Microbiological Detoxification of Mycotoxins: Focus on Mechanisms and Advances

Abstract

Some fungal species of the genera Aspergillus, Penicillium, and Fusarium secretes toxic metabolites known as mycotoxins, has become a global concern that is toxic to different species of animals and humans. Biological mycotoxins detoxification has been studied by researchers around the world as a new strategy for the mycotoxin removal. Bacteria, fungi, yeast, molds, and protozoa are the main living organisms appropriate for the mycotoxin detoxification. Enzymatic and degradation sorption are the main mechanisms involved in microbiological detoxification of mycotoxins. Regardless of the method used, proper management tools that consist of before-harvest prevention and after-harvest detoxification, are required. Here, in this review we focus on the microbiological detoxification, and mechanisms involved in decontamination of mycotoxins.

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REVIEW ARTICLE
Microbiological Detoxification of Mycotoxins: Focus on Mechanisms and
Advances
Milad Abdi1, Arezoo Asadi1, Farajolah Maleki2, Ebrahim Kouhsari3,4,*, Azam Fattahi5,
Elnaz Ohadi1, Ensieh Lotfali6, Alireza Ahmadi4 and Zahra Ghafouri7
1Department of Microbiology, Faculty of Medicine, Iran University of Medical Sciences, Tehran, Iran; 2Department of
Laboratory Sciences, School of Allied Medical Sciences, Ilam University of Medical sciences, Ilam, Iran; 3Clinical Mi-
crobiology Research Center, Ilam University of Medical Sciences, Ilam, Iran; 4Laboratory Sciences Research Center,
Golestan University of Medical Sciences, Gorgan, Iran; 5Center for Research and Training in Skin Disease and Lep-
rosy, Tehran University of Medical Sciences, Tehran, Iran; 6Department of Medical Parasitology and Mycology,
School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran; 7Department of Biochemistry, Bio-
physics and Genetics, Faculty of Medicine, Mazandaran University of Medical Sciences, Sari, Iran
ARTICLE HISTORY
Received: January 09, 2020
Revised: April 10, 2020
Accepted: April 10, 2020
DOI:
10.2174/1871526520666200616145150
Abstract: Some fungal species of the genera Aspergillus, Penicillium, and Fusarium secretes toxic
metabolites known as mycotoxins, have become a global concern that is toxic to different species
of animals and humans. Biological mycotoxins detoxification has been studied by researchers
around the world as a new strategy for mycotoxin removal. Bacteria, fungi, yeast, molds, and proto-
zoa are the main living organisms appropriate for the mycotoxin detoxification. Enzymatic and
degradation sorptions are the main mechanisms involved in microbiological detoxification of myco-
toxins. Regardless of the method used, proper management tools that consist of before-harvest pre-
vention and after-harvest detoxification are required. Here, in this review, we focus on the microbi-
ological detoxification and mechanisms involved in the decontamination of mycotoxins.
Keywords: Biological detoxification, microbiological decontamination, mycotoxins.
1. INTRODUCTION
The mycotoxins are secondary metabolites with low--
molecular-weight produced by some filamentous fungi or
molds, including: Aspergillus species (spp.), Alternaria spp.,
Penicillium spp., Fusarium spp., Claviceps spp., Stachy-
botrys spp., Alternaria spp., Boletus spp., Amanita spp., Co-
prinus spp., Myrothecium spp., Pithomyces spp. etc., may de-
velop on various foods and feeds, causing severe risks to hu-
man and animal health” [1-3]. Human exposure to myco-
toxins occurs via direct contact (consumption of plan-
t-derived foods and animal products) and inhalation (expo-
sure to air and dust containing toxins) [4]. Currently, more
than 300 mycotoxins are known and are estimated more than
25% of the world’s agricultural commodities to be contami-
nated with mycotoxins [1, 5, 6]. These mycotoxins are
known to be either carcinogenic (e.g. aflatoxin B1, ochra-
toxin A, fumonisin B1), estrogenic (zearalenone), neurotox-
ic (fumonisin B1), nephrotoxic (ochratoxin), dermatotoxic
(trichothecenes) or immunosuppressive (aflatoxin B1, ochra-
toxin A, and T-2 toxin) [5]. Some studies have reviewed the
health hazards of mycotoxicosis to humans or animals [2, 6].
The symptoms of a mycotoxicosis can be effected on energy
* Address correspondence to this author at the Clinical Microbiology Re-
search Center, Ilam University of Medical Sciences, Ilam, Iran;
Tel/Fax: +98(843)2227101; P.O. Box: 6939177143;
E-mail: Kouhsari-E@medilam.ac.ir
production, nervous system, inhibition of synthesis of nucle-
ic acids, hormonal activities, reproductive systems and im-
mune system [9], which depends on the type of mycotoxin,
the concentration and length of exposure, the age, health, di-
et, interactions with other toxins and sex of the exposed indi-
vidual [3, 7]. Several methods applied for mycotoxins detoxi-
fication are classified as physical, chemical and biological.
For example, the biological methods consist of the use of mi-
croorganisms to degrade mycotoxins. Summary of microbio-
logical detoxification of mycotoxins is displayed in Table 1.
In this paper, we reviewed recent advances and mechanisms
involved in microbiological detoxification of mycotoxins.
2. DETOXIFICATION BY PROBIOTIC
Probiotics are living microorganisms that put out in ade-
quate amounts can give a health benefit on the host. Some of
the protective roles of probiotics are antagonistic effects
against pathogens, anticarcinogenic and antimutagenic activi-
ties [10]. Different probiotic strains of Lactobacillus and Bifi-
dobacterium genera possess important and widely acknowl-
edged health-promoting and immunomodulatory properties.
Application of biocontrol agents (BCA) such as lactic acid
bacteria (LAB) as biological food preservatives has long
been used as a cost-effective and safe method of food stor-
age. Interaction between LAB and contaminating organisms
induces production of low molecular weight compounds:
phenyllactic acid, reuterin, cyclic dipeptides, benzoic acid,

2 Infectious Disorders - Drug Targets, 2020, Vol. 20, No. 0 Abdi et al.
Table 1. Summary of microbiological detoxification of mycotoxins
Type of
Mycotoxins
Type of Detoxifica-
tion Type of Microorganisms Rate of Detoxification
(%)
Mechanisms of
Action Ref.
Total afla-
toxins
Bacterial Detoxifi-
cation
Lactobacillus acidophilus ATCC 4495
Lactobacillus acidophilus ATCC 20552 61-100 extracellular
metabolites [177]
Lactobacillus acidophilus ATCC 20552
Lactobacillus rhamnosus TISTR 541
Lactobacillus sanfrasiscensis DSM 20451
Bifidobacterium angulatum DSMZ 20098
11.5-84.7 Cell-binding [178]
Bifidobacterium longum
Lactobacillus rhamnosus
Bifidobacterium species 420
Lactobacillus acidophilus
Lactobacillus acidophilus NCFM 150B
Lactobacillus casei Shirota
31.9-35.6 Cell-binding [179]
Bifidobacterium bifidum PTCC 1644 Lactobacillus fermentum
PTCC 1744 88.8-99.8
Cell-binding,
extracellular
metabolites
[28]
Fungal Detoxifica-
tion Candida parapsilosis IP1698 54.54-92.98 extracellular
metabolites [180]
Aflatoxin B1
Bacterial Detoxifi-
cation
Lactobacillus delbrueckii,
Streptococcus thermophilus 100 - [181]
Lactobacillus plantarum (PTCC 1058) 45 - [22]
Lactobacillus casei 14-49 - [23]
Lactobacillus casein 26.06 - [182]
Pleurotus ostreatus 81.7-89.4 - [183]
Bifidobacterium 18–49 - [25]
B. subtilis ANSB060 81.5 - [184]
Stenotrophomonas maltophilia 82.5 - [77]
Rhodococcus erythropolis 33 - [78]
R. erythropolis DSM 14303
Nocardia corynebacterioides DSM 12676, DSM 20151
Mycobacterium fluoranthenivorans DSM 44556
60 - ˃ 90 - [79]
Flavobacterium aurantiacum 34.5-94.5 - [81]
Bacillus subtilis 38.4 - [182]
Bacillus TUBF1 90 - [185]
Bacillus licheniformis CFR1 91.2 - [186]
Rhodococcus. globerulus AK36 95 - [85]
R. rhodochrous NI2 & ATCC 12674 96.1-99.98 - [187]
Staphylococcus warneri 47.4 - [188]
Lysinibacillus, Fusiformis, Sporosarcina sp. 46.9-61.3 - [188]
Staphylococcus sp. VGF2 56.8 - [189]
Pseudomonas Anguilliseptica VGF1 Pseudomonas fluorescens 51.7
47.7 - [189]
Brevundimonas sp. 78.1-76.8 [77]
L. paracasei BEJ01 30- 91.2
Decrease of
immunotoxicity
and oxidative
stress
[190]
lactic acid bacteria 85
Production of
organic acids;
acetic, citric and
lactic
acids
[191]
L. plantarum,
L. rhamnosus,
L. brevis,
Lactobacillus delbrueckii subsp. lactis
48.9-79.5 Cell-binding [192]
L. rhamnosus GG
L. rhamnosusLC-705
L. acidophilusLC1
L. lactissubsp.lactis
L. acidophilusATCC 4356
L. plantarum
L. caseiShirota
L. delbrueckiisubsp.bulgaricus
L. helveticus
P. freudenreichiisubsp.shermaniiJS
87- 97.3 Cell-binding [193]

Microbiological Detoxification of Mycotoxins Infectious Disorders - Drug Targets, 2020, Vol. 20, No. 0 3
(Table 1) contd....
