Food Reviews International, 31:147–171, 2015

Copyright © Taylor & Francis Group, LLC

ISSN: 8755-9129 print / 1525-6103 online
DOI: 10.1080/87559129.2014.981825

The Two Faces of Leuconostoc mesenteroides in Food

Systems

ALINE T. DE PAULA1, ANA BEATRIZ

JERONYMO-CENEVIVA1, SVETOSLAV D. TODOROV2,
AND ANA LÚCIA B. PENNA1
1
Department of Food Engineering and Technology, UNESP—Sao Paulo State
University, São José do Rio Preto, Brazil
2
Department of Food Science and Experimental Nutrition, Faculty of
Pharmaceutical Sciences, USP—São Paulo University, São Paulo, Brazil

Leuconostoc mesenteroides is a lactic acid bacterium (LAB) that has been isolated from
different sources. Some of its strains are able to produce bacteriocins, and most of them
belong to class IIa and shows anti-Listeria activity. Additionally, Lc. mesenteroides
species can be a probiotic candidate; promising studies have shown the potential of
this species to survive and grow under various stress conditions present in the gas-
trointestinal tract. On the other hand, this microorganism can cause spoilage in some
types of food matrices, and scarce reports have shown the pathogenic potential of this
species. In this review, we focus on an overview of Lc. mesenteroides bacteriocin-pro-
ducing strains and their probiotic potential, in contrast with Lc. mesenteroides spoilage
and pathogenic cases reported in the literature.

Keywords Bacteriocins, Biopreservation, Pathogenic, Probiotic, Spoilage

Introduction
Leuconostoc genus belongs to Firmicutes phylum, which includes gram-positive, het-
erofermentative (fermenting glucose to D-lactic acid, ethanol/acetic acid, and CO2 from
phosphoketolase pathway) microorganisms, and presents coccoid or rod-like shape. These
bacteria are usually presented in pairs or short chains, nonmotile, non–spore forming, cata-
lase negative, anaerobic facultative, and mesophilic and do not produce ammonia from
arginine. They display complex nutritional requirements, including different amino acids.
Furthermore, they exhibit absence of H2 S formation, growth in presence of 7% NaCl, and
low guanine-cytosine (GC) content on the DNA molecule (31–49%). These microorgan-
isms have mesophilic characteristics, with optimal growth between 20 and 30 ◦ C. Species
belonging to genus Leuconostoc (Lc. argentinum, Lc. carnosum, Lc. citreum, Lc. fallax, Lc.
ficulneum, Lc. fructosum, Lc. gasicomitatum, Lc. gelidum, Lc. inhae, Lc. kimchii, Lc. lactis,
Lc. mesenteroides, Lc. pseudomesenteroides) can be found mainly in vegetables, cereals,
silage, fruits, wine, fish, meat, and dairy products.(1−9) A significant review published by
Hemme and Foucaud-Scheunemann(3) presents an overview about Leuconostoc species,

Address correspondence to Ana Lúcia B. Penna, Department of Food Engineering and

Technology, UNESP—Sao Paulo State University, Rua Cristovão Colombo, 2265, 15.054-000, São
José do Rio Preto, Brazil. E-mail: analucia@ibilce.unesp.br

147
148 de Paula et al.

their habitat, taxonomy, metabolism, and genetics, their implications in health and safety,
and their potential use in dairy technology and functional foods.
Despite the recent studies that show many benefits attributed to lactic acid bacteria
(LAB), only a few reports about probiotic potential and bacteriocin applications using Lc.
mesenteroides species have been found in the literature. Moreover, Leuconostoc spp. has
a promising future for application in dairy foods as bacteriocinogenic and/or probiotic
microorganism through enhancement of physicochemical characteristics of these products,
mainly due to the production of organic acids, CO2 and volatile compounds, which con-
tribute to the flavor and texture of butter, cream, and cheeses. In this paper, we review the
potential of Lc. mesenteroides for application as a probiotic and bacteriocin-producing cul-
ture, in contrast with its relationship to spoilage process and pathogenic cases reported in
the literature.

Probiotic and Bacteriocinogenic Potential

Probiotics are defined as live, nonpathogenic microorganisms that, when administrated in
adequate amounts, confer a health benefit to the consumer.(10) The candidate strain to be
considered as a probiotic culture should be able to survive under the stressful conditions of
the gastrointestinal tract, be able to compete with, adhere to, and colonize the intestine cells,
present therapeutic benefits, be safe for application in food (be nonpathogenic, not present
virulence genes nor antibiotics resistance, and be genetically stable), and have adequate
technological features (viable during the storage period, bacteriophage resistant, production
in large scale). All of these properties should be validated and documented, and replicated
results, found by in vitro trials, should be confirmed by in vivo assays.(10–12)
There are a remarkable number of reports in the literature that describe various LAB
strains as potential probiotic cultures. Giraffa(2) presented a general overview of the main
criteria and methods that were considered important in the selection process of probiotic
strains, such as characterization of strain identity and taxonomy followed by selection
through validated in vitro and in vivo assays. However, several researchers limited their
studies to the in vitro assays because the list of criteria for a strain to be considered as a
probiotic is extensive and strict.
Nowadays, multiple studies in the literature describe countless benefits of probiotic
cultures; these include increase in the host’s immune response, alleviation of symptoms
of lactose intolerance, production of some vitamins, usefulness in the treatment of many
types of diarrhea, competition and inhibition of pathogenic microorganisms, production
of antibacterial components in the gastrointestinal tract (GIT) (e.g., bacteriocins, lactic
acid, hydrogen peroxide, and others), decrease of cholesterol levels, reduction of risk of
colon cancer, alleviation of allergic symptoms, suppression of the gastric infection caused
by Helicobacter pylori, improvement of oral health, influence on the course of critically
ill patients, and others.(12−16) However, some of these mechanisms by which probiotics
strains exert beneficial effects are largely unknown, not clearly understood, or unproven.
Additional information about infection control, disease treatment, and health benefits and
the characterization of antimicrobial compounds produced by LAB can be obtained in the
articles published by Amara and Shibl(14) and Reis and coworkers,(17) respectively.
Bacteriocins are an abundant and diverse group of ribosomally synthesized
antimicrobial peptides or proteins produced by bacteria and archaea that can be used as
biopreservatives in foods or be produced by LAB in the GIT, as a competitive factor.(18)
The production of bacteriocins by microorganisms, which can protect food against contam-
ination and/or prevent the growth of foodborne pathogens and spoilage microorganisms,
 Leuconostoc mesenteroides in Food Systems 149

