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Protective role of Spirulina platensis against glyphosate induced toxicity in marine mussel Mytilus galloprovincialis

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Glyphosate is a toxic environmental pollutant that has the ability to induce biochemical and physiological alterations in living organisms. Several studies have focused on the research of protective techniques against the stress induced by this contaminant. In this context, we studied the protective effect of Spirulina against the disturbances induced by glyphosate. A biomarker approach was adopted to determine the impact of glyphosate, Spirulina and their mixture, during two time slots (4 and 7 days), on Mytilus galloprovincialis. Glyphosate treated mussels revealed significantly increased malondialdehyde and decreased acetylcholinesterase (AChE) levels. Spirulina normalized catalase (CAT), glutathione-S-transferase (GST), and AChE activities. Furthermore, it reduced glyphosate-induced malon-dialdehyde (MDA) levels. The current study suggests a protective effect of Spirulina against glyphosate-induced oxidative stress by strengthening the antioxidant system, sequestering ROS and inhibiting cellular damage.
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Journal of Environmental Science and Health, Part C
Toxicology and Carcinogenesis
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Protective role of Spirulina platensis against
glyphosate induced toxicity in marine mussel
Mytilus galloprovincialis
Ouarghi Wided, Khazri Abdelhafidh, Mezni Ali & Samir Touaylia
To cite this article: Ouarghi Wided, Khazri Abdelhafidh, Mezni Ali & Samir Touaylia
(2021): Protective role of Spirulina�platensis against glyphosate induced toxicity in marine
mussel Mytilus�galloprovincialis, Journal of Environmental Science and Health, Part C, DOI:
10.1080/26896583.2021.1954833
To link to this article: https://doi.org/10.1080/26896583.2021.1954833
Published online: 04 Aug 2021.
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Protective role of Spirulina platensis against glyphosate
induced toxicity in marine mussel Mytilus
galloprovincialis
Ouarghi Wided, Khazri Abdelhafidh, Mezni Ali, and Samir Touaylia
Environmental Biomonitoring Laboratory (LBE), Faculty of Sciences of Bizerte, University of
Carthage, Zarzouna, Tunisia
ABSTRACT
Glyphosate is a toxic environmental pollutant that has the
ability to induce biochemical and physiological alterations in
living organisms. Several studies have focused on the research
of protective techniques against the stress induced by this
contaminant. In this context, we studied the protective effect
of Spirulina against the disturbances induced by glyphosate. A
biomarker approach was adopted to determine the impact of
glyphosate, Spirulina and their mixture, during two time slots
(4 and 7 days), on Mytilus galloprovincialis. Glyphosate treated
mussels revealed significantly increased malondialdehyde and
decreased acetylcholinesterase (AChE) levels. Spirulina normal-
ized catalase (CAT), glutathione-S-transferase (GST), and AChE
activities. Furthermore, it reduced glyphosate-induced malon-
dialdehyde (MDA) levels. The current study suggests a protect-
ive effect of Spirulina against glyphosate-induced oxidative
stress by strengthening the antioxidant system, sequestering
ROS and inhibiting cellular damage.
KEYWORDS
Glyphosate; Mytilus
gallorovincialis; oxidative
stress; Spirulina; biomarkers
Introduction
Glyphosate (N-(phosphonomethyl) glycine) is a substituted glycine origin-
ally developed and patented as a broad-spectrum herbicide.
1
The use of
glyphosate has risen considerably. It can be considered one of the most
used herbicides and its use has increased more than 12 times from 67 mil-
lion kg in 1995 up to 826 million kg in 2014.
2
Due to its widespread use in
agriculture, forestry, aquaculture and urban areas, glyphosate can easily
spread throughout ecosystems, including surface waters, thus Reaching
plants, animals, and the food chain.
3
Glyphosate has been detected in
aquatic environments at concentrations ranging between 10 and 45 mg/L,
4
while much higher concentrations (>320 mg/L) were detected in wetland
environments and ponds after glyphosate application.