Fungal detoxifica-
tion
Lactococcus lactissubsp.cremoris
Streptococcus thermophilus
Lactobacillus spp
Bifidobacteria spp
Lactococcus spp
5.6 - 59.7 Cell-binding
[25]
Lactobacillus plantarum 13-54 [194]
Lactobacillus pentosus
Lactobacillus beveris 17.4-34.7 Cell-binding
- [195]
Pseudomonas putida MTCC 1274
and 2445 10-90 extracellular
metabolites [164]
Aspergillus
niger D15-
Lcc2#3
55 enzymatic
degradation [103]
Peniophora sp SCC0152 52.4 enzymatic
degradation [103]
Pleurotus
treatus St2-3 76 enzymatic
degradation [103]
S. cerevisiae 10-53 - [18]
A. niger (ND-1) 58.2 - [107]
S. cerevisiae
Rhizopus oligosporus 22.6-64.5 - [106]
Candida utilis 21.08 -
[182]
Streptomyces sp. 1.6-88.4 - [196]
Alternaria sp. 83 - [197]
Trichoderma. Reesi QM9414 100 - [198]
Absidia repens 50-60 - [199]
Rhizopus
oryzae
NRRL 395
58 - [200]
Saccharomyces cerevisiae 90.4-99.3 Surface binding [201]
Phoma glomerata PG41 66-78 extracellular
metabolites [202]
R. oryzae
CCT7560 100 - [198]
Aspergillus
niger D15-
Lcc2#3
55 Enzymatic
degradation [103]
Peniophora sp SCC0152 52.4 Enzymatic
degradation [103]
Pleurotus
treatus St2-3 76 Enzymatic
degradation [103]
Aflatoxin
M1
Bacterial detoxifica-
tion
Lactobacillus acidophilus, Lactobacillus rhamnosus, Lactobacillus
casei
Bifidobacterium lactis
24.2-98.8 Cell-binding
[203]
Lactobacillus 29 - [26]
Bifidobacterium spp
Lactobacillus spp. 4.5-73.1 - [19]
LAB 12 - 46 - [20]
Lactobacillus rhamnosus 18.8 - [173]
Streptococcus thermophilus 14.8-39 -
[26]
Lactobacillus, Bifidobacterium 7.85−25.94 - [168]
Lactobacillus bulgaricus 87.6 - [204]
Lactobacillus. acidophilus 27 - [203]
ZEA Bacterial detoxifica-
tion
Lactobacillus casein 19.05 - [182]
Lactobacillus pentosus 81.7- 83.2 - [205]
Pediococcus pentosaceus 29.4-68.13 - [206]
Pseudomonas alcaliphila TH-C1
Pseudomonas plecoglossicida TH-L1
68
57 - [86]
Bacillus subtilis 42.18 - [182]
Lactobacillus plantarum 38.06-47.8 binding [207]
ZEA Fungal detoxifica-
tion
Gliocladiumroseum NRRL 1859 80–90 - [110]
Aspergillus nigri
Streptomyces spp 0-96 - [112]

4 Infectious Disorders - Drug Targets, 2020, Vol. 20, No. 0 Abdi et al.
(Table 1) contd....
Streptomyces griseus (ATCC 13273) Streptomyces rutgersensus
(NRRL-B 1256) Rhizopus arrhizus (IFO-6155)
Aspergillus niger (ATCC 111394)
S. rutgersensus (NRRL-B 1256)
F. oxysporum S-F3
10-40 - [114]
Trichoderma spp. 9 - 97 - [208]
Candida utilis 40.7 - [182]
Streptomyces sp. 35.4-99.6 - [196]
Gliocladiumroseum NRRL 1859 80–90 - [110]
Aspergillus nigri
Streptomyces spp 0-96 - [112]
Streptomyces griseus (ATCC 13273) Streptomyces rutgersensus
(NRRL-B 1256) Rhizopus arrhizus (IFO-6155)
Aspergillus niger (ATCC 111394)
S. rutgersensus (NRRL-B 1256)
F. oxysporum S-F3
10-40 - [114]
Trichoderma spp. 9 - 97 - [208]
Candida utilis 40.7 - [182]
Fumonisin
B1, B2
Bacterial and Fungal
detoxification
Lactic acid bacteria
Propionic acid bacteria 55-100 - [39]
L. paracasei BEJ01 30- 91.2
Decrease of
immunotoxicity
and oxidative
stress
[190]
Lactobacillus paraplantarum CNRZ 1885
Streptococcus thermophiles RAR1
Streptococcus thermophilus CNRZ 1066
Strep.
thermophilus JIM 8752
Lactococcus lactis subsp. cremoris MG1363
2-99
Cell-binding
(Peptidoglycan
and tricarballylic
acid)
[175]
S. cerevisiae 25->75 - [124]
Pleurotus eryngii 0-61 - [209]
Lactobacillus brevis. N195
Lactobacillus brevisN197
Klebsiella variicolaVA26
Bacillus sp. N339
Klebsiella oxytocaN186
Candida glabrrataN353
Candida glabrrataN345
Candida glabrrataN346
Piichia fermenttansN183
6-33 - [210]
PAT
Bacterial detoxifica-
tion
Fungal detoxifica-
tion
Lactobacillus plantarum 39 - [45]
Lactobacillus rhamnosus 80.4 - [47]
B. bifidum 671 52.9-54.1 - [51]
lactic
acid bacteria 47 - 80 biosorption [47]
Alicyclobacillus spp 11.4-60.2 [211]
LAB 2-97 Cell-binding [45]
Gluconobacter oxydans > 96 - [130, 212,
213]
P. ohmeri 158 > 83- >99 - [132]
Deoxyniva-
lenol
Bacterial detoxifica-
tion
Lactic acid bacteria
Propionic acid bacteria 55-100 - [39]
LAB 55 - [71]
lactic acid bacteria 16.41- 71.19 enzymatic
degradation [214]
L. plantarum (ATCC14917T),
L. brevis (ATCC14869T),
L. brevis (ATCC 8287),
Oenococcus oeni (RM8,RM11,RM1),
L. plantarum (RM28, RM35),
L. brevis (RM273), Leuconostoc mesenteroides (RM54), Pediococ-
cus acidilactici (RM86)
8 - 28 Cell-binding [57]
LAB 2-97 Cell-binding [45]
Fungal detoxifica-
tion S. cerevisiae > 37 - [124]
Beauvericin
Bacterial detoxifica-
tion
Probiotic
Bifidobacteria, lactobacilli, Eubacterium crispatus, Salmonella
fecalis, Salmonella termofilus
66-83 - [215]
OTA Fungal detoxifica-
tion
Saccharomyces sensu stricto 66 - 100 - [123]
Yeast 4.67- 99.87 extracellular
metabolites [216]

Microbiological Detoxification of Mycotoxins Infectious Disorders - Drug Targets, 2020, Vol. 20, No. 0 5
hydroxylated fatty acids, methylhydantoin, mevalonolac-
tone, lactic acid [11] and antagonistic compounds, such as
hydrogen peroxide, ethanol, and bacteriocins [12]. LAB pre-
vent germination of mould spores and reduce mycotoxin pro-
duction in food products [7]. The LAB could detoxify myco-
toxins through penetration of bacterial structure or the degra-
dation of its metabolism [8]. It is estimated that 25% of the
world’s crop production is contaminated by mycotoxins dur-
ing the pre-harvest period, transport, processing or storage
[9]. New preservation systems including antifungal LAB
strains could be used in the future as strategies for bio-con-
trolling mould growth [10].