has attracted the attention of food companies.(19) Moreover, the increased demand of con-
sumers for “bioproducts” with the addition of less chemical preservatives is drawing the
attention of food companies, which are searching for new biopreservatives compounds,
such as bacteriocins. In addition, the resistance to high temperatures, low pH, and organic
solvents, together with the fact that they are easily digested by human proteolytic enzymes,
makes them an interesting tool for application in food preservation.(19−21) However, since
the discovery of nisin, which is the only bacteriocin approved by Food and Agriculture
Organization/World Health Organization (FAO/WHO), US Food and Drug Agency (FDA),
and EU Directive,(22) the search for new successful bacteriocins, produced by LAB, is still
labor intensive.
Generally, bacteriocins are small cationic and amphipathic molecules, presenting α-
helix and/or β-sheet protein structures, which can aggregate when present in liquid media
or in high concentrations.(23) Bacteriocin production is common for LAB. Furthermore,
some characteristics seem to be common, such as (1) innate immunity to their own
bacteriocin, (2) resistance or sensitiveness to other bacteriocins, (3) production of more
than one antimicrobial compound, (4) the same bacteriocin can be produced by differ-
ent genus, and (5) the same subspecies can produce different compounds.(19,23) Details
about the biology of bacteriocins, their resistance, the molecular biology, and their appli-
cations were summarized by Cotter and coworkers.(19) In addition, the book Bacteriocins
Ecology and Evolution, edited by Riley and Chavan,(24) offers an extensive review about
the diversity of bacteriocins produced by gram-positive and gram-negative bacteria.
Different classifications of bacteriocins have been proposed in the last few years. They
are classified based on their structure, molecular weight and mode of action.(19,25) One
of the most accepted classifications was proposed by Klaenhammer,(26) which divides
bacteriocins in four classes: (I) lanthionine-containing bacteriocins, (II) non–lanthionine-
containing bacteriocins, (III) large heat-labile bacteriocins, and (IV) complex moiety
bacteriocins in combination with lipids and carbohydrates. This classification was refor-
mulated by Cotter et al.(19) in two categories: (I) lanthionine-containing bacteriocins, (II)
non–lanthionine-containing bacteriocins and bacteriolysins. Although bacteriocin classifi-
cation is still under discussion and continuously changing over time, the most consolidate
and acceptable classification for bacteriocins is that proposed by the latter authors.
Most bacteriocins produced by Leuconostoc belong to class II, which are small
(<10 kDa), heat-stable, non–lanthionine-containing bacteriocins with no posttranslational
modification.(26) As mode of action, these peptides present an amphiphilic helical struc-
ture, which allows them to be inserted into the membrane, leads to depolarization, leakage
of molecules and cell death.(19) Moreover, the bacteriocins belonging to this group have
an N-terminal region commonly called a “pediocin-box.” This region is conserved among
bacteriocins and presents a consensus sequence (YGNGVXaaC), which is responsible
for the anti-Listeria activity. The C-terminal domains are less conserved and thought to
determine the nonlisterial antimicrobial spectrum.(19) Different studies have reported the
characteristics of class II bacteriocins; however, an overview published by Kjos et al.(27)
highlighted some important recent progress regarding target recognition, resistance, immu-
nity, and genome of the nonlantibiotic (class II) bacteriocins. This review introduces
an overview of Lc. mesenteroides as a bacteriocin producer and a potential probiotic
strain.
The literature also describes bacteriocin production(28,29) and potential probiotic
of Leuconostoc species.(30,31) However, some of these studies are too preliminary for
considering their application in food process and preservation.
150 de Paula et al.

Studies with Lc. mesenteroides as a Potential Probiotic Strain

Resistance to Gastric Acidity and Bile Salts

The ability to tolerate and survive under the acid stomach environment and the resistance to
bile salts found in the small intestine are criteria for the characterization of microorganisms
as a potential probiotic strain. According to the literature, different methodologies have
been used to evaluate potential probiotic strains. Different isolates of Lc. mesenteroides
have demonstrated the ability to survive at low pH, including strains H4 and H5 from
seafood products,(32) strain B-1 from natural yogurt,(33) strain PLsr-1(w) from whey,(34)
strains KFRI818, KFRI821, LA89406, YML003, PH1, and DM1, all isolated from
kimchi,(35−37) strains CLFP 68 and LAB-4, both isolated from fish intestine,(30,38) and
strain Lnm-1RM3 from narezushi.(39) In contrast, Lc. mesenteroides IM082 did not survive
after 60 minutes in a stomach reactor that simulates the human upper GIT.(40)
Bile is produced in the liver, concentrated in the gall bladder, and released into the
duodenum, where it aids fat digestion by emulsifying and solubilizing lipids.(41) The phys-
iological concentration level of human bile varies and depends on race, physiological
conditions, and gender. Moreover, bile is an antimicrobial substance, which is composed
of bile acids, cholesterol, and phospholipids. Studies suggest that all probiotic strains
should be able to grow and survive in the presence of up to 0.3% of bile salts.(42)
Probiotic strains with high tolerance (>0.3%) to bile develop better in the upper small
intestine than strains with a low bile tolerance(35) ; however, the presence of these com-
pounds in the duodenum can affect the viability of probiotic bacteria. In addition, the
interaction between probiotic and bile salts is not very well understood. Some studies
have shown that strains of Lc. mesenteroides can survive under different concentrations
of bile salts (Table 1).(32,35−37,39,40) However, this substance limited the growth of some
Lc. mesenteroides subsp. mesenteroides strains.(30,43)

Bile Salt Hydrolase Activity

Some LAB have the ability to hydrolyze bile salts by enzymes. These enzymes detoxify
bile by deconjugating bile acids.(44) Studies have shown that this phenomenon promoted
by LAB increases the demand for cholesterol, which, in turn, prompts the synthesis of

Table 1
Survival of Leuconostoc mesenteroides strains in different oxgall concentrations

Leuconostoc
mesenteroides strain Oxgall survival (%) Origin
HK11 0.5% for 18 hours Korean fermented food(32)
KFRI189, KFRI818, 0.5% for 24 hours Kimchi(35)
KFRI821, LA75215
LA89406 0.3% for 24 hours Kimchi(35)
PH1, DM1 0.3% for 3 hours Kimchi(36)
YML003 5% for 5 hours Kimchi(37)
Lnm-1RM3 0.3% Japanese fermented food(39)
IM082 0.3% for 90 minutes Kefir(40)
 Leuconostoc mesenteroides in Food Systems 151

more bile salts in the liver. This process may lead to a reduction of serum cholesterol level;
however, researchers have not yet established the dose-effect relationship.(45) Nonetheless,
to the best of our knowledge, only Lc. mesenteroides subsp. mesenteroides SJRP55 showed
the ability to deconjugate bile salts.(46)

