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Advances in Environmental Biology, 6(5): 1823-1833, 2012
ISSN 1995-0756
This is a refereed journal and all articles are professionally screened and reviewed
ORIGINAL ARTICLE
Study of Atmospheric Pollution emitted rated A plant of Fertilizers (Algeria) by the use
of bioindicator plants: lichens
Khaldi Fadila, Berrebbah Houria, & Djebar Mohammed- Réda
Cellular Toxicology Laboratory, Biology Department, Annaba University, P.BOX :12, 23000, Algeria
Khaldi Fadila, Berrebbah Houria, & Djebar Mohammed- Réda; Study of Atmospheric Pollution
emitted rated A plant of Fertilizers (Algeria) by the use of bioindicator plants: lichens
ABSRACT
In this study, we applied the method of transplantation that involves exposing in a polluted environment of
branches covered in lichen thalli after collection in its natural environment of the control area (Séraidi).
Subsequently, we transferred at different sites chosen previously. The lichen species was chosen for this
transplant is: Ramalina farinacea. To better estimate the levels of air pollution in the Annaba region, it is
important to correctly choose 5 sites distributed near the main source of NOx pollution (industrial source:
Complex of fertilizer company in Algeria).We also noted variations of some parameters: rate of proline, FW /
DW, levels of soluble sugars, total protein content.The experimental study also shows disruption of chlorophyll
content (a, b and a + b). The use of antioxidant enzymes, namely glutathione-S-transferase (GST), glutathione
reductase (GR) as biomarkers of air pollution has been shown using the species Ramalina farinacea (lichens)
transplanted at 5 sites. Dosages of these biomarkers confirmed the disruption of lichens by the air pollutant
(NOx) emitted by the industrial complex.The photosynthetic and respiratory metabolism following fluctuations
at different sites.
Key words: Air pollution, NOx, lichens, Chlorophyll, Proline, FW / DW, total protein, GSH and GST,
respiratory and photosynthetic metabolism.
Introduction
The air pollution by emissions of gas, dust, odor
is a nuisance forms to which the opinion is, rightly,
the most sensitive. To protect air quality, it is
necessary to know the nature of pollutants namely
dosing and treatment. This action is fundamental
because it is that it relies on the development
strategies of reductions in the amount of pollutants
released into the atmosphere [8].
Research applied to air pollution using lichens as
bioindicators have multiplied. Initial estimates of air
pollution, by such plants were initially concerned
acid pollution [24]. Then came the first work on the
accumulation of radionuclides and heavy metals by
lichens [22,33].
The problem is whether lichens, already likely to
detect a fluoride pollution [51] or an acid cleanup can
attest to the reduction of NOx abatement. The
phenomenon of exsorption already demonstrated in
favor of the retransplantation of samples in their
original, unpolluted, suggests that lichens respond
rapidly to an air pollution control [18].
The objectif of complex Annaba is part of the
promotion of Algerian agriculture represents an
indispensable tool for the country's independence in
terms of food self-sufficiency.
This plant is located on the coast east of the city
of Annaba. Therefore, it contributes to the relatively
large levels of dust, NOx and NH3.Il is interesting to
use of indicator plants in order to estimate the impact
of these pollutants on the environment.
Study refers to bio estimate of overall pollution
after an incineration plant with lichens [38].
Bioaccumulation potential of lichens appeared to us a
sensible approach to assess the impact of plant
fertilizers on the environment [39].
I. Transplantation technique lichens:
1-History:
The first lichen transplants were performed there
a hundred years in the city of Munich (ARNOLD
1891 to 1901). Since both techniques have been used
extensively for transplants of epiphytic lichens.
The first technique was developed by Brodo
(1961). It involves grafting a hard bark supporting a
lichen on a phorophyte of the same species. In
absence of trees, Schönbeck (1969) proposes to set
hard bark on boards.