5,6
Glyphosate
CONTACT KHAZRI Abdelhafidh khazri27@gmail.com Environmental Biomonitoring Laboratory (LBE),
Faculty of Sciences of Bizerte, University of Carthage, Zarzouna, Tunisia
ß2021 Taylor & Francis Group, LLC
JOURNAL OF ENVIRONMENTAL SCIENCE AND HEALTH, PART C
https://doi.org/10.1080/26896583.2021.1954833
concentrations ranging from 13 mg/L to 1377 mg/L have been reported in
seawater.
7
While the mode of action of glyphosate is specific to plants, several
studies have demonstrated a wide range of toxicological effects in vertebrate
and invertebrate species, including aquatic organisms.
8,9
Glyphosate and its
commercial formulation Roundup have been shown to increase oxidative
stress in fish species by enhancing ROS generation and altering antioxidant
defenses.
10
Due to their high reactivity, ROS may damage macromolecules
such as lipids, proteins, carbohydrates and nucleic acids.
11
To neutralize
ROS, organisms have an antioxidant defense pathway constituted of antioxi-
dant enzymes as well as non-enzymatic antioxidants. When the animals
defenses are insufficient to neutralize ROS, oxidative damage may occur, and
one of the most serious damages is membrane lipid peroxidation.
12
The mussel, Mytilus galloprovincialis, is a globally distributed mollusk
found in coastal areas. Many environmental monitoring programs choose
mussels as bioindicators due to their sessile filter feeding life-style and cap-
acity to accumulate contaminants.
13
Marine mussels are listed as bioindica-
tors in the Mussel Watchprogram, which is a global marine
environmental monitoring program.
14
Spirulina is rich in antioxidants, including proteins, polysaccharide, vita-
mins, carotenoids, and other bioactive compounds, which impart Spirulina
strong anti-oxidation properties. Numerous animal studies and clinical tri-
als have proved that Spirulina improved a variety of oxidative stress-
induced symptoms by enhancing the bodys anti-oxidation capacity.
15
Owing to its free radical scavenging and potent antioxidant activity,
Spirulina administration has been shown to limit the pesticide-induced
toxic effects of deltamethrin on Oreochromis niloticus.
16
The present study examines the role of Spirulina platensis in mitigating
the effects of glyphosate-based herbicide contamination on the gills and
digestive glands of M. galloprovincialis. Investigations included measure-
ment of the antioxidant status and oxidative stress damage.
Material and methods
Chemicals
Glyphosate is a pesticide of the herbicide family (99% purity), it was sup-
plied by the company Sigma-Aldrich and it was used, in this experiment,
in the form of a white crystalline powder. Spirulina (SP) pure powder was
purchased from (Herbaforce, UK).
Experimental design
The mussel M. galloprovincialis (average size of 6 ± 0.5 cm) were collected,
during the month of November, from the private shellfish farm located in
2 O. WIDED ET AL.
Menzel Jemil east of the Bizerta lagoon in a relatively quiescent area, next
to the Soci
et
e Tunisia Lagoon. Upon arrival at the laboratory (Faculty of
Sciences of Bizerte), harvested mussels were placed in glass aquariums filled
with seawater, which is the only food source. The mussels were acclimat-
ized for 7 days under physicochemical conditions similar to their natural
conditions (temperature ¼18C, pH ¼8 and salinity ¼30 psu). The sea-
water was renewed every 48 hours. The aquariums were constantly venti-
lated by bubbling in an air-conditioned room and were subjected to a
controlled photoperiod of 12 h/12h. After acclimation, the experiment was
started: three jars were prepared for each time point (4 and 7 days), with
each jar containing a set of 5 mussels. Six treatment groups containing 5
mussels each were established: (a) the first group served as the control, (b)
the second group was provided Spirulina powder-supplemented diets
(1 mg/L), (c) the third group was exposed to 50 mg/L glyphosate (C1), (d)
the fourth group received 50 mg/L of glyphosate and Spirulina powder-sup-
plemented diets (1 mg/L), (e) the fifth group was exposed to 100 mg/L gly-
phosate (C2), and (f) fourth group received 100 mg/L glyphosate and
Spirulina powder-supplemented diets (1 mg/L).