2.1. Aflatoxins
Aflatoxins (AF) are secondary metabolites of fungal spe-
cies, including Aspergillus flavus, A. snomius and A. parasiti-
cus. AF is a group of potent mycotoxins with mutagenic, ter-
atogenic, carcinogenic, hepatotoxic and immunosuppressive
properties [11]. AFB1, AFB2, AFG1 and AFG2 are natural-
ly occurring aflatoxins. Aflatoxin structure permits the for-
mation of DNA adducts with guanine, inducing cancerous
cell formation [12]. Aspergillus flavus produces the B group
whereas A. parasiticus produces both B and G groups of afla-
toxins. AFB1 is the most common and toxic molecule
among aflatoxin’s family. Hydroxylation of AFB1, leading
to the formation of AFM1 (4-hydroxy-AFB1) [13]. This hy-
droxylation process appears to be realized in the rumen of
dairy mammals as the direct intake by these animals of afla-
toxin B1 (AFB1) contaminated feed leading to the accumula-
tion of AFM1 in milk. Thus, the AFM1 content in milk is
strongly correlated with the level of AFB1 in raw feedstuff.
AFM1 mycotoxin exerts a direct cytotoxic effect on human
cells that do not require prior metabolic activation. It is resis-
tant to pasteurization or sterilization [14]. The European
Community and Codex Alimentarius (ECCA) recommended
that the maximum limit of AFM1 in liquid milk is 0.05
mg/L [15]. According to USA regulations, the level of
AFM1 in milk should not be higher than 0.5 mg/L [16].
Some strains of LAB; Lactobacillus bulgaricus and Strepto-
coccus thermophilus have been reported to be effective in re-
moving AFB1 and AFM1 from contaminated liquid media
and milk [17]. Different binding sites may be present in dif-
ferent strains, and there are differences between binding
sites in each bacteria and variation, among them. AF binding
ability to both the microorganisms enhances by heating.
Heat treatments are also significantly enhancing the ability
of bacteria to degrade AFM1 [18]. Some researchers as-
sessed the ability of Bifidobacterium spp., Lactobacillus
spp. and Lactococcus spp. to bind AFM1 in solution; they
observed that the percentages of AFM1 binding to these
strains were 0 to 14.6% after 24 hours and 4.5% to 73.1% af-
ter 96 hours [19]. Also, previous data evaluated the ability
of LAB to remove AFM1 in PBS and skimmed milk. These
authors found that tested strains bound AFM1 within a range
from 12.42% to 45.67% for heat-inactivated bacteria and
within 5.6% to 33.54% for viable bacteria exposed to the
aflatoxin for 15 min or 24 h, respectively [20]. L. reuteri NR-
RL B-14171 strain bound up to 85.3% of AFB1 in PBS after
4 h. According to the study conducted by El-Nezami et al.,
binding of AFM1 is different to binding of AFB1 due to the
presence of an additional MeOH group in the AFM1
molecule, resulting in increasing polarity of the AFM1
molecule, making it more hydrophilic and thus increasing its
tendency to dissolve in aqueous solutions [21]. Khanafari et
al. (2007) studied the efficacy of L. plantarum PTCC 1058
to bind AFB1 and reported that 45% of AFB1 was removed
from the solution after 1 hour [22]. Mendoza et al. (2009)
screened eight strains of Lactobacillus casei for their ability
to bind AFB1, and the percentage bound ranged from 14 to
49%. They mentioned that Lactobacillus caseiShirota (LcS)
could bind AFB1 into the bacterial cell envelope and that
the documents also revealed that aflatoxin binding produced
structural changes that modified the bacterial cell surface
[23]. Shah and Wu assessed the antimutagenic activity of
killed and living cells of six strains of Lactobacillus aci-
dophilus on eight chemical mutagens and promutagens [24].
The destruction of specific components of the bacterial cell
wall, (carbohydrates and proteins), resulted in a reduction in
AFB1 binding. The amount of AFM1 is increased by reduc-
ing the acidity of the environment. Peltonen et al. found that
Bifidobacterium strains are bound to 18%–48.7% of AFB1.
They showed that the acid and heat treatment of the cells sig-
nificantly increased their ability to capture aflatoxin B1 in
the liquid medium [25]. Sarimehmetoğlu et al., reported per-
centages of AFM1 binding near to 29.42% for strains of the
genus Lactobacillus [26]. Also, high-performance liquid
chromatography (HPLC) analysis showed that quantitation
of AFB1 in supernatant samples of Lactobacillus spp., Bifi-
dobacterium spp. and Lactococcus spp. were 17.3 to 59.7%,
18.0 to 48.7%, and 5.6 to 41.1% of mentioned mycotoxin, re-
spectively [27]. Ghazvini et al. [28] assessed antifungal ef-
fects of two LAB against growth and aflatoxin production of
Aspergillus parasiticus. Their results showed that B. bifidum
and L. fermentum extensively decreased aflatoxin produc-
tion and growth rate in comparison with the controls
(p≤0.05). The most significant reduction (> 99%) by LAB in
total aflatoxins, B1, B2, G1 and G2 fractions was also report-
ed. Furthermore, bacterial metabolites reduced the level of
standard AFB1, B2, G1, and G2 from 88.8% to 99.8%
(p≤0.05).
2.2. Zearalenone (ZEA or ZEN)
The Fusarium family, including Fusarium cereals, F.
graminearum, F. semitectu, F. culmorum, and F. equiseti
produced ZEA. It can produce toxic secondary metabolites
(mycotoxins) that interfere with grain quality by destroying
its amylose, cellulose, and protein reserves, and reducing
productivity, consequently causing significant losses to in-
dustrial production and crops [29]. ZEA or ZEN is described
as 6-[10-hydroxy-6-oxotrans-1-undecenyl]-B-resorcyclic
acid lactone, similar to the natural estrogens [30]. It can
change their mechanism of metabolism and synthesis, and in-
terfere with the synthesis of the receptor, which contributes
to change neoplastic prostate cancer or breast cancer [31].
ZEA biotransformation in animals leads to the formation of
two essential metabolites, α-zearalenol and β-zearalenol (α--

6 Infectious Disorders - Drug Targets, 2020, Vol. 20, No. 0 Abdi et al.
ZOL and β-ZOL); alpha zearalenol is higher estrogenicity
than ZEA [32]. Streptomyces rutgersensus, Rhizopus ar-
rhizus., and Streptomyces griseus were able to metabolize
zearalenone to α- zearalenol. Although, L. plantarum., L.
rhamnosus and L. acidophilus can reduce the concentration
of mycotoxins in food [8]. Other microorganisms such as Ba-
cillus subtilis, Saccharomyces cerevisiae, Pseudomonas and
Rhizopus spp. are toxin neutralizing agents [33]. The mech-
anism of the toxin is not entirely understood, but there is
some evidence of cytogenic effect and apoptosis caused by
ZEA [19]. Lioi et al. [34] found that ZEA increased DNA
fragmentation in three cell lines (DOK, Caco-2, and Vero)
after 24 h [35]. ZEA and its metabolization can cause dam-
ages of bacterial cells and lead to death. Peptidoglycan struc-
ture and amino acid composition are important for ZEA bio-
control [36]. The authors mentioned that both heat-treated
and acid-treated bacteria were able to remove ZEA and α-
zearalenol. ZEA predominantly binds to carbohydrate of the
cell wall of LAB by using hydrophobic interactions. This
bacterium-mycotoxin is unstable because hydrophobic inter-
actions are relatively weak [37]. Fourier-transform infrared
(FTIR) spectroscopy indicates that in the neutralization of
ZEA by LAB, the deprotonated carboxyl group (mainly
from glutamine and asparagine) of bacterial proteins and
peptidoglycan are mainly involved. Finally, LAB seem to be
promising alternatives for the development of new anti-my-
cotoxin agents [38].