Corresponding Author
Khaldi Fadila, Cellular Toxicology Laboratory, Biology Department, Annaba University, P.BOX:
12, 23000, Algeria
E-mail: [email protected]
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Adv. Environ. Biol., 6(5): 1823-1833, 2012
The second technique involves exposing in
polluted thalli branches covered with epiphytes. The
one we selected in our work.
from donor sites (Séraidi : located at 850 m above
the sea (Annaba) the same day as the transplanted
lichens. Our choice was made on this area because it
is a zone considered as not polluted.
2- Duration of transplantation:
3-Strategy and places of transplantation:
Transplants were performed twice, on January
22 and February 21 (2008 and 2009) on five sites.
The maximum duration of transplantation did not
exceed 1 month. The first sample is taken on the day
of the second transplant, and the latter the sample
was performed on 22Mars (2008 and 2009).
Transplanted thalli were always taken on the
same day for each site and samples were harvested
The sampling strategy implementation for
collecting lichens and the establishment of
transplants is based on the distance of the industrial
complex and the prevailing wind direction [25]
(compass provided by the station of Annaba located
approximately 5 km from the plant). (Figure 01).
Fig. 1: The Wind Rose (according to the meteorological Airport, Annaba).
Five transplant sites were selected: 400m, 800m,
1200m, 1600m and 2000m from the industrial
complex (Figure 02).
4-Harvest of lichen species in situ:
A census carried out on lichen Greater Séraidi
allowed to choose the lichen species Ramalina
farinacea. It is indeed well-developed and abundant
and fruticose thallus is easily taking.Several thalli of
Ramalina farinacea were harvested from the bark of
trees of several stations under standardized
conditions (height of 1.50 to 2 m in samples of soil)
(Sémadi and Deruelle, 1993).
Sampling was conducted in January and
February 2008 and 2009 in the town according to the
sampling strategy defined above.
3.Determination of total protein:
The proteins are assayed by the Bradford
method (1976) using BSA as standard.
4.Determination of total sugars:
Soluble sugars were determined by the method
of Schields and Burnett (1960) using anthrone in
sulfuric acid.
5.Determination of report FW / DW:
II.Methodes:
Having collected fresh samples of thalli of
Ramalina farinacea we weighed the samples before
and after oven drying samples at 105 ° C for 48
hours. This report is established to obtain the value
of the pollution index.
1.Determination of chlorophyll:
6.Determination biomarkers:
The method used for extraction of chlorophyll is
the traditional method established by Holden,( 1975)
which is a maceration of the plant in acetone.
6.1-Determination of Glutathione (GSH):
2.Determination of proline:
For the determination of proline, the technique
used is that of Monneveux and Nemmar, (1986).
The glutathione was assayed by the method of
Weckberker & Cory (1988), based on measuring the
absorbance of the 2-nitro-5 mercapturic resulting
from the reduction of the acid 5-5 'thiol-bis-2nitrobenzoic acid (DTNB) by the thiol groups (-SH)
glutathione.
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Adv. Environ. Biol., 6(5): 1823-1833, 2012
Fig. 2: Representation of the sampling area and the area of transplantation in relation to complex fertilizer (map
of the drainage of the plain of Annaba, 2008).
6.2-Determination
transferase (GST):
of
activity
Glutathione
S-
The glutathione S-transferase activity is
performed by the method of Habig et al., [26]. It is
based on the conjugation reaction between GST and
a substrate, CDNB (1-chloro 2, 4 dinitrobenzene) in
the presence of a cofactor: glutathione (GSH). This
activity is measured at a wavelength of 340nm by a
spectrophotometer visible / UV (Jenway 63000).
7.Study of
metabolism:
respiratory
and
photosynthetic
The apparatus used is an oxygen electrode,
HANSATECH type, which allows the measurement
of the production or consumption of oxygen.
The intensity of photosynthesis of lichens
transplanted is measured by the oxygen electrode as
for the respiration rate when the sample is hidden by
a black box to speed up the metabolic process [15].
