Critical Reviews in Food Science and Nutrition

ISSN: 1040-8398 (Print) 1549-7852 (Online) Journal homepage: https://www.tandfonline.com/loi/bfsn20

Lactobacillus fermentum: a bacterial species with

potential for food preservation and biomedical
applications

Karim Naghmouchi, Yanath Belguesmia, Farida Bendali, Giuseppe Spano,

Bruce S. Seal & Djamel Drider

To cite this article: Karim Naghmouchi, Yanath Belguesmia, Farida Bendali, Giuseppe Spano,
Bruce S. Seal & Djamel Drider (2019): Lactobacillus�fermentum: a bacterial species with potential
for food preservation and biomedical applications, Critical Reviews in Food Science and Nutrition,
DOI: 10.1080/10408398.2019.1688250

To link to this article: https://doi.org/10.1080/10408398.2019.1688250

Published online: 15 Nov 2019.

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CRITICAL REVIEWS IN FOOD SCIENCE AND NUTRITION
https://doi.org/10.1080/10408398.2019.1688250

REVIEW

Lactobacillus fermentum: a bacterial species with potential for food preservation

and biomedical applications
Karim Naghmouchia,b, Yanath Belguesmiac, Farida Bendalid, Giuseppe Spanoe, Bruce S. Sealf, and Djamel Driderc
a
Department of Pharmaceutical Chemistry, College of Clinical Pharmacy, Al Baha University, Saudi Arabia; bFacult
e des Sciences de Tunis,
Universit
e de Tunis El Manar, LR01ES05 Biochimie et Biotechnologie, Tunis, Tunisie; cUniversit
e Lille, INRA, ISA, Universit
e d’Artois, Universit
e
Littoral C^ote d’Opale, EA 7394-ICV Institut Charles Viollette, Lille, France; dLaboratoire de Microbiologie Appliqu
ee, Facult
e des Sciences de
la Nature et de la Vie, Universit
e de Bejaia, Bejaia, Algeria; eDipartimento di Scienze Agrarie, degli Alimenti e dell’Ambiente, Universita di
Foggia, Foggia, Italy; fBiology Program, Oregon State University Cascades, Bend, Oregon, USA

ABSTRACT KEYWORDS
Lactic acid-producing bacteria are the most commonly used probiotics that play an important role Alcoholic liver disease;
in protecting the host against harmful microorganisms, strengthening the host immune system, cholesterol-lowering agents;
improving feed digestibility, and reducing metabolic disorders. Lactobacillus fermentum (Lb. colorectal cancer;
fermenticin; food
fermentum) is a Gram-positive bacterium belonging to Lactobacillus genus, and many reportedly preservation; lactic acid
to enhance the immunologic response as well as prevent community-acquired gastrointestinal bacteria; medical
and upper respiratory infections. Additionally, Lb. fermentum strains produce diverse and potent application; probiotic
antimicrobial peptides, which can be applied as food preservative agents or as alternatives to
antibiotics. Further functions attributed to probiotic Lb. fermentum strains are their abilities to
decrease the level of blood stream cholesterol (as cholesterol-lowering agents) and to potentially
help prevent alcoholic liver disease and colorectal cancer among humans. Finally, Lb. fermentum is
a key microorganism in sourdough technology, contributing to flavor, texture, or health-promoting
dough ingredients, and has recently been used to develop new foods stuffs such as fortified and
functional foods with beneficial attributes for human health. Development of such new foodstuffs
are currently taking important proportions of the food industry market. Furthermore, an increasing
awareness of the consumers prompts the food-makers to implement alternative environmental
friendly solutions in the production processes and/or suitable biological alternative to limit the
use of antibiotics in feed and food. Here, we give an account on the application of Lb. fermentum
strains in the biomedical and food preservation fields, with a focus on probiotic features such
as bacteriocin production. We also summarize the use of Lb. fermentum as cell factories with the
aim to improve the efficacy and health value of functional food.

Introduction species widely distributed in nature, often isolated from fer-

menting plant materials (Nielsen et al. 2007), dairy products
Lactic acid bacteria (LAB) are in the phylum Firmicutes,
(Coton, Berthier, and Coton 2008), bread (Russo et al.
class bacilli, order Lactobacillales that play important roles
2014), naturally fermented sausages (Kaban and Kaya 2008),
during food production, nutritional supplementation, agri-
breast milk (Mart
ın et al. 2003), and saliva (Dal Bello and
culture, and human-animal medicine (Bintsis 2018). LAB
Hertel 2006; Sonomoto and Yokota 2011). The beneficial
constitute a diverse group of Gram-positive bacteria, devoid
effects of Lb. fermentum has resulted in the development
of catalase activity and producing lactic acid as the main
of different probiotic preparations as listed in Table 1.
end-product of carbohydrates fermentation. The LAB
group is composed of genera including Aerococcus, Lb. fermentum antagonistic properties and particularly
Carnobacterium, Enterococcus, Lactobacillus, Lactococcus, production of antimicrobial peptides (called fermenticins)
Leuconostoc, Oenococcus, Pediococcus, Streptococcus, are presented as potential means for medical application and
Tetragenococcus, Vagococcus, and Weissella (Cholakov et al. food preservation processes (Fuochi, Volti, and Furneri
2017). LAB are present in different ecological niches, and 2017). Remarkably, there are several strains from LAB
many studies have established differences at their genetic especially Lactobacillus, Bifidobacteria, and Enterococcus with
and physiological levels (Ait Seddik et al. 2017). With more probiotic characteristics (Franz et al. 2003; Vaughan et al.
than 240 species (http://www.bacterio.net/lactobacillus.html), 2005). Within Lactobacillus, Lb. fermentum is not as well-
Lactobacillus is certainly the most studied genus in the LAB studied relative to other species of the genus. For example,
group. Lb. fermentum lactic acid bacterium is an obligatory investigators have proposed using Lb. fermentum for
treatment and prevention of gastrointestinal disorders,

CONTACT Djamel Drider [email protected] Institut Charles Viollette, Cit
e scientifique, avenue Paul Langevin, Batiment C, bureau C315, 59655
Villeneuve d’Ascq, France.
Color versions of one or more of the figures in the article can be found online at www.tandfonline.com/bfsn.
ß 2019 Taylor & Francis Group, LLC
2 K. NAGHMOUCHI ET AL.

