Biocatalysis and Agricultural Biotechnology 50 (2023) 102702

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Biocatalysis and Agricultural Biotechnology

journal homepage: www.elsevier.com/locate/bab

The inhibitory effects of lactic acid bacteria isolated from

sourdough on the mycotoxigenic fungi growth and mycotoxins
from wheat bread
Imane EL Houssni a, *, Khadija Khedid b, Ahmed Zahidi c, Rachida Hassikou a
a Botany and Valorization of Plant Resources Team, Plant and Microbial Biotechnology, Biodiversity and Environment Research Center, Faculty of
Sciences, Mohammed V University, Rabat, Morocco
b Department of Microbiology, National Institute of Health, Rabat, Morocco
c Department of Drug Sciences, Laboratory of Medicinal Chemistry, Faculty of Medicine and Pharmacy, Mohammed V University, Rabat, Morocco

ARTICLE INFO ABSTRACT

Handling Editor: Ching Hou Bread is a food stable for human nutrition. Its nutritional profile not only meets the nutritional
and metabolic needs of humans but also is a suitable substrate for the growth of mycotoxigenic
Keywords:
fungi. Chemical preservatives are often used as food preservatives to control the contamination of
Wheat bread
bread by potentially mycotoxigenic fungi. However, their long-term consumption may increase
Sourdough
LAB
the risk of chronic diseases. With the growing consumer demand for healthy foods with minimal
Mycotoxigenic fungi use of chemical preservatives, the use of biological preservatives, including lactic acid bacteria
Mycotoxins (LAB), has gained renewed interest in recent years. LABs have been used for centuries in the
preparation and preservation of bread and are generally recognized as safe (GRAS). The aim of
this study is to yield knowledge about lactic acid fermentation and the activity of lactic acid bac-
teria against mycotoxigenic fungi and their mycotoxins. A search was conducted on a range of
databases (MEDLINE via PubMed, Scopus, and Web of Sciences), over the period from 1979 to
2021 using keywords related to the capacity of lactic acid bacteria isolated from sourdough to
control the growth of mycotoxigenic fungi and detoxify their mycotoxins. In addition to improv-
ing the organoleptic and nutritional quality of wheat bread, the use of LAB in sourdough ensures
the microbiological safety by acting as potential natural preservatives against contamination
with mycotoxigenic fungi. Their action mechanisms involve the production of antagonistic com-
pounds that inhibit the growth of mycotoxigenic fungi (organic acids, reuterin, fatty acids, hydro-
gen peroxyde, and cyclic dipeptides compounds), and parietal adsorption and biotransformation
into non-toxic by-products to detoxify the wheat bread from mycotoxins. The promising effects of
LAB against mycotoxigenic fungi and their mycotoxins will lead to many applications in the agri-
food sector that meet health and environmental concerns. The pathways and mechanism of ac-
tion of lactic acid bacteria as detoxifying could be also investigated by clinicians-toxicologists for
targeted food poisoning therapy by clinicians associated with toxicology. Overall, the use of LAB
as a biological alternative to chemical preservatives for reducing mycotoxigenic fungi and myco-
toxins contamination has the potential to transform the agri-food sector while improving human
health and environmental outcomes.

* Corresponding author.
E-mail addresses: imaneelhoussni@gmail.com (I. EL Houssni), kkhedid200605@yahoo.fr (K. Khedid), a.zahidi@um5r.ac.ma (A. Zahidi), r.hassikou@um5r.ac.ma
(R. Hassikou).

https://doi.org/10.1016/j.bcab.2023.102702
Received 23 February 2023; Received in revised form 30 March 2023; Accepted 12 April 2023
Available online 13 April 2023
1878-8181/© 2023 Elsevier Ltd. All rights reserved.
I. EL Houssni et al. Biocatalysis and Agricultural Biotechnology 50 (2023) 102702