8.Statistical study:
The statistical analysis is performed by the
Student “t” test that compares the averages of two
populations using data from two independent
samples, conducted using a data analysis software:
Minitab (Version 16.0) [12].
Results:
The figure (03), highlights the changes in proline
content, which increase with the distance from the
complex, this corresponds to concentrations of
pollutants (the most polluted area). The highest
values are recorded at Site 5, although other sites
have higher values than those of the control.
In 2008, no significant difference between the
proline content in control samples and samples
transplanted at the (site 1) (p> 0.05), while very
highly significant differences were found for samples
transplanted at other sites (2,3,4 and 5) (P <0.001).
For 2009, this analysis reveals significant
differences between the rate of proline in the control
samples and samples transplanted at the (site 1) (p
<0.05), and very highly significant differences for
samples transplanted at other sites (2,3,4 and 5) (P
<0.001).
The figure (04), highlights the changes in total
protein content in Ramalina farinacea, according to
the transplant sites (2008 and 2009). We find that in
transplanted samples at selected sites to farthest from
the pollution source, the total protein tends to
increase site-dependent manner. In 2008, the highest
value is recorded at site 5 is: 28.39 µg / mg of FW
compared to a site 1 which is: 16.22 µg / mg of FW.
While,in 2009, the maximum value at the same site
(5) is: 35.69 µg / mg of FW.
Statistical analysis revealed no significant
difference between the levels of total protein in
control samples and samples transplanted at the (site
5) (2008), and between control samples and samples
transplanted at the (site 4) (2009) (p> 0.05), while
very highly significant differences were revealed
between control samples and samples transplanted at
other sites (p <0.001).
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Fig. 3: Variations in the rate of proline in Ramalina farinacea at different sites.
Fig. 4: Changes in levels of total protein in Ramalina farinacea at different sites.
Fig. 5: Changes in levels of total sugar in Ramalina farinacea at different sites.
The figure (05) highlights the changes in total
sugar content in Ramalina farinacea according to the
transplant sites (2008 and 2009). We find that in
transplanted samples at selected sites to the further
from the pollution source the rate of total sugar tends
to increase site-dependent manner. The highest value
was recorded at site 5 (2009), is: 193.99 µg / mg of
FW compared to the control site which is: 148.32 µg
/ mg of FW.
In 2008, statistical analysis showed significant
differences between the content of total sugars in
control samples and samples transplanted at the (site
1) (p <0.05), while highly significant differences
were revealed for samples transplanted at the (site 2)
(p <0.01). As for the other sites (3, 4 and 5), the
differences are very highly significant (p <0.001).
In 2009, this analysis reveals some very highly
significant between the control samples and samples
transplanted at 4 sites (2, 3, 4 and 5) compared to
control (p <0.001). However, insignificant
differences were found between controls and samples
(site 1) (p> 0.05).
The figure (06) shows the ratio FW / DW, at 5
sites is small compared to the control.In 2008,
statistical analysis revealed highly significant
differences transplanted samples at site 1 compared
to control (p <0.01). However, these differences are
very highly significant between controls and samples
sites (2,3,4 and 5) (P <0.001).While this analysis
(2009), reveals very high significant differences
between the rate FW / DW in controls and samples
transplanted at 5 sites (P <0.001).
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Fig. 6: Changes in the rate FW / DW in Ramalina farinacea at different sites.
Fig. 7: Changes in GSH levels in Ramalina farinacea at different sites.
The figure (07), shows variations in the GSH
levels at 5 selected sites where you can see a
decrease in the GSH samples transplanted at 5 sites
compared to control. During the two years (2008 and
2009), site 5 shows the lowest rate is: (0.099 µM /
mg of protein) compared to the control that is: (0.706
µM / mg of protein) (2008) and this rate is: 0.602 µM
/ mg of protein compared to control (2009).
During the two years (2008 and 2009), statistical
analysis revealed very highly significant differences
in the rate of GSH between the control samples and
samples transplanted at 5 sites (p <0.001).
Fig. 8: Changes in GST activity in Ramalina farinacea at different sites.