Biochemical analyses
Contamination by glyphosate makes it possible to demonstrate the bio-
chemical response of mussels. Four biochemical biomarkers have been
studied to achieve this goal, AChE, CAT, GST activities and MDA levels.
The gills and digestive glands were removed for each individual and placed
in pillboxes which were used for tissue crushing. After homogenization by
polytron homogenizer in 10 mM Tris/HCl, pH 7.4, containing 500 mM
sucrose, 1 mM EDTA and 1 mM phenylmethylsulfonyl fluoride, the hom-
ogenate obtained was centrifuged at 9000 g for 30 min at 4 C. The resulting
supernatants (S9) were used as for measuring AChE, CAT, and GST
enzyme activities and MDA levels. Protein content was estimated by the
Bradford method Bradford (1976),
17
using bovine serum albumin (BSA).
The determination of the enzymatic activity of catalase was carried out
according to the method of Aebi (1983).
18
The activity was measured at
240 nm using a spectrophotometer. One unit of the enzyme was expressed
as mM of H
2
O
2
utilized/mg protein.
The activity of GSTs is measured, according to the method of Habig
et al. (1974),
19
by providing the enzyme with a general substrate 1-chloro-
2,4-dinitrobenzene (CDNB). The optical density measured at 340 nm is dir-
ectly proportional to the quantity of conjugates formed, itself linked to the
intensity of the GST activity.
JOURNAL OF ENVIRONMENTAL SCIENCE AND HEALTH, PART C 3
AChE activity was determined based on the colorimetric method described
by Ellman et al. (1961)
20
using S9 tissue supernatants. In brief, 10 mLportions
of S9 supernatants were placed in a cuvette with 200 ml phosphate buffer
0.1 mol/L (pH 8), 100 mL of DTNB 0.01 mol/L, 5,50-dithiobis (2-nitrobenzoic
acid) (DTNB) and 20 mL of 0.075 mol/L acetylthiocholine iodide were added to
them. The changes in optical density at 412 nm for 30 min (kinetic absorb-
ance) against blanks were used to calculate AChE activities.
Lipid peroxidation was estimated in terms of thiobarbituric acid reactive
species, using malondialdehyde (MDA) as standard by the method of
Buege and Aust.
21
S9 samples (100 lL) were mixed with 75 lL of phosphate
buffer 0.1 mol/L and 125 lL of 20% v/v trichloroacetic acid (TCA). The
mixture thus formed was vortexed and centrifuged for 15 min at 9000 g.
After centrifugation, 200 lL of the supernatants were reacted with 160 llof
Trishydroxym
ethylaminomrthane- 2-thiobarbituric acid in the presence of
40 ll HCl 5%. The tubes containing these solutions were then placed in a
water bath at 80C for 15 min. A pink complex appears as a result of the
reaction of thiobarbituric acid (TBA) with MDA. The absorbance at
532 nm were measured using a microplate reader. Lipid peroxidation was
expressed as lmol of MDA/mg protein.
Statistical analyses
Data were expressed as mean ± standard deviation (SD) and statistical anal-
yses were performed using STATISTICA 8. The variation of behavioral
response among treatment was tested by one-way analysis of variance
(ANOVA) compared to controls. In addition, three-way ANOVA was used
to analyze interaction between organs, condition and duration. Whenever
ANOVA detected significant differences, post hoc comparisons were made
using the Tukey HSD test. A probability level of less than 0.05 was consid-
ered significant (95% confidence interval).
