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Colloids and Surfaces B: Biointerfaces 125 (2015) 284–290
Contents lists available at ScienceDirect
Colloids and Surfaces B: Biointerfaces
journal homepage: www.elsevier.com/locate/colsurfb
Toxic potential of iron oxide, CdS/Ag2 S composite, CdS and Ag2 S NPs
on a fresh water alga Mougeotia sp
E. Jagadeesh, Behlol Khan, Preethy Chandran, S. Sudheer Khan ∗
Centre for Nanotechnology and Advanced Biomaterials, School of Chemical and Biotechnology, SASTRA University, Thanjavur 613401, Tamil Nadu, India
a r t i c l e
i n f o
Article history:
Received 14 May 2014
Received in revised form 27 October 2014
Accepted 6 November 2014
Available online 13 November 2014
Keywords:
Iron oxide nanoparticles
Cadmium sulfide nanoparticles
Silver sulfide nanoparticles
Nanocomposite
Toxicity
Mougeotia sp.
a b s t r a c t
Nanoparticles (NPs) are being used in many industries ranging from medical, textile, automobile, consumer products, etc. This may increase the probability of their (NPs) release into the environment and
fresh water ecosystems. The present study focuses on testing the potential effect of iron oxide, nanocomposite of cadmium sulfide and silver sulfide, cadmium sulfide and silver sulfide nanoparticles (NPs) on a
fresh water alga Mougeotia sp. as the model organism. The alga was treated with different concentrations
of NPs (0.1–25 mg/L). The NPs exposure caused lipid peroxidation and ROS production, and suppressed the
antioxidant defense system such as catalase, glutathione reductase, and superoxide dismutase. Adsorption of NPs on algal surface and membrane damage were confirmed through microscopic evaluation and
increase in protein content in extracellular medium. The present investigation pointed out the ecological
implications of NPs. The study warrants the need for regulatory agencies to monitor and regulate the use
of NPs.
© 2014 Elsevier B.V. All rights reserved.
1. Introduction
Metal oxide NPs are being manufactured in recent years at
industrial level and are used in treatment of water, medicines and
engineering works [1,2]. Due to the increased use of NPs in recent
years it was predicted that these NPs can find their way to the
environment where their behavior can pose severe threat to the
various components of ecosystem [3,4]. Magnetite (Fe3 O4 ) NPs
are thermodynamically unstable in the presence of oxygen and
are mainly used as information carriers, drug delivery systems,
etc [5,6].
CdS and Ag2 S are some of the important transition metal sulfide semiconductor nanomaterials because of their direct as well
as relatively lesser band gap, chemical stability, effective high
absorption coefficient and even extremely good optical properties [7,8]. For CdS NPs the energy band gap increases with the
decrease of the size [9,10]. Ag2 S is being used in various nano sized
optical devices, and electronic applications including IR detectors,
manufacturing fuel cells and battery-based super ionic conductors, photoconductors, photovoltaic cells resistive switching and
∗ Corresponding author. Tel.: +91 9047286362.
E-mail addresses: sudheerkhan@scbt.sastra.edu, ssudheerkhan@gmail.com
(S.S. Khan).
http://dx.doi.org/10.1016/j.colsurfb.2014.11.008
0927-7765/© 2014 Elsevier B.V. All rights reserved.
solar selective coatings [11–13]. Due to their chemical nature and
size these NPs remain in the environment for a longer time. The
indiscriminate use of these NPs may lead to its release into the
environment. The present study evaluated the potential toxic effect
of these NPs once it is released into the environment. Here we
choose Mougeotia sp. as the model system to evaluate the toxicological effect of NPs to represent the toxic potential of these
NPs to the aquatic organisms, since it has been shown to be tolerant to high level of heavy metal concentration [14]. Mougeotia
sp. is fast growing fresh water green algae found generously in the
water bodies. This alga was found to be interesting due to its vigorous and luxuriant growth in its habitat throughout the year. The
present study used low concentrations of NPs, from 0.1 to 25 mg/L
in comparison with previously reported studies. Most of the previous studies were used at very high concentration of NPs to test
the toxic potential on algal cells and it varies from mg/l to g/L
[15–18].
