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Ecotoxicity and toxicity of nanomaterials with potential for wastewater treatment applications.

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Chapter 13
DOI: 10.4018/978-1-5225-0585-3.ch013
Nanotechnology holds the promise of develop new processes for wastewater treatment. However, it is
important to understand what the possible impacts on the environment of NMs. This study joins all the
information available about the toxicity and ecotoxicity of NMs to human cell lines and to terrestrial and
aquatic biota. Terrestrial species seems more protected, since effects are being recorded for concentra-
tions higher than those that could be expected in the environment. The soil matrix is apparently trapping
and filtering NMs. Further studies should focus more on indirect effects in biological communities rather
than only on effects at the individual level. Aquatic biota, mainly from freshwater ecosystems, seemed
to be at higher risk, since dose effect concentrations recorded were remarkable lower, at least for some
NMs. The toxic effects recorded on different culture lines, also give rise to serious concerns regarding
the potential effects on human health. However, few data exists about environmental concentrations to
support the calculation of risks to ecosystems and humans.
Ecotoxicity and Toxicity
of Nanomaterials with
Potential for Wastewater
Treatment Applications
Verónica Inês Jesus Oliveira Nogueira
University of Porto, Portugal
Ana Gavina
University of Porto, Portugal
Sirine Bouguerra
Engineering School of Sfax, Tunisia
Tatiana Andreani
University of Porto, Portugal & CITAB-
University of Trás-os-Montes and Alto Douro,
Isabel Lopes
University of Aveiro, Portugal
Teresa Rocha-Santos
University of Aveiro, Portugal
Ruth Pereira
University of Porto, Portugal
Ecotoxicity and Toxicity of Nanomaterials with Potential for Wastewater Treatment Applications
Surface and ground water resources are continuously facing profound changes and quality deteriora-
tion, caused by anthropogenic activities, such as, mining operations, manufacturing and agro-industries.
With the industrial development, the generation and accumulation of waste products has tremendously
increased and one of the major challenges is the proper management and safe disposal of the vast amount
and array of such solid and liquid wastes. Industrial wastewaters are one of the major sources of direct
and often continue input of pollutants into aquatic ecosystems (Kanu & Achi, 2011). Due to the lack
of effluent treatment facilities, proper treatment methodologies and disposal systems, huge amounts
of industrial wastewater, containing high loads of organic and inorganic chemicals with high toxicity
and recalcitrant properties, are being discharged into aquatic environments. Depending on the type of
industry, the wastewater produced can contain different pollutants such as dyes, phenolic compounds,
surfactants, pharmaceuticals, pesticides, organic solvents, chlorinated by-products, metals and microor-
ganisms, which can cause the increase in biological oxygen demand (BOD), chemical oxygen demand
(COD) and total dissolved solids (TDS) in the receiving water systems promoting their deterioration.
In the last few years, nanomaterials (NMs) with their unique proprieties have been extensively studied
for water and wastewater treatment. Nanotechnology holds the promise of enhancing the performance of
existing treatment technologies but also offers the potential for developing new treatment solutions (Qu,
Alvarez, & Li, 2013). In 2011, the European Commission (EC) has adopted the following definition for
NMs: “a natural, incidental or manufactured material containing particles, in an unbound state or as an
aggregate or as an agglomerate and where, for 50% or more of the particles in the number size distribu-
tion, one or more external dimensions is in the size range 1–100 nm”(EC, 2011). Within this definition,
several NMs have received considerable attention for wastewater treatment, namely metal (silver (Ag),
gold (Au)) and metal or metalloid oxides of titanium (TiO2), silica (SiO2), iron (Fe2O3), cerium (CeO2)
(García et al., 2011; Jarvie et al., 2009; Kaegi et al., 2011). Due to their reduced size, NMs display unique
physical, chemical and biological proprieties compared to their bulk counterparts (Stone et al., 2010;
Zhang & Fang, 2010). At the nanoscale, the specific surface area and the surface/volume ratio increases,
leading to an increase in the number of surface atoms and therefore contributing for enhanced optical,
electrical and magnetic properties (Mohmood et al., 2013). The properties that make NMs suitable for
wastewater treatment, in particular, include high surface areas with more active sites available for adsorp-
tion; high reactivity and catalytic potential for use in photocatalysis process, antimicrobial activity, high
mobility in solution, as well as, super magnetism proprieties for particle separation (Hariharan, 2006;
Qu, Brame, Li, & Alvarez, 2013; Sánchez et al., 2011). Therefore, these unique characteristics can be
useful for efficient removal of metals or to degrade persistent organic compounds.