1. Introduction
Currently, microbial foodborne diseases are one of the major concerns in terms of public health worldwide, with millions of cases
reported annually (Centers for Disease Control and Prevention, 2022). The pathogenicity of microbial contaminants in foodstuffs de-
pends on the health effect of infectious, invasive, or toxic microbial contaminants. The toxigenicity of certain fungi is related to the
ability to produce toxins in foods, resulting in harmful effects on consumers. Examples of such fungi include Aspergillus, Penicillium,
and Fusarium species, which are known to produce mycotoxins such as aflatoxins, ochratoxins, and trichothecenes, respectively (Pitt
and Miller, 2017). The production of mycotoxins by fungi is influenced by several factors, including the type of fungus, the type of
food, and the environmental conditions (Mahato et al., 2020). The ability of fungi to produce mycotoxins is systematically involved in
the growth of toxic fungi in foodstuffs. In addition, the production conditions of these metabolites are generally more restrictive than
their growth conditions (Dubois-Brissonnet and Guillier, 2020).
Toxic compounds causing ailments relates to susceptibility to the effect. Instead, bread can serve as a substrate for the growth of
toxigenic fungi. These fungi may originate from unintentional contamination of raw materials and manufacturing environments. The
presence of toxigenic fungi can alter the sensory quality of bread due to the undesirable appearance of fungi mycelium visible in the
crust, odors, or unpleasant tastes generated by these fungi metabolisms. This metabolism also produces toxins that deteriorate the
quality of bread, which may lead to a potential microbial food-borne intoxication and have significant commercial implications
(Bryden, 2007; Coton and Dantigny, 2019). In order to solve this problem, many methods have been developed to control toxinogenic
fungi contamination of bread. Currently, these methods focus on physical techniques (radio frequency sterilization, microwave steril-
ization, drying, pulsed-light, and low-pressure mercury lamp treatment) and chemical preservatives (calcium propionate, sorbate,
benzoate, EDTA, nitrite, and sulfite) (Salaheen et al., 2014). These methods have proved to be very effective in inhibiting the growth
of toxinogenic fungi, but they aren't without disadvantages. These disadvantages result in the degradation of the nutritional composi-
tion by physical methods compared to chemical preservatives, which can in the long-term increase the risk of chronic diseases. It is,
therefore, necessary to find a safe and cost-effective solution to the problem of fungal contamination of bread by mycotoxigenic fungi
(Qian et al., 2021). Due to the growing demand for healthy foods and avoiding chemical preservatives and physical preservation
methods, organic preservatives have attracted increasing interest. Among these organic preservatives, lactic acid bacteria (LAB) ex-
hibit strong efficacy by producing certain antagonistic compounds that control the growth of mycotoxigenic fungi (Salaheen et al.,
2014). These microorganisms are widely used in the production of fermented foods such as sourdough. During bread-making, this
functional ingredient, which is mainly composed of LAB, has high antifungal activity against mycotoxigenic fungi and their mycotox-
ins that contaminate bread (Blagojev et al., 2012; Crowley et al., 2013; Varsha and Nampoothiri, 2016). This review aims to present
updated literature on the ability of LAB isolated from sourdough to control the growth of toxigenic fungi, the antagonistic compounds
involved in this process, and the interactions of these microorganisms with the mycotoxins responsible for their elimination in wheat-
based bread.

2. Research methodology
In this review, bibliometric research was done globally, with exclusion and/or inclusion criteria, from databases, including MED-
LINE via PubMed, Scopus, and Web of Sciences. The review used the search terms: Wheat Bread Contamination, Sourdough Microbiota,
Lactic Acid Bacteria, Mycotoxigenic Fungi, LAB as biopreservative, Antagonistic Compound, Mycotoxins parietal adsorption, and Mycotoxins
Bio-transformation. They were searched in sources from 1979 to 2021. There was no language restriction for documentary searches.
All data were extracted, fully read, and validated by the first author. 309 articles were identified; 171 of them were retained, of which
87% concerned full text and 13% were abstract data. The data collected were classified according to different sections. Then, the pub-
lications of each section were organized in tables and explored. These data were finally discussed and highlighted.

3. Results and discussion

3.1. Wheat bread mycotoxigenic fungi contamination
Bread is a food matrix that promotes the development of microbial contaminants during or after production, which causes its dete-
rioration due to its pH (5.0–6.0), and water activity aw (0.95–0.97) (Garcia et al., 2019a). This deterioration can be caused by myco-
toxigenic fungi, mainly belonging to the genera Aspergillus, Penicillium, Fusarium, Mucor, and Rhizopus (Asri et al., 2020). The growth
of these fungi affects the appearance, texture, odor, and taste of wheat bread, while also compromising its hygienic quality through
the production of highly toxic metabolites known as mycotoxins (Cauvain, 2012; Dutton and Kinsey, 1995; Naicker et al., 2007).
These mycotoxins are mainly produced by Aspergillus, Fusarium, and Penicillium genera (Garcia et al., 2019b; Pitt and Hocking, 2009).
While some mycotoxins have antibiotic properties, such as penicillin, others are potential toxins (Oueslati et al., 2012). These toxins
can cause toxic effects when ingested, inhaled, or absorbed by the skin even at low concentrations. Their toxicological effects are vari-
able (Table 1). Some mycotoxins are known or suspected to be carcinogenic, while others are hepatotoxic (Aflatoxins), others are es-
trogenic (zearalenone), immunotoxic, hematotoxic (Patulin, Trichothecenes, Fumonisins), or dermonecrotic (Trichothecenes)
(Bunger et al., 2004; Zain, 2011).

3.2. Sourdough microbiology overview

Wheat is a privileged source of human and animal nutrition. It is mainly a carbohydrate food that contains a significant amount of
fibers, proteins, minerals, vitamins, and secondary metabolites (Slavin, 2004). This nutritional profile not only meets human nutrition
and metabolic needs but provides an appropriate substrate for microbial development (Magallanes López and Simsek, 2020). Gener-

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I. EL Houssni et al. Biocatalysis and Agricultural Biotechnology 50 (2023) 102702

Table 1
- Toxic effects and toxin-producing fungi commonly reported in wheat bread.