The main objective of our report was to characterize the toxic
effects of NP in Mougeotia sp. To evaluate these effects, we investigated the growth of algae by evaluating the chlorophyll content
after being exposed to NP. Furthermore, we also investigated several biomarkers related to oxidative stress as well, such as reactive
oxygen species (ROS) formation, lipid peroxidation and enzymatic
antioxidant activities of catalase, glutathione reductase (GR) and
Superoxide dismutase (SOD).
E. Jagadeesh et al. / Colloids and Surfaces B: Biointerfaces 125 (2015) 284–290
Fig. 1. Scanning electron microscopic images of (a) iron oxide, (b) CdS/Ag2 S composite, (c) CdS and (d) Ag2 S NPs.
Fig. 2. Size distribution of (a) iron oxide, (b) CdS/Ag2 S composite, (c) CdS and (d) Ag2 S NPs.
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Fig. 3. X-ray powder diffraction analysis of (a) iron oxide, (b) CdS/Ag2 S composite, (c) CdS and (d) Ag2 S NPs.
2. Materials and methods
2.1. Chemicals
FeCl3 ·6H2 O, Trisodium citrate, polyvinyl pyrrolidone (PVP),
AgNO3 , CdCl2 and Na2 S were purchased from Merck, Germany.
FeCl2 and dichlorofluorescein diacetate (DCFH-DA) were purchased
from Sigma-Aldrich, USA. Glutathione, nitro-blue Tetrazolium
(NBT), 5,5 -dithiobis (2-nitrobenzoic acid) (DTNB), thiobarbituric
acid (TBA) were obtained from Himedia, Mumbai, India. The present
study used previously characterized particles for toxicological evaluation.
2.2. Collection and culture of algae
Fresh water algae that were collected from a natural pond and
identified as Mougeotia sp. were filtered to remove debris, and
cultured in Bold’s 3 N modified medium. Equal amount of samples were weighed (1 g) and transferred into the flasks containing
medium. The flasks were incubated on shaker at room temperature,
under fluorescent light at 8 h and 16 h day/night rhythm.
2.3. Synthesis of NPs
The nanoparticles were synthesized as described earlier
[19–21]. Briefly, 0.1 M of FeCl2 and FeCl3 were taken in a 1:2 ratio
in deionized water and heated up to 80 ◦ C for 1 h on magnetic stirrer. Ammonia (acting as a base to form iron oxide NPs) was added
drop wise until the solution turned dark black in color indicating the formation of iron oxide NPs. After 1 h of heating, PVP was
Fig. 4. Effect of NPs on algal growth. (a) Toxicity after 5th day and (b) toxicity after
10th day. Values are the mean of n = 3 (mean ± standard error).
E. Jagadeesh et al. / Colloids and Surfaces B: Biointerfaces 125 (2015) 284–290
287
Fig. 5. Microscopic image of Mougeotia sp. After interaction with NPs: (a) control image of Mougeotia sp. (without interacting with NPs), (b) iron oxide NPs, (d) cadmium
sulfide NPs, (f) silver sulfide NPs and (h) nanocomposite after interaction with algae. Adsorption of NPs on algal cells can be clearly seen in the figure. Membrane damage of
algal cells were observed after the interaction of (c) iron oxide NPs, (e) cadmium sulfide NPs, (g) silver sulfide NPs and (i) nanocomposite.
added. The solution was centrifuged at 12,000 × g for 30 min, pellet was lyophilized and the smooth powder obtained was taken
for characterization. CdS and Ag2 S NPs were prepared by adding
Na2 S to CdCl2 and AgNO3 solution separately. The nanocomposite
(CdS/Ag2 S) was prepared by adding Na2 S to the mixture of CdCl2
and AgNO3 solution (1:1 ratio). The pellet obtained was lyophilized
and characterized.
2.4. Characterization of nanoparticles
The synthesized particles were characterized by scanning electron microscopy (SEM), X-ray diffraction (XRD), particle size
analyzer and zeta sizer. The surface state, morphology and structure of NPs were recorded using a field emission scanning electron
microscopy (JEOL JSM-6701F, Japan) at a magnification level of 6K
with an acceleration voltage of 3–35 kV. The lyophilized NPs were
coated in XRD grid and the spectra was recorded using Bruker AXS
(Diffractometer D8, Germany) operated at voltage of 40 KV using
Cu K␣ radiation used to determine lattice parameter, crystallite
size and phase identification. The particle size was measured using
a particle size analyzer (Microtrac Blue Ware, Nikkiso, Japan). For
measuring the particle size, 10 mg of NPs were dispersed in 100 mL
of de-ionized water. The particle size was calculated based on the
volume% (3 mL was used for the analysis). The zeta potential measurement was done using a Malvern (UK) zeta analyzer.