Results
Antioxidants enzymes activities
Antioxidant enzymes in gills and digestive glands of M. galloprovincialis were
measured. Glyphosate modulated CAT activity in mussel gills and digestive
glands (Figure 1). A significant increase of CAT activity was detected for a
low and higher concentrations C1 ¼50 mg/L and C2 ¼100 mg/L measured
4 days. The activity of CAT was significantly increased in S9 fractions of gills
from mussels exposed to glyphosate in comparison to controls. The co-treat-
ment with spirulina recovered the CAT activity to its normal levels in glypho-
sate-intoxicated groups (Figure 1). CAT activity was also significantly
4 O. WIDED ET AL.
(p<0.05) induced in gland digestive tissue S9 homegenates from glyphosate-
treated mussles, whereas the co-treatment of Spirulina reversed the glyphosate-
induced alterations when compared to the group treated with glyphosate alone
(Figure 1)
The induction of catalase activity after 7 days of exposure to glyphosate
(Figure 2), in gills, is similar to that observed at 4 days. Likewise, this activity,
in the digestive gland showed a highly significant increase (p<0.001) for a
lower glyphosate concentration and a significant increase (p<0.05) for a
higher concentration compared to the control group. Likewise, the treatment
of the mussels with glyphosate with spirulina supplementation showed a
modulation of the CAT activity compared with the group treated only with
glyphosate. In fact, a significant drop (p<0.05) in this activity was recorded
for one concentration (C
1
þSp), while for a high concentration (C
1
þSp) a
highly significant decrease (p<0.001) in this activity is noted. Additionally,
factorial two-way ANOVA showed significant differences in CAT activity
between organs (F ¼32.271, p<0.0001) and treatments (F ¼9.993, p<0.0001)
Table 1.Figure 3 shows after 4 days of exposure, a significant increase
(p<0.05), compared to the normal control, in the activity of GST follow-
ing the treatment of mussels with the two concentrations of glyphosate;
this increase was observed at the level of the two organs tested. However,
the co-treatment of the mussels with spirulina and glyphosate, for the two
concentrations considered, showed a marked significant decrease
(p<0.05) in the activity of GST in the gills and the digestive gland of the
treated mussels compared with in conjunction with that treated only
with glyphosate.
By increasing the duration of contamination of the mussels by glyphosate
(Figure 4), a significant decrease (p<0.05) is observed, at the level of the
gills and the digestive gland, in the activity of the GST compared to the
normal control, considering the two concentrations tested. By treating the
Figure 1. Variation in catalase activity in the gills and digestive gland of M. galloprovincialis
mussels exposed to two concentrations of glyphosate without or with spirulina for 4 days. Bars
represent the group means ± SD, n ¼5; a, b, c, d and e: differences at the 5% threshold.
JOURNAL OF ENVIRONMENTAL SCIENCE AND HEALTH, PART C 5
mussels for 7 days with combined spirulina and glyphosate, a significant
increase (p<0.05) in GST activity, compared to the groups treated with
glyphosate alone, is detected in the organs tested. Factorial two-way
ANOVA showed no significant differences in GST activity between organs
(F ¼2.071, p¼0.154) and significant differences between treatments
(F ¼4.401, p¼0.001) Table 1.
Lipid peroxidation
The levels of lipid peroxidation in the gills and the digestive gland tissue of
control and experimental mussels are illustrated in Figures 5 and 6.Infact,
the formation of MDA indicates the presence of lipid peroxidation. These fig-
ures then show an increase in the level of MDA following the treatment of
the mussels with two concentrations of glyphosate during the two time periods
considered (4 and 7 days). This increase is significant (p<0.05) compared to
the control group, at the level of the gills as well as at the level of the digestive
glands of the treated mussels. Indeed, the co-treatment of mussels by spirulina
with glyphosate significantly reduced (p<0.05) the level of MDA in the gills
and digestive glands of mussels in conjunction with mussels treated with gly-
phosate only. Factorial 2-way ANOVA showed no significant difference in
MDA levels between organs (F ¼0.001, p¼0.970) and showed significant dif-
ference between treatments (F ¼4.132, p<0.002) Table 1.
Neurotoxicity biomarker
Glyphosate altered AChE activity in the gills and the digestive glands depend-
ing on the concentration considered. The attenuation of AChE activity by gly-
phosate and the prevention of its neurotoxicity by spirulina was observed for
4and7days(Figure 7 and 8). In fact, during the two time slots, a significant
Figure 2. Variation in CAT activity in the gills and digestive gland of M. galloprovincialis mussel
exposed to two concentrations of glyphosate without or with spirulina for 7days. Bars represent
the group means ± SD, n ¼5; a, b, c and d: differences at the 5% threshold.