Although there are great advances with the use of nanotechnology for wastewater treatment, health
effects and environmental impacts associated to NMs are attracting considerable concern in the scientific
field and regulatory agencies. The unique proprieties of NMs, which make them so appealing, can also
be responsible for ecotoxicological effects. Hund-Rink & Simon (2006) for example, were one of the
first authors reporting the effects caused by the potential formation of reactive oxygen species (ROS)
during UV-irradiation of TiO2 NMs used as photocatalysts on Daphnia magna and Desmodesmus sub-
spicatus (Hund-Rinke & Simon, 2006). Also, it was recognized that the nanosize of these materials can
favour the cross through cell membranes and their interaction with cellular components (Colvin, 2003).
In the last two decades, some reviews were published joining data about the toxicity of NMs to several
organisms (Baun, Hartmann, Grieger, & Kusk, 2008; Menard, Drobne, & Jemec, 2011; Navarro et al.,
Ecotoxicity and Toxicity of Nanomaterials with Potential for Wastewater Treatment Applications
2008; Peralta-Videa et al., 2011). However, there still exists a considerable gap between the available
ecotoxicological data and the large amount of NMs that are being produced worldwide. Further, it is
important to take into account that few is known about the fate of NMs in the environment, and their
toxic effects will not only depend on morphologic proprieties, composition, size or synthesis method,
but also on the physicochemical characteristics of the receptor medium (Xiaoke Hu, Cook, Wang, &
Hwang, 2009; Lowry, Gregory, Apte, & Lead, 2012). Therefore, it is imperative to access the eco/cy-
totoxicity of NMs before their use for water and wastewater treatments purposes, as well as to perceive
their stability and fate in the environment.
In this context, the aim of the present chapter is to highlight the potential health and environmental
impacts of NMs with potential for wastewater treatment, in order to join information that will contribute
for safe uses in the future.
The ability of NMs to trap metals is well known. Recillas et al. (2011) explored the ability of CeO2, Fe3O4
and TiO2 NMs for the removal of Pb(II) through adsorption, reporting adsorption capacities of 189 mg
Pb g-1, 83 mg Pb g-1 and 159 mg Pb g-1, respectively (Recillas et al., 2011). Pena et al. (2005) reported
another example, in which nanocrystalline TiO2 were used both as adsorbent to remove arsenate [As(V)]
and arsenite [As(III)] as well as to complete convert As(III) to As(V), through photocatalytic oxida-
tion (Pena, Korfiatis, Patel, Lippincott, & Meng, 2005). In a recent review, Hua et al. (2012) reported
several studies demonstrating the efficiency of nanosized metal oxides for metal’s removal, as well as
other strategies involving the functionalization of NMs, such as surface modification with amino groups,
supporting with zeolites or coating with poly(3,4-ethylenedioxythiophene) to enhance the efficiency
of metal removal (Hua et al., 2012). Furthermore, research on the removal of organic compounds has
also being performed. Iron oxide NMs found application on the efficient removal of organic pollutants
(Iram, Guo, Guan, Ishfaq, & Liu, 2010; Parham, Zargar, & Rezazadeh, 2012; Hui Wang & Huang, 2011).
Special attention has being focused on the use of NMs for photocatalysis to degrade a variety of organic
compounds such as dyes (M. Faisal, Abu Tariq, & Muneer, 2007; Giwa, Nkeonye, Bello, & Kolawole,
2012; Shu, Chang, & Chang, 2009), phenols (Chiou, Wu, & Juang, 2008; Morales-Flores, Pal, & Sánchez
Mora, 2011), pesticides (Mahmoodi, Arami, Limaee, & Gharanjig, 2007), drugs (El-Kemary, El-Shamy,
& El-Mehasseb, 2010), as well chlorinated aromatic compounds (Lu et al., 2011; Selli, Bianchi, Pirola,
Cappelletti, & Ragaini, 2008). The major drawbacks in available studies are typically the use of synthetic
water that obviously does not represent real wastewaters. Further, several of these studies focused on
individual compounds forgetting the interaction in the complex mixtures where they are included like
industrial wastewaters.