Table 1. List of commercially available Lactobacillus fermentum probiotic strains.

Industry manufacturing Lb.
Product name capsule and powder fermentum probiotic product Sources/Strains References
FloraFITV Probiotics
R
Danisco USA, Inc Lb. fermentum SBS-1 Morovic (2017a, 2017b)
Lb. fermentum PCCV
R
Pro-Bio PCC Phamanex, LLC. West et al. (2011)
BioOneTM Lb. fermentum ME-3V
R
SpectrumceuticalsPty Ltd., Australia Lb. fermentum ME-3 Mikelsaar and Zilmer (2009)
Life-SpaceProbiotic Lifespace communities, inc. Lb. fermentum CECT5716 Lara-Villoslada et al. (2009)
HEREDITUMV Probiotic
R
BIOSEARCH S.A. Granada (Spain) Lb. fermentum LC40 (CECT5716) Popova, Mitev, and Nikolov (2016)
LACTEOL Lacteol Laboratory, France Mixture of Lb. fermentum and Lb. Salazar-Lindo et al. (2007)
delbrueckii
Lactobacillus fermentum AMBIO Co., Ltd., Korea Lb. fermentum Cox et al. (2010)
probiotic powder
Lactobacillus fermentum Powder Wuhan Healthdream Biological Lb. fermentum Strompfov
a, Laukov
a, and Cilik (2013)
mixed with inulin Technology Co. Ltd., China

attenuation of colorectal cancer (CRC) risk, and prevention Crum-Cianflone 2016). Theoretical risks exist and include
of alcoholic liver disease (Barone et al. 2016; So, Wan, and systemic infections, deleterious metabolic activities, and
El-Nezami 2017; Liu et al. 2019). Also, Owusu-Kwarteng excessive immune stimulation in susceptible individuals, and
et al. (2015) reported on the potential of Lb. fermentum as a potential gene transfer (Doron and Snydman 2015).
technological starter for fermented food products, and as a Notwithstanding these sporadic cases, probiotics are consid-
food preservative agent. For instance, Lb. fermentum is a key ered as safe supported by their long history of applications.
microorganism in sourdough technology, contributing to fla- The most widely used species belonging to Lactobacillus
vor, texture, or health-promoting dough ingredients (De genera include Lb. rhamnosus, Lb. acidophilus, Lb. corynefor-
Vuyst et al. 2009). Recently, Weckx et al. (2010) using a mis, Lb. paracasei, Lb. plantarum, and Lb. jensenii (Su
arez-
meta-transcriptomic approach, revealed that mature wheat Garc
ıa et al. 2012; Franko et al. 2013; Datta et al. 2017; Ait
sourdoughs represent a stabilized ecosystem with Lb. planta- Seddik et al. 2017; Rossi, Amadoro, and Colavita 2019).
rum and Lb. fermentum as the dominating LAB species. Interestingly, Lb. fermentum is included in the list of
Prevalence of both species was also found in sourdoughs taxonomic units proposed by the European Food Safety
from different origins such as rye, spelt, and African amyla- Authority (EFSA 2007) for the qualified presumption of
ceous fermented foods. Genes involved in probiotic and safety (QPS) status (Lara-Villoslada et al. 2009). The main
nutritional functions, including riboflavin synthesis, were representative of this group is Lb. fermentum CECT-5716 a
identified opening new perspectives in the field of the func- probiotic strain isolated from breast milk and selected for its
tional foods based on cereals matrix (Turpin, Humblot, and safety, functionality (EFSA 2007), anti-infectious, and
Guyot 2011; Russo et al. 2014). In Figure 1, the main func- immunomodulatory properties (Zarłok _ 2016). Moreover,
tions and beneficial affects attributed to this species Gil-Campos et al. (2012) and Maldonado et al. (2012)
are reported. established the safety and tolerance of an infant formula
The present review summarizes some of the important supplemented with Lb. fermentum strains among infants
benefits from utilizing Lb. fermentum as a species relative to and suggested the use of such a formula for prevention
the medical sector and as probiotic with multifunctional of community-acquired infection and upper respiratory tract
applications in food preservation, such as the fermenticin infections. Also, this species has been proposed as an
producing strains. efficient mean to treat infectious mastitis during lactation
(Arroyo et al. 2010).
Recently, Jayashree et al. (2018) established the potency
Safety assessment and beneficial attributes of
of Lb. fermentum MTCC 8711 to prevent the adhesion
Lb. fermentum
of methicillin-resistant Staphylococcus aureus (MRSA) to
The use of LAB strains as potential probiotics and medical human colon adenocarcinoma cells, Caco-2. Another
applications has spread out worldwide. The health-promot- research group reported the capability of Lb. fermentum
ing effects of probiotic bacteria are well supported by con- TCUESC-01 to tolerate conditions mimicking the human
vincing clinical trials and studies completed in animal stomach and intestine along with its ability to undergo
models. These health-promoting effects include anti-infective autoaggregation. These attributes accompanied by its sus-
properties (Isolauri et al. 1991), anti-inflammatory activities ceptibility to antibiotics may increase its application as a
(Peran et al. 2006; Rodr
ıguez-Nogales et al. 2017), immuno- potential probiotic strain (Melo et al. 2017). Interestingly,
modulatory activity (Mart
ın et al. 2003) or prevention of encapsulation of Lb. fermentum NCIMB 5221 in poly-L-
allergic diseases (Furrie 2005). Risks and adverse effects lysine-alginate was reported as an effective oral delivery
associated with probiotics use remains rare and often has system (Tomaro-Duchesneau et al. 2012). This encapsula-
not been assessed in randomized controlled trials (Hempel tion permitted the bacterium to survive simulated gastro-
et al. 2011; Zawistowska-Rojek and Tyski 2018). Different intestinal conditions and a 2.5 log gain in viability versus
investigators, have nevertheless, reported bacteriemia, endo- free cells (non-capsulated cells) with, respectively,
carditis, ulcerative colitis, and other associated risks espe- 5.50
106 ±1.00
105 and 1.10
104 ±1.00
103 CFU/mL.
cially in immunocompromised patients upon probiotics Another relevant application of fresh or lyophilized cul-
uptake (Franko et al. 2013; Meini et al. 2015; Haghighat and tures containing (107 to 109 CFU) of Lb. fermentum
 CRITICAL REVIEWS IN FOOD SCIENCE AND NUTRITION 3