6 O. WIDED ET AL.
decrease (p<0.05), compared with the control group, of the enzymatic activity
was observed at the level of the two organs tested. Supplementation of spiru-
lina with glyphosate prevented the deactivation of AChE by significantly
increasing (p<0.05) its activity compared to the group treated only with gly-
phosate. Factorial 2-way ANOVA showed no significant difference in AChE
activity between organs (F ¼0.123, p¼0.727) and showed significant differ-
ence between treatments (F ¼71.844, p<0.000) Table 1.
Table 1. Results of three-way ANOVA analysis.
Effects Dependent variable Df F-value p-value
Organs CAT activity 1 32.271 0.000
GST activity 1 2.071 0.154
MDA content 1 0.001 0.970
AChE activity 1 0.123 0.727
Conditions CAT activity 5 9.993 0.000
GST activity 5 4.401 0.001
MDA content 5 4.132 0.002
AChE activity 5 8.008 0.000
Duration CAT activity 1 30.978 0.000
GST activity 1 68.146 0.000
MDA content 1 118.884 0.000
AChE activity 1 71.844 0.000
OrganConditions CAT activity 5 1.658 0.158
GST activity 5 1.997 0.087
MDA content 5 1.124 0.354
AChE activity 5 1.015 0.415
OrgansDuration CAT activity 1 4.065 0.048
GST activity 1 14.344 0.000
MDA content 1 0.182 0.671
AChE activity 1 0.008 0.927
ConditionsDuration CAT activity 5 0.654 0.659
GST activity 5 8.505 0.000
MDA content 5 1.249 0.293
AChE activity 5 0.677 0.642
OrgansConditionsDuration CAT activity 5 1.695 0.149
GST activity 5 2.209 0.060
MDA content 5 0.254 0.937
AChE activity 5 0.399 0.848
Figure 3. Variation in GST activity in the gills and digestive gland of M. galloprovincialis
exposed to two concentrations of glyphosate without or with spirulina for 4days. Bars represent
the group means ± SD, n ¼5; a, b and c: differences at the 5% threshold.
JOURNAL OF ENVIRONMENTAL SCIENCE AND HEALTH, PART C 7
Discussion
Many pollutants can induce the formation of reactive oxygen species
(ROS), such as hydrogen peroxide (H
2
O
2
), superoxide anion O
2-
, and
hydroxyl radical (
-
OH).
22
Due to their high reactivity, these species may
Figure 4. Variation in GST activity in the gills and digestive gland of M. galloprovincialis
exposed to two concentrations of glyphosate without or with spirulina for 7days. Bars represent
the group means ± SD, n ¼5; a, b, c and d: differences at the 5% threshold.
Figure 5. Variation in the level of MDA in the gills and the digestive gland of M. galloprovincia-
lis exposed to two concentrations of glyphosate without or with spirulina for 4days. Bars repre-
sent the group means ± SD, n ¼5; a, b, c and d: differences at the 5% threshold.
Figure 6. Variation in the level of MDA in the gills and digestive gland of M. galloprovincialis
mussels exposed to two concentrations of glyphosate without or with spirulina for 7 days. Bars
represent the group means ± SD, n ¼5; a, b, c and d: differences at the 5% threshold.
8 O. WIDED ET AL.
damage lipids, proteins, carbohydrates and nucleic acids.
23
Several studies
have shown that glyphosate exposure in aquatic animals induced oxidative
stress, which if maintained for long periods can cause oxidative cell dam-
age.
24,25
In the face of oxidative stress, organisms utilize powerful defense
mechanisms, among which is the antioxidant system, an anti-free radical
weapon.
26
In this present study, we demonstrated that glyphosate affects
biochemical parameters such as CAT, GST, AChE, and MDA in M.
galloprovincialis.
Our results show that CAT activity was significantly increased in gills
and digestive glands after exposure to glyphosate during four days. The
increased activity of this enzyme indicates that glyphosate has a potential
ability to stimulate increased ROS. Similar results have been reported by
Nwonumara and Okogwu,
27
in C larias gariepinus juveniles; these investi-
gators explained the increased CAT activity as a result of upregulated levels
of H
2
O
2
or as a response to oxidative stress.
GST is an enzyme that detoxifies, via conjugation with glutathione, vari-
ous endogenous and exogenous toxic compounds.