Ecotoxicity Assessment of NMs for Aquatic Compartments
The increasingly use of NMs for wastewater and water treatment purposes as well as for environmental
remediation will lead to the release of substantial amounts of these materials in the aquatic environ-
ment. Although the environmental concentrations of NMs are still largely unknown there are evidences
of the presence of NMs in wastewater streams and waste leachates which in turn will be discharged into
rivers and lakes endangering aquatic organisms (Brar, Verma, Tyagi, & Surampalli, 2010; Hennebert,
Ecotoxicity and Toxicity of Nanomaterials with Potential for Wastewater Treatment Applications
Table 1. Toxicity of metal nanomaterials in different aquatic organisms
NMs Size (nm) Species Endpoint Effect Reference
TiO221 Daphnia magna
Japanese medaka
Acute phototoxicity
under simulated
solar radiation (SSR)
48 h LC50 = 29.8 mg L-1
96 h LC50 = 2.2 mg L-1
(Hongbo Ma,
Brennan, &
Diamond, 2012b)
72 h growth
EC50 = 241 mg L-1
EC50 = 71.1 mg L-1
EC50 = 145 mg L-1
(Hartmann et al.,
15–30 Thalassiosira
Skeletonema costatum
Dunaliella tertiolecta
Isochrysis galbana
96 h growth
inhibition under UV
NOEC = 1 mg L-1
NOEC = 1 mg L-1
NOEC < 1 mg L-1
(Miller, Bennett,
Keller, Pease, &
Lenihan, 2012)
5-10 Lemna minor 7 days growth
Inhibited plant growth at high
concentrations (> 200 mg L-1)
(G. Song et al.,
---- Danio renio Reproduction 29.5% reduction in the cumulative
number of zebrafish eggs after 13
(J. Wang, et al.,
NiO 20 Chlorella vulgaris 72 h growth
EC50 = 32.28 mg L-1 (Gong et al., 2011)
Vibrio fischeri
Lemna minor
Daphnia magna
Brachionus plicatilis
Artemia salina
72 h growth
7 days growth
Immobilization and
EC50 (10-20) = 15.2 mg L-1
EC50 (100) = 8.25 mg L-1
EC50 (100) = 4.39 mg L-1
NOEC (10-20) = 6.55 mg L-1
LC50 (100) = 9.74 mg L-1
LC50 (10-20) = 9.76 mg L-1
NOEC (100) = 0.04 mg L-1
NOEC (10-20) = 0.11 mg L-1
(Nogueira et al.,
CuO ≈ 30 Vibrio fischeri
Daphnia magna
Growth inhibition
48 h Mortality
24 h Mortality
EC50 = 79 mg L-1
LC50 = 3.2 mg L-1
LC50= 2.1 mg L-1
Ivask, Blinova,
Dubourguier, &
Kahru, 2008)
≈ 30 Raphidocelis
72 h growth
EC50 = 0.71 mg L-1 (Aruoja, et al., 2009)
Danio rerio Hatching and
Affects hatching and increase
malformations at concentrations ≥
1 mg L-1
(Vicario-Parés et al.,
ZnO 50– 70 Vibrio fischeri
Daphnia magna
Growth inhibition
48 h Mortality
24 h Mortality
EC50 = 1.9 mg L-1
LC50 = 3.2 mg L-1
LC50= 0.18 mg L-1
(Heinlaan, et al.,
100 Marine algae
Dunaliella tertiolecta
96h growth
EC50 = 2.42 mg L− 1 (Manzo, Miglietta,
Rametta, Buono, &
Di Francia, 2013)
40–100 Xenopus laevis Malformations EC50 = 10.3 mg L-1 (Nations et al., 2011)
Danio rerio Hatching and
Affects hatching at ≥ 5 mg L-1 (Vicario-Parés, et al.,
continued on following page
Ecotoxicity and Toxicity of Nanomaterials with Potential for Wastewater Treatment Applications
Avellan, Yan, & Aguerre-Chariol, 2013; Westerhoff, Song, Hristovski, & Kiser, 2011). In particular this
applies to NMs that are already being massively produced, such as metal-based and metal oxides, and
applied in water/wastewater treatment (Baker, Tyler, & Galloway, 2014). Thus, since water resources are
particularly exposed to the contamination with NMs it is imperative to address their potential toxicity to
aquatic organisms, before the damage is unavoidable. In Table 1, we summarize some toxicity studies
of NMs applied in wastewater treatment to several aquatic species.