Figure 1. Schematic representation of probiosis, immunobiosis, and biopreservative activity of Lactic Acid Bacteria (LAB).

CCM-7421 was in healthy dogs and for those suffering the effect of Lb. fermentum LA-12 for the prevention of
from gastrointestinal disorders during 4-days to 14-days alcoholic steatohepatitis in a rat model, via the gut-liver
treatment (Strompfov
a, Kubasov
a, and Laukov
a 2017), axis. Four-week administration of Lb. fermentum LA-12
arguing for a positive impact on the health of restored the intestinal barrier function and reduced alcohol-
these animals. induced inflammatory mediators, indicating a potential
claim of this strain, in attenuating leaky gut and liver dam-
age, or preventing the progression of alcoholic steatohepati-
Lactobacillus fermentum as probiotic for health tis (ASH). Barone et al. (2016) reported in mice that Lb.
applications fermentum, reduced considerably ethanol-induced tissue
Alcoholic liver disease (ALD) prevention damage and can be used as probiotic with therapeutic
potential for alcoholic liver disease. According to Sharma
Alcoholism is a devastating disease, with its pathogenesis et al. (2014), which led a study on ageing mice, Lb. fermen-
characterized by progressive accumulation of lipids in the tum could be utilized to protect the liver for preventing
liver, inflammation, steatohepatitis, and in some individuals, endotoxemia by improving the intestinal barrier function or
the final stages include fibrosis and cirrhosis (Barone et al. by enhancing the antioxidant activity of glutathione peroxid-
2016). Probiotics have received increasing attention in the ase and glutathione reductase. However, no clinical study
past few years due to their well-documented gastrointestinal has been conducted with humans. So, the beneficial effects
health-promoting claims. Byoung-Kook et al. (2017) studied of probiotic strains of Lb. fermentum on diseases related to
4 K. NAGHMOUCHI ET AL.

alcohol over-consumption remain to be established among the gene expression level of MUC2 mRNA in both the
human patients. jejunum and ileum of broiler chickens (Cao et al. 2012).
Remarkably, Lb. fermentum CECT-5716 was able to pro-
duce glutathione, a natural antioxidant, which reportedly
Lactobacillus fermentum effect on gastrointestinal and
protects the intestine from oxidative damage (Peran et al.
upper respiratory tract infections
2006). Lb. fermentum Lee (LF-Lee) also had a potential
Probiotics are becoming increasingly popular as a nutrition functional activity and a preventive effect on constipation
supplement to reduce susceptibility to common infectious in mice. After LF-Lee treatment, the time to the first black
illnesses, such as upper respiratory tract (URT) and stool defecation was only marginally longer than that in
gastrointestinal (GI) illness. Investigators have reported that mice treated with bisacodyl with reportedly improved acid
probiotic supplementation could be useful for enhancing resistance, bile tolerance and improved hydrophobic
immunity and reducing the duration of URT and GI illness properties (Qian et al. 2015). Lb. fermentum Lc40 (200
among endurance athletes (Tiollier et al. 2007; Gleeson et al. million CFU/day) was also shown to decrease the incidence
2011). Nevertheless, both studies present a lack of proper of infantile gastrointestinal and respiratory infections in
control studies using conventional formulations to compare a 3 years follow-up study in infants (Maldonado-Lob
on
the effects observed with Lb. fermentum probiotics. et al. 2015).
West et al. (2011) reported that Lb. fermentum (PCCV) can
R

be a useful nutritional adjunct for healthy exercising males.