2.3. Fumonisins
The fumonisins are derived from Fusarium. They have
substantial structural analogue to sphinganine. Inhibit ce-
ramide synthase, inducing an adverse effect on the sphinga-
nine/sphingosine ratio. Amine groups play a vital role in fu-
monisin toxicity, so deamination of FB1 induces a loss of
toxicity. Niderkorn et al. showed that ability of L. paraplan-
tarum to bind fumonisins B1 and B2 (FB1, FB2) in foods
and feeds. Peptidoglycan and tricarballylic acid chains of
LAB and FB play a significant role in binding interactions
[39]. They revealed that FB2 was removed more efficiently
than FB1. The ability of three strains of Propionibacterium
to remove FB1 and FB2 from acidified MRS broth samples
(pH 4.0) was evaluated and demonstrated that FB1 was not
as effectively removed as FB2. The acidity of the environ-
ment affects the process of binding since, at pH 7, LAB is
not able to trap FB1 and FB2. Niderkorn suggested that pep-
tidoglycans were the most plausible fumonisin binding sites
[39].
One study showed that F. graminearum IDM623 was
sensitive to 25 different strains of LAB tested. These results
are following those reported by Corsetti et al. [40]. They
evaluated the inhibition of F. culmorum, F. avenaceum, F.
oxysporum, and F. graminearum by viable cell extracts of L.
plantarum and did not find any relation or influence among
the lactic acid concentration.
2.4. Patulin (PAT)
PAT (4-hydroxy-4H-furo [3, 2c] pirano- 2(6H)-one), is
produced during colonisation by ubiquitous mould and has
been shown to induce toxicosis in the rat and genotoxicity in
Chinese hamster V79 cells [41]- [42]. PAT is the major my-
cotoxin from P. expansum. The maximum accepted levels of
patulin in the EU is 50 mg/L for fruit juice [43]. PAT is pro-
duced by a large number of fungi within several genera such
as Byssochlamys, Eupenicillium, Penicillium, Paecilomyces,
and Aspergillus [44] and predominantly found in vegetables
and fruits (in particular in apples and apple-derived product-
s) [45]. The PAT causes oxidative damage, has a negative
impact on reproduction in males via interaction with hor-
mone production and affects the immune system. PAT
caused potent genotoxic effects in experiments with mam-
malian cells but is devoid of activity in bacterial mutagenici-
ty assays [46]. Since DNA damage is causally related to can-
cer induction and some other diseases, it was suspected that
PAT might possess carcinogenic properties, LAB has been
reported to reduce the amount of PAT in liquid media [47].
Other studies using S. cerevisiae, Rhodosporidium kra-
tochvilovae and Gluconobacter oxydans demonstrated detox-
ification of patulin to potentially less toxic compounds such
as estradiol and desoxypatulinic acid [48]. Both L. plan-
tarum B1 and S1 strains were able to degrade PAT, and the
degradation seemed to follow the well-documented pathway
to estradiol [49]. The degradation activity is performed by a
heat-labile factor that is present in the LAB and secreted and
is therefore likely to be protein based [47]. Fuchs et al.
studied the effect of the LAB on PAT and noticed that the
most substantial decline of PAT (39%) was detected by L.
plantarum [45]. Hateb et al. (2012) [50] reported that the
maximum PAT uptake from aqueous solution was achieved
by L. rhamnosus 6149 strains after 24-h incubation. Results
revealed that removal of PAT contamination from apple
juice by using 10 different inactivated LAB, showed that L.
rhamnosus caused a decrease of PAT by 80.4%. Recently,
they reported that the maximum uptake of PAT was
achieved by B. bifidum .671 (52.9%) for viable and (54.1%)
for killed cells after 24-h incubation [51].
2.5. Ochratoxins (OTAs)
OTAs are produced as secondary metabolites by several
fungi of Penicillium spp. or Aspergillus spp. Ochratoxin-A
(OTA) is the carcinogenic fungal toxin found in a variety of
food commodities. OTA causes severe nephrotoxic effects
in animals and humans, and its genotoxic and carcinogenic
effects are well documented [52]. Ochratoxins affect protein
synthesis and inhibit ATP production. It has been shown in a
few earlier investigations that LAB cause removal of OTA
from liquid medium [53, 54]. Lactobacillus spp. and Strepto-
coccus spp. have the ability to degrade of OTA in milk. Hei-
dler and Schatzmayr [55] demonstrated that Lactobacillus vi-
tulinus was able to cleave OTA into the amino acid pheny-
lalanine and the nontoxic metabolite ochratoxin α (OTα)
[56]. Del Prete et al. [57] performed a study on the interac-
tion between OTA and wine LAB (Lactobacillus spp., Oeno-
coccus oeni spp., Pediococcus spp.). They found that a de-
crease in OTA concentration by wine LAB strains. Lević et
al. indicated that the greatest adsorption (more than 50% of
the initial OTA content) was obtained with L. rhamnosus

Microbiological Detoxification of Mycotoxins Infectious Disorders - Drug Targets, 2020, Vol. 20, No. 0 7
GG, L. acidophilus, L. plantarum BS, L. sanfranciscensis
and L. brevis [58].
2.6. Trichothecene
Trichothecenes are one of the most important of myco-
toxins, leading to a significant economic impact on grain
crops and cereal each year [59]. Trichothecenes are pro-
duced by fungi of genera Fusarium spp., Cephalosporium
spp., Trichoderma spp., Spicellum spp., Myrothecium spp.,
Stachybotrys spp., and Trichothecum spp. Amphipathic tri-
chothecenes can move passively across cell membranes
[60]. They are easily absorbed via gastrointestinal systems
and have a rapid effect on proliferating tissues [61]. These
toxins can induce vomiting, hemorrhagic lesions, immuno-
logical problems, and skin dermatitis. They are also phyto-
toxic and can cause inhibition of root elongation, chlorosis,
and dwarfism [62]. Studies showed that trichothecenes had
prevented peptide bond formation at the peptidyl transferase
center of the 60S ribosomal subunit and inhibiting eukaryot-
ic protein synthesis [63]. This inhibition typically affects
elongation and polypeptide chain termination may also be in-
hibited. Trichothecenes inhibit mitochondrial protein synthe-
sis and interact with protein sulfhydryl groups [61]. The ac-
tivity of trichothecenes eventually produces harmful levels
of oxidative stress due to the production of free radicals.
Based on the substitution pattern of tricyclic 12,13-epoxytri-
chothec-9-ene (EPT), trichothecenes classified into four
groups (Types A, B, C, and D) [64]. Trichothecenes have
12,13-epoxytrichothecene group responsible for their cyto-
toxicity and 9,10-double bond with various side-chain substi-
tutions [65]. The position of the acetyl-ester and hydroxyl
groups can influence the relative toxicity within eukaryotic
cells. Their relative capacity to interfere with protein synthe-
sis has been attributed to a combination of different factors;
the rate of transport into cells, changes in affinity for the ac-
tive binding site, metabolism by cytosol enzymes or the abili-
ty to interfere with protein synthesis [66].
Deoxynivalenol (DON) is produced by certain Fusarium
spp. that infect corn, barley, rice, wheat, oats, and other
grains in the field or during storage. The risk for human is di-
rectly through foods of plant origin or indirectly through
foods of animal origin. DON affects animal and human
health causing acute temporary headache, nausea, vomiting,
abdominal pain, diarrhea, dizziness, and fever [67]. Tri-
chothecenes can be removed by a mechanism other than bio-
transformation or biodegradation. Polysaccharide and pepti-
doglycan of the cell wall are the two primary moieties re-
sponsible for the binding to Lactobacillus spp.. The thick-
ness of peptidoglycan may change by heating [68]. This per-
turbation of the bacterial cell wall may allow the tri-
chothecenes bind to the cell wall and plasma membrane con-
stituents that are not available when the bacterial cell is in-
tact [69]. DON and T-2 toxin induce apoptosis in hemopoiet-
ic progenitor cells and immune cells, and they also inhibit
the protein, ADN and ARN synthesis, whereas their toxicity
is induced by the epoxy structure [70]. Many of LAB strains
such as L. plantarum., L. acidophilus, L. helveticus., L. rham-
nosus, S. thermophilus, Lactobacillus casei strain GG have
the capacity for removing DON in acidified liquid medium
(pH 4) and the results indicated removal levels up to 55%
for DON [71]. Although the molecular structure of tri-
chothecenes is entirely different from aflatoxins, the mech-
anisms involved in binding aflatoxins and trichothecenes are
similar. These results indicate that the binding is a physical
phenomenon and that deoxynivalenol (DON), nivalenol
(NIV), and fusarenon-X (FX) are bound to the bacteria by
weak non-covalent interactions such as those associated
with hydrophobic pockets on the bacterial surface. A recent
study confirmed to reduce the intestinal absorption of myco-
toxins from the human diet and animal feeds [71]. DON-in-
duced significant increases in apoptosis rates compared to
controls in mouse thymocytes in vivo. Also, DON signifi-
cantly decreased the proliferation indexes of the treated
cells. Preliminary cultures had shown that DON induced ne-
crosis of the explants after 4 h of incubation [72].