28
Alterations of GST
Figure 7. Variation of AChE activity in the gills and digestive gland of M. galloprovincialis
exposed to two concentrations of glyphosate without or with spirulina for 4days. Bars represent
the group means ± SD, n ¼5; a, b and c: differences at the 5% threshold.
Figure 8. Variation in AChE activity in the gills and digestive gland of M. galloprovincialis mus-
sel exposed to two concentrations of glyphosate without or with spirulina for 7 days. Bars rep-
resent the group means ± SD, n ¼5; a, b, c and d: differences at the 5% threshold.
JOURNAL OF ENVIRONMENTAL SCIENCE AND HEALTH, PART C 9
activity have been reported in bivalves exposed to pesticides and polluted
environments,
29,30
and in fish and oligochaetes exposed to glyphosate and
its formulations.
31
In this study, significant increases in GST activity were
observed at two glyphosate concentrations tested. Enhanced GST activity
during this exposure period of four days indicates increased biotransform-
ation process of the xenobiotic and indicates activation of the defense
mechanisms. This result is in agreement with that of Modesto and
Martinez,
31
who observed increased GST activity in the liver of Prochilodus
lineatus exposed to Roundup herbicide. Similar results have been found in
P. lineatus after Roundup exposure (10 mg/L) by Cavalcante et al.,.
32
Ferreira et al.
33
reported enhanced GST activity in Rhamdia quelen after
Roundup exposure in field study. Our results are also in agreement with
those reported, at the level of the digestive gland, in oysters.
34,35
This
enzymatic activation of GST may be due to an early defense mechanism of
the organism by exposure to glyphosate. By extending the duration of
exposure to this xenobiotic, a significant decrease in the activity of GST, at
the level of gills and digestive gland, was implemented. This hypothesis was
put by S
eguin et al. (2017)
36
which explains the overwhelming of cellular
defenses after subchronic exposure to glyphosate.
MDA, an aldehyde, may be formed as a result of ROS-induced damage
at the cell membrane level.
37
The present study reveals that the two con-
centrations of glyphosate induced lipid peroxidation, translated by a release
of malondialdehyde MDA, during 4 and 7 days of contamination, at the
level of gills and digestive gland. The results obtained during the two time
points showed that the variation in the MDA rate is time dependent.
However, a dose-dependent increase was pronounced only after 4 days of
exposure to glyphosate. The results found are in agreement with results
found in the clam Corbicula fluminea exposed to herbicide (Roundup) and
those found in the mussel Limnoperna fortunei, exposed to different con-
centrations of glyphosate.
38
In line with our result, an increase in MDA
level has been observed in the sea cucumber Holothuria forskali following
glyphosate based herbicide exposure.
39
Acetyl cholinesterase, mainly found in basal lamina of synapses and
neuromuscular junctions, is responsible for the termination of cholinergic
impulses by the hydrolysis of acetylcholine (ACh) to choline and acetic
acid
4042
and it plays a vital role in many physiological functions, such as
predator evasion, prey location and orientation toward food. The activities
of acetylcholinesterase after exposure to glyphosate herbicide in all the
investigated tissues of the concerned test mussels gills and digestive gland
in the laboratory condition were significantly decreased (p<0.05) and a
dose-dependent response was evident at each time point. These observa-
tions are in agreement with the results from Hong et al
43
when Chinese
10 O. WIDED ET AL.
mitten crab, Eriocheir sinensis was exposed to glyphosate. This significant
decrease in AChE activity was also obtained as results in other work on the
mussel Mytilus galloprovincialis
44
and other aquatic species, exposed to glypho-
sate,
45
such as fish. In fact, the decrease in this activity can be explained either
by the deterioration of the cholinergic system under the effect of glyphosate,
or by the deterioration (oxidation) of AChE itself, under the effect of free radi-
cals released due to oxidative stress induced by the pollutant.
46
Salbego et al.,
45
proposed that the impairment of the enzyme activity could be due to the oxi-
dative stress situation generated by herbicide exposure. On the other hand,
Glusczak et al.,
47
attributed the inhibition of AChE activity to the effect of the
surfactant rather than to an effect of glyphosate itself.