Supplementation with the probiotic PCCV reportedly Lactobacillus fermentum as preventive agent in
R

reduced the severity of self-reported symptoms and severity colorectal cancer (CRC)
of gastrointestinal symptoms at higher training regimens Several probiotic formulations containing Lb. fermentum,
among male athletes (West et al. 2011). The increased fre- typically those surviving in both gastrointestinal (Gardiner
quency of mild, low-grade symptoms of GI illness can reflect et al. 2002a) and genital environments (Gardiner et al.
short-term adaptive responses in the GI tract with probiotic 2002b), and were found to reduce infection (Lopez-Huertas
with use of PCCV. On the other hand, prophylactic adminis-
R

2015) and overgrowth of harmful bacteria (Stotzer et al.

tration of probiotic Lb. fermentum (PCCV) at a daily dose of
R

1996). Lb. fermentum has also been associated with benefi-

1.26
1010 as a freeze-dried powder in gelatin capsules
cial properties by attenuating the risk of colorectal cancer
resulted in a substantial reduction in the severity of respira-
(CRC) development (Kahouli et al. 2017; So, Wan, and El-
tory illness among athletes (Cox et al. 2010). Affirmative
Nezami 2017; Nazir et al. 2018). Kahouli et al. (2015) uti-
conclusions remain difficult to establish in the case of con-
lized an Apc Min/þ mouse model to demonstrate the use of
comitant uptake of traditional medications that could poten-
probiotics as a preventive agent for colorectal cancer. It was
tially interfere with the results expected from the use of a
suggested based on clinical and pre-clinical studies; this was
probiotic (Cox et al. 2010; West et al. 2011).
often linked to the potency of short-chain fatty acids
Other investigators reported that administration of
(SCFAs) in the gut. Lb. fermentum NCIMB-5221 showed
a follow-on formula with Lb. fermentum CECT-5716 can be
useful for the prevention of community-acquired gastro- resistance to simulated intestinal fluid (SIF) (16.3 ± 1.9%
intestinal and upper respiratory infections among infants minimum, 72 h, p ¼ .006) and produced SCFAs in SIF at
between 6 and 12 months old (Maldonado et al. 2012; concentrations high enough to significantly inhibit Caco-2
Lopez-Huertas 2015). The experimental group showed 46% proliferation (74.73 ± 2.1%, 72 h). It was concluded that
reduction in the incidence rate of gastrointestinal infections NCIMB-5221 strains could potentially be considered as bio-
and 27% reduction in the incidence of upper respiratory therapeutic agent against CRC.
tract infections at the end of the study period compared Other investigators documented that Lb. fermentum
with the control group. Lb. fermentum CECT-5716 is also NCIMB-5221 has a significant antioxidant, anti-proliferative,
capable of fermenting a variety of carbohydrates in the and pro-apoptotic effect on CRC cells, principally when
intestine and producing short-chain fatty acids (SCFAs), used in combination with Lb. acidophilus ATCC 314 (La-
which are an important source of energy for intestinal cells Lf). The anti-cancer activity of La-Lf co-culture was
(Peran et al. 2006). SCFAs increase the absorption of water significantly enhanced in vitro with significant reduced pro-
and salt in the intestine, participate actively in colon liferation (30 8.8 ± 6.9%, p ¼ .009) and increased apoptosis
epithelial cell metabolism and reduce the pH value, thereby (413 RUL, p < .001) toward cancer cells, as well as signifi-
supporting the growth of healthy bacteria and inhibiting the cant protection of normal colon cell growth from toxic
growth of pathogenic microorganisms. Olivares et al. (2006) treatment (18.6 ± 9.8%, p ¼ .001) (Kahouli et al. 2017).
reported that Lb. fermentum CECT-5716 inhibited the adhe- The concomitant administration of Lb. fermentum and
sion of pathogens to the intestinal mucosa and caused Lb. plantarum showed a synergistic impact for the control
elimination of some pathogens. Notably, Lb. fermentum also of colorectal cancer in mice. An increase in body weight,
induced the production of mucin which is the initial barrier a decrease in ammonia concentration, a decrease in b gluco-
of the intestinal epithelium as protection against infections. sidase and b glucuronidase enzyme activity and a reduction
An in vivo study showed that Lb. fermentum 1.2029 sig- in the number of crypts (level of inhibition of about 90%) in
nificantly increased goblet cell density in the jejunum and the mice in the pre-carcinogen-induced group was reported
 CRITICAL REVIEWS IN FOOD SCIENCE AND NUTRITION 5

when compared to these variables in the post-carcinogen- studies and the capability of probiotic Lactobacillus strains
induced group (Asha 2012a). to remove cholesterol from media, especially under simu-
lated intestinal conditions, demonstrates their potential use
as cholesterol-lowering agents (Zhuang et al. 2012; Tomaro-
Lactobacillus fermentum and immune health Duchesneau et al. 2014; Bendali et al. 2017). Tomaro-
Investigators have reported the immunological effects of Lb. Duchesneau et al. (2015) reported that Lb. fermentum
fermentum among healthy adults and infants. Specifically, NCIMB (5221 and 2797) can offer multiple advantages, such
oral administration of lactobacilli enhanced both innate and as cholesterol assimilation, colon epithelial adhesion, and
adaptive immunity by increasing IgA synthesis, which may inhibition of cholesterol uptake by colon epithelial (Caco-2)
contribute to the LAB anti-infectious properties in combat- cells in vitro. It was reported that Lb. fermentum NCIMB
ing infectious diarrhea (Kaila et al. 1992) and improved the 5221 decreased cholesterol uptake by about 85.98 ± 2.07%
function of natural killer (NK) cells (Nagao et al. 2000). A comparatively to the untreated group in animal models.
human RCT performed by Olivares et al. (2007) determined Among artificially induced hyperlipidemia imprinting con-
that oral administration of Lb. fermentum CECT-5716 trol region (ICR) mice, Lb. fermentum SM-7 in feed was
enhances the immunologic response of an influenza vaccine able to reduce cholesterol by 66.8% while also reducing total
(12% increase in specific antibodies) and protects against triglyceride levels, low-density lipoprotein (LDL), cholesterol
subsequent infection by increasing the Th-1 response concentrations, and atherogenic index (Pan, Zeng, and Yan
and virus-neutralizing antibodies (37.5% reduction in the 2011). Utilizing human volunteers Kullisaar et al. (2016)
incidence of an influenza-like illness). The vaccination reported that the level of LDL cholesterol as well as total
stimulated an increase in Th-1 cytokines and in T-helper cholesterol and oxLDL decreased significantly in all partici-
and T-cytotoxic proportions; however, some of these pants and high-density lipoprotein (HDL) cholesterol
increases were significantly higher after administration of showed a tendency of improvement after 4 weeks of con-
Lb. fermentum CECT-5716-probiotic group (10 billion sumption of Lb. fermentum ME3 containing the food sup-
CFU). Remarkably, antibody induction was observed in the plement Reg’Activ Cholesterol.
probiotic group with a significant increase in antigen-spe-
cific IgA. Similarly, probiotic Lb. fermentum VRI-003
Lactobacillus fermentum and food processes
(PCCV) enhances the mucosal immune system of elite ath-
R