3. OTHER BACTERIA
Sangare et al., 2014 [73] reported that Pseudomonas
aeruginosa N17-1 could degrade AFB1, AFB2, and AFM1,
82.8%, 46.8% and 31.9%, respectively. Some species of Ba-
cillus such as B. subtilis and B. licheniformis displayed afla-
toxin reduction activity [74, 75]. Gao et al. evaluated the
ability of B. subtilis (isolated from a different source) to
transform aflatoxins [76]. The results showed that B. subtilis
ANSB060 from the fish gut had the most potent ability to de-
toxify aflatoxins B1, M1, and G1 with 81.5%, 60%, and
80.7%, respectively. Guan et al. [77] found that Stenotropho-
monas maltophilia could reduce AFB1 by 82.5% in the
liquid medium at 37 °C for 72 hrs. Alberts et al., (2006) [78]
investigated the biological degradation of aflatoxins B1 (AF-
B1) in cell-free, extracellular extracts of Rhodococcus ery-
thropolis liquid cultures. They reported a significant reduc-
tion (33.2%) of AFB1 from 72 h when treated with R. ery-
thropolis extracellular extracts. Also, studies from Teniola et
al., (2005) [79] were conducted on biological degradation of
AFB1 by cell-free extracts of four bacterial strains: R. ery-
thropolis DSM 14303, Nocardia corynebacterioides DSM
12676, N. corynebacterioides DSM 20151, and Mycobacteri-
um fluoranthenivorans nov. DSM 44556 in cell-free extracts
under different incubation conditions. A significant detoxifi-
cation activity rates of aflatoxin B1 after 24 h by cell-free ex-
tracts of N. corynebacterioides DSM 12676 and DSM 20151
were 60%, ˃ 90%, respectively. Also, R. erythropolis and
M. fluoranthenivorans nov. DSM 44556 T have shown ˃
90% degradation of AFB1 within 4 h at 30 °C. Biological
degradation of AFB1 was optimized under a range of temper-
atures from 25°C to 40 °C and pH values of 4 to 8 by using
three Actinomycete, Rhodococcus erythropolis ATCC 4277,
Streptomyces lividans TK 24, and Streptomyces aureofa-
ciens ATCC 10762, in liquid cultures [80]. All species were
able to degrade the AFB1 at the end of the first 24 h in a
range 0.81 to 2.78 µg/mL. A study evaluated the ability of
aqueus protein extract from Flavobacterium aurantiacum to
degradation of AFB1 [81]. Degradation of AFB1 after incu-
bation with heat-treated, non-heat-treated, DNase I–treated
and Proteinase K–treated of crude protein extracts were

8 Infectious Disorders - Drug Targets, 2020, Vol. 20, No. 0 Abdi et al.
94.5%, 74.5%, 80.5%, and 34.5% respectively. Some
studies on the bio-transformation of ZEA by the bacterial mi-
crobiome of pigs [82], mixed culture (Alcaligenes, Bacillus,
Achromobacter., Flavobacterium, and Pseudomonas spp.)
[83], Acinetobacter spp [84]. have been released. Cserh ati
et al. (2013) have reported that Rhodococcus. Erythropolis,
Rhodococcus ruber, and Rhodococcus pyridinivorans had
ZEA degrading capacity [85]. Tan et al., (2014) determined
Pseudomonas alcaliphila TH-C1 and Pseudomonas pleco-
glossicida TH-L1 had degradation rate of ZEA about 68%
and 57%, respectively [86]. Altalhi (2007) [87] described
Pseudomonas putida ZEA-1 isolated from rhizosphere of
corn plant, can utilize ZEA as energy source and transform
ZEA along with a and b zearalenol, without generating harm-
ful metabolites. Later, Altalhi and El-Deeb (2009) [88] local-
ized and cloned the fragment containing genes encoding for
ZEA detoxification in the plasmid of P. Putida ZEA-1, and
the cloned genes were actively expressed in E. coli. The re-
sults showed that ZEA degradation by recombinant E. coli
was relatively rapid and effective, leaving no detectable
ZEA after 24 hours. The efficient abilities of B. lichenifor-
mis CK1 and B. subtilis to degrade ZEA in the culture media
were also reported [33, 89]. To date, several microorganisms
from various sources such as soils, animal guts, and plants
have been reported to have the ability to degrade DON [90].
4. BIOLOGICAL DETOXIFICATION BY FUNGI
Miazzo et al. removed mycotoxins via structural modifi-
cations in the mycotoxin molecule without the generation of
any toxic by-products or metabolites [91]. This is generally
implemented by using some yeasts, bacteria, or fungal en-
zymes which decompose mycotoxins into non-toxic com-
pounds [92]. However, because yeast is particularly suitable
for post-harvest use, has fast growth and has been proven in
decreasing the incidence of fungal pathogens, the applica-
tion of yeasts has great potential in reducing the economic
damage caused by toxigenic fungi in the agriculture [93,
94]. Furthermore, it has been reported that by binding the
mycotoxins in the gastrointestinal tract, yeast cell wall ex-
tract, containing polysaccharides and protein, was able to de-
crease adverse effects of mycotoxins in chickens, cows, and
pigs [95-98]. Some experimental studies indicated that the
isolates of phyllosphere yeast have the capability of con-
trolling sour rot that is caused by Aspergillus carbonarius in
wine-producing vineyards [99]. Also, Cryptococcus spp. is
very active against Fusarium spp. head blight (up to 59% re-
duction) ondurum wheat in the field [[100]].
4.1. Aflatoxin (AF)
The role of fungal species in the degradation of AF has
been investigated in several research in recent years [101].
This finding is based on microbial processes involved in the
degradation of complex organic aromatic compounds such
as lignin. Regarding polyphenolic compounds in nature,
lignin is undeniably the most plentiful and probably the
most heterogeneous and recalcitrant compound to be degrad-
ed microbially [102]. The degradation of AFB1 by white rot
fungi could be a crucial bio-control measure to reduce the
level of this mycotoxin in food commodities. As investigat-
ed in the Salmonella typhimurium mutagenicity assay, degra-
dation of AFB1 by laccase enzyme from T. versicolor and re-
combinant laccase enzyme produced by A. niger D15-Lc-
c2#3 and production of recombinant laccase enzyme by A.
niger D15-Lcc2# resulted in loss of mutagenicity of AFB1
[103]. Moreover, it was found that a live yeast, S. cerevisiae
could reduce the negative effects of aflatoxicosis in poultry
[104]. Later, Huynh et al. employ (NH4)2SO4 at 80% to
100% precipitation to extract a crude mycelial protein from
a 16-day-old culture of A. parasiticus in which AFB1could
be detoxified. In their study, the main breakdown product of
AFB1 was isolated and confirmed to be non-fluorescent,
non-mutagenic, and non-toxic for ducklings. The result
showed that the dialyzedmycelial protein destructed AF by
degradation of the cyclopentenone moiety, principally the
lactone ring, via infrared spectralanalysis of the main break-
down product [105]. To avoid aflatoxin contamination in
feed, Kusumaningtyas et al. introduced S. cerevisiae and Rhi-
zopus oligosporus. In this approach, A. flavus is cultured to-
gether with S. cerevisiae and Rhizopus oligosporus and their
combination (SCRO) in chicken feed and the content of AF-
B1 is observed at day 0, 5, 10, and 15. The results of this
study indicated that AFB1 contaminations in feed were re-
duced by SC, RO and SCRO addition. The highest and best
decline of AFB1 content was at day five by Ro [106]. Based
on Shetty et al. study, even at the highest concentration test-
ed (20 µgmL -1), S. cerevisiae cells were able to bind high
amounts of AFB1. They also indicated that the ability of S.
cerevisiae to bind AFB1 was strain-specific with seven
strains binding 10%–20%, eight strains binding 20–40% and
three strains binding more than 40% of the added AFB [18].