Figure (08), represents the variations of the
activity of GST at 5 selected sites (2008 and 2009).
Our results show that the GST activity of
transplanted samples at different sites increases
compared to control. There is also a marked decrease
in the activity at site 4 and 5 compared to control
((0.292 and 0.213) x10-4μM/min/mg of protein
(2008); (0.216 and 0.14) x10-4μM / min / mg of
protein (2009)).
In 2008, statistical analysis reveals some very
highly significant between control and transplanted
samples at 5 sites (p <0.001).While in 2009, this
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statistical analysis reveals differences very highly
significant between control and transplanted samples
at sites 2,4 and 5 (p <0.001) and significant
differences are recorded at site 1 (p < 0.05) and
highly significant differences for samples of site 3 (p
<0.01) compared to control.
Table 1: Changes in chlorophyll (a, b, a + b) in Ramalina farinacea at 5 sites (Year 2008).
Sites
Chl. a (mg g-1)
Chl. b (mg g-1 )
Chl. a+b (mg g-1 )
Control
1,77±1,2
3,40±0,20
5,17±0,31
1
4,75±0,23
4,85±0,93(*)
9,60±0,46
2
4,20±0,34
6,31±0,44 (**)
10,56±1,18
3
2,24±0,10
9,6±0,12
12,90±0,03
4
4,3±1,11(**)
7,2±1,90(*)
12,1±0,3
5
4,40±0,2
6,15±0,37(**)
10,60±0,96
ANOVA
P≤0,001
P≤0,001
P≤0,001
The chlorophyll a + b increased at all sites compared to the control that have the lowest content (5.17 (2008) and 7.27 mg / g FW
(2009)).The content of Chl a + b is maximum : 12.90± 0,03 (2008) and 16.90 ± 0.02 mg / g of FW (2009) at site 3.
Statistical analysis showed very highly
significant differences between control samples and
those transplanted at different sites, and those for Chl
a + b and also for Chl a sites 1,2,3 and 5 and Chl b
site 3 (P <0.001). However, highly significant
differences were recorded for Chl a site 4 and Chl b
sites 2 and 5 (p <0.01). Statistical analysis also
revealed significant differences of Chl b in site
samples 1 and 4 (p <0.05).
Table 2: Changes in chlorophyll (a, b, a + b) in Ramalina farinacea at 5 sites (Year 2009).
Chl. b (mg g-1)
Sites
Chl. a (mg g-1)
Control
3,62±0,07
3,68±0,06
1
4,90±0,13
4,79±0,09
2
6,18±0,24
5,43±2,44(NS)
3
6,8±0,15
10,16±0,14
4
5,46±0,06
10,12±1,10
5
5,14±0,3
9,07±0,57
ANOVA
P≤0,001
P≤0,001
Statistical analysis showed very highly
significant differences between control samples and
those transplanted at different sites and on (Chl a, b
and a + b) (P <0.001). However, Chl b site 2 stores
Chl. a+b (mg g-1)
7,27±0,01
9,66±0,04
11,56±2,18(**)
16,90±0,02
14,91±0,3
14,16±0,26
P≤0,001
differences are not significant compared to control
(p> 0.05). Chl a + b of the same site presents
significant
differences
(p
<0.05).
Fig. 9: Effects of air pollution on photosynthetic metabolism of lichens transplanted in 2008.
The figure (09) below shows a marked increase
in the amount of O2 produced in the middle, dice the
second minute of recording for samples transplanted
at 5 sites.The maximum amount of oxygen produced
is recorded at 10min for the sample site that reaches
3: 16.30nmole O2 /ml.
Transplantation samples at 5 sites, causing an
acceleration of the oxidation rate is: 14 nmol of O 2 /
min at site 3.