Adherence to Mucus and/or Human Epithelial Cells and Cell Lines

An important condition for LAB to colonize and survive in the GIT is its ability to adhere
to mucus and the intestinal epithelial cells.(47) The cell surface of LAB is composed of pro-
teins, polysaccharides, and lipoteichoic acid, which can be responsible for the attachment
of bacteria to different surfaces. Furthermore, the mechanisms of adherence to an epithelial
surface involve both receptor-specific binding and charge and hydrophobic interactions.(48)
Once attached to this system, the microorganisms can promote health benefits to the host,
enhance the stimulation of human immune system, compete for nutrients, and produce
antimicrobial compounds, which can interact positively or negatively with other microor-
ganisms present in the GIT. The adhesion ability of probiotic strains has been studied using
the in vitro model systems; however, different factors of the in vitro tests (food matrix, shelf
life, temperature, growth medium, oxygen, pH, different types of cell lines) can modify the
physicochemical properties of the bacterial surfaces and, consequently, their adhesion to
the intestinal mucosa.(36,49) Moreover, the in vitro results should be interpreted with caution
because the ability to adhere in vitro does not necessarily mean in vivo adhesion.
Adhesion of microorganisms is generally tested with monolayers of intestinal cul-
ture cells. The mucus layer works as a barrier or can provide the adhesion of the
microorganism.(50) The mucus gel (gel covering the intestinal epithelial surface) is also
used for adhesion studies. The mucus layer is the first contact between ingested bacte-
ria and intestinal mucous membrane. Therefore, the results obtained with mucus adhesion
assay can provide important additional data on probiotic adhesion properties and supple-
ment the data obtained with cell lines without mucus-secreting ability (Caco-2 and HT-29).
These cells lines can differentiate into enterocytes and can thus be used as a model for
the small intestine epithelium. However, bacterium adhesion is strain dependent and the
ability to adhere in Caco-2 and HT-29 does not mean the adhesion to mucus gel.(51)
Xu and coworkers(47) suggested that in vitro adhesion to Caco-2 cells is correlated with
competitive inhibition for attachment sites, which can competitively exclude foodborne
pathogens. According to Russo and coworkers(52) and Ryu and Chang,(36) bacterial adhe-
sion increases with exopolysaccharides (EPS) synthesis, which is commonly produced by
Lc. mesenteroides species.(2,53,54)
Most of the time, in vitro adhesion studies can be poor and not very well understood.
Moreover, in vivo trials are very limited due to ethical considerations, laborious tech-
niques, and lack of volunteers. Several studies showed the adhesion of Lc. mesenteroides
strains to cell lines (Caco-2 and/or HT-29 cells): strain B-1 isolated from yogurts,(33) strain
CLFP 68 isolated from intestine of rainbow trout,(38) and strains DM1 and PH1 isolated
from kimchi.(36) In addition, strain PLsr-1(w) showed strong adherence to ileal epithelial
cells of rats.(34) The ability to adhere cells lines seems to be strain dependent; therefore,
the interpretation of these results should be evaluated with caution because the adherence
feature to intestine does not necessarily mean an in vivo adhesion would occur. Few stud-
ies discuss the adhesion properties of Lc. mesenteroides species; however, the adhesion
values can be linked with exopolysaccarides (EPS) producing, which bacterial adhesion
increases with EPS production.(36) Moreover, the production of this material is frequent by
Lc. mesenteroides species.(2,53)
152 de Paula et al.

Hydrophobicity is another physicochemical property that can facilitate the first contact
between microorganisms and host cells.(55) The bacterial cell surface contains proteins and
polysaccharides with hydrophobic and hydrophilic properties (carboxylic groups and Lewis
acid–base interactions), which are responsible for the adhesion of bacteria to surfaces.(46,56)
Moreover, the cell surface hydrophobicity is strain specific, and the presence of differ-
ent nutrients or carrier food matrix may influence the expression of adhesion genes in the
microorganisms.(57,58) The hydrophobicity of Lc. mesenteroides CLFP 68 (11.42%) was
significantly lower (P < 0.05) than that observed for Lactobacillus plantarum (24.99%) and
Lactococcus lactis (31.59%).(38) The ability to adhere with different hydrocarbons provides
evidence that Lc. mesenteroides PLsr-1(w) strain can adhere and colonize the intestinal
tract. Furthermore, sodium docecyl sulfate electrophoresis analysis of its surface protein
showed a prominent protein band of 42 kDa, which is the S-layer protein responsible for
the adhesion of the culture.(34) Lc. mesenteroides 2M isolated from skin of healthy frogs
exhibited a higher degree of hydrophobicity and contained basic components in the cell
surface, according to their adhesion to chloroform compared with other LAB strains iso-
lated from water and balanced animal feed. These characteristics could be associated with
the interaction with components of mucosal surfaces, such as epithelial cells and mucus
that contain acid glycoconjugates.(59)
Another adhesion property frequently evaluated is the aggregation and co-aggregation
capability, which can help probiotic cultures to adhere to the oral cavity, GIT, and uro-
genital tract and modulate the immune system in the GIT.(42,50) The aggregation between
microorganisms of the same strain (auto-aggregation) or between genetically different
strains (co-aggregation) is the major importance in several ecological niches, especially
for probiotics. The aggregating bacteria may achieve an adequate mass to form biofilm or
adhere to the mucosal surfaces of the host and exert their benefic functions.(60) The organ-
isms with the ability to aggregate with other bacteria (co-aggregation) can help to prevent
colonization by invading foodborne pathogens.(47) Moreover, co-aggregation of probiotic
strains has been related to the ability to closely interact with pathogens, increasing the
competition of receptor epithelial intestine cells and potentially decreasing the presence of
undesired microorganism in the intestine due to the production of antimicrobial compounds
or other factors, blocking the dissemination of pathogens to other attachment sites, and
enhancing the competition in the GIT.(61) These characteristics can increase the immune
system and protect the host agaisnt undesire pathogens.

Metabolic Activity
The metabolic activity is an important subject to study due to the production of significant
metabolites by microorganims. Lc. mesenteroides subsp. mesenteroides showed the ability
to produce high concentrations of conjugated linoleic acid,(62) which has shown numerous
health benefits, including antiatherogenic, antidiabetic, anti-inflammatory, and anticarcino-
genic properties. The introduction of probiotic strains (Lc. mesenteroides MTCC 5442 and
Bacillus subtilis natto RG4365) in the probiotic ragi malt (functional food) resulted in the
presence of high amounts of beneficial fatty acids such as linoleic and linolenic acid and
increased the mineral content (iron and zinc) of the product.(63)
Another health issue that could be positively influenced by probiotic culture
metabolism is lactose intolerance. Some consumers of dairy products are lactose intolerant
due to the absence or low production amounts of β-galactosidase enzyme, which causes
discomfort after milk digestion.(58) β-Galactosidase hydrolyzes lactose to galactose and
glucose, aiding lactose digestion in the intestine. When people have limited digestion or
 Leuconostoc mesenteroides in Food Systems 153

are lactose intolerant, the consumption of dairy products causes discomfort, gases, and flat-
ulence. Different Lc. mesenteroides strains showed β-galactosidase activity.(34,64,65) Since
LAB cultures can produce β-galactosidase, it is interesting for the dairy industry to explore
the probiotic strains that produce this enzyme, in order to help the lactose maldigestion
problem and enhance the consumption of dairy food.