Recently, Zhang et al. reported that screened strain of A.
niger (ND-1) could degrade 58.2% of AFB1 after 48 h of fer-
mentation and this degradation was meaningfully powerful
in culture supernatant compare to cells and cell extracts
[107].
4.2. Zearalenone
Transformation of ZEA by fungi and actinomycetes was
initially introduced by El-Sharkawy and Abul-Hajj in 1987,
in which ZEA-4-O-b-glucoside substance was characterized
[108]. In another study, they suggested that the most impor-
tant detoxification was the lactone bond cleavage of ZEA by
the mycoparasite Gliocladium roseum [109]. El-Sharkawy et
al. reported that screening with 150 fungal species showed
that ZEA was transformed by many microbes leading to a re-
duction of the C-6’ carbonyl, saturation of the 1’-,2’- double
bond and hydroxylation at 3’ and 8’. They also showed that
one microbe, namely Gliocladium roseum NRRL 1859, was
capable of metabolizing ZEA in 80%–90% yields. The prod-
uct consisting of a mixture of two isomeric hydroxyl ketones
and far less oestrogenic compare to ZEA, rendered the reac-
tion irreversible [110]. Molnar et al. introduced a new yeast
strain, Trichosporon mycotoxinivorans that was capable in
ZEA degrading to carbon oxide, and other non-toxic metabo-
lites, neither a- nor b-ZEA were detected. They indicated
that Trichosporon mycotoxinivorans was useful in detoxifica-

Microbiological Detoxification of Mycotoxins Infectious Disorders - Drug Targets, 2020, Vol. 20, No. 0 9
tion of the respective mycotoxins in animal feeds [111]. Jard
et al. showed the ability of A. niger to transform ZEA over a
broad range of ZEA concentrations (5 to 150 μg/mL) and
that sulfonation could lead to a less toxic compound [112].
Also, Vekiru et al. indicated that ZOM-1, a new ZEA
metabolite, was characterized by an opening of the macro-
cyclic ring of ZEA at the ketone group at C60. This new
ZEA metabolite did not interact in vitro with the estrogen re-
ceptor protein and was not estrogenic in vivo, indicating the
loss of ZOM-1 (novel ZEA metabolite) estrogenicity. They
also showed that ZEA was found to be entirely degraded by
several Rhizopus including R. stolonifer, R. oryzae and R. mi-
crosporus [113]. Moreover, one another study showed that
Rhizopus arrhizus catalyzes sulfation of ZEA at the C-4 hy-
droxyl group [114]. Based on the study of Utermark J et al.,
the Gliocladium roseum (mycoparasitic fungus) produces a
ZEA -specific lactonase which catalyzes the hydrolysis of
ZEA, followed by a spontaneous decarboxylation. The
growth of G. roseum was not inhibited by ZEA, and the lac-
tonase may protect G. roseum from the toxic effects of this
mycotoxin [115]. Using strains of S. cerevisiae, G. fermen-
tans, K. marxianus, and M. pulcherrima yeasts, J.
Repecˇkiene et al. eliminated ZEA from wheat flour and fod-
der [116].
4.3. Ochratoxins
Based on some research, reduction of OTA production
of Penicillium verrucosum can be caught by several S. cere-
visiae and also some non-Saccharomyces yeasts such as
Hanseniaspora spp., Trichosporon spp., Rhodotorula spp.,
and Cryptococcus spp., Trichosporon spp., Rhodotorula
spp., and Cryptococcus spp. were able to split the amide
bond of the OTA molecule and release non-toxin ochratoxin
an (OTα) [117, 118]. In addition to the effects of Pichia ano-
mala, Pichia kluyveri and Hanseniaspora uvarum predomi-
nant during coffee processing on the growth of Aspergillus
ochraceus and production of OTA on malt extract agar
(MEA) and coffee agar (CA) were studied by Utermark J et
al. [115] when three yeasts co-cultured in MEA and CA,
they showed capability to inhibit growth of A. ochraceus.
Moreover, Molnar et al. also isolated, characterized, and re-
searched the ability of T. mycotoxinivorans, to detoxify
OTA in a mineral solution [111]. Ochratoxin is detoxified
by the cleavage of the phenylalanine moiety to form the deri-
vate ochratoxin-A, a virtually nontoxic metabolite compared
to the parent compound [111]. Velmourougane et al., in
their study, employed yeast suspension (S. cerevisiae) in cof-
fee post-harvest. In result, total mould incidence and ochra-
toxin-A contamination were mitigated meaningfully without
any effects on cup quality. Also, the use of yeast culture in
coffee processing was found to be an affordable and cost-ef-
fective approach in the management of A. ochraceus and
OTA in parchment and cherry coffee preparation [119].
Based on the study of Bejaoui et al., S. cerevisiae and
Saccharomyces bayanus. showed OTA absorption ability in
synthetic grape juice [120]. There is some evidence on the
destroyable effects of some baker's yeast (S. cerevisiae)
strains on the growth of Aspergillus carbonarius and Fusari-
um graminearum effectively. Based on another study, total
mold incidence (A. ochraceus and A. niger) and contamina-
tion of OTA on a coffee can be decreased by S. cerevisia
[119]. Furthermore, the growth rate of ochratoxin-producing
Aspergillus spp. and the amount of the accumulated OTA in
vitro and on detached grape berries can be reduced by
Lachancea thermotolerans (formerly Kluyveromyces)
[121]. One investigation about biocontrol activity of the na-
tive yeast flora indicated that OTA biosynthesis could be in-
hibited by Debaryomyces spp., Candida spp., and Hy-
phopichia spp. Based on this study, the indigenous yeasts
had an antagonistic effect on the Penicillium nordicumas.
well growth. Also, the growth and biosynthesis of OTA can
be effectively reduced by H. burtonii and C. zeylanoides
[122]. In another study, detoxification capabilities of S. cere-
visiae, Geotrichum fermentans, Kluyveromyces marxianus,
and Metschnikowia pulcherrima have been tested on wheat
flour and composite fodder contaminated with different my-
cotoxins, and the DON content was significantly reduced in
the samples with greater effectiveness in the fodder [116].
Based on the study of Caridi et al., wine yeast (S. sensus-
tricto) could remove OTA from the synthetic medium. They
resulted that seven out of 20 yeast strains removed high lev-
els of OTA, ranging from 66% to 100% [123].
4.4. Deoxynivalenol
Styriak et al. indicated that after incubation with yeast
culture, the concentration of DON reduced up to 37% [124].
Also, Paskevicius et al. reported that in fodder inoculated
with several yeast genera resulted in the loss of DON [125].
P. Karlovsky et al. supposed that these results might have
been caused by adsorption [126]. Chenghua He et al. [127]
used the biotransformation system to decrease DON toxici-
ty. They isolated a Aspergillus spp. (NJA-1) from soil and
cultured it in an inorganic salt medium containing DON. An
unknown factor in NJA-1 caused DON toconvertinto
another product. Recent investigations indicated that NJA-1
could hydrolyze DON [127].
4.5. Fumonisins
There are not reliable and available documents about the
effects of yeast and fungal strains on fumonisins degrada-
tion. However, the ability of 12 S. cerevisiae strains has
been tested for the degradation of fumonisins and
zearalenone in Sabouraud broth. In the result, one strain de-
creased the concentration of mycotoxin up to 25% and one
strain up to 75% of the original amount. On the contrary, the
effects of two strains on fumonisins degradation were partial
[124].
4.6. Patulin
The investigation of yeast effects on PAT degradation
has been developed properly. For example, Stinson et al. in-
dicated that the PAT content in contaminated apple juice
with yeast reduced during alcoholic fermentation [128].