2.5. Toxicity evaluation
Freshly grown algae (1 g) was suspended in Bold’s 3 N modified medium along with NPs and incubated for 10 days under
fluorescent light with a day/night rhythm of 8 h/16 h. Chlorophyll
pigment from the samples was extracted by adding 10 mL of 80%
acetone and leaving over night at 4 ◦ C followed by centrifugation at 10,000 × g for 10 min. Supernatant was collected and the
absorbance was measured at 652 nm using EQUIP-TRONICS double
beam spectrophotometer (EQ-824., India). Microscopic evaluation
was done to understand the adsorption of particles on cell surface and to evaluate the membrane damage by the particles (Zeiss
AX-10, ProgRes C5, Germany).
2.6. Lipid peroxidation assessment
Lipid peroxidation was assessed by measuring the amount of
thiobarbituric acid reactive species (TBARS). 0.5 g of algae was
suspended into flasks containing solutions of culture medium,
1 mM NaCl and NPs, and incubated for 24 h, then centrifuged at
10,000 × g for 5 min. The pellet was collected from each sample and
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2.8. Protein estimation
The supernatant was collected after the interaction of algal
species with NPs. The amount of protein left in the supernatant
was calculated by Lowery method. A control experiment was run
without NPs.
2.9. Enzyme assay
Reduced glutathione (GSH) content was obtained by treating the
algae culture with varying concentrations of different NPs which
was then centrifuged and lysates were prepared by ultrasonicating
the pellets using ultra sonic vibration (Sonics Vibra-Cell Ultrasonicator) suspended in 0.1 M phosphate buffer solution. GSH content
was measured through the oxidation of it by 5,5 -dithiobis(2nitrobenzoic acid) (DTNB) forming 5-thio(2-nitrobenzoic acid)
(TNB) [22], absorbance was measured at 405 nm using a double
beam Lambda 25 UV–visible spectrophotometer (Perkin Elmer,
USA). Catalase activity was calculated by measuring the decreasing
amount of H2 O2 [23]. 0.5 mL of cell lysates was taken and 0.1 M
H2 O2 in 0.1 M phosphate buffer was added to them. Absorbance
was measured at 240 nm for 5 min with 1 min time interval.
Superoxide dismutase (SOD) activity was done by adding 1.5 mM
nitro-blue Tetrazolium (NBT) along with 0.1 M 2-mercaptoethanol
and 10 mM MgSO4 to the lysate [22]. Absorbance was measured
at 350 nm for 5 min with 1 min time interval. Glutathione reductase (GR) activity was measured by adding phosphate buffer (0.1 M)
containing 1 mM EDTA, 400 ␮M DTNB and 300 ␮M NADPH to the
lysate [23], and checking the absorbance at 405 nm for 5 min with
1 min time interval.
3. Results and discussion
3.1. Characterization of NPs
Fig. 6. Effect of NPs on (a) Lipid peroxidation of algae assessed after the interaction
with NPs, (b) ROS generation in algal cells due to NPs effect and (c) Extracellular
protein content after interaction of algal cells with NPs. Values are the mean of n = 3
(mean ± standard error).
homogenized using 5% trichloroacetic acid (TCA). The homogenates
were centrifuged at 10,000 × g for 5 min. Equal volumes of supernatant and 0.5% of thiobarbituric acid (TBA) in 20% TCA were taken
and incubated in water bath at 96 ◦ C for 30 min. The solutions are
then centrifuged at 10,000 × g for 5 min and the absorbance of the
supernatant collected was measured at 532 nm using Tecan Multi
Mode Scanner in a 96 well plate.
2.7. ROS estimation
ROS determination was done by measuring formation of
dichlorofluorescein by the oxidation of dichlorofluorescein diacetate (DCFH-DA). Algae culture incubated with NPs was centrifuged
at 10,000 × g for 10 min, suspended in phosphate buffer saline (pH
7.8) containing 30 ␮g/mL DCFH-DA and incubated for 30 min in a
shaker. The fluorescence values were measured at an excitation
wavelength of 485 nm and emission wavelength of 520 nm.