Name of Source Toxic effects References

Mycotoxin

Aflatoxin Aspergillus flavus Carcinogen causing hepatocellular carcinoma and also involved in Halt (1994)
Aspergillus parasiticus malnutrition and growth suppression and immunomodulation Magan et al. (2014)
Rushing and Selim
(2019)
Fumonisins Fusarium species particularly Fusarium Immunosuppressing Cendoya et al. (2018)
proliferatum and Fusarium verticillioides Neurotoxic Chen et al. (2018)
Aspergillus niger Nephrotoxic Marìn et al. (2004)
Esophageal cancer Mogensen et al.
Hepatotoxic (2010)
Ochratoxin A Penicillium verrucosum Oxidative stress Mally et al. (2007)
Aspergillus niger DNA damage Pfohl-Leszkowicz et
Aspergillus carbonarius Carcinogenicity al. (1998)
Aspergillus ochraceus Nephrotoxic Wang et al. (2016)
Aspergillus alliaceus Neurotoxic Zhihong et al. (2015)
Kidney damage
Patulin Penicillium and Aspergillus species Carcinogenic Boussabbeh et al.
Immunotoxic (2015)
Neurotoxic Lopez-diaz and
DNA damage Flannigan (1997)
Mansouri et al.
(2014)
Moake et al. (2005)
Trichothecene Fusarium graminearum Alimentary Toxic Aleukia (ATA) Abramson et al.
Fusarium culmorum Immunotoxic (2001)
Fusarium avenaceum Actue toxicity Ilgen et al. (2009)
Haematological disorders Rocha et al. (2005)
Wagacha and
Muthomi (2007)
Zearalenone Fusarium species Reproductive disorders Abd Alla (1997)
Hematotoxic Zaied et al. (2012)
Genotoxic Zinedine et al. (2007)
Hepatotoxic
Immunotoxic

ally, wheat grains are naturally contaminated by eukaryotic (mold and yeast) and prokaryotic (bacteria), concentrated mainly on the
outer layer (Eglezos, 2010; Thielecke and Nugent, 2018). This microbial biota forms a fragile equilibrium, which may affect the nutri-
tional, hygienic, and technological quality of wheat grains. Moreover, this equilibrium is influenced by many factors, especially cli-
mate conditions (mainly temperature and humidity) and biotic factors associated with insect and fungi attacks and the application of
pesticides (Corsetti et al., 2007a; Laca et al., 2006).
Among microorganisms that are naturally associated with wheat grains and their derivatives include LAB. These bacteria may be
endophytic or derived from the outer layer of wheat grains (Berghofer et al., 2003; Gobbetti et al., 2016; Minervini et al., 2015a). In
the latter case, the LAB of paleols, lemmas, glumes, and rachis can be transferred to grains during threshing. After milling, some of the
LAB initially concentrated in wheat grains can be transferred to flour. In fact, the cleaning and conditioning that precedes milling and
the removal of husks reduce the number of LAB (Laca et al., 2006). Therefore, the flour produced should theoretically contain a lower
charge of LAB than grains. However, subsequent conditioning stages can increase the flour LAB content (Berghofer et al., 2003). As a
result, the load will reach levels ranging from 1.3 to 4 log CFU/g presumptive E. faecium, E. casseliflavus, Lc. Lactis, P. pentosaceus, Ln.
Citreum, Lb. Coryniformis, Lb. Brevis, E. mundtii, Lb. plantarum, Lb. sakei, Lb. sanfranciscensis, Ln. mesenteroides, Ln. pseudomesenteroides,
P. acidilactici, E. faecalis, E. hirae, W. cibaria, and W. confusa (Alfonzo et al., 2013, 2017; Corsetti et al., 2001, 2007a; Ennadir et al.,
2014; Nachi et al., 2019; Robert et al., 2009). The presence of Lb. sanfranciscensis is attributed to external contamination, as it is de-
tected in the air surrounding the storage room (Minervini et al., 2015b; Scheirlinck et al., 2009).
These LABs have been found to play a decisive role in sourdough production by inhibiting undesirable indigenous microorgan-
isms, thus preparing the environment for the growth of a typical wheat flour sourdough species (Corsetti et al., 2007b). These species
belong mainly to the genus Lactobacillus (Alfonzo et al., 2013). Frequently, they are represented by the following species Lb. sanfran-
ciscensis, Lb. plantarum, Lb. brevis, Lb. reuteri, Lb. alimentarius, Lb. rossiae, Lb. delbrueckii, Lb. fermentum, Lb. paralimentarius, and Lb.
amylovorus (De Vuyst et al., 2014; Van Kerrebroeck et al., 2017; Minervini et al., 2014). In addition, P. pentosaceus, Ln. mesenteroides,
Lb. brevis, E. pseudoavium, Lb. Curvatus, and Lb. plantarum were also isolated from wheat-based sourdough (Bartkiene et al., 2017).
The LAB microflora in sourdough is significantly dependent how the sourdough is produced.
➢ The sourdough type I produced using a fermentation process characterized by low-temperature incubation and continuous
stirring is primarily dominated by the following Lactobacillus species: Lb. brevis, Lb. paralimentarius, Lb. rossiae, and Lb.
sanfranciscensis (De Vuyst et al., 2009; Liu et al., 2018);

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I. EL Houssni et al. Biocatalysis and Agricultural Biotechnology 50 (2023) 102702

➢ In sourdough type II, Lb. amylovorus, Lb. fermentum, Lb. pontis, and Lb. reuteri species dominate the fermentation characterized
by high temperatures and longer fermentation times with high water content (De Vuyst et al., 2009; Hansen and Schieberle,
2005; Minervini et al., 2014);
➢ On the other hand, type III sourdoughs are known to be colonized mainly by drying-resistant LAB, namely Lb. brevis, P.
pentosaceus and Lb. plantarum (De Vuyst and Neysens, 2005).