Moss et al. [129] found that three commercial cider strains
of S. cerevisiae were able to degrade PAT, but this was
achieved during active fermentative growth, but not when

10 Infectious Disorders - Drug Targets, 2020, Vol. 20, No. 0 Abdi et al.
growing aerobically. The polarity of the PAT degradation
products was more than PAT itself and remained in the clari-
fied fermented cider. Richelli et al. [130] showed that ac-
cording to the change of chemical structure and the degrada-
tion product (ascladiol), the capability of Gluconobacter oxy-
dans to PAT degradation was more than 96% after twelve-
hour treatment. In another study and in order to ferment ap-
ple juice including 15 mg of patulin/L, eight yeast strains
were used in three typical American processes. In the result,
except for two cases, patulin was decreased to less than the
minimum detectable level of 50 µg/L. In all cases and dur-
ing alcoholic fermentation, the level of PAT was diminished
by over 99% [131]. The culture supernatant of P. ohmeri
158 was able to inhibit mycelial growth (66.17%). The ini-
tial PAT concentration of 223 µg in the presence of P. oh-
meri 158 cells was decreased over 83% of the original con-
centration, when incubated at 25ºC for 2 days and > 99% af-
ter 5 days incubation time, with undetectable PAT level af-
ter 15 days. The results of this study showed that P. ohmeri
158 could be a suitable and efficient alternative for the inhi-
bition of P. expansum growth and PAT degradation [132].
[137] According to the study of Ianiri et al. [133] Basi-
diomycete yeasts, which have shown capability for degrad-
ing PAT effectively, could be explored by various methods
to realize this degradation process.
Based on this study, Sporobolomyces strain IAM 13481
was able to degrade PAT (which produced by the mold) to
form two various breakdown products, desoxypatulinic acid,
and (Z)-ascladiol. Compare to PAT; these products have less
toxicity. Based on their study, pre-incubated cells in a low
concentration of PAT had stronger resistance to PAT toxici-
ty and faster kinetics of degradation. When extracts of
Sporobolomyces spp. were prepared from the cells pre-treat-
ed with mycotoxin, the degradation of PAT was faster [133].
Moreover, the yeast species that showed their effects on my-
cotoxins, there are some other yeast species containing
Sporobolomyces roseus, P. ohmeri, M. pulcherrima, and R.
kratochvilovae analysed for their ability to degrade PAT
[132-135].
5. MECHANISMS INVOLVED IN DETOXIFICATION
Biological detoxification of mycotoxins occurs mainly
via two primary mechanisms, enzymatic and degradation
sorption. Both of these mechanisms can be performed by mi-
croorganisms.
Living microorganisms can absorb mycotoxins by attach-
ing or actively internalizing them. Enzymatic degradation
can be occurred by either extra or intracellular enzymes. Dif-
ferent chemical structures of mycotoxin groups make it im-
possible to equally deactivate all mycotoxins using only one
single strategy [136].
5.1. Degradation
5.1.1. Fumonisins
Degradation of the fumonisins mostly occurs through the
removal of TCA groups and a free amino group. It has been
observed that Sphingomonas spp. ATCC 55552 can degrade
fumonisin B1 through the action of an aminotransferase
[137] and a carboxylesterase [138]. Also, in Sphingopyxis
spp. MTA 144, a similar pathway was found [139].
Exophiala spp. can degrade the fumonisins through the ac-
tion of a carboxylesterase and an oxidative deaminase. Two
products that result from fumonisin degradation include a
new compound, 2-oxo-12,16-dimethyl-3,5,10,14,15- icosane-
pentol hemiketal, and in fewer amounts the N-acetylated
aminopentol backbone (N-acetylAP1). Strain NCB 1492,
gave rise to four tentative degradation products of fumonisin
B1: heptadecanone (C17H34O), isononadecene (C19H38),
octadecenal (C18H34O) and eicosane (C20H42) [140]. It
seems that the first steps of degradation occur extracellular-
ly, with deaminase (and possibly esterase) activity after a
slower degradation of the aliphatic chain. Due to structural
similarity of Alternaria toxins AAL-T to Fumonisins, it is
possible that fumonisin degrading organisms also be able to
degrade AAL-toxin [141].
5.1.2. Zearalenone
Recently, two significant mechanisms of Zearalenone
(ZEN) inactivation were discovered. Both mechanisms of ac-
tion inactivate through the cleavage in a ring structure.
The first mechanism is the cleavage of the lactone ring,
which is the one that appears in some fungal species. In the
case of Gliocladiumroseum NRRL1859, two degradation
products of ZEN toxins were obtained: by obtained 1-(3,5-di-
hydroxyphenyl)-10′-hydroxy-1-undecen- 6′-one and 1-(3,5-
dihydroxyphenyl)-6′-hydroxy-1-undecen-10′-one [110].
Matthies et al. showed that derivatives zearalanol and α-
zearalanol induced production of the ZEN-degrading en-
zyme in G. roseum DSM 62726 [142]. A near isogenic
strain, Clonostachys rosea degrade ZEN through the action
of a ZEN lactonohydrolase enzyme (zhd101) which cata-
lyzes the hydrolysis of ZEN at the ester bond in the lactone
ring, followed by spontaneous decarboxylation. Only the
first metabolite (1-(3,5-dihydroxyphenyl)-10′-hydroxy-1-un-
decen- 6′-one) was observed after degradation [143]. Based
on this knowledge, Popiel et al. studied on a collection of
Trichoderma spp., and Clonostachys spp., to find a function-
al ZEN lactonohydrolase in mycoparasitic Trichoderma ag-
gressivum [144]. A similar process might also exist in Bacil-
lus spp. such as B. natto CICC 24640 and B. subtilis 168
that cause complete degradation of ZEN [145]. A second
cleavage pathway is shown by the yeast Trichosporum myco-
toxinivorans to ZOM-1 intermediate (cleavage at the C6-ke-
tone group) [111], suggested taking place through a lactone
intermediate and subsequent activity by unspecified a/b-hy-
drolase. Similar pathway (but without the decarboxylation)
was seen in C. rosea strain FS10 convert ZEN into two inter-
mediate products, ZEN-A, and ZEN-B [146]. Similarly,
Acinetobacter spp. SM04 produces two degradation prod-
ucts (ZEN-1 and ZEN-2) from ZEN [147]. Pseudomonas
spp. ZEA-1 was shown to harbor the responsible genes for
degradation of ZEN and its derivatives on a 120 kb plasmid.
Rhodococcus spp., as a metabolically highly versatile genus,

Microbiological Detoxification of Mycotoxins Infectious Disorders - Drug Targets, 2020, Vol. 20, No. 0 11
showed considerable potential for biodegradation and to the
complete loss of ZEN estrogenic activity and also simultane-
ously degradation AFB1, ZEN, and T2-toxin [85, 148].
5.1.3. Trichothecenes
Trichothecenes toxicity results from their epoxide-group
and depends on their acylated side chains. Two main groups
of trichothecenes are; acylated (e.g., T-2 toxin) and non-acy-
lated trichothecenes (e.g., DON) [141]. The first step in dis-
abling the acylated trichothecenes is de-acylation. Curtobac-
terium spp. strain 114-2 degrade T-2 toxin to HT-2 toxin
and subsequently to T-2 triol, which is less toxic [149]. The
next step of trichothecenes detoxification is de-epoxidation.
Eubacterium spp. BBSH 797 can degrade several tri-
chothecenes [150, 151]. This strain has been developed into
a commercial product (Biomin BBSH 797) for detoxifying
trichothecenes in animal feed [152]. It is known for its abili-
ty to detoxify DON into deepoxy-deoxynivalenol (DOM-1)
and de-epoxidization of NIV, T-2 tetraol, scirpentriol, and
HT-2 toxin. Further, 4-acetyl NIV and 3-acetyl NIV was de-
acetylated and/or de-epoxidized [150]. Degradation of DON
occurs through de-epoxidation, oxidation, or isomerization.
Microbial culture C133 of fish guts transformed DON to
DOM-1 [153]. Citrobacter freundii could transform DON in-
to DOM-1 aerobically [154]. DON can also be oxidized to
3-keto DON which is 10 times less toxic than DON evaluat-
ed with a bioassay based on mitogen-induced and mito-
gen-free proliferation of mouse spleen lymphocytes [155].
The bacterium strain E3-39 which degraded DON to 3-keto--
DON, is belonging to the Agrobacterium-Rhizobium spp.
group. A mixed culture from environmental sources could
degrade DON into 3-keto-DON, whereas 15-acetyl DON, 3-
acetyl DON, and fusarenon-X were also transformed [156].
The metabolite 3-epi-DON was also formed by degradation
of DON through Nocardioides spp. strain WSN05-2 [157].
Moreover, lastly, nine Nocardioides spp. (Gram-positive)
and four Devosia spp. (Gram-negative) produced 3-epi--
DON aerobically. The Gram-positive strains showed DON
assimilation, whereas the Gram-negatives did not showed
[158].