In Vivo Studies
The principal outcome of efficacy studies on probiotics should consist of proving benefits
in human trials.(10) The in vivo studies using Lc. mesenteroides as a potential probiotic
strain are still scarce in comparison with the ones published about other Lactobacillus
species, such as Lactobacillus rhamnosus or Lactobacillus plantarum. It is important to
look carefully at the positive in vivo results, since most of them are inconsistent, unclear,
and controversial. However, improvements on the knowledge about the interactions of
potential probiotic microorganisms in the GIT are important to understand better the behav-
ior of these microorganisms in the host. Few in vivo studies about the potential probiotic
Lc. mesenteroides strains have been described in the scientific literature.
Agarwal and Bhasin(66) conducted a study in order to control diarrhea in chil-
dren (6 months to 5 years of age) by feeding them with fermented milk preparations
(group 1: Actimel from Danone, containing 108 colony-forming units [CFU]/g of each
of Lactobacillus casei DN-114001, Lactobacillus bulgaricus, and Streptococcus ther-
mophilus; group 2: Indian Dahi, containing 108 CFU/g of each of Lactococcus lactis,
Lactococcus lactis subsp. Cremoris, and Lc. mesenteroides subsp. cremoris; and group
3: ultra-heat-treated yogurt preparation—no live bacteria). Fermented milks that belong
to groups 1 and 2 showed a reduction in the duration of diarrhea in children in a com-
munity. However, the Indian Dahi presented a minor reduction, with the time taken to
control diarrhea decreased by 0.3 day. In another study, the administration of symbiotic
formula consisted of a combination of four probiotics (1011 CFU/g of each: Pediococcus
pentosaceus 5, Lc. mesenteroides 32, L. paracasei subsp. paracasei 19, and L. plantarum
2), with inulin, oat bran, pectin, and resistant starch as prebiotics. This mixture was used
during 15 treatment days of critically ill, mechanically ventilated, multiple trauma patients.
The administration of this symbiotic formula in the patients exerted beneficial effects.
Symbiotic-treated patients exhibited a significantly reduced rate of infections (P = 0.01),
systemic inflammatory response syndrome, severe sepsis (P = 0.02), and mortality. Days of
stay in the intensive care unit (P = 0.01) and days under mechanical ventilation were also
significantly reduced in relation to placebo (P = 0.001). Besides, it improved the patient’s
immune response, which required ventilatory support for a shorter period of time and less
intensive care treatment.(67) Some clinical studies demonstrated that supplies of pre- and
probiotics reduced the bacterial infection rates in patients submitted to liver transplanta-
tion, antibiotic therapy following by pylorus-preserving pancreticoduodenectomy (PPPD),
or patients who underwent other high-risk surgeries.(67−70)
The potential probiotic properties of Lc. mesenteroides cultures have also been stud-
ied in animal models. The effect of probiotic supplementation (107 CFU/g of each of
Lc. mesenteroides CLFP 196 and Lactobacillus plantarum CLFP 238) on the control of
lactococcosis in rainbow trout for 30 days showed a significant reduction of fish mortal-
ity, from 78% in the control group to 46–54% in the probiotic groups.(71) Furthermore,
Pérez-Sánchez and coworkers(38) conducted a study in order to understand the effect of
some LAB (106 CFU/g of each of Lactobacillus plantarum subsp. plantarum CLFP 3,
Lactococcus lactis subsp. cremoris CLFP 25, and Lc. mesenteroides CLFP 68) on the
154 de Paula et al.

control of lactococcosis for 36 days, as well as to assess the impact of probiotics on

the expression of immune-related genes in the head, kidney, and intestine of rainbow
trout (Oncorhynchus mykiss). Diet containing Lactobacillus plantarum had significant
lower fish mortality rates than diets containing Lactococcus lactis, Lc. mesenteroides, or
control.(71) Askarian and coworkers(72) investigated the effect of Lactobacillus curvatus
and Lc. mesenteroides (109 CFU/g in combination or alone), originally isolated from
beluga (Huso huso) and Persian sturgeon (Acipenser persicus) GIT, respectively, on the
growth, survival, and digestive enzyme (amylase, lipase, and protease) activities and the
population level of LAB in the GIT for 50 days. The highest specific growth rate, sur-
vival, and improved intestinal enzyme activities were noted in the rearing group fed with
Lc. mesenteroides (2 × 109 CFU/g). Similar results were found in the beluga study, where
Lactobacillus curvatus had a positive effect. In another study, lactose-intolerance-induced
rats were fed with a diet supplemented with an effective dose 108 CFU/mL of potential
probiotic Lc. mesenteroides PLsr-1(w) strain, isolated from whey. After 4 days of probiotic
feeding, the diarrhea disappeared when compared with control group, which received
only skim milk without culture and continued to show diarrhea. No changes in mor-
phology and treatment-related toxicity/bacterial translocation was observed on probiotic
feeding.(73) Further, a reduction of acute induced-peritonitis lung injury in rats was shown
with preoperative enteral administration of symbiotic composition (109 CFU/g of each of
Pediococcus pentosaceus 5, Lc. mesenteroides 32, Lactobacillus paracasei subsp. para-
casei 19, and Lactobacillus plantarum 2; inulin, oat bran, pectin, and resistant starch as
prebiotics), during 3 study weeks, using a cecal ligation and puncture model. Heavy infiltra-
tion of lung tissue with neutrophils was observed only in fiber-treated (302.20 ± 7.92) and
placebo-treated (266.90 ± 8.92) animals. This was totally abolished in the symbiotic-
treated group (34.40 ± 2.49). Lung edema (wet-to-dry lung weight ratio) was significantly
reduced in the symbiotic-treated group (4.92 ± 0.13 vs. 5.07 ± 0.08 and 5.39 ± 0.10,
respectively).(74)
Further studies in animal models and humans, using Lc. mesenteroides strains alone,
should be done in order to confirm and understand the behavior of this microorganism in
the host GIT. Furthermore, the potential probiotic effects are always strain dependent.

Therapeutic Benefit Studies of Lc. mesenteroides

The therapeutic benefits provided by potential probiotic LAB are frequently described in
the literature. According to FAO/WHO,(10) a list of various tests (in vitro and in vivo
trials) should be performed in order to assure that a strain is approved as a probiotic
microorganism. Nonetheless, to fulfill all of the probiotic criteria is a hard task.
Kekkonen and coworkers(75) confirmed that all potentially probiotic tested bac-
terial (Streptococcus, Lactobacillus, Bifidobacterium, Lactococcus, Leuconostoc, and
Propionibacterium) genera induced tumor necrosis factor (TNF)-α production. Production
and mRNA expression of TNF-α, interleukin (IL)-12, interferon (IFN)-γ, and IL-10 were
determined by enzyme-linked immunosorbent assay (ELISA) and Northern blotting. The
best inducers of Th1-type cytokines IL-12 and IFN-γ were Streptococcus and Leuconostoc
strains. The stimulation of cytokine production in human peripheral blood mononuclear
cells with any bacterial combinations (control) did not result in enhanced cytokine produc-
tion, suggesting that different bacteria, whether gram-positive or gram-negative, compete
with each other during host cell interactions. These results suggest that probiotic bacteria
in a genera-specific way direct immune responses to either the Th1-type or the anti-
inflammatory side. Understanding of the immunological properties of probiotic bacteria
 Leuconostoc mesenteroides in Food Systems 155

is important to development of probiotic bacteria for targeted treatment of different disease