3.3. Sourdough lactic acid bacteria as antifungal controlling agent

Many physical and chemical methods have been developed to control the contamination of bread by toxigenic fungi, but there is
no effective practice to eliminate their existence (Fig. 1). Indeed, some fungi are resistant to chemical treatment and certain preserva-
tives. For example, some Penicillium can grow in potassium sorbate, while others can degrade it (Nielsen and De Boer, 2000). Conse-
quently, preventive practices are crucial to limit the development of toxinogenic fungi but are not sufficient to eliminate the risk of
contamination. For this reason, the development of effective and safe processes is of great interest to this purpose. The approach of
controlling a microorganism by another from the same ecosystem has received considerable interest (Magnusson et al., 2003). This
practice applies to cereal cultivation by inoculating wheat fields with non-toxigenic fungal strains. The inoculated strains grow due to
the presence of nutrients, inhibiting the growth of Mycotoxigenic fungi according to the competitive exclusion phenomenon (Galtier
and Draggaci, 2011). In addition, the use of LAB in sourdough can be used to further reduce the risk of contamination during the
bread manufacturing process.
LABs are traditionally used as a natural biopreservative in bread-making. Their preservation effect has gained increasing interest
in recent years due to the growing consumer demand for healthy foods using minimal chemical preservatives, such as sorbates, ben-
zoates and propionates, most often used in bread-making (Gioia et al., 2017). Therefore, the use of sourdough with specific LAB can
be a promising alternative to these additives. Table 2 represents LAB strains isolated from sourdough starters that inhibit the growth
of Mycotoxigenic fungi. The incorporation of P. acidilactici in the bacterial biota of sourdough has enhanced the inhibition of Curvu-
laria lunata compared to sodium benzoate (Mandal et al., 2007). Similarly, fermented sourdough bread with L. plantarum showed an
absence of fungal contamination during storage of 7 days, similar to calcium propionate (Yan et al., 2017). In addition, in situ spraying
of certain Leuconostoc and Lactobacillus strains on bread crust and other bakery products delays the development of certain Mycotoxi-
genic fungi resistant and semi-resistant to sodium propionate, potassium sorbate, and sodium benzoate (Lay et al., 2016). The LAB of
flour/semolina can also have inhibitory effects comparable to some synthetic preservatives. Citing the example of Ln. Citreum, W.
cibaria, and Lb. rossiae species isolated from wheat semolina that inhibit the development of Aspergillus niger, P. roqueforti, and En-
domyces fibuliger similarly or more intensively than calcium propionate (Valerio et al., 2009). In some situations, LAB and chemical
preservatives can synergistically control undesirable microorganisms. A combination of calcium propionate and sourdough fer-
mented by L. plantarum was found to have a strong synergistic effect against Fusarium culmorum, A. niger, and P. expansum. The reduc-
tion in the use of calcium propionate to 1000 ppm only maintained the inhibition when antifungal sourdough was added. Further-
more, the shelf life was significantly longer than the only use of calcium propionate (3000 ppm) (Ryan et al., 2008). This antifungal
effectiveness can be attributed to the action of organic acids produced during fermentation, competition for nutrients with other mi-
crobial contaminants, and the production of antagonistic compounds by metabolizing available macronutrients and micronutrients.

Fig. 1. - Conventional practices for the prevention and decontamination of mycotoxins adapted from Pankaj et al. (2018).

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I. EL Houssni et al.
Table 2
- Sourdough lactic acid bacteria and their activity spectrum against Mycotoxigenic fungi.
LAB species
Lactobacillus species
Lactococcus species
Pediococcus species
Leuconostoc species
Others
3.4. Antifungal compounds produced by lactic acid bacteria
The antifungal efficacy of sourdough LAB can be explained by the production of various antagonistic compounds during fermenta-
tion. The identification and the mechanisms of action of these compounds are discussed further here (Fig. 2).
3.4.1. Organic acids
During fermentation, organic acids production is an important process that inhibits the activity of LAB against toxinogenic fungi
in bread (Piard and Desmazeaud, 1991). This inhibitory effect is due to the diffusion of these organic acids through the cell membrane
Biocatalysis and Agricultural Biotechnology 50 (2023) 102702
Activity spectrum
Lactobacillus acidophilus Aspergillus flavus
Aspergillus fumigatus
Lactobacillus amylovorus Aspergillus fumigatus
Fusarium culmorum
Lactobacillus brevis Aspergillus niger
Fusarium culmorum
Lactobacillus casei Aspergillus flavus
Aspergillus niger
Fusarium spp
Penicillium citreum
Penicillium expansum
Lactobacillus coryniformis Aspergillus fumigatus
Fusarium culmorum
Fusarium graminearum
Penicillium roqueforti
Lactobacillus delbrueckii Penicillium expansum
Lactobacillus fermentum Aspergillus flavus
Aspergillus niger
Penicillium spp
Lactobacillus paracasei Fusarium graminearum
Penicillium brevicompactum
Penicillium chrysogenum
Lactobacillus plantarum Aspergillus flavus
Aspergillus niger
Fusarium graminearum
Penicillium corylophilum
Penicillium expansum
Penicillium roqueforti
Lactobacillus reuteri Aspergillus niger
Lactobacillus rhamnosus Aspergillus flavus
Fusarium spp
Penicillium brevicompactum
Lactobacillus rossiae Aspergillus niger
Penicillium corylophillum
Penicillium roqueforti
Lactobacillus sanfranciscensis Aspergillus spp
Fusarium spp
Penicillium spp
Lactococcus lactis Aspergillus flavus
Aspergillus fumigatus
Aspergillus parasiticus
Penicillium expansum
Pediococcus acidilactici Aspergillus fumigatus
Aspergillus japonicum
Aspergillus niger
Aspergillus parasiticus
Fusarium culmorum
Penicillium roqueforti
Pediococcus pentosaceus Aspergillus fumigatus
Fusarium culmorum
Fusarium graminearum
Penicillium expansum
Penicillium roqueforti
Leuconostoc citreum Aspergillus niger
Penicillium roqueforti
Leuconostoc mesenteroides Aspergillus niger
Penicillium roqueforti
Weissella cibaria Aspergillus niger
Penicillium roqueforti
5
References
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Kabak and Var (2004)
Ryan et al. (2011)
Mauch et al. (2010)
Tropcheva et al. (2014)
Bueno et al. (2006)
Florianowicz (2001)
Gerez et al. (2010)
Gourama (1997)
Mäyrä-Mäkinen et al. (1994)
Magnusson and Schnurer (2001)
Florianowicz (2001)
Adedokun et al. (2016)
Fadime (2014)
Fernandez et al. (2017)
Hassan and Bullerman (2008b)
Lãcanin et al. (2017)
Lavermicocca et al. (2000)
Sadeghi et al. (2019)
Bueno et al. (2006)
Lãcanin et al. (2017)
Stiles et al. (2002)
Le Lay et al. (2016)
Valerio et al. (2009)
Corsetti et al. (1998)
Florianowicz (2001)
Kim (2005)
Luchese and Harrigan (1990)
Bustos et al. (2018)
Juodeikiene et al. (2018)
Mandal et al. (2007)
Ilavenil et al. (2015)
Juodeikiene et al. (2018)
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Sellamani et al. (2016)
Valerio et al. (2009)
Yépez et al. (2017)
Valerio et al. (2009)
I. EL Houssni et al. Biocatalysis and Agricultural Biotechnology 50 (2023) 102702