The maximum amount of oxygen produced was
recorded at 10 min for the sample site that reaches 3:
20 nmol O2 /ml.We also note that the oxygen
produced stored with the samples from both sites 4
and 5 eventually join after 10 minutes of recording,
in contrast to samples from other sites. We can note
that the control samples exhibit a respiration quite
normal with O2 consumption proportional to the time
of measurement, the oxidation rate is 8 nmol O 2 /
min. The latter is higher in samples from all sites is:
10 nmol of O 2 / min (site1), 12.5 nmol of O 2 / min
(site2), 12 nmol of O 2 / min (site 5) and 13 nmol O2 /
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min (site4). Site 3 samples exhibit the maximum
oxidation rate of 16 nmol O 2 / min.
Statistical analysis revealed very highly
significant differences between photosynthesis of
the control samples and those transplanted at five
selected sites (2008 and 2009) (p <0.001).
Fig. 10: Effects of air pollution on respiratory metabolism of lichens transplanted in 2008.
Fig. 11: Effects of air pollution on photosynthetic metabolism of lichens transplanted in 2009.
Fig. 12: Effects of air pollution on respiratory metabolism of lichens transplanted in 2009.
Statistical analysis revealed very highly
significant differences between respiration of the
control samples and those transplanted at five
selected sites (2008 and 2009) (p <0.001).
Discussion and Conclusion:
The Annaba region was particularly affected by
air pollution, it was important to address this problem
through the bioindication plants and not only by the
sensor measurements. The detection and estimation
of air pollution with lichens are possible insofar as
these plants meet the conditions you would expect of
biological indicators [56,46]. Besides the qualities:
-Remarkable sensitivity to pollution linked to an
exceptional power to accumulate rapidly from the
atmosphere;
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-Ease of use due to their continuous activity and
longevity;
-High-density of their distribution, abundance of
species;
-Lichens have the ability to respond rapidly to lower
pollution through the mechanism of sorption which
reflects quantitatively ex reducing pollution [18].
The results obtained showed that the observation
of parameters measured in plant material occurs
naturally or transplanted was entirely appropriate for
a study monitoring the impact of a fertilizer plant on
the environment.
To confirm the state of stress induced in our
samples, we also followed changes in the rate of
proline, known as a marker of stress in plants. Our
results showed, increased levels of proline in
transplanted samples, are consistent with those of [7]
which recorded an increase of proline during stress in
the NH4NO3 in mosses and lichens. This
accumulation has been demonstrated in many
varieties of wheat and several types of stress
(osmotic, water, heat) [6,30,31,44]. Lagadic et al.,
[37] argue that an increase in proline may occur if
plants are subjected to oxidative stress created by air
pollution. For most pollutants (SO2, NOx and O3 ......
etc.), the symptoms of their effects include changes
in concentration of certain compounds (amino acids)
[40,5,19].
The main element of an effective indicator of
stress in the plant is the increase of proline. In our
work, we demonstrated a significant increase of
proline in lichens transplanted. Proline may play a
role osmoprotecteur [14,45], protein stabilizer
[53,36], an inhibitor of metals [20] and inhibitor of
peroxidation [41]. This rate increase can be
explained according proline [44], by an effect of
stress in plants. The synthesis of proline may also
involve a reduction of acidification of the cytoplasm
that maintains the ratio (NADP / NADPH) to a value
compatible with that of metabolism [27]. According
to Monneveux and Nemmar, [42], accumulation of
proline is associated with plant resistance to stress,
which could be one of the factors that best explain
the strategy of plant adaptation.
To confirm this stress in a polluted environment,
we looked to changes in total protein levels in
transplanted samples of lichens. According to
[48,49], in the presence of xenobiotics, the plant
increases protein synthesis of phytochelatins in
particular whose role is the detoxification of
xenobiotics, particularly metals. Stalt et al., [55]
reported that nearly 80% of the xenobiotic is
detoxified by this type of protein.Which are
consistent with our results that show an increased
rate of total protein in lichen thalli of the species
(Ramalina farinacea). According to [60], the
increase of enzymes of detoxification.
The other indicator of a disruptive effect of
stress in plants is the increased levels of total sugars.