Nano-TiO2 is probably one of the most extensively studied NMs, whether if it is for water and
wastewater treatment applications or for evaluating its ecotoxicological effects on aquatic organism.
TiO2 was efficiently applied to remove different metals but also several organic compounds (Khattab et
al., 2012; Mahdavi, Jalali, & Afkhami, 2012; Mu et al., 2010; Recillas, et al., 2011). However, several
studies also described the toxicity of nano-TiO2. Arouja et al. (2009) reported an effective concentration
(EC50) for Pseudokirchneriella subcapitata of 5.83 mg L-1, six times lower than the bulk-TiO2 (Aruoja,
Dubourguier, Kasemets, & Kahru, 2009). In another study, Zhu et al. (2010) found that the toxicity of
nano-TiO2 to Daphnia magna increased when the exposure time of the acute test was extended from
48 h to 72 h (EC50 > 100 mg L-1 and EC50=1.62 mg L−1, respectively) (Xiaoshan Zhu, Chang, & Chen,
2010). These authors also reported sub-lethal effects on reproduction at 0.1 mg L-1 and mortality at 2 mg
L-1 after 21 days of exposure (Xiaoshan Zhu, et al., 2010). Wang et al. (2011) also demonstrated that a
chronic exposure (13 week) to 0.1 mg L-1 nano-TiO2 can negatively affect the reproduction of zebrafish
(Danio rerio) (J. Wang et al., 2011).
NMs Size (nm) Species Endpoint Effect Reference
Fe2O350-150 Chironomus tentans
Survival and growth
(10 days)
NOEC = 5 mg kg-1 (Oberholster et al.,
30 Danio rerio Embryo/larva
Embryo hatching
LC50 = 53.35 mg L-1
EC50 = 36.06 mg L-1
(X. Zhu, Tian, &
Cai, 2012)
Fe3O46Vibrio fischeri
Daphnia magna
EC50 = 0.24 mg L-1
LC50 = 0.00023 mg L-1
(García, et al., 2011)
20–40 Ceriodaphnia dubia Immobilization
C. dubia significantly accumulated
nano-Fe2O3 in the gut, with the
maximum accumulation achieved
after 6 h of exposure.
(J. Hu, Wang, Wang,
& Wang, 2012)
Ag 50 Chlorella vulgaris
Dunaliella tertiolecta
Cellular viability Decrease in chlorophyll content,
viable algal cells, increased ROS
formation and lipids peroxidation
Bras, Perreault, &
Popovic, 2012)
50 Lemna paucicostata Growth inhibition EC50 = 13.8 mg L-1 (E. Kim et al., 2011)
Daphnia magna Immobilization EC50 = 0.004 mg L-1
EC50= 0.002 mg L-1
EC50 = 0.187 mg L-1
(Asghari et al., 2012)
<100 Chironomus riparius Gene expression Induction of genes related to
oxidative stress and detoxificatio
(Nair, Park, & Choi,
TEM: Transmission electron microscope
Table 1. Continued
Ecotoxicity and Toxicity of Nanomaterials with Potential for Wastewater Treatment Applications
There are several studies focusing the toxicity of other metal-based NMs to aquatic biota, besides
nano-TiO2, that are also used in wastewater treatment (Bour et al., 2015; García et al., 2012; Heinlaan,
et al., 2008; S.-W. Lee, Kim, & Choi, 2009; Nations, et al., 2011; Nogueira, et al., 2015; H. Zhu, Han,
Xiao, & Jin, 2008). For example, Nogueira et al. (2015) tested the toxicity of NiO (with two different
particle sizes), TiO2 and Fe2O3 NMs in several aquatic organisms (Nogueira, et al., 2015). Nano-sized
iron oxides (including nano-Fe2O3) are promising for industrial wastewater treatment due to their strong
adsorption ability and photocatalytic activity (Xu et al., 2012). The same occurs for nickel oxide NMs
that have been efficiently used in the photocatalytic degradation of phenol, adsorption of dyes and re-
moval of metals from wastewaters (Hayat, Gondal, Khaled, & Ahmed, 2011; Hristovski, Baumgardner,