Fig. 2. - Antifungal compounds produced by lactic acid bacteria.

of targeted fungi in their non-dissociable hydrophobic form, causing acidic stress responsible for the cessation of their metabolic ac-
tivities, hence the fungistatic and sometimes fungicidal effect of organic acids (Jin et al., 2021). Lactic acid and acetic acid are the
most important organic acids produced from carbohydrate fermentation by LAB. Lactic acid has been identified as the main antimi-
crobial compound against E. Faecium, L. rhamnosus, L. Plantarum, and some species of Aspergillus, Fusarium, and Penicillium genera
(Nasrollahzadeh et al., 2020). For other fungi of the same genera, the inhibitory effect of lactic acid is lower than that of acetic acid.
This efficiency is due to the high dissociation constant of acetic acid (Batish et al., 1997). A synergistic combination of lactic and
acetic acids can be produced to improve the inhibitory effect performed separately (Crowley et al., 2013; Dagnas et al., 2015). In gen-
eral, the synergistic contribution of acetic acid occurs in sourdough fermented with Lactobacillus species (Nasrollahzadeh et al.,
2019). In the same ferment, carboxylic acids, including benzoic acid, vanillic acid, azelaic acid, hydroxy-cinnamic acid, and hydroxy-
benzoic acid, were isolated as antifungal compounds (Guo et al., 2012). Propionic fermentation of lactic acid produces propionic acid.
This acid is efficiently produced by Lb. buchneri and Lb. diolivorans, inhibiting the growth of Aspergillus clavatus, Cladosporium spp,
Moritierella spp, and Penicillium roquefortii (Zhang et al., 2010). Other organic acids, such as phenyl lactate, have been identified. This
acid was isolated for the first time in Lb. plantarum culture, showing significant inhibition against P. roquefortii, the major bread conta-
minant (Yan et al., 2017). A similar effect was reported against P. expansum, A. niger, A. flavus, F. graminearum, A. fumigatus, and R.
stolonifera (Lavermicocca et al., 2000; Prema et al., 2010). In addition to phenyllactic acid, Lb. plantarum produces 4-hydroxy-
phenyllactic acid, which has shown significant inhibition of Eurotium, Fusarium, and Penicillium, comparable to sodium benzoate
(Lavermicocca et al., 2000). Compared to the inhibitory effects of lactic acid, phenyllactic acid, and 4-hydroxyphenyllactic acid pro-
duced by the same strain Lb. plantarum and evaluated separately against A. flavus, phenyllactic acid showed the highest inhibitory ac-
tivity (Guimarães et al., 2018). Furthermore, the synergy between these three organic acids produced by Lb. plantarum and W. para-
mesenterides showed significant inhibition of A. tubingensis, A. niger, and P. crustosum (Ndagano et al., 2011).

3.4.2. Reuterin
Reuterin (3-hydroxypropionaldehyde) is an antifungal agent produced mainly by L. reuteri in the anaerobic fermentation of glycerol
(Chung et al., 1989). The Lb. brevis, Lb. buchneri, Lb. Collinoides and Lb. Coryniformis species are also recognized as reuterin producers
(Claisse and Lonvaud-Funel, 2000; Schütz and Radler, 1984). The reuterin produced by L. reuteri completely inhibits the growth of
spores of Fusarium culmorum, Aspergillus niger, and Penicillium expansum (Schmidt et al., 2018). The inhibitory mechanism involves in-
ducing oxidative stress by binding the reuterin's aldehyde group to the thiol group of the constituent proteins of the fungi cells pro-
teins (Schaefer et al., 2010). Another inhibitory mechanism proposed by reuterin is the suppression of the activity of ribonuclease, the
main enzyme involved in DNA biosynthesis (Talarico and Dobrogosz, 1989).