The synthesized NPs were subjected to SEM for the morphological evaluation. Fig. 1 shows the morphology and surface structure
of iron oxide, composite of CdS/Ag2 S, CdS and Ag2 S NPs. Spherical to
oval shaped particles were observed in all the particles. Fig. 2 shows
the particle size distribution of the synthesized particles where the
mean diameter of iron oxide, composite of CdS/Ag2 S, CdS and Ag2 S
NPs were determined to be 60 ± 3, 50 ± 3, 35 ± 2 and 45 ± 3 nm
respectively. Zeta potential values are a pre requisite to study the
stability of the particles. The higher the zeta potential indicates
the particle with greater stability. The zeta potential of iron oxide,
composite of CdS/Ag2 S, CdS and Ag2 S NPs were determined to
be −33.26 ± 1.57, −29.78 ± 1.37, −31.93 ± 1.76 and −29.69 ± 1.26
respectively. The XRD pattern of synthesized Fe3 O4 NPs showed
their polycrystalline nature (Fig. 3a). The peak position at 2Â values
of 30.3, 34.4, 43.1, 53.6, 56.2 and 62.9 are indexed to (2 2 0), (3 1 1),
(4 0 0), (4 2 2), (5 1 1) and (4 4 0) respectively. The results obtained
agree with standard magnetite (Fe3 O4 ) XRD patterns and identified
that the Fe3 O4 NPs were in a cubic spinel structure. Similarly, the
XRD pattern of CdS/Ag2 S nanocomposite is shown in Fig. 3b. XRD
patterns at 2Â values were matching perfectly with (1 0 1), (1 0 2),
(1 1 0) and (1 1 2) crystalline planes of CdS and the diffraction peaks
can be indexed to the hexagonal mesoporous structure of CdS. The
2Â values of Ag2 S matching with (1 1 1), (−1 1 2), (−1 2 1), (1 2 1),
(1 0 3), (0 3 1), (2 0 0), (−1 2 3), (0 1 4) and (−2 2 3) crystalline planes
and these diffraction peaks can be indexed to monoclinic ␣-Ag2 S.
XRD patterns at 2Â values of 28.9, 37.3, 44.1, 47.9 and 51.7 matching perfectly with the (1 0 1), (1 0 2), (1 1 0), and (1 1 2) crystalline
planes of CdS (Fig. 3c). All of the diffraction peaks can be indexed
to the hexagonal CdS. No cubic phase or impurity peaks can be
detected from the XRD measurement. XRD pattern of Ag2 S NPs is
E. Jagadeesh et al. / Colloids and Surfaces B: Biointerfaces 125 (2015) 284–290
289
Fig. 7. Effect of NPs on different antioxidant enzyme activities (a) Catalase, (b) Superoxide dismutase, (c) Glutathione reductase and (d) Glutathione content in algal cells.
Values are the mean of n = 3 (mean ± standard error).
displayed in Fig. 3d. Here the main sharp peaks were assigned to
(1 1 1), (1 1 2), (1 2 1), (1 0 3), (0 3 1), (2 0 0), (2 1 3) and (1 3 4) originate from Ag2 S NPs. No impurity peaks can be observed in the XRD
measurement. Sharp facets that were observed in all the graphs
indicates the crystalline nature of the particles.
algal membrane. Adsorption of NPs on cell surface may cause the
damage of cell membrane. Fig. 5c, e, g and i shows the membrane
damage of Mougeotia sp. cells after NPs treatment.
3.2. Toxicity evaluation
The membrane damage of algal cell membrane was supported
by lipid peroxidation analysis. The lipid peroxidation of algae by
NPs was performed by measuring the formation of thiobarbituric
acid reactive species (TBARS). The progressive increase in the formation of TBARS was observed up on treatment with increase in
concentration of NPs (Fig. 6a). The lipid peroxidation analysis was
supported by ROS estimation. Excessive generation of ROS have
the ability to induce algal membrane damage, lead to cell lysis
and eventually cell death [26]. Fig. 6b shows the ROS generation
due to NPs. The cell membrane damage was further confirmed by
cellular protein estimation after the NPs-algal treatment. The damage of membrane could lead to the release of intracellular protein
content to the interaction medium, thereby increasing the extra
cellular protein content compared to control. The results show
that the progressive increase in the concentration of extracellular protein content was observed upon treatment with increase in
concentration of NPs (Fig. 6c). The results indicate the release of cellular protein content upon membrane damage. The amount of ROS
formed/generated is related to the range of biological responses
and oxidative stress [27]. According to Melegari et al. [15] the
concentration of CuO NPs induced for ROS generation and lipid peroxidation in Chlamydomonas reinhardtii is 1000 ␮g/mL. The present
study found ROS formation and lipid peroxidation in Mougeotia sp.