letes. Probiotic (PCCV) given at a daily dose of 1.26
1010

R
Bioprocessing (fermentation) has been used to produce a
(as a freeze-dried powder in gelatin capsules), elicited a sig- wide range of foods and food ingredients ever since the ear-
nificant increase in whole-blood culture interferon gamma liest recorded food preservation by humans. Bioprocessing
(IFNc), compared with placebo used as control treatment technology has developed this further, with specialized pro-
(Cox et al. 2010). Recently, Lim et al. (2017) reported that duction of food and feed ingredients or processing aids
Lb. fermentum IM12 attenuates inflammation in mice by (Bernardeau, Guguen, and Vernoux 2006). Lactobacilli are
inhibiting the NF-jB-STAT3 signaling pathway. Oral microorganisms that are extensively used in food microbiol-
administration of probiotic IM12 (0.2
109, 1
109 or ogy as technological starters among fermented products, for
5
109 CFU/mouse, once a day for 3 days) in mice with preserving food by inhibiting contamination causing food-
carrageenan-induced hind-paw edema (CIE) significantly borne illness or food spoilage and as probiotics due to their
suppressed the increase of edema volume. The treatment strain-specific, health-improving properties (Arena et al.
also activated nuclear factor kappa beta (NF-jB) and the 2016). LAB producing exopolysaccharides (EPS) have
signal transducer and activator of transcription 3 (STAT3). received attention in recent years, due to their useful role in
Lb. fermentum CECT-5716 could support the natural and improvement of physical, rheological, and sensory properties
acquired immune response which was shown by an activa- of fermented milks such as dahi, yoghurt, lassi, and cultured
tion of the NK cells and T-reg cells in vitro (Perez-Cano, buttermilk (Behare et al. 2013). Lb. fermentum is an exopo-
Dong, and Yaqoob 2010). lysaccharides (EPS) producing and heterofermentative LAB
Recently, the probiotic strain Lb. fermentum UCO-979C (Leo et al. 2007; Dan et al. 2009). Low fat artisanal cheese
was reported to differentially modulate the immune (dahi) prepared using the EPS producing strain Lb. fermen-
response of intestinal epithelial cells (IECs) via Toll-like tum V10 exhibited optimum acid production, less whey sep-
receptor 4 (TLR4) activation and through the modulation of aration, high viscosity, increased adhesiveness and stickiness,
TLR negative regulators expression (Garcia-Castillo et al. decreased firmness conversely to non-inoculated cheese
2019). And, this has been demonstrated in vivo to increase (Behare et al. 2013). Recently, Nielsen et al. (2017) reported
intestinal IgA (Garcia-Castillo et al. 2019). that in a fermented milk product, Lb. fermentum (107 CFU/
g) is capable of helping maintain a pH above 4.0 when
stored for at least 14 days at 25  C.
Lactobacillus fermentum cholesterol-lowering effect
Owusu-Kwarteng et al. (2015) reported Lb. fermentum as
Human cardiovascular and coronary artery disease risks are functional starter cultures, with inherent functional charac-
correlated with high cholesterol levels and are significant teristics contributing to more organoleptic, nutritional, and
health concerns (Ait Seddik et al. 2017). LAB have been technological or health-promoter benefits (probiotics). For
demonstrated to have cholesterol-reducing effects in many instance, the application of Lb. fermentum strains were able
6 K. NAGHMOUCHI ET AL.