3.4.3. Fatty acids

During fermentation, some LAB can produce unsaturated fatty acids, which have significant antifungal properties (Leyva Salas et
al., 2019). An example of caproic acid is defined as the main antifungal compound isolated from Lb. sanfrancisco (Corsetti et al.,
1998a,b). This fatty acid can act synergistically with other organic acids, such as propionic acid, butyric acid, and valeric acid. Due to
their detergent properties, antifungal fatty acids can destroy the entire plasma membrane and cause the disintegration of the targeted
cells by releasing proteins and intracellular electrolytes (Sjögren et al., 2003). Myristic acid analogs can inhibit protein synthesis. In
addition, the action of acetylenic fatty acids inhibits metabolism and topoisomerase activity (Méndez-Vilas, 2011). The hydroxylated
form of fatty acids has a broad spectrum of inhibition. This antifungal performance depends on the length of the aliphatic chain, the
number of hydroxyl groups, and the amount of unsaturation. Thus, fatty acids with a chain length of 18 carbons are the most active.
Unsaturated mono-hydroxyl fatty acids are antifungal, while saturated hydroxy fatty acids and unsaturated fatty acids such as oleic
and stearic acids are not (Black et al., 2013). Mentioned the examples of 3-hydroxy-5-dodecanoϊque acid produced by Lb. plantarum

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I. EL Houssni et al. Biocatalysis and Agricultural Biotechnology 50 (2023) 102702

against A. fumigatus (Mun et al., 2019) and mono-hydroxyl octadecenoϊc acid produced by Lb. hammesii against A. niger and P. roque-
forti, major bread contaminants (Black et al., 2013).

3.4.4. Hydrogen peroxyde

The metabolism of LAB in the presence of oxygen leads to the accumulation of another powerful antifungal agent, hydrogen per-
oxyde, which prevents fungi growth. Most LABs do not contain catalase, but they remove toxic hydrogen peroxyde by peroxidase en-
zymes (Nes et al., 1996). Oxygen peroxyde accumulation oxidizes the lipidic membrane and the proteins of the targeted fungi
(Lindgren and Dobrogosz, 1990). At a non-lethal percentage in the sourdough, hydrogen peroxyde completely suppresses the growth
of P. expansum (Venturini et al., 2002), while it shows weak antifungal activity against Cladosporium, Scopulariopsis, Aspergillus, and
Eurotium (Bundgaard-Nielsen and Nielsen, 1996). This low activity is explained by the ability of these fungi to degrade oxygen perox-
yde. Its exogenous accumulation stimulates catalase and superoxide dismutase, two key enzymes implicated in detoxification (Gild-
Ad and Mayer, 1999).

3.4.5. Cyclic dipeptides

Protein compounds are also used to inhibit the growth of toxigenic fungi. It is widely reported that sourdough LABs synthesize
cyclic peptides through cyclopeptidase synthase enzymes and non-ribosomal peptide synthases (Rhee, 2004). This enzymatic synthe-
sis is favored by the acidification produced during fermentation (Ryan et al., 2009). Cyclic dipeptides have been identified as poten-
tial antifungals. Cyclo (L-His-L-Pro), cyclo (L-Pro-L-Pro), cyclo (L-Met-L-Pro), cyclo (L-Leu-L-Pro), and cyclo (L-Try-L-Pro) produced
by Lb. amylovorus effectively inhibit the growth of Aspergillus fumigatus (Ryan et al., 2011). Similarly, the cyclo (Gly-L-Leu) produced
by Lb. plantarum retards the growth of Fusarium avenaceum (Niku-Paavola et al., 1999). The mechanism of action of these antifungal
peptides is to bind to lipid bilayers and perforate channels by disrupting the functions and structural integrity of the plasma mem-
brane of targeted fungi (Shai, 1995).

3.4.6. Factors affecting the production of antifungal compounds

Fermentation conditions, including temperature and incubation time choice and the growth medium composition, could modulate
the production of antifungal compounds, thus, the preservative effect of the sourdough. These parameters vary depending on the fer-
mentative bacterial species of the sourdough. Generally, the production of antifungal compounds is maximal at the end of the loga-
rithmic phase of growth. This finding was confirmed by analyzing Lb. pentoseus cultures (T = 25 °C; Ip = 24 h) (Shehata et al.,
2019), Lb. Lactis (T = 25 °C; Ip = 72 h) (Reddy and Ranganathan, 1985), Lb. plantarum (T = 30 °C; Ip = 72 h), Ln. mesenteroides
(T = 37 °C; Ip = 48 h) (Muhialdin et al., 2018), and Lb. acidophilus (T = 30 °C; Ip = 48 h) (Batish et al., 1990). At the beginning of
the stationary phase, the production of antifungal compounds decreases, resulting in a decrease in antifungal activity. This diminu-
tion is due to bacterial metabolization or enzymatic degradation of these bioactive compounds (Batish et al., 1990). Supplementation
with nutritional additives can increase the antifungal efficacy of sourdough. These additives usually have a protein nature, such as
phenylalanine, which increases the production rate of phenyllactic acid and 4-hydroxyphenyllactic acid by Lb. plantarum (Valerio et
al., 2004). Adding carbohydrate, especially glucose, increases the production of antifungal metabolites by Pediococcus acidilactici and
Lb. Rhamnosus (Effat et al., 2001). While adding NaCl to the sourdough formulation improves its antifungal performance (Effat et al.,
2001). This improvement can be related to a synergistic effect between NaCl, organic acids, and other antifungal substances (Effat et
al., 2001). However, high concentrations of NaCl reduce the antifungal production rate by the lactic biota of the sourdough (e.g. Lc.
lactis) (Batish et al., 1989).