observed at the NPs exposure of 0.1 mg/L. It has been reported that
the induction of intracellular oxidative stress by suppressing the
cellular antioxidant defence system seems to be a key event of the
toxicity mechanisms of many nanomaterials [28]. Once the NPs
reached inside a cell, the NPs induced the intracellular oxidative
Toxicity of the NPs was evaluated by the chlorophyll extraction method in which the percentage of the chlorophyll present
in the acetone is measured using a visible spectrophotometer. The
amount of chlorophyll present in the supernatant is directly proportional to the number of live cells remained after the interaction.
On day five all the NPs showed toxicity (Fig. 4a) except iron oxide
NPs which enhanced the growth in lower concentrations (0.1 and
1 mg/L), but it induced the toxicity in higher concentration of iron
oxide NPs (in 5, 10 and 25 mg/L NPs). The CdS/Ag2 S nanocomposite
showed relatively higher toxicity when compared to other NPs. On
day 10 all the NPs including iron oxide NPs showed increase in the
percentage of toxicity (Fig. 4b). Nanocomposite shows the highest
toxicity compared to other NPs. Jing et al. [24] and Lee and An [25]
studied the potential toxic effect of oxide NPs on Chlorella sp. and
Pseudokirchneriella subcapitata respectively. They found that the
metal oxide NPs were capable to induce the toxicity. More over the
toxicity was induced by the dissolved metal ions. The present study
used iron oxide NPs, CdS NPs, Ag2 S NPs and CdS/Ag2 S nanocomposite for the toxicological evaluation in green algae due to the
lack of adequate information about the potent toxic effect of these
NPs once it is released into the environment. The results show that
these NPs possess toxicity and the toxicity may also be induced due
to the dissolution of metal ions [24,25]. Microscopic evaluation of
the samples was done in order to support the toxicity studies. The
control of the algae (Fig. 5a) shows clear filament of the Mougeotia
sp. whereas Fig. 5b, d, f and h shows adsorption of NPs on to the
3.3. Lipid peroxidation, ROS formation and oxidative stress
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stress by disturbing the balance between oxidant and anti-oxidant
processes. The oxidative stress on algal cells by NPs was evaluated
by measuring the activity of antioxidant enzyme such as catalase,
SOD and glutathione reductase. Fig. 7 shows the activity of antioxidant defence enzyme against NPs exposure. A significant decrease
in the level of antioxidant enzymes activity and Glutathione content was observed. The suppression of antioxidant enzymes may
be due to the excess production of ROS. The NPs may induce the
cell’s apoptosis through a ROS-mediated mechanism [29]. In addition, excessive oxidative stress may also modify the cellular protein,
lipid and nucleic acid components, eventually leading to the death
of the cells [30].
4. Conclusions
The present study highlighted the impact of iron oxide, composite of CdS and Ag2 S, CdS and Ag2 S NPs once it is released into
the environment. A fresh water algae Mougeotia sp. was used as
a model organism to test the potential toxic effect. Compared to
the other NPs in this study, the iron oxide NPs showed the least
toxic effect. Lipid peroxidation and ROS generation were increased
upon NPs treatment. NPs exposures suppressed the antioxidant
defence system, thereby increasing the oxidative stress, leading to
the death of the cells. The literature shows the divergent results
of the nanoparticles toxicity which further suggest the need for
conducting nanotoxicity with a systematic approach.
Acknowledgments
The authors sincerely thank Science and Engineering Research
Board (SB/FT/LS-281/2012), Department of Science and Technology, Government of India and SASTRA University (TR Rajagopalan
grant) for providing support to carry out the research work. The
authors also thank Dr. Aswathy Ravindran, Assistant Professor, SASTRA University for proof reading our manuscript.
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