conditions.
The effect of the pretreatment of LAB and bifidobacteria on inflammatory events, fol-
lowing by IL-8 induction by Salmonella typhimurium DT104, was investigated by Carey
and Kostrzynska.(76) As compared with the control, a significant decrease (P < 0.05) in
IL-8 secretion was observed when the HT-29 cells were preincubated for 1 hour with
Bifidobacterium adolescentis FRP 61, Bifidobacterium longum strains FRP 68 and FRP
69, Bifidobacterium breve FRP 334 L. kefir IM002, and Leuconostoc mesenteroides IM080,
followed by stimulation with Salmonella typhimurium DT104. Real-time polymerase chain
reaction (PCR) and ELISA were employed to determine the effect of pretreatment with
LAB and bifidobacteria on IL-8 gene expression and extracellular protein secretion by
HT-29 cells, respectively.
Balcázar and coworkers(77) demonstrated a positive effect on humoral immune
response following oral probiotic administration (106 CFU/g of Lc. mesenteroides,
Lactococcus lactis subsp. Lactis, and Lactobacillus sakei, isolated from salmonids) in
brown trout (Salmo trutta). The plasma total immunoglobulin level in the LAB groups
(week 4) was found to be higher than that of the control group (∼6.2 mg/mL), especially
in the groups that received diets containing Lc. lactis subsp. lactis (∼8.3 mg/mL) and Lc.
mesenteroides (∼7.6 mg/mL). The serum lysozyme activity was significantly higher in the
LAB groups; however, only the Lc. lactis subsp. lactis group showed a statistical difference
at the end of the fourth week.
Further studies about potential probiotic Lc. mesenteroides should be done in order to
better understand the therapeutic effects in animal models and humans; however, ethical
constraints are barriers that need to be overcome. It is noteworthy to highlight that more
flexibility in the laws for laboratory tests using animal models and humans, and trans-
parency of scientific tests and results for nonscientific citizen, could be a way to improve
and understand better the therapeutic benefit studies of potential probiotic strains.

Antimicrobial Activity against Potentially Pathogenic Bacteria

The intestinal microbiota is a complex and dynamic ecosystem that contains differ-
ent bacterial species and representing an important contribution to the health of the
host. The relationship between probiotic microorganisms and commensal intestinal bac-
teria remains uncertain.(78) The probiotic microbiota play a key role by promoting the
integrity of the epithelial barrier and the development of mucosal immunity.(79) On the
other hand, the mucosal surfaces of the GIT are particularly susceptible to the adher-
ence and colonization of foodborne pathogens, such as Salmonella typhymurium, Listeria
monocytogenes, Staphylococcus aureus, Shigella spp., and Escherichia coli.(47) Potential
probiotic Lc. mesenteroides strains (PLsr-1(w), DM1, and PH1) produced antimicrobial
activity against some pathogen species (E. coli O157:H7 and other serotypes, S. aureus,
Pseudomonas aeruginosa, Vibrio cholerae, Yersinia enterocolitica, Salmonella thyphi,
Salmonella parathyphi, and Shigella dysenteriae), using the agar well diffusion method.
Different inhibition zones in diameter were found, ranging from 7.42 to 16.00 mm.(34,36)
Probiotics can promote a positive balance in the GIT microbiota by increasing the con-
centration of beneficial microorganisms and inhibiting pathogenic bacteria.(79) Different
types of antimicrobial compounds can be produced by LAB, such as carbon dioxide,
hydrogen peroxide, diacetyl, organic acids (lactic acid, acetic acid, and formic acid),
ethanol, bacteriocins, and others. These antimicrobial substances can inhibit undesirable
microorganisms found in the GIT, and some of these antimicrobial compounds, such
156 de Paula et al.

as bacteriocins, can also be used as biopreservatives by food industry. Moreover, the

production of a physiologically restrictive environment (pH, redox potential, and hydrogen
sulfide production) can inhibit the presence of undesirable microorganisms.(79)
Nakamura and coworkers(39) reported that competition for Caco-2 cell binding recep-
tors and the antimicrobial activity against Listeria monocytogenes were observed for Lc.
mesenteroides 1RM3, which presented strong inhibition against the pathogen invasion to
Caco-2 cells. In addition, when A/J mice were orally infected with Listeria monocyto-
genes, the recovery of the pathogen from the spleen was suppressed by the administration
of water containing 9 log CFU/mL of Lc. mesenteroides 1RM3 cells. The inhibitory effects
were also shown by Lc. mesenteroides 1RM3 cells heated at 100 ◦ C for 10 minutes. An in
vitro assay using Madin–Darby canine kidney (MDCK) cell line and hemagglutination
showed that Lc. mesenteroides YML003 presented an antiviral activity against H9N2 low-
pathogenic avian influenza (LPAI), as well as for in vivo specific-pathogen-free (SPF)
chickens. The microscopic observation demonstrated that MDCK cells treated with Lc.
mesenteroides YML003 cell-free supernatant and LPAI after 72 hours were nearly similar
to the control (cells without any treatment). Complete inhibition of hemagglutination was
observed in eggs treated with cell-free supernatant (CS) and heat-treated supernatant (HS)
of Lc. mesenteroides YML003. The immunomodulatory activity of probiotic bacteria is
mainly because of their ability to induce cytokine production, which leads to the regulation
of innate and adaptive immune responses.(37)
Another in vitro study, using pure cultures of Lc. mesenteroides MTCC 5442 (Lm) and
Bacillus subtilis natto RG4365 (Bs), showed that each probiotic strain was able to inhibit
the planktonic growth of Vibrio cholerae (Vc). Maximum inhibition (7.5 mm and 6.5 mm)
using Lc. mesenteroides MTCC 5442 and Bacillus subtilis natto RG4365 were found after
96 hours, when 12% inoculum was added. When both the cultures were supplemented
equally to make initial inoculum totally as 4%, 8%, and 12%, a synergistic effect was found
on the antagonistic activity maximum (10 mm), being at 96 hours. Additionally, at a pro-
portion of 1:1 of Vc cells:cell-free supernatant (1 μL each), negligible biofilm was formed
by the pathogens and synergistically cell-free supernatants (Bs and/or Lm) produced no
biofilm.(63)

Behavior of Lc. mesenteroides in Food as a Probiotic Microorganism

The presence of LAB plays an important role in food preservation, health benefits, and
production of antimicrobial compounds. Probiotic LAB are commonly applied in dairy
products, being widely used in industrial applications, mainly as starter or complementary
cultures. The probiotic candidate strain should survive both food processing and biologi-
cal stresses, which includes extreme temperatures and pH values, as well as osmotic and
oxidative stresses and bacteriophage attack.(2) Moreover, depending on the product, other
requirements should be fulfilled, such as production of aroma, acidification, and viability
during shelf life.
Leuconostoc spp. can form significant amounts of diacetyl from citrate in milk, which
is an important compound produced mainly by Lc. mesenteroides subsp. cremoris and
related to aroma and flavor. This substance plays an important role in the production of
butter and cheese. The production of exopolysaccharides by this species is extraordinary.
Its slime-forming property is commonly used by the dairy industry, especially in the pro-
duction of thick, viscous fermented milk products. Furthermore, this species can grow over
a wide range of temperatures and tolerate higher salt concentrations up to 7% NaCl.(3)
Despite these technological characteristics, studies on Lc. mesenteroides as a potential
probiotic microorganism are rare in the literature. One of these studies was conducted
 Leuconostoc mesenteroides in Food Systems 157

recently by Beganovic and coworkers.(80) The probiotic strains Lactobacillus plantarum

L4 and Lc. mesenteroides LMG 7954 were applied for fermentation control of cabbage
heads. The starter cultures applied for cabbage heads fermentation allowed a decrease of
NaCl concentration from 4.0% to 2.5% (w/v) and acceleration of fermentation process by
14 days. The produced sauerkraut heads were considered as a probiotic, as viable probiotic
cultures cells counts in the final product were higher than 106 CFU/g.