3.5. Sourdough lactic acid bacteria against fungal mycotoxins

In addition to inhibiting the growth of toxigenic fungi, the antifungal LABs in sourdough detoxifies the surrounding environment
by eliminating secreted mycotoxins to ensure the safety of the produced bread.

3.5.1. Binding of mycotoxins by lactic acid bacteria

The mechanism involves the adsorption of mycotoxins on the typical parietal structures of LAB. Polysaccharides and peptidogly-
cans are considered the main parietal components implicated in the removal of mycotoxins (Chapot-Chartier and Kulakauskas, 2014).
These two components show significant structural variability, which explains the difference in the mycotoxin binding capacity of LAB
(De Ambrosini et al., 1996). In contrast to Lb. delbrueckii, Lb. acidophilus, Lb. rhamnosus, Lb. plantarum, Lb. brevis, and Lb. sanfranciscen-
sis efficiently remove ochratoxin A (OTA) through binding, which is influenced by cell wall hydrophobicity and electron donor-
acceptor interactions (Piotrowska, 2014). Supplementation with some compounds, such as ethyl methanosulfate at non-lethal con-
centrations, promotes OTA binding (Khattab et al., 2018).
Many LABs can bind to Aflatoxin B1, whereas Aflatoxins B2, G1, and G2 are less sensitive to this binding process (El-Nezami et al.,
2002a). Among these LABs, Lb. rhamnosus, Lb. Casei, Lb. reuteri, and Lb. fermentum strains, isolated from a sourdough culture, effi-
ciently bind Aflatoxin B1 through hydrogen bonds and Van Der Waals interactions involving peptidoglycans and parietal teichoic
acids (Fig. 3) (Fazeli et al., 2009; Yian-nikouris et al., 2006). The acid stress produced during fermentation increases the interactions
between LAB and Aflatoxin B1 due to the denaturation of cell surface proteins which releases more Aflatoxin B1 binding zones (Yian-
nikouris et al., 2006).
Some binding zones may have the affinity to bind several mycotoxins simultaneously to the same bacteria. For example, Lb. rham-
nosus has been shown to bind Zearalenone (ZEA) and its derivative α-Zearalenol simultaneously (El-Nezami et al., 2002b). The mech-
anism involved may include interactions with proteins through electrostatic or hydrophobic interactions, binding to cell wall peptido-
glycans, or engulfment within the LAB used during the operation (Fig. 3) (Król et al., 2018).

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I. EL Houssni et al. Biocatalysis and Agricultural Biotechnology 50 (2023) 102702

Fig. 3. - Different ways of interactions between Aflatoxin B1 and Zearalenone with bacterial cell wall components.

Cell wall binding is the only known mechanism responsible for Trichothecene mycotoxins elimination. Among these mycotoxins,
T-2 and Deoxynivalenol (DON) are efficiently eliminated by Lc. Lactis and Lb. Paracasei by binding to protein and non-protein compo-
nents of their cell walls (Hassan and Bullerman, 2008a; Zhou et al., 2017).
Furthermore, peptidoglycans are found to be responsible for the interaction and adsorption of Fumonisins B1 and B2 by Lb. plan-
tarum and Lb. Pentoseus (Zhao et al., 2016). The binding efficiency can be affected by the pH of the surrounding medium culture since
at pH 7 these LABs were unable to trap Fumonisins B1 and B2 (Niderkorn et al., 2006).
Due to its microbial diversity of LAB, sourdough has shown a significant capacity to reduce the availability of mycotoxins during
fermentation. This anti-Mycotoxigenic effect depends significantly on the interaction strength and the relative stability of the com-
plexes formed. For example, Lb. Casei was reported to be the most effective binder of Aflatoxin compared to Lb. plantarum and Lb. Fer-
mentum (Fazeli et al., 2009). This capacity is largely influenced by the structure of the parietal components responsible for mycotoxin
binding (Niderkorn et al., 2009). When mycotoxins are substantially bound to cell surface proteins, the binding capacity after acidifi-
cation during fermentation can be reduced. This effect was reported for Lb. johnsonii, Lb. bulgaricus and Lb. salivarius with against
ochratoxin (Luz et al., 2018). The degradation of glycosidic and amine bonds of polysaccharides and proteins, respectively, involved
in the adsorption process may explain the above-mentioned effect. In some cases, the acidification of the medium culture can increase
the sensitivity against some mycotoxins (Li et al., 2021). These include Aflatoxin B1, which adsorbs efficiently by Lb. plantarum and
Lb. buchneri at pH 2.5 and weakly at pH 8.5 (Ma et al., 2017). Unlike acidification, the thermal treatment promotes mycotoxin binding
to peptidoglycans by denaturing or condensing proteins and parietal polysaccharides during the Maillard reaction (Haskard et al.,
2001).
Furthermore, the number of LAB and the concentration of mycotoxins can influence the binding mechanism and, thus, the anti-
Mycotoxigenic efficiency of the lactic acid biota. A positive correlation was recorded between the number of bacterial cells and myco-
toxin removal. Against Aflatoxin, Lb. Casei, at initial concentrations of 4.6 μg/mL and 6 μg/mL, adsorbed 50% and 98% of AFB1, re-
spectively (Hernandez-Mendoza et al., 2009; Liew et al., 2018). Similarly, Lb. plantarum, at initial concentrations of 0.1 μg/mL and
12.3 μg/mL, adsorbs 48% and 64% of ZEA, respectively (Vega et al., 2017).