to enrich, in situ, the riboflavin content of fermented foods 1967). This inhibitory compound, called bacteriocin 466,
of cereal origin, as reported by Russo et al. (2014). Also, Lb. was later reported to have similar characteristics as lactacin
fermentum produces antimicrobial substances to inhibit the 27 produced by L. helviticus (Upreti and Hinsdill 1975). Still
growth of spoilage and/or pathogenic bacterial strains in terms of bacteriocins production by this species, Yan and
(Barman et al. 2017). The production of lactic acids leads to Lee (1997) identified a bacteriocin, fermenticin B, produced
a decrease in pH value in the intestine by which pathogenic by Lb. fermentum Beijerinck CCRC 14018. This bacteriocin
microorganism growth is reduced compared to controls. showed the common characteristic of small bacteriocins,
Lb. fermentum CECT-5716 also increases the membrane with a molecular size less than 3–5 kDa with heat and pH
permeability of Gram-negative bacteria, thereby reducing stability as well as sensitivity to the action of proteolytic
their viability and enhancing their exposure to bactericidal enzymes.
compounds (Olivares et al. 2006). Bacteriocins produced by LAB generally have a narrow
Since Lb. fermentum is also present in fermented plant activity spectrum (Soomro, Masud, and Anwaar 2002),
material, it constitutes a part of the bioprocessing phenom- nevertheless some bacteriocins produced by Lb. fermentum
enon occurring in their transformation (Madoroba et al. strains designated as fermenticins are endowed with wide
2011; Oguntoyinbo et al. 2011; Illeghems et al. 2012). spectrum activities. This is the case of fermenticin L23 and
Among plants by-products, chocolate is a product of cocoa fermenticin SD11, which were reportedly inactivated both
bean fermentation where Lb. fermentum is reported as the Gram-positive and Gram-negative bacteria, and even were
predominating bacterial species (Lefeber et al. 2010). active against some fungi (Pascual et al. 2008; Wannun,
Sawadogo-Lingani et al. (2007) reported that Lb. fermentum Piwat, and Teanpaisan 2016). The first report establishing
is the dominating LAB species for Sorghum (Sorghum antagonistic activity was provided by Aslim et al. (2005),
caffrorumor and S. vulgare), an alcoholic beverage produced who isolated from various dairy products several lactobacilli
by malting and characterized by a two-stage (lactic followed strains, including Lb. fermentum 25 with antagonism toward
by alcoholic) fermentation (Tamang, Watanabe, and Gram-positive Staphylococcus aureus, and against Gram-
Holzapfel 2016). negative pathogens such as Escherichia coli and Yersinia
enterocololitica. These activities were ascribed to production
of bacteriocin-like inhibitory substance which was unique
Lactobacillus fermentum bacteriocinogenic strains
for its heat-stability and structurally for its high molecular
Like other lactobacilli, many Lb. fermentum strains produce size of 29 kDa based on the SDS-PAGE data. The antimicro-
antimicrobial peptides, bacteriocins, which are ribosomal bial activity was reportedly a potential large bacteriocin
synthesized peptides produced by both Gram-negative and relative to the majority of LAB bacteriocins from previous
Gram-positive bacteria (Drider and Rebuffat 2011). These publications (Aslim et al. 2005). Furthermore, Klayraung
compounds were found to be involved in the antimicrobial and Okonogi (2009) described the mode of action of
activities observed for lactobacilli strains in food bio-preser- a bacteriocin produced by two Lb. fermentum strains
vation and in the biomedical field (Mokoena 2017; Singh FTL2311 and FTL10BR isolated from Miang, a traditional
2018). Although most of the bacteriocinogenic lactobacilli Thai fermented tea leaves. These strains were active against
strains are isolated from various sources, including meat, Listeria monocytogenes DMST 17303, Salmonella Typhi
fish, fruits, vegetables and milk (Ait Seddik et al. 2017; DMST 5784, Shigella sonnei DMST 561 (ATCC 11060) and
Mokoena 2017), Lb. fermentum, producing such antimicro- Staphylococcus aureus subsp. aureus DMST 6512. Scanning
bial compounds, are mostly isolated from fermented Electron Microscopy (SEM) images revealed that the inhibi-
food, raw milk, human vaginal microbiota, the oral ecosys- tory compounds from Lb. fermentum strains FTL2311 and
tem, breast milk or gastrointestinal tract (von Mollendorff, FTL10BR targeted the cell membrane ultrastructure leading
Todorov, and Dicks 2006; Ilayajara, Radhamadhavan, and to disruption and shrinking of the pathogenic bacteria cells
Nirmala 2011; Kaewnopparat et al. 2013; Kaur et al. 2013a; (Klayraung and Okonogi 2009). However, the lack of data
Riaz, Nawaz, and Hasnain 2010; Sabia et al. 2014; Zahid on the characterization of the inhibitory compounds from
et al. 2015; Morovic 2017a). Interestingly, bibliographic these strains did not allow their classification.
references related to bacteriocinogenic Lb. fermentum strains Interestingly, von Mollendorff, Todorov, and Dicks
are less abundant comparatively to other species such as Lb. (2006) described two strains reported as Lb. fermentum
plantarum, Lb. gasseri or Lb. salivarius. In the first report on JW11BZ and JW15BZ isolated from Boza, a Balkan
an antagonistic Lb. fermentum strain, the latter was isolated fermented food. The inhibitory activity was expressed in a
from human saliva and was able to produce a proteinaceous strain-dependent manner against one Gram-negative bacter-
inhibitory compound (De Klerk and Coetzee 1961). ium Klebsiella pneumoniae (strain referred as K. pneumoniae
Later De Klerk and Smit (1967), published a report on the 30) and other bacteria including Listeria spp. as well as
same Lb. fermentum strain, mentioning the production of an other LABs, mostly Enterococcus and Lactobacillus strains.
antimicrobial lipid-carbohydrate heat stable complex. The The biochemical characterization of these inhibitory
characterization of this inhibitory compound has resulted in compounds resulted in identification of a low molecular size
identification of at least 16 amino acids in the peptide and peptide of approximatively 2.3–3.3 kDa. Because of the
was sensitive to proteolytic enzymes (Trypsin and Pepsin) increase in bacterial antibiotic resistance worldwide during
but remained insensitive to lysozyme (De Klerk and Smit the last decades, different alternatives are currently being
 CRITICAL REVIEWS IN FOOD SCIENCE AND NUTRITION 7

Table 2. Characteristics of some bacteriocins produced by Lb. fermentum strains.