Studies on Bacteriocinogenic Lc. mesenteroides

Bacteriocins Produced by Lc. mesenteroides

The bacteriocins produced by Lc. mesenteroides can be applied as biopreservatives in the
food industry; however, the process required from discovery of new bacteriocins until its
final application in food systems remains a challenge. The complex biochemical nature of
the bacteriocins including their stability and interactions with food matrices, the best way to
obtain high amounts of these compounds, and how to diminish the losses in the purification
processes are just some of the aspects that should be observed in order to enable application
of bacteriocins as food biopreservatives.
Most bacteriocins produced by Lc. mesenteroides show anti-Listeria
activity.(8,9,33,81−93) Listeria monocytogenes is a public health concern, since this
microorganism is a foodborne pathogen able to adapt their cellular physiology to overcome
various forms of stress, such as ability to multiply under refrigeration temperatures and per-
sist in food-processing environments. It can cause abortions, gastrointestinal diseases, and
septicemia and exhibits high mortality rates in children, elderly, and immunocompromised
and organ-transplanted individuals.(90) In addition, some unusual bacteriocins produced
by Lc. mesenteroides showed antimicrobial activity against gram-negative bacteria such
as Salmonella typhimurium and E. coli(20,33) and gram-positive bacteria such as Bacillus
cereus(20) and S. aureus.(8, 91)
It is important to point out that some encoding genes for bacteriocins seem to be
very well conserved during the evolution of Leuconostoc genus. Most probably some
bacteriocin genes are part of complex genetic structure and may have some other functions.
Once the bacteriocinogenic bacteria are able to inhibit competing species, the transmis-
sion of these genetic elements to daughter cells may help to explain their unique ecology
and evolution to preserve these genes.(93) Different strains of Lc. mesenteroides, isolated
from various matrices and environments, were able to produce the same bacteriocins:
mesentericin B105 and mesentericin Y105 or leucocin A-TA33a and leucocin A-UAL 187
(Table 2)(8,9,84,85,87,89,93−95) ; nevertheless, the production of different bacteriocins were
observed for different strains of Lc. mesenteroides: mesenterocin 5,(82) leucocin A-UAL
187,(84) mesenterocin 52A and 52B,(89) leucocin A-, B-, C-TA33a,(87) leucocin C,(96)
mesentericin ST99,(91) bacteriocin ST33LD,(97) mesenterocin E131,(9) and leucocyclicin
Q.(20) Different bacteriocins produced by the same strains can help these microorgan-
isms to explore other niches, attack other targets, and be used in different food matrices.
Furthermore, molecular studies indicated that the genes encoding mesentericins Y105 and
B105 are located on the chromosome, which leads to a higher stability of the genes, with
lower chances of occurrence of mutation or losses.(86)

Bacteriocins Produced by Lc. mesenteroides in Food

Bacteriocins produced by LAB can be applied in food by three different ways: introduction
of producer strains, addition of partial purified or purified concentrates, and utilization of
158 de Paula et al.

Table 2
Characteristics of bacteriocins produced by Leuconostoc mesenteroides strains

Bacteriocin Amino acid sequence Mass (Da)

(83)
Mesentericin Y105 KYYYGNGVHCTKSGCSVNWGE 3666
AASAGIHRLANGGNGFW
Mesentericin 52B(87) KGVLGWLSMASSALTGP 3446
QQPNSPWLAKIKNHK
Leucocin A-UAL 187146 KYYGNGVHCTKSGCSVNW 3932.3
GEAFSAGVHRLANGGNGFW
Leucocin B-TA33a(85) KGKGFWSWASKATSWLTG 3466
PQQPGSPLLKKHR
Leucocin C-TA33a(85) KNYGNGVHCTKKGCSVDWGY 3744
AATNIANNSVMNGLTG
Leucocin C(92) KNYGNGVHCTKKGCSVDWGYAW 4595
TNIANNSVMNGLTGGNAGWHN
Leucocyclicin Q(20) MFLVNQLGISKSLANTILGAIAV 6115.59
GNLASWLLALVPGPGWATK
AALATAETTVKHEGKAAAIAW

fermented ingredients.(19,98) However, the production of bacteriocins can be affected by

various factors, such as NaCl concentration, temperature, enzymes, pH, food matrices, and
food contamination.
Various studies have described bacteriocins produced by Lc. Mesenteroides; nonethe-
less, few reports described their potential for application in food biopreservation.
Metaxopoulos and coworkers(99) inoculated sliced cooked cured pork shoulder with the
bacteriocin-producing strains Lc. mesenteroides L124 and L. curvatus L422. In the non-
inoculated samples, under vacuum packaging, the growth of spoilage microflora was
observed, whereas in the inoculated ones the counts of Brochothrix thermosphacta and
enterococci decreased (1.5 log CFU/g) during storage.
Studies have shown that bacteriocins produced by Lc. mesenteroides can be used in var-
ious food applications. For example, excess malolactic fermentation (production of L-malic
acid from L-lactic acid) by LAB can yield undesirable flavor compounds in wine fermen-
tation, but the bacteriocin-like inhibitory substance produced by Lc. mesenteroides subsp.
cremoris displayed antimicrobial activity against malolactic activity of autochthonous LAB
in wines.(100) Also, Lc. mesenteroides strains presented potential application for inhibition
of L. monocytogenes in wounds of Golden Delicious apples and Iceberg lettuce leaf cuts.(8)
The use of these LAB strains as bioprotective agents in food matrices provided inhibitory
results against the pathogenic microorganism. This application is supported by the safe
nature of the mentioned bacterial group. Lc. mesenteroides produced class II bacteriocins
with high antilisterial activity, identical to mesentericin Y105. Moreover, the application of
these strains in fresh fruits and vegetables did not cause sensory modifications, although
longer assays should be performed to confirm that the application of these bioprotective
strains do not alter the shelf life of the product.(8)
An interesting field that is still in progress is the use of bioengineering techniques that
can create a new era of powerful hybrid bacteriocins with a wide antibacterial spectrum and
high specific activity.(101) A fusion of different bacteriocin-encoding genes with different
 Leuconostoc mesenteroides in Food Systems 159

targets can create a new bacteriocin that could act more efficiently in food biopreservation.
A novel recombinant hybrid peptide, combining enterocin CRL35 and microcin V (named
Ent35–MccV), displayed an antimicrobial activity against enterohemorrhagic E. coli and L.
monocytogenes clinical isolates.(102) More details about the development of wide-spectrum
hybrid bacteriocins were reported by Acuña and coworkers.(101)
It is noteworthy to highlight that once bacteriocins are useful as biopreservatives in
foods, the potential of target species for the development of resistance to these compounds
is another subject of concern. It is important to emphasize that bacteriocins should be an
additional tool used in food systems to protect against undesirable microorganisms and
must be applied in combination with other barriers, such as pH control, aw, tempera-
ture, and oxygen, in the hurdle technology.(19) To understand better the hurdle technology
and its use in combination with antimicrobial compounds, Leistner and Gorris(103) and
Leistner(104) published two reviews about the subject. In addition, it is important to stress
that the use of the hurdle techniques does not replace the systematic preventive approach
for food safety, such as Hazard Analysis and Critical Control Points (HACCP) and Good
Manufacturing Practice (GMP).