According Deraissac [16], the process of
concentration of soluble sugars and / or proline in
leaf tissue of plants under stress is recognized as a
feature adaptation. This stress is due to air pollution.
Our results show that as one moves away from the
industrial complex, the rate of sugar tends to
increase, which implies a subsequent disruption of
the photosynthetic process in the species Ramalina
farinacea at contaminated areas (plus the site is
polluted, the higher the rate of total sugar is high).
This confirms that the rate of total sugar varies with
the distance from the pollution source, the nature of
the plant species, its vegetative stage and
morphology [4].
The report FW / DW is a good indication of the
state of the air quality, the more air is polluted, the
greater the development of the plant is disturbed.
Thus the ratio FW / DW in polluted areas will be
lower than that recorded at the lower pollution zone
(Semadi, 1989).Our results on the relationship fresh
weight / dry weight at different study sites, we can
conclude that the sites representatives a report low
compared to the control, specifically at site 1.The
proportion of fresh weight in relation to dry weight
(FW /DW) decreases with distance from the
pollution source has been determined by several
authors Woodbury and Hudler, [59]. These decreases
may be due to tissue damage plant material in
transplanted samples of lichens, which leads to
wilting and drying of thalli or water loss [56,1].
Air pollution can cause damage to plants and
implies the decrease of fresh and dry weight [10,59].
Indeed, Chakhparonia [11] showed in Arabidopsis
thaliana subjected to air pollution decreased fresh
and dry weight.
The induction of detoxifying enzymes of plants
under stress conditions is often reported [43]. Plant
cells are able to protect their lives through the use of
enzyme mechanisms (GST) and no-enzymatic (GR)
[2]. Contrary to previous results, the site of
transplantation 3 (2008 and 2009) present a
maximum activity of GST biomarquer subsequently
decreases parallel at site 4 and 5. From these results,
we can see that the site 3 is the most polluted site.
Induction of the GST enzyme system can be
explained by the entry of Xenobiotics in plant cells
(lichens) and induction of detoxification system [37].
Our results agree with those obtained with Dazy et
al., [13], where they found maximal activities of
GST and a significant decrease of GSH in samples
exposed to heavy pollution.
The metabolism of chlorophyll is certainly the
most visible biochemical process. Its biosynthesis
leaves appear green color of plants, while its
degradation is manifested by loss of pigment [21].
According to our results, we observed a marked
variation of chlorophyll according to the different
selected sites. These variations may be associated
with changes in the life cycle of the plant [21,23].
The results of experiments conducted by Knudson et
al., [35]; Bechulal and Ambasht [3], Renaud et al.,
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[47]; Tretiach et al., [57], suggest that plants
subjected to air pollution have changes in the rate of
chlorophylls. This confirms our results.
From Deruelle and Lallement, [17], disruption of
photosynthesis appears to be due to a change of
chlorophyll resulting from a displacement of Mg
molecules of chlorophyll by a pollutant. Our results
are in perfect agreement with this work because they
have shown a reduction in photosynthetic activity
resulting in a maximum increase of chlorophyll
concentrations observed at site 3. The photosynthetic
metabolism following fluctuations at different sites.
At high air pollution levels and different distances of
the sites in relation to sources of pollution,
photosynthesis remains active and still higher than
the control. Our results are consistent with those
obtained by [32]. On respiration, we noticed that the
transplantation of lichen samples at different selected
sites stimulates the respiratory activity. This increase
in respiration of lichens is due to absorption of
various substances and pollutants contained in air.
The perturbation of the respiration and
photosynthesis of lichens transplanted can explain
the degradation of the plant material and the
disappearance of certain species from our ecosystem.
According to work Bensoltane et al., [7]; Khaldi,
[34], the penetration of xenobiotics within the lichen
is the cause for triggering the phenomena of
detoxification / biodegradation, this phenomenon
involves the cytochrome P450 oxygenases, where the
activity of oxygen resulted in respiratory drive
observed.
7.
8.
9.
10.
11.
12.
13.
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