial
mode of action is created by deactivating key enzymes, which results in a modification of
catalytic activity. This deactivation is a result of the dicarbonyl group of diacetyls reacting
with arginine in the enzymes [37–39].
Under aerobic conditions, LAB synthesize hydrogen peroxide (H
2
O
2
) in the absence
of intracellular catalase, pseudocatalase, or peroxidase. H
2
O
2
has bacteriostatic activity,
and its mode of antimicrobial activity is enhanced in raw milk by the stimulation of the
lactoperoxidase-thiocyanate system. In the presence of H
2
O
2
and lactoperoxidase enzymes
in raw milk, a hypothiocyanite anion is generated. This compound has the potential to
destroy cellular components in Gram-negative bacteria, such as the membrane proteins,
due to oxidation of the SH group. Reuterin is synthesized by some species of L. reuteri,
which are usually small antimicrobial molecules and possess antimicrobial properties
that inhibit several Gram-positive and Gram-negative bacteria. Reuterin inactivates key
Foods 2021,10, 3131 6 of 13
enzymes, such as ribonucleotide reductase. Reuterin is resistant to an array of lipolytic and
proteolytic enzymes in foods and has a broad working pH range [40,41].
Table 3. Antimicrobial compounds produced by LAB and examples of food pathogens and food application.
Small Molecules Example of Prominent LAB Producer Example of Food Pathogen
Application Application in Food
Hydrogen Peroxide Lactobacillus johnsonii [37]
Escherichia coli O157:H7 [38]
Salmonella enterica [38]
Listeria monocytogenes [38]
Lettuce [38]
Reuterin Limosilactobacillus reuteri [40]Campylobacter spp. [40]
Escherichia coli O157:H7 [41]Meat [40]
Diacetyl Streptococcus diacetyl lactis [42]Escherichia coli O157:H7 [43]
Salmonella typhimurium [43]Meat [43]
4. Prevention of Foodborne Pathogens and Elimination of Food Spoilage Bacteria
The causative agents of most reported foodborne illnesses include pathogenic bacteria,
such as Campylobacter jejuni,S. aureus,L. monocytogenes,E. coli, and Salmonella. spp. Con-
sumer demand for minimally processed foods has obiligated the food industry to search
for new methods of ensuring food safety. It can no longer rely on traditional heat treatment
methods to create microbiologically safe foods. Minimally processed foods, such as fresh
fruits and vegetables, have been shown to contain pathogenic bacteria. LAB may increase
the nutritional value of food and also support intestinal health through the production of
antimicrobial agents. There are many mechanisms for preventing foodborne pathogens
and eliminating food spoilage bacteria, such as producing antimicrobial substances that
can prevent adhesion of pathogens to epithelial and mucosal surfaces. One of the probiotic
mechanisms of action is the competition for adhesion sites [44].
LAB are used as bioprotective agents in fishery products. Wiernasz et al. (2017) [
1
]
evaluated the antimicrobial activity of LAB that impeded six common food spoilage bacte-
ria in seafood products (Brochothrixthermosphacta,Serratiaproteamaculans Shewanellabaltica,
Photobacteriumphosphoreum,Lactobacillus sakei, and Hafnia alvei) and one pathogenic bac-
terium (L. monocytogenes) in a co-culture inhibitory assay. An assessment of antimicrobial
and spoilage activity, conducted in salmon and cod juice, elucidated strain-specific sensory
and inhibition profiles [
1
]. LAB prevent the clinging of the pathogenic bacteria to their host
cells by strengthening the barrier effect of the intestinal mucosa. Another effect of LAB
is the influence of the microbial flora through the synthesis of antimicrobial compounds.
Several studies have reported the antimicrobial effects of LAB on foodborne pathogens
(Table 4).
LABs are also suitable for inhibiting fungi (molds) that are responsible for food
spoilage and mycotoxin production. LABs are endowed with bacteriocin-like substances
and produce organic acids that have characteristic fungistatic and fungicidal properties
and inhibit fungi and yeast, such as Aspergillus versicolor,Debaryomyces hansenii,Penicillium
expansum,Fusarium culmorum,Aspergillus fumigatus,Candida parapsilosis,Aspergillus niger,
and Penicillium chrysogenum [56].