The Other Side of Lc. mesenteroides

Pathogenic Strains
Few reports on systemic infections caused by pathogenic Lc. mesenteroides are described
in the literature. The characterization of microbiota in celiac disease in children was studied
by Sanz and coworkers.(105) The diversity of the fecal microbiota was significantly higher in
coeliac patients than in healthy controls. The prevalence of the species Lactobacillus cur-
vatus, Lc. mesenteroides, and Lc. carnosum was higher in celiac patients than in healthy
controls. Opposite results were found for Lactobacillus casei group, which was more
prevalent in healthy controls. Most LAB species detected in celiac patients were probably
transient (allochthonous), whereas in healthy samples species of the Lactobacillus casei
group could be regarded as both endogenous and food-related bacteria.(105) However, at
present, little is known about the potential role of the microbiota in coeliac patients.
Isolated cases of Lc. mesenteroides as an emerging pathogen have been reported.
Some authors commented that Lc. mesenteroides strains were related with the occur-
rence of bacteremia,(106) nosocomial infection,(107) short bowel syndrome,(108) brain
abscess,(109) short GIT syndrome, parenteral nutrition and continuous enteral feeding,(110)
endocarditis,(111) septicemia,(112) meningitis,(113) and odontogenic infection.(114) The gate-
way for Leuconostoc-caused infections is still unclear, and most of clinical symptoms in
patients are fever, leukocytosis, and gastrointestinal disorders. Because of the rarity of
infections, insignificant knowledge is known about the harmful effects or optimal therapy
for these conditions.(108) The great majority of cases of pathogenic Lc. mesenteroides is
related to underlying diseases and immunocompromised patients. Immune system changes
can expose the patients to different opportunistic pathogens such as Lc. mesenteroides,
increasing the rates of opportunistic illness. Moreover, the intake of dairy products
containing this microorganism is not related to any disease.(106)

Antibiotic Resistance and Virulence Genes

Transferable resistance genes may pose a risk for the utilization of LAB in food processing,
as they can be transferred from pathogenic bacteria to nonpathogenic organisms.(81,115)
160 de Paula et al.

LAB in food may act as reservoirs of antibiotic resistance genes.(116) These genes may be
transferred by different bacteria from normal GIT microbiota, normal GIT microbiota and
pathogens, or between pathogens, which use this strategy as a way of adapting to an ever-
changing environment.(41) It is noteworthy to highlight that, in some cases, the resistance
to specific antibiotics can be desirable, such as in treatments involving antibiotic-induced
diarrhea.(117)
Similar to Lactobacillus and Pediococcus genera, Leuconostoc spp. has an intrin-
sic resistance to vancomycin,(42,118) due to particular characteristics of its cell wall
that presents D-lactate instead of a D-alanine in the peptidoglycan layer.(3) In addi-
tion, the intrinsic or natural resistance is encoded by chromosomal genes and is
therefore nontransferable.(117) Previous studies with Lc. mesenteroides, isolated from
different sources, reported the presence of vancomycin resistance among the tested
strains.(36,38,55,81,117,119−122)
Natural (horizontal) gene transference may also occur,(123) but it has been rarely
found.(3) Interesting reviews about antibiotic resistance in LAB and horizontal gene transfer
were published by Dicks and coworkers(123) and Van Rennen and Dicks.(41) The literature
describes several cases of Lc. mesenteroides resistance to antibiotics, other than van-
comycin (Table 3). In contrast, a study conducted by Vermeiren and coworkers(125) showed
that strain Lc. mesenteroides LM4 did not show resistance to any of the 11 antibiotics
tested. In summary, Lc. mesenteroides antibiotic resistance seems to be strain dependent
and related to the environment in which the strain was isolated. The concern over antibi-
otic resistance is in part due to the excessive and indiscriminate use of these compounds in
humans, agriculture, and livestock. Lc. mesenteroides can acquire and/or transmit antibi-
otic resistance and virulence genes by transposons and plasmids, resulting in conjugation
or transformation.(126) Since this microorganism can be used in dairy food, a subject of
concern is the transference of resistance genes to pathogenic bacteria present in the GIT,
which may pose a risk for the host.(81)
Gene encoding virulence factors commonly found in Enterococcus genus, such as
cytolysin (cylA and cylB), aggregation substance (asp1, asc10, and asa1), Enterococcus
surface protein (esp), adhesins (ace and acm), adhesin-like endocarditis antigens (efaA),
gelatinase (gelE), hyaluronidase (hyl), and biogenic amines are not commonly described for
Lc. mesenteroides strains. For example, Lc. mesenteroides 875 did not present gelatinase
and hyaluronidase activity.(65)
Biogenic amines are generated by decarboxylation of the corresponding amino
acids through substrate-specific enzymes derived from microorganisms present in food.
Cadaverine and putrescine can contribute to food spoilage in several products, and they
have toxicological effects, observed in many critical functions for both humans and ani-
mals by the consumption of foods containing high amounts of these compounds.(127) In a
study conducted by Pircher and coworkers,(128) isolated strains of Lc. mesenteroides were
unable to produce more than 10 mg/L of amine at high inoculum level, in a medium
rich in nutrients, and under in vitro conditions. In another study with Leuconostoc spp.
strains, just 1/76 strains of Lc. mesenteroides subsp. mesenteroides produced >100 mg/L
of putrescine and cadaverine. The toxic levels seemed to depend on the characteristics
of different individuals.(129) In addition, Lc. mesenteroides strains isolated from differ-
ent foods, such as fermented sausage,(81) processed fish from Eastern Himalayas,(130)
Spanish cheese,(54) meat products from Eastern Himalayas,(131) musts,(132) and traditional,
starter-free cheeses,(133) did not produce biogenic amines.
 Leuconostoc mesenteroides in Food Systems 161

Table 3
Profiles of antibiotics for resistance of Lc. mesenteroides strains isolated from different
sources

Food matrix Resistance Reference

Cheddar cheese Tetracycline, gentamicin, Shobharani and
neomycin, streptomycin, and Agrawal(55)
sulfisoxazole
Clinical isolates Trimethoprim-sulfamethoxazole Vay and coworkers(122)
Fermented olives Kanamycin Argyri and
coworkers(117)
Fermented sausage Gentamicin, ampicillin, Aymerich and
penicillin G, and tetracycline coworkers(81)
Intestinal Streptomycin Allameh and
microflora of coworkers(30)
snakehead fish
Intestine of Ampicillin, clindamycin, Pérez-Sánchez and
rainbow trout enrofloxacin, flumequine, coworkers(38)
kanamycin, nalidixic acid,
oxolinic acid, penicillin,
tetracycline, and
trimethoprim-
sulfamethoxazole
Olive brine Nalidixic acid, Todorov and Dicks(97)
sulfamethoxazole, neomycin,
tobramycin, ciprofloxacin,
amikacin, streptomycin,
metronidazole, and
sulfafurazole
Spanish goat milk Ampicillin, augmentin, Herreros and
cheese cefoxitin, cephalotoxin, coworkers(124)
oxacillin, vancomycin,
teicoplanin, cloramphenicol,
clindamycin, rifampicin, and
tetracycline
Whey Cephalothin, gentamicin, and Rani and Agrawal(34)
oxacillin

Linares and coworkers(129) published a review regarding relevant aspects of biogenic

amine production in dairy products. Included were the effects of environmental condi-
tions, the microorganisms that produce them, the genetic organization and regulation of
the biosynthetic pathways involved, and the available methods for detecting the presence
of either these compounds or the biogenic-amines-producing microorganisms.