5.1.4. Aflatoxins
For the first time, the biological detoxification of AFB1
mediated by Flavobacterium aurantiacum (now called No-
cardia corynebacterioides) has been reported in 1966 [79,
159].
After this first report, while many studies focused on the
detoxification of AFB1, only a few studies detected the
degradation products and analyzed their toxicity. There are
two major pathways of detoxification of aflatoxins which in-
clude modification of the difuran ring and the coumarin
structure. Several studies reported modification of the difu-
ran ring moiety. Degradation of AFB1 into AFB1-8,9- dihy-
drodiol was performed by manganese peroxidase from the
white rot fungi Phanerochaete sordida [160] and the “afla-
toxin-detoxifizyme (ADTZ)” of fungus Armillariella tabes-
cens [161]. The authors suggested that AFB1 degradation ini-
tially involves the formation of AFB1-8,9-epoxide, after
which hydrolysis resulted in a dihydrodiol-derivate. Another
metabolite was detected with the white rot fungus Pleurotus
ostreatus GHBBF10 which degraded 91.76% of AFB1 into
a component which could be a hydrolyte of AFB1, namely
dihydro hydroxy aflatoxin B1 (AFB2a) [162]. Many studies
have shown a modification of the lactone ring in the cou-
marin moiety of AFB1. In a study, a Pseudomonas putida
strain has shown the ability of degradation of AFB1 into
AFD1 and subsequently into AFD2 that have lower muta-
genicity and toxicity [163, 164]. In some studies, no degrada-
tion product was identified, but toxicity tests were per-
formed on the treated AFB1. Similarly to F. aurantiacum, as
mentioned before, a pure laccase enzyme from Trametes ver-
sicolor and a recombinant laccase enzyme produced by A.
niger degraded AFB1 with a significant loss of toxin muta-
genicity [103]. Also, in Rhodococcus eryhtropolis extracellu-
lar enzymes were able to degrade AFB1 with a loss of muta-
genicity [78].
5.1.5. Ochratoxins
The primary detoxification pathway of OTA is the hydro-
lyzation of the amide bond between the isocoumarin residue
and phenylalanine by a carboxypeptidase. Two classes of
carboxypeptidases have been associated with degradation of
OTA which include carboxypeptidase A (CPA) [103] and
carboxypeptidase Y (CPY) [165]. Peptidase enzyme has an
essential role in the efficient degradation of OTA. Other en-
zymes are also able to carry out this reaction: Dioxygenases,
lipases, amidases, and several commercial proteases [166].
Although depending on the enzyme, intermediates may be
different, but the end product is always OTα. Trichosporon
mycotoxinivorans was able to convert OTA into the nontox-
ic OTα. Also, Phenylobacterium immobile can convert OTA
to ochratoxin α (OTα) through a dioxygenase step on the
phenylalanine moiety, a dehydrogenation to catechol, a ring
cleavage and the final formation of OTα via ahydrolase
[141].
5.2. Adsorption
The most common technique used for reducing exposure
to mycotoxins is the use of mycotoxin-binding agents or ad-
sorbents, which reduce mycotoxin uptake. Lactic acid bacte-
ria and Bifidobacterium species are the two most important
groups of microorganisms that have been much studied.
5.2.1. Bifidobacterium Species
Peltonen et al. studied the AFB1 binding ability of five
Bifidobacterium strains in phosphate buffered saline (PBS),
and they noticed that Bifidobacterium spp. bound
18%–48.7% of AFB1 [25]. Recently, Fuchs et al. investigat-
ed the detoxification of two abundant mycotoxins, namely
OTA and PAT, by Bifidobacterium and they found that two
Bifidobacterium longum (LA 02, VM 14) strains were high-
ly effective and caused a decrease of OTA by approximately
50%, whereas with PAT, the most potent effect (ca. 80% de-
crease) was seen with a B. animalis (VM 12) strain [45]. Re-
cently, Hatab et al. reported that the maximum PAT uptake

12 Infectious Disorders - Drug Targets, 2020, Vol. 20, No. 0 Abdi et al.
was achieved by B. bifidum 671 by (52.9%) for viable and
(54.1%) for nonviable cells after 24-h incubation [167]. On
studying the ability of two dairy strains of B. bifidum to re-
move AFM1 from PBS and reconstituted milk, results re-
vealed that viable (108 CFU mL−1) and heat-killed Bifi-
dobacterium spp. ranged from 14.04% to 28.07%, and from
12.85 to 27.31% in PBS and reconstituted milk, respectively
[168]. Previous studies also revealed that the binding abili-
ties of AFM1 by B. longum and B. bifidum reached 26.7 and
32.5%, respectively [169].
5.2.2. Lactic Acid Bacteria
5.2.2.1. Aflatoxins
Specific dairy species of LAB such as Lactobacillus and
Lactococcus have been shown to bind and remove AFB1,
the most common aflatoxin [170, 171]. The toxin-removing
capacity of a combination of strains of LAB is not the sum
of their capacities. Thus suggesting that pure, single strains
should be used when the goal is to remove single com-
pounds and that the use of combinations of strains may be
beneficial when several compounds are removed together
[172].
The binding abilities of AFM1 by viable Lactobacillus
spp. at 108 CFU mL−1 in PBS ranged from 10.22 to 26.55%
depending on the contamination level and incubation period
[168]. They added that the percentage of AFM1 removal by
heat-killed bacteria from PBS ranged from 14.04 to 28.97%.
Similarly, Kabak and Var found that the binding abilities of
AFM1, by Lactobacillus spp. in PBS and reconstituted milk,
ranged from 25.7 to 30.5% [169]. These results were consid-
ered to be lower than those reported by Pierides et al., who
found that the AFM1 binding abilities of viable Lactobacil-
lus spp. within 15–16 h ranged from 18.1 to 50.7% [173].
5.2.2.2. Ochratoxin A
Degradation of OTA was observed in milk due to the ac-
tion of Lactobacillus and Streptococcus spp [174]. Lactoba-
cillus spp. such as L. rhamnosus spp., L. bulgaricus spp., L.
helveticus spp., and L. acidophilus were efficiently able to re-
move OTA [51]. Wine LAB (Lactobacillus spp., Pediococ-
cus spp., and Oenococcus oeni spp.) caused a decrease in
OTA concentration [57].
5.2.2.3. Patulin
The effect of LAB on PAT, was shown by the decline of
PAT (39%) by Lactobacillus plantarum [45]. Hatab et al. it
has been reported that the high PAT uptake from aqueous so-
lution was achieved by Lactobacillus rhamnosus 6149 strain
[167]. At pH 4.0 and 37 ° C, the highest removal of PAT
was seen Lactobacillus rhamnosus caused 80.4% decrease
of PAT in apple juice [47].
5.2.2.4. Fusarium Toxins
Certain LAB strains have been the detoxifying effect on
other mycotoxins such as fusarium toxins (T-2 toxin, DON,
NIV, HT-2 toxin) [51]. Binding is the mode of action of re-
moval of Fusarium mycotoxins by fermentative bacteria
[39]. The consistency of the mycotoxin-LAB interaction
was due to the amino acid composition of the peptidoglycan
structure [175]. The ability of Lactobacillus rhamnosus
strains to remove ZEN, and its derivative α-zearalenol, from
a liquid medium, was reported by El-Nezami et al. [176].
Haskard et al. studied the mechanism of binding between
AFs and Lactobacillus rhamnosus and found that binding oc-
curs predominantly with the carbohydrate and to some ex-
tent, the protein components in the cell wall. These results
were based on the inhibitory effects of periodate and pro-
nase E on AFB1 binding by Lactobacillus rhamnosus Perio-
date and pronase E can be used to degrade relatively non-
specifically both carbohydrates and proteins, respectively.
They also described the primary role of hydrophobic interac-
tions in binding and found that electrostatic interactions play
only a minor role [69].
CONCLUSION
Microbiological decontamination of mycotoxins has
been considered as a main and effective approach for myco-
toxin biodegradation. Regardless of the method used, proper
management tools that consist of before-harvest prevention
and after-harvest detoxification, are required. However, the
use of this approach depends on its effectiveness from both
a practical and economic perspective.
CONSENT FOR PUBLICATION
Not applicable.
FUNDING
None.
CONFLICT OF INTEREST
The authors have no conflicts of interest, financial or
otherwise.
ACKNOWLEDGEMENTS
We are grateful for the useful comments and suggestions
from anonymous referees.
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