Several genera of fungi such as Aspergillus,Fusarium,Penicillium,Alternaria, and Clav-
iceps spp. produce mycotoxins. Mycotoxins, such as aflatoxins, fumonisins, ochratoxin,
patulin, tricothecenes, and zearalenone, are produced as secondary metabolites. These
metabolites exhibit carcinogenic, teratogenic, immunotoxic, neurotoxic, hepatotoxic, and
nephrotoxic effects. Of the approximately 400 compounds identified as mycotoxins, 30 of
them are considered as problematic for the human health. Therefore, the control of myco-
toxin contamination is crucial, either by preventing their production or by detoxification.
Mycotoxin control becomes harder because conventional cooking processes cannot destroy
all of them. Consequently, food processing methods are needed to eliminate mycotoxins.
LABs (Lacticaseibacillus casei and Limosilactobacillus reuteri) are known effectively bind afla-
Foods 2021,10, 3131 7 of 13
toxins (AFs) in aqueous solutions. Therefore, the control of these microbes using LAB is a
natural method of food preservation [57].
Table 4. Inhibition of food pathogens by lactic acid bacteria.
Foodborne Pathogen Lactic Acid Bacteria Reference
Staphylococcus aureus
Lactococcus spp., Pediococcus spp., Lactobacillus spp., Weissella spp., and
Enterococcus spp.
Lactobacillus curvatus,Lactiplantibacillus plantarum,Lactobacillus sakei,Pediococcus
acidilactici, and Pediococcus pentosaceus (industrial products)
Levilactobacillus brevis,Lactobacillus coryniformis,Lactobacillusparacasei,Lactobacillus
paraplantarum,Leuconostoc mesenteroides, and Weisella halotolerans (traditional products)
Enterococcus faecium QPII, Lactiplantibacillus plantarum CC10, Lactiplantibacillus
plantarum TF711, Lacticaseibacillus rhamnosus IMC 501, Lacticaseibacillus paracasei IMC
502, Lactobacillus sakei KTU05-6, Lactobacillus helveticus KLDS 1.8701, Pediococcus
acidilactici KTU05-7, Pediococcus pentosaceus KTU05-8, KTU05-9, and KTU05-10
[45–50]
Listeria innocua
Lactobacillus curvatus,Lactiplantibacillus plantarum,Lactobacillus sakei,Levilactobacillus
brevis,Lactobacillus coryniformis,Lacticaseibacillus paracasei,Lactobacillus paraplantarum,
Leuconostoc mesenteroides,Pediococcus acidilactici, and Pediococcus pentosaceus (industrial
products), Weisella halotolerans (traditional products)
[45,47]
Escherichia coli
Lactobacillus curvatus,Lactiplantibacillusplantarum,Lactobacillus sakei,
Levilactobacillus brevis,Lactobacillus coryniformis,Lacticaseibacillus paracasei,Lactobacillus
paraplantarum,Lactobacillus helveticus KLDS 1.8701, Limosilactobacillus reuteri,
Leuconostoc mesenteroides,Pediococcus spp. Acidilactici,Pediococcus pentosaceus
(industrial products), Weisella halotolerans (traditional products)
[45,47,50,51]
Salmonella enteritidis Limosilactobacillus reuteri [45,50–52]
Salmonella typhimurium
Levilactobacillus brevis CM22, Lactobacillus helveticus KLDS 1.8701, Pediococcus
pentosaceus CM16
Salmonella cholerae Levilactobacillus brevis CM22, Lactobacillus helveticus KLDS 1.8701, Pediococcus
pentosaceus CM16 [45,50,52]
Bacillus cereus
Lactobacillus sakei KTU05-6, Lacticaseibacillus rhamnosus IMC 501, and Lacticaseibacillus
paracasei IMC 502, Lactiplantibacillus plantarum TF711, Pediococcus acidilactici KTU05-7,
Pediococcus pentosaceus KTU05-8, KTU05-9, and KTU05-10
[49,53]
Pseudomonas
Lactobacillus sakei KTU05-6, Lactobacillus curvatus,Lactiplantibacillus plantarum,
Levilactobacillus brevis,Lactobacillus coryniformis,Lacticaseibacillus paracasei,Lactobacillus
paraplantarum,Leuconostoc mesenteroides,Pediococcus acidilactici KTU05-7, Pediococcus
pentosaceus KTU05-8, KTU05-9, and KTU05-10, Weisella halotolerans
(traditional products)
[47]
Enterococcus faecium
DSM 13590
Lactobacillus sakei KTU05-6, Lacticaseibacillus rhamnosus IMC 501 and Lacticaseibacillus
paracasei IMC 502, Pediococcus acidilactici KTU05-7, Pediococcus pentosaceus KTU05-8,