Spirulina is a microalga with a rich composition, since it presents important
nutritional values including amino acids, minerals, essential fatty acids, vita-
mins and fat-soluble antioxidants.
48
The latter gives this alga detoxifying and
protective properties against oxidative stress. In the present study, the results
found showed that spirulina has no harmful effect, but on the contrary it has
a protective effect against the aggression posed by the contaminant. The
decrease in catalase and GST activity when administering spirulina to mussels
confirms the protective effect of spirulina against oxidative stress. This protect-
ive effect is likely to be due to the presence of a phycocyanin, a free radical
scavenger, in the soluble composition of this microalgae.
49
A potential explan-
ation for the decreased GST activity observed by Spirulina supplementation
alone may be that Spirulina has a role in reducing superoxide and hydrogen
peroxide radicals
50
which slows down the rate of oxygen radical production.
51
On the other hand, Spirulina contains rich sources of enzymatic and nonenzy-
matic antioxidants which protect cells against reactive oxygen species dam-
age.
15,52
Thus, in this study, the stimulation of GST and catalase activity when
the antioxidant capacities of the mussels were exhausted indicated a strength-
ening of the antioxidant system by Spirulina.
53
Our results also show a
decrease in the level of MDA suggesting the utility of Spirulina in the protec-
tion of cells against lipid peroxidation. In fact, our results are in agreement
with those found in fish
54,55
and the freshwater mussel Unio ravoisieri.
56
The
results, obtained by the present work, showed that the administration of
Spirulina to the species M. galloprovincialis induced a restoration of the activity
of AChE which was altered by glyphosate. They go in the same direction as
those found by Sayed et al. (2017).
57
These researchers have shown that the
alteration of AChE activity by lead in the fish Clarias gariepinus was corrected
following administration of Spirulina.
Conclusion
The treatment of M. galloprovincialis with glyphosate for two periods (4
and 7 days), leads to the induction of oxidative stress at the level of the two
JOURNAL OF ENVIRONMENTAL SCIENCE AND HEALTH, PART C 11
organs considered. The results showed the modulation of the antioxidant
defense in gills and digestive gland. Spirulina supplementation at a rate of
1 mg/L improves tolerance of test M. galloprovincialis toward glyphosate
toxicity manifested by noticeable reduction in oxidative. Spirulina could be
an effective supplement in mussels feed and a promising treatment against
glyphosate-induced oxidative stress in M. galloprovincialis Based on the
results of this laboratory condition study, Spirulina could be cultured in
polluted aquatic environments to develop a sustainable aquaculture tech-
nology in general and shellfish in particular.
Funding
The conducted study was unded through grants from the "Minist
ere de lenseignement
sup
erieur et de la recherche scientifique (Tunisia)."
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JOURNAL OF ENVIRONMENTAL SCIENCE AND HEALTH, PART C 15
... However, previous studies have determined that GA 3 is not exempt of toxicity. The hematotoxicity of GA 3 has been studied using animal models such as rats and mice (Tuluce and Çelik 2006;Muthu et al. 2011;Troudi et al. 2012a;Ali et al. 2021Ali et al. , 2022Ahmed and Nofal 2021;Galal et al. 2021;Soliman et al. 2021aSoliman et al. , b, 2022aBushra and Shenouda 2022), hens and quail hens (Elsebai et al. 2003b;Elkomy et al. 2008;Ismail 2009), and rabbits (El-Sebai 2004). Nevertheless, the impacts of GA 3 on the hematological parameters and erythron profile of fish have not been investigated . ...
... This could be ascribed to the antioxidant components of Spirulina, which scavenge free radicals to reduce oxidative DNA damage (Chu et al. 2010). Spirulina has been long known for its antioxidant activity (Piñero Estrada et al. 2001;Dartsch 2008) and has been shown to exert antioxidant activity on several animals model exposed to known oxidant chemicals, such as cadmium (Amin et al. 2006 (Wided et al. 2021), and γ-irradiation and thioacetamide (Salem and Ismail 2021). Spirulina has also been implicated in the prevention of oxidative damage and inflammation resulting from excessive physical activity (Brito et al. 2020). ...
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