Strain Origin Bacteriocins characteristics Sensitive bacteria Reference
Lb. fermentum 25 Fermented dairy product Large peptide of 29 kDa S. aureus, E. coli, Yersinia Aslim et al. (2005)
enterocolitica
Lb. fermentum Lf3 Fecal sample Estimated molecular weight Vibrio cholerae subsp. inaba, Asha (2012b)
on SDS-PAGE (104 kDa) Shigella dysenteriae
Lb. fermentum SK5 Vagina of healthy women ND E. coli, G. vaginalis Kaewnopparat et al. (2013)
Lb. fermentum HV6b Human vaginal ecosystem Fermenticin HV6b Class IIa Bacillus fragilis, B. ovatus, B. Kaur et al. (2013a, b)
vulgatus, Candida albicans,
C. sporogenes, E. coli,
Enterococcus faecalis, G.
vaginalis, Klebsiella
pneumoniae, Leuconostoc
mesenteroides, L.
monocytogenes,
Mariniluteicoccus flavus,
Neisseria. gonorrhoeae, N.
mucosa, P. aeruginosa, P.
mirabilis, Staphylococci,
Streptococci, Salmonella
typhi, Vibrio cholerae.
Lb. fermentum L23 Vagina of healthy women Bacteriocin L23 (7kDa) Gram-positive and Gram- Pascual et al. (2008)
negative food spoilage and
pathogenic bacteria, C.
albicans, C. glabrata
Proteus and clinical strains
of C. albicans
Lb. fermentum 466 Human saliva Bacteriocin 466 Other LAB De Klerk and Smit (1967)
(>16 aminoacids)
Lb. fermentum Milk product Approximatively 8 kDa E. coli, S. aureus, S. typhi, Saranya and
Pseudomonas and Klebsiella Hemashenpagam (2011)
Lb. fermentum SBS001 Marine water sample Large peptide (78 kDa) Kleibsiella oxytoca, P. Singh et al. (2013)
aeruginosa, E. coli, S.
paratyphi, P. mirabilis, V.
cholerae, K. pneumoniae.
Lb. fermentum JW11BZ Boza brevage BacJWBZ, bacJW15BZ (2 LAB, Streptococcus sp. TL2R, S. von Mollendorff, Todorov,
and JW15BZ to 3kDa) caprinus, L. innocua and Dicks (2006)
Lb. fermentum SD11 Human saliva Fermenticin SD11 (33 kDa) LAB, Streptococcus mutans, S. Wannun, Piwat, and
sobrinus, C. albicans, Teanpaisan (2016)
Flavobacterium nucleatum,
Porphyromonas gingivalis
Lb. fermentum GA715 Goat milk Fermenticin SA715 (2 kDa) Micrococcus luteus ATCC Wayah and Philip (2018)
10240, Corynebacterium
spp. GH17, Bacillus cereus
ATCC, P. aeruginosa PA7
and E. coli UT181
Lb. fermentum Beijerinck Collection of Fermenticin B (<3 kDa) LAB, Micrococcus luteus Yan and Lee (1997)
CCRC 14018 Culture and Research
Center (CCRC) Taiwan
Lb. fermentum CS57 Vaginal secretion Peptide (>30 kDa) S. agalactiae, C. albicans Sabia et al. (2014)

considered to address this issue. The use of probiotics stands Ross, and Hill 2013; Allen et al. 2014). Remarkably,
as one potential alternative but also LAB bacteriocins are many Lb. fermentum strains were assessed as protective
emerging as a new group of therapeutic agents (Drider et al. against urinary tract and oral infections, vaginosis (Ilayajara,
2016; Vieco-Saiz et al. 2019). Currently, most published Radhamadhavan, and Nirmala 2011; Kaur et al. 2013a,
studies on LAB bacteriocins have been focused on biomed- 2013b; Asha 2012b; Adebayo, Afolabi, and Akintokun 2014;
ical applications, searching for alternative strategies against Wannun, Piwat, and Teanpaisan 2016; Ouarabi et al. 2019)
cancer, systemic infections, oral-care, vaginal infections, and mainly against multidrug resistant strains including
contraception, skincare, and emerging multidrug resistant MRSA or against pathogenic yeasts such as Candida albicans
bacteria (Al Atya et al. 2016a, 2016b; L
opez-Cuellar, or C. glabrata (Pascual et al. 2008; Zahid et al. 2015) as
Rodr
ıguez-Hern
andez, and Chavarr
ıa-Hern
andez 2016; Kang reported in Table 2. Kaur et al. (2013a) showed the spectra
et al. 2017). To highlight this point, studies as that published of Fermenticin HV6b, a class IIa bacteriocin produced by
by Riaz, Nawaz, and Hasnain (2010) described antagonistic Lb. fermentum HV6b MTCC 10770 isolated from human
activities of Lb. fermentum 45 against cephalosporin resistant vaginal ecosystem. Indeed, Fermenticin HV6b reported
E. coli isolated from a patient in a Lahor hospital (Pakistan). antagonistic activities against many pathogenic microorgan-
This inhibition was ascribed to production of a heat stable isms associated with vaginal infections such as Bacteroides,
bacteriocin (Riaz, Nawaz, and Hasnain 2010). Since then, Gardnerella vaginalis, Mobiluncus, Staphylococci, and
investigations addressing suitability of bacteriocinogenic Streptococci (Kaur et al. 2013a, 2013b).
strains as alternatives to treat infections or as probiotics Tulumoglu, Kaya, and Şimşek (2014) investigated
promoting the health of the host have increased (Cotter, two strains of Lb. fermentum LP3 and LP4 isolated from
8 K. NAGHMOUCHI ET AL.