KTU05-9, and KTU05-10
[46,47]
Listeria monocytogenes
Enterococcus faecium QPII, Lactobacillus sakei KTU05-6, Lacticaseibacillus rhamnosus IMC
501 and Lacticaseibacillus paracasei IMC 502,
Lactobacillus curvatus,Levilactobacillus brevis,Lactobacillus coryniformis,Lacticaseibacillus
paracasei,Lactobacillus paraplantarum,Lactiplantibacillus plantarum CC10, Lactobacillus
helveticus KLDS 1.8701, Limosilactobacillus reuteri,
Leuconostoc mesenteroides,Pediococcus acidilactici KTU05-7, Pediococcus pentosaceus
KTU05-8, KTU05-9, and KTU05-10, Weisella halotolerans (traditional products)
[46,48,50,54]
Clostridiumsporogenes Lactiplantibacillus plantarum TF711 [49]
Shigella sonnei Lactiplantibacillus plantarum TF711 [49]
Klebsiella pneumoniae Lactiplantibacillus plantarum TF711 [49]
Acinetobacter baumannii
Lactobacillus spp. [55]
Foods 2021,10, 3131 8 of 13
5. Bacteriocin-Antimicrobial Synergy
The exponential rate of increase in foodborne diseases and their impact on public
health warrants immediate action, such as the adoption of comprehensive surveillance
measures and the application of synergistic antimicrobial concepts. Thus, the synergistic
effect of bacteriocins in conjunction with various antimicrobial agents, such as organic acids,
phenolic compounds, essential oils, and chelating agents (for example, EDTA), have proven
to be highly effective and thus have been recommended by many authors, due to these
products’ extensive spectra of antimicrobial action [
58
,
59
]. Bacteriocins are considered
as great alternatives to the use of chemical preservatives in dairy products, due to the
fact that they are safe antimicrobial peptides. Most bacteriocin producers belong to LAB
and they do not pose any health risk concerns. Their mechanism of action is based on
their ability to target the cell membrane, DNA, or protein metabolism of the microbial
strain, whose function is distinct from those used by antibiotics. Besides, bacteriocins
can also be used in the dairy industry in order to enhance fermentation, accelerating
cheese ripening, and improve its flavor [
60
]. One recent technology approaching the
problem, that has gained attention and widespread use, is referred to as hurdle technology.
Hurdle technology developed as a result of the emergence of physical treatments, such
as pulsed electric field, modified atmosphere packaging, gamma irradiation, and heat
treatments, in combination with bacteriocins to control food spoilage and pathogenic
bacteria [
60
]. Thus, a major factor that should be considered with regard to the adoption
of bacteriocins in a hurdle technological approach is the food matrix and its inherent
microflora [
61
,
62
]. Bacteriocins, alone or combined with other treatments, may enhance
the microbiological safety and improve the sensory properties in dairy products. Several
studies have reported the effect of the hurdle technology in controlling pathogens [
63
].
For example, Sivarooban et al. (2008) [
64
] have shown that nisin blended with a grape
seed extract (GSE) or an extract from green tea (GTE) was effective in damaging targeted
cells of a strain of L. monocytogenes [
64
]. Both GSE and GTE contained purified phenolic
compounds (GSE: 0.02% catechin and 0.02% epicatechin; GTE: 0.02% epicatechin and
0.02% caffeic acid), respectively, and complemented the antimicrobial action of nisin [
64
].
Another study reported the effect of combining bacteriocins with chelating agents, such as
EDTA, whereby a complex of nisin–sodium–diacetate–EDTA and a combination of nisin–
potassium sorbate–EDTA were potent in decreasing the population of L. monocytogenes
on a shrimp sample containing the pathogen [
65
]. Other authors reported the inhibitory
activity of nisin of over 90% of L. monocytogenes in minimally processed ready-to-eat foods,
such as lettuce [66].