3.5.2. Bio-transformation of fungal mycotoxins by lactic acid bacteria

Another mechanism of bacterial decontamination of mycotoxins in bread is the biodegradation of mycotoxins by LAB in sour-
dough. The efficiency of biodegradation has been demonstrated by monitoring OTA, DON, 3-ADON, and Nivalenol (NIV) levels in
bread making. During fermentation, a significant reduction in mycotoxin concentrations was reported, ranging from 29.8% to 33.5%.
During baking, a further reduction was observed, and the reduction rates in the finished product reached 32.9%, 76.9%, 65.6%, and
47.9% for OTA, NIV, 3-ADON, and DON, respectively (Valle-Algarra et al., 2009).
During this bioprocess, the metabolic conversion of mycotoxins can produce more toxic metabolites. For example, it was reported
that aflatoxin B1 is converted to Aflatoxicol, a compound that is three to four-times more toxic (Mirocha et al., 1979; Verheecke et al.,
2016). For this reason, the parietal adsorption mechanism remains advantageous even though the efficiency of biodegradation for
some mycotoxins. These mycotoxins include OTA, which is converted to α-OTA, a non-toxic by-product of enzymatic degradation by

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I. EL Houssni et al. Biocatalysis and Agricultural Biotechnology 50 (2023) 102702

Fig. 4. - Bioconversion of ochratoxin A to α-ochratoxin and l-β-phenylalanine.

Fig. 5. - Bioconversion of zearalenone to α-zearalenol

Pediococcus parvulus. The mechanism involved is the hydrolysis of the amide bond of OTA, resulting in the release of α-OTA and
phenylalanine (Fig. 4). This hydrolysis is hypothesized to be promoted by the effective production of peptidase by P. parvulus
(Abrunhosa et al., 2014).
Complementarily, highly toxic metabolites released during biodegradation can be removed by adsorption. For example, it has
been reported that biodegradation of zearalenone by Lb. delbrueckii produces highly toxic α-zearalenol as a by-product (Fig. 5),
which is effectively adsorbed by Lb. Rhamnosus (El-Nezami et al., 2002c; Mokoena et al., 2005). The biodegradation capacity of zear-
alenone can be significantly increased by genetic manipulation. It has been reported that the introduction of the plasmid (pNZ-
zhd101), containing genes encoding an enzyme that degrades zearalenone, significantly increases the biodegradation capacity of Lb.
reuteri from 9.1% to 99% for an initial concentration of 4.5 mg/L zearalenone (Yang et al., 2017).

3.6. Conclusion and future perspectives

The review of the literature over the period 1979 to 2021 concerning the inhibitory effects of LAB isolated from sourdough on the
growth of mycotoxigenic fungi and mycotoxins in wheat bread, allowed to conclude that LAB in sourdough can minimizes the micro-
biological safety of bread by acting as potential natural preservatives against toxigenic fungi growth. This inhibiting capacity is attrib-
uted to the ability of these LABs to produce antifungal metabolites, such as organic acids, fatty acids, reuterin, hydrogen peroxyde,
and antifungal protein compounds.
Many LAB isolated from sourdough can also eliminate mycotoxins in bread by several mechanisms. This detoxification consists
mainly of removing mycotoxins by binding to LAB cell wall components. The ability of LAB to bio-transform mycotoxins into non-
toxic by-products has also been reported. Their detoxification action may be influenced by several factors, including the pH of the
medium culture, the LAB load, and the incubation time.
The promising effects of LAB against toxigenic fungi and their mycotoxins will lead to many applications in the agri-food sector
that meet health and environmental concerns, which allow the maintenance of food safety, and a reduction of devastating losses of
food products due to fungal contamination and the presence of mycotoxins.

Abbreviation list
LAB: Lactic Acid Bacteria; AFB1: Aflatoxin B1; ZEA: Zearalenone; NIV: Nivalenol; α-OTA: α-ochratoxine; OTA: Ochratoxine;
DON: Deoxynivalenol; 3-ADON: 3-acetyldeoxynivalenol.

Competing interests and funding

The authors have no competing interests to declare that are relevant to the content of this article.
No funding was received for conducting this study.

CRediT authorship contribution statement

I.H.: Conceptualization, Methodology, Investigation, Formal analysis, Writing Original Draft. K.H. and A.Z.: Methodology, Valida-
tion, Review & Editing the manuscript. R.H.: Supervision, Methodology, Validation, Review & Editing the manuscript, Project admin-
istration. All authors read and approved the final manuscript.

Declaration of competing interest

The authors have no conflicts of interest to declare.
All co-authors have seen and agree with the contents of the manuscript and there is no financial interest to report. We certify that
the submission is original work and is not under review at any other publication.

Data availability
Data will be made available on request.

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I. EL Houssni et al. Biocatalysis and Agricultural Biotechnology 50 (2023) 102702

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