a traditional Tulum Turkish cheese, which were selected biofuels such as alcohol because of their tolerance to low pH
for their antagonistic effect towards a set of pathogenic or high alcohol concentrations. Lb. fermentum among other
microorganisms. Moreover, the authors established the lactobacilli are homolactic, but can produce alcohol as a
probiotic potential of both Lb. fermentum LP3 and LP4. metabolic byproduct. However, the bacterium was not resist-
In addition to producing potent inhibitory compounds, ant to ethanol and low pH, but apparently will replicate in
these strains have fulfilled the criteria to be considered the presence of 5% NaCl (Bosma, Forster, and Nielsen
as potential probiotics (Tulumoglu, Kaya, and Şimşek 2014). 2017). Another potential health benefit of LAB is the pro-
A previous study by Kaewnopparat et al. (2013) established duction of vitamins such as riboflavin and overproduction
that a bacteriocinogenic strain Lb. fermentum SK5, of this metabolite could potentially be utilized as cell facto-
with high adhesion abilities to Caco-2, HT-29, and HeLa ries (Arena et al. 2014; Thakur, Tomar, and De 2016).
epithelial cells prevented binding and growth of E. coli and Reportedly, riboflavin production in Lb. fermentum KTLF1
G. vaginalis onto intestinal and vaginal epithelial cells there- occurs in MRS medium (Thakur and Tomar 2016) and
fore providing a protective barrier against these pathogens. Jayashree, Jayaraman, and Kalaichelvan (2010) reported an
The study by Kaewnopparat et al. (2013) revealed the efficient riboflavin-producing bacterium Lb. fermentum
potential of Lb. fermentum SK5 to reduce the proliferation strain MTCC 8711 produced 2.29 mg/l of riboflavin in
of some pathogens potentially via co-aggregation traits. Also, chemically defined media after 24 h. Moreover, Lb. fermen-
Lb. fermentum SK5 produces a potent BLS. Taken together, tum can be genetically engineered for production of manni-
these studies indicate that the Lb. fermentum SK5 strain tol and pure L-lactic acid or pyruvate (Aarnikunnas et al.
is a good candidate for probiotic development mainly 2003) which opens the possibility for further research in the
for its protective claims against GI and vaginal microbial over production of metabolites by this bacterium as well as
infections (Kaewnopparat et al. 2013). other LABs.
The use of bacteriocinogenic Lb. fermentum strains for
food preservation was reported also for use in several dairy Conclusions
products, vegetables, fruits or juices (Saranya and
Hemashenpagam 2011; Nithya et al. 2012; Adebayo, Afolabi, In conclusion, Lb. fermentum could potentially be more
and Akintokun 2014; Adedokun et al. 2016; Wayah and widely utilized as a probiotic to control gastrointestinal
Philip 2018). These investigators studied the effect of these infections due to Campylobacter jejuni (Lehri, Seddon,
Lb. fermentum strains and their bacteriocins to control a wide and Karlyshev 2017b) and other foodborne bacterial disease
range of spoilages microorganisms such as E. coli, S. aureus, agents. Additional benefits include applications to reduce
Salmonella typhi, Proteus mirabilis, Pseudomonas aeruginosa, inflammation during colitis (Rodr
ıguez-Nogales et al. 2017)
Bacillus cereus, L. monocytogenes, and Micrococcus luteus and provide alternative antimicrobials against other patho-
(Nithya et al. 2012; Wayah and Philip 2018). These bacterio- gens such as multi-resistant Staphylococcus aureus (Kang
cins reportedly also had anti-biofilm inhibitory activities et al. 2017). Importantly, Lb. fermentum has also been inves-
(Rybalchenko et al. 2015). Most of the recently identified bac- tigated as a potential anti-cancer treatment (Liu et al. 2019),
teriocins have a wide activity spectra, including antagonism even as an anti-aging agent (Hor et al. 2019; Schifano et al.
against Gram-positive and Gram-negative pathogens, and 2019) and as a potential anti-diabetic in combination with
likely against pathogenic yeasts. Nevertheless, a number other LAB (Yadav et al. 2018). Although the investigations
of these molecules are high molecular size, up to 30 kDa, are preliminary and were completed in animal models, these
as depicted in Table 2. Despite these unusual biochemical results indicate potential future use as treatments among
characteristics, bacteriocin-like activities from Lb. fermentum humans. The antimicrobial activities due to bacteriocins
strains need to be investigated to gather insights into produced by Lb. fermentum have been reported herein and
characterization of potential new antimicrobials and their further add to the list of positive effects produced by this
mechanisms of action. Even so, all the studies performed on bacterium to improve human and animal health.
bacteriocinogenic Lb. fermentum strains provide promising
beneficial applications in food preservation and medical areas. Acknowledgements
A recently developed in silico genome approach has allowed
investigators to assess the probiotic-associated traits after ana- YB and DD would like to thank la region des Hauts-de-France for
providing funds.
lysis of the genome of Lb. fermentum 3872 strain (Lehri,
Seddon, and Karlyshev 2017a). Indeed, upon a comparative
genomic analysis, several genes contributing to probiotic prop- Funding
erties such as those coding for mucus and collagen-binding
Funded by R
egion des Hauts de France through ALIBIOTECH CPER/
proteins, exopolysaccharides and a putative class III bacteriocin FEDER project (2016-2020).
were reported (Lehri, Seddon, and Karlyshev 2017a, 2017b).

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