A study by Branen and Davidson (2004) [
67
] also confirmed the synergistic effect
of nisin and EDTA (at very low concentrations) that were highly effective against L.
monocytogenes [
67
]. Consequently, organic acids have been reported to be highly effec-
tive in combination with bacteriocins in controlling foodborne pathogens. According to
Moon et al. (2002) [68]
a bacteriocin from Pediococcus acidilactici K10 that was mixed with
succinic acid, lactic acid, and acetic acid was synergistically effective against target cells of
E. coli O157:H7
in vivo
and
in vitro
[
68
]. Moreover, the same bacteriocin from Pediococcus
acidilactici K10 mixed with 0.25% acetic acid and 0.35% lactic acid decreased the population
of E. coli O157:H7, inoculated in a ground beef sample [
68
]. Therefore, it is noteworthy
that a combination of organic acids with bacteriocins is a very promising alternative for
bio-preservatives [63].
6. Competitive Growth Interactions between LAB and Other Microorganisms
Microorganisms are encompassed by several strains and various species, resulting in
intense competition for limited nutrients in their niche. Microbes generally compete for
environmental nutrients in two ways. The first is through passive competition, namely ex-
ploitation, and the second is by severe competition. Species compete directly for resources,
with one species demonstrating higher consumption of resources and thus limiting the
other. The second type of competition is direct competition (interference competition),
Foods 2021,10, 3131 9 of 13
whereby individual cells harm each other by positioning themselves in a state to ward
off already established competitors or to entirely destroy competitors, as well as through
territorial colonization, especially in uninhabited areas. Many microorganisms are shielded
from environmental and microbial risks due to biofilm formation. Biofilms serve as protec-
tive barrier for microbial cells. Antimicrobial production is a classic example of competition,
whereby antimicrobial agents synthesized from distinct strain-specific bacteriocins have a
broad-spectrum effects [7,34].
Due to the growing demand from the food industry to meet the consumer needs of
long shelf-life foods that are safe to eat and able to maintain their nutritional and organolep-
tic qualities, research is increasingly focusing on the role of antimicrobial compounds
secreted by natural compounds (such as LAB) as a defense mechanism against intestinal
pathogens. LAB can inhibit harmful microorganisms through a competitive exclusion
mechanism, based on competition for binding sites and nutrients. Lactic acid bacteria
are used to produce fermented products, such as yogurt butter, cheese, kefir, sauerkraut,
buttermilk, brined vegetables, sourdough, soya curd, koumiss, idly batter, fermented meat
products, and beverages [
27
]. Several authors investigated the potential applications of
lactic microbiota in food products such as milk [
69
], yogurt [
70
], cheddar cheese [
71
],
gouda cheese [
72
], semi-hard Vidiago cheese [
73
], tenerife cheese [
5
], italian soft cheese [
74
],
greek feta cheese [
75
], camembert cheese [
76
], fresh meat [
77
], dry-fermented sausages [
78
],
fermented vegetable products [
79
], fermented vegetables, and fruit drinks [
80
] in order to
improve the products’ safety and quality while preventing pathogenic microorganisms.
In addition, among the outstanding benefits and contributions of lactic acid bacte-
ria, is their use as potential alternatives to antibiotics (in the fight against clinical and
subclinical infectious diseases) in the agricultural sector in poultry, pigs, ruminants, and
aquacultures [78].
For example, Adeyemo et al. [
81
] determined the antimicrobial substances produced
by LAB isolated from ‘pupuru’ (African traditional cassava food) against food borne
pathogens. They reported that four species were tested for antagonistic activity and L. plan-
tarum showed the highest zone of inhibition with respect to S. aureus and Pseudomonas aerug-
inosa, while the antimicrobial activity decreased with time. Additionally, Rahmeh et al. [
52
]
characterized the antimicrobial traits of LAB in raw camel milk. According to their findings,
Enterococcus,Lactococcus,Pediococcus genera, and bacteriocins obtained, exhibited inhibitory
activity against a broad spectrum of Gram-positive and Gram-negative bacteria, including
multi-drug-resistant Salmonella. Among them, Pediococcus pentosaceus CM16 and L. brevis
CM22 were selected for their strong bacteriocinogenic antilisterial activity. Carnobacterium
spp., Lactobacillus spp., Leuconostoc spp., Weissella spp., and Enterococcus spp. were the
genera isolated from ready-to-eat seafood (cold-smoked salmon, gravlax, and sushi). LAB
isolated from sushi demonstrated a significantly higher antimicrobial effect than LAB from
cold-smoked salmon and gravlax [82].