Hemolytic Potential
The presence of certain enzymes in potential probiotic microorganisms has been related
to pathogenicity for human beings. For this reason, the lack/low levels of such enzyme
162 de Paula et al.

activity is a positive aspect for strains that are intended to be used as probiotics or
starters cultures.(65) Hemolytic potential is not desirable in probiotic cultures. Some studies
comment that strains of Lc. mesenteroides present nonhemolytic characteristics when tested
on sheep blood agar,(108) which was also reported by Lc. mesenteroides DM1 and Lc.
mesenteroides PH1 isolated from kimchi(36) and Lc. mesenteroides 875 isolated from
raw ewe’s milk cheese.(65) Once Lc. mesenteroides can be used in different food matri-
ces, the absence of hemolytic enzymes is an important characteristic for food industry
application.
The absence of β-glucosidase, N-acetyl-β-glucosaminidase, and β-glucuronidase
enzymes is one of the selection criteria for probiotic LAB to be used in foods. The
activity of these enzymes can be harmful and are associated with health disorders or
intestinal diseases, such as the ability to convert procarcinogens to carcinogens in the
colon.(2,51) Studies with Lc. mesenteroides strains isolated from different sources have
shown the absence of β-glucosidase, N-acetyl-β-glucosaminidase, and β-glucuronidase
enzymes.(36,65,132,134) However, some Lc. mesenteroides strains isolated from fermented
cassava,(135) sourdoughs,(136) meat products from Eastern Himalayas,(131) musts,(132) dairy
samples,(64) and kimchi(36) showed positive β-glucosidase activity. It is important to point
out that the production of this enzyme by Lc. mesenteroides is an undesirable characteristic
and a subject of concern, because this microorganism can be used as starter, nonstarter, or
potential probiotic strain in different food matrices.

Spoilage in Food and Beverage Production

Lc. mesenteroides can be considered as a spoilage agent in certain foods, such as meat
products, alcoholic beverages, and sugar cane and beet, causing a critical impact on their
quality.(7) The main origin of Lc. mesenteroides contamination in processed food is the
environment (plant surface and soil), but natural contamination of the raw material can also
occur. The presence of this microorganism in wine, cachaça, and sugar cane can result in
the development of undesirable characteristics, such as the formation of exopolysaccharide
slimes, producing ropy products (dextrans and other polysaccharides), and the development
of off-flavor (acetic acid, diacetyl, and mannitol).(137)
In sugar production, the first step is the removal of the leafy parts from the sugar canes.
After this, the raw material is ferried to the mills. During these steps, there is a considerable
contamination with Lc. mesenteroides, which leads to the production of a gum that causes
problems during extraction of sugar cane.(138) When beet is used as raw material for sugar
extraction, the presence of Lc. mesenteroides subsp. dextranicum is a major problem. This
microorganism is able to produce extracellular slimes, which can cause filtration problems
in sugar factories.(139)
Leuconostoc strains are also frequently associated with spoilage problems during alco-
holic fermentation, such as acid production and yeast flocculation. This phenomenon can
cause industrial problems, such as interruption of cell centrifugation, occurrence of phase
separation between yeast cells and substrate, and yeast loss at the bottom of the reactor,
mixed with other solid particles.(140) Nonetheless, Leuconostoc genus is sensitive to ethanol
and presents a short-life inside the tanks.(141)
In wine fermentation, the glycerol oxidation carried out by Lc. mesenteroides and lac-
tobacilli strains generates acrolein. This aldehyde reacts with tannins and anthocyanins,
forming bitter compounds.(137) Also, Montersino and coworkers(5) reported that Lc.
mesenteroides strains, isolated from grape juice or wine, were able to produce exopolysac-
charides. These compounds are responsible for an alteration known as ropiness or oiliness,
 Leuconostoc mesenteroides in Food Systems 163

characterized by the appearance of viscous thick and oily texture. Although these defects
do not cause significant changes in taste, it makes the product unpleasant to the palate.
Other studies have confirmed the spoilage effect assigned by Lc. mesenteroides.
Processed cactus pear fruit packaged in modified atmosphere during the storage at 4 ◦ C
resulted in a more homogeneous bacterial population and favored the growth of lactic
acid bacteria Lc. mesenteroides. After 8 days of storage in minimal processing, Lc.
mesenteroides (43%), Enterobacter agglomerans (42%), and Enterobacter sakazakii (15%)
were present in fruit microbiota.(142)
Some studies have demonstrated that high-pressure treatment and pasteurization
were able to delay the occurrence of spoilage caused by Weissella viridescens and Lc.
mesenteroides in blood sausages. Without treatment, Lc. mesenteroides produced sour
smell, and milky exudates that were not as viscous as slime, and caused the appearance
of green spots.(143,144)
Under modified atmosphere, the presence of Lc. mesenteroides in meat package can
cause the increase of carbon dioxide levels, especially in refrigerated raw meat, which is
a characteristic of heterofermentative LAB. Lc. mesenteroides present in air-stored (4 and
10 ◦ C) Greek taverna sausage caused the appearance of slime and gas production in the
product.(145)
Although Lc. mesenteroides spoilage has been confirmed in various food matrices,
further studies should be carried out in order to better understand the behavior of this
microorganism under the mentioned conditions. Nonetheless, it is important to point out
the relevance of the use of hurdle techniques and improvement of the hygienic conditions,
which can help to avoid the presence of spoilage Lc. mesenteroides in the first place.

Conclusion
Lc. mesenteroides presents promising characteristics, such as probiotic potential and
bacteriocin production. Nonetheless, rare strains exhibit pathogenic profile and cause
spoilage in different food matrices. The two faces of Lc. mesenteroides show that further
studies should be performed to better understand the behavior of this microorganism in
different fields, and the judgment of every bacterial species needs to be evaluated based on
each specific strain.

Funding
The authors are grateful to Fundação de Amparo à Pesquisa do Estado de São Paulo
(FAPESP, Brazil, Project No. 2010/09302-1) and Coordenação de Aperfeiçoamento de
Pessoal de Nível Superior (CAPES, Brazil) for the financial support.

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