As a result of the quantitative evaluation of E. coli, LAB dairy starter culture, and S.
aureus, it became obvious that the LAB starter culture demonstrated the ability to induce
an early stationary phase of S. aureus and E. coli populations at varying temperatures (for
example, from 12 to 37
◦
C) and for the inocula of lactic acid bacteria (estimated at 10
3
to
106CFU/mL) [83].
L. lactis subsp. lactis NCK401, a LAB strain, was employed as a prototype system
in competition with L. monocytogenes F5069B, a pathogenic bacterium, in an extract from
vegetable broth. Results confirmed the minimum inhibitory concentration of lactic acid to
be 6.43 mM for L. monocytogenes in a medium of cucumber juice with a stable pH at 5.6 and
an ionic strength of 0.342. It was, however, observed that the growth limiting factor for
the mixed culture, as well as that of L. monocytogenes in the pure culture, was due to pH.
Consequently, the growth of the competing bacteria is highly impeded by lactic acid. The
inhibitory mechanism of lactic acid (an organic acid) has been explained to be due to the
protonated form of the acid that easily permeates and crosses cellular membranes, as they
carry no charged ions. Therefore, this results in the conglomeration of acid anions within
Foods 2021,10, 3131 10 of 13
the cell, leading to the acidification of the cytoplasm and ultimately setting off growth
inhibition [9].
7. Conclusions
Lactic acid bacteria (LAB) are utilized in the production of a number of fermented
foods that provide health benefits and can help to extend the shelf-life of food products.
LAB also produce natural antimicrobial compounds that improve the safety of food. For
example, LAB produce organic acids, such as lactic, acetic, and formic acids, which cause
a drop in pH and thereby inhibit the growth of foodborne pathogens. LAB also produce
several antimicrobial compounds, such as bacteriocins. Moreover, LAB are live microor-
ganisms that confer probiotic benefits in the human gastrointestinal tract. In the present
review, we discussed a wide range of LAB potential applications in different food products.
With regard to our findings in this review, future research should be directed toward novel
applications of LAB, including the isolation and selection of new strains. Moreover, the
selection of LAB strains with probiotic effects, such as those that produce essential fatty
acids, amino acids, vitamins, and functional enzymes (such as lactase), is of importance to
both the food industry and consumers. Such new strains can then be adapted for various
food applications. In addition, there is a need for the isolation of LAB that can produce
unique antimicrobial compounds with a wide range of inhibitory effects against pathogenic
microorganisms.
Author Contributions:
Conceptualization, S.A.I., R.D.A. and H.F.; formal analysis and investigation,
S.A.I., R.D.A. and H.F.; resources, S.A.I.; writing—original draft preparation, S.A.I., R.D.A., H.F., T.Z.,
S.A.S., A.B.A., T.E. and R.V.B.; writing—review and editing, S.A.I., R.D.A., H.F., T.Z., S.A.S., A.B.A.,
T.E. and R.V.B.; visualization, S.A.I., R.D.A., H.F., T.Z., S.A.S., A.B.A., T.E. and R.V.B.; supervision,
S.A.I.; project administration, S.A.I.; funding acquisition, S.A.I. All authors have read and agreed to
the published version of the manuscript.
Funding:
Grants or project numbers NC.X337-5-21-170-1 and NC.X341-5-21-170-1 from the National
Institute of Food and Agriculture (NIFA).
Institutional Review Board Statement:
This review article is not subject to the institutional
review process.
Informed Consent Statement: Not Applicable.
Data Availability Statement: No new data were created or analyzed in this study.
Acknowledgments:
This publication was made possible by grants or project numbers NC.X337-5-
21-170-1 and NC.X341-5-21-170-1 from the National Institute of Food and Agriculture (NIFA). Its
contents are solely the responsibility of the authors and do not necessarily represent the official views
of NIFA. The authors would also like to acknowledge the financial support of the Department of
Family and Consumer Sciences and the Agricultural Research Station at North Carolina Agricultural
and Technical State University (Greensboro, NC 27411, USA).
Conflicts of Interest: The authors declare no conflict of interest.
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