& Westerhoff, 2007). Nogueira et al. (2015) found that apparently Fe2O3 NMs seemed to be the one
with less risk for the aquatic environment when applied to wastewater treatment. On the contrary, the
freshwater species (Raphidocelis subcapitata, Lemna minor and D. magna) were acutely and chronically
affected by NiO NMs (Nogueira, et al., 2015). In opposition, to freshwater species, these authors did
not record any toxicity, for the range of concentration tested, in the assays with marine species (Vibrio
fischeri, Artemia salina and Brachionus plicatilis) (Nogueira, et al., 2015).
In another study, the acute effects of Fe2O3, TiO2, ZnO and CuO NMs on Xenopus laevis embryos
was evaluated (Nations, et al., 2011). The exposure to these metal oxides caused no mortality, however,
CuO and ZnO NMs induced the development of abnormalities at very low concentrations. Zinc oxide
NMs is a semiconductor, very similar to nano-TiO2, however, ZnO presents a greatest advantage since
it adsorbs a large fraction of the solar spectrum (Sakthivel et al., 2003). Studies already proved the ef-
ficiency of ZnO as photocatalyst in the degradation of some organic compounds (Jang, Simer, & Ohm,
2006; Q. I. Rahman, Ahmad, Misra, & Lohani, 2013; Huihu Wang et al., 2007). However, when in
aquatic environment, ZnO NMs have the tendency to dissolve and this soluble form of ionic zinc (Zn2+)
has been recognized as the main factor of toxicity to several aquatic organism (Hongbo Ma, Williams, &
Diamond, 2013). Arouja et al. (2009) showed that the toxicity of nano-ZnO to the algae P. subcapitata
was attributed to soluble Zn2+ ions (Aruoja, et al., 2009). Besides, the toxicity has been attributed to the
dissolution of ZnO, the generation of ROS is also the mode of action for this NM, specially associated
with its photocatalytic activity (Hongbo Ma et al., 2014). Metal-oxide NMs have been the subject of
numerous toxicological and ecotoxicological tests, however only few studies address the photoreactiv-
ity of some of these NMs, which is the property that makes them particularly attractive for wastewater
treatment applications. Miller et al. (2012) reported that even low levels of UV lamps can induce pho-
totoxicity of nano-TiO2 to marine phytoplankton (Thalassiosira pseudonanan, Skeletonema marinoi,
Isochrysis galbabana, and Dunaliella tertiolecta), however, when the UV light was blocked, no toxic
effects were recorded (Miller, et al., 2012). In a more realistic study, conducted under simulated solar
radiation, (Hongbo Ma, et al., 2012b) assessed the acute toxicity of nano-TiO2 to both aquatic species
D. magna and Oryzias latipes. These authors reported a 48 h lethal concentration (LC50) of 29.8 mg L-1
for D. magna and a 96 h LC50 of 2.2 mg L-1 for Oryzias latipes. The phototoxicity of nano-TiO2, under
simulated sunlight, increased by two to four orders of magnitude when compared to the toxicity under
laboratory light. Being nano-TiO2 a photocatalyst (as well other semiconductor metal oxides such ZnO)
with a band gap energy of 3.2 eV (for anatase TiO2) it can be photo-activated in the presence of UV
light enhancing the generation of ROS, the main factor responsible for breaking down contaminants in
wastewater treatments (Robichaud, Uyar, Darby, Zucker, & Wiesner, 2009). Unfortunately, the genera-
tion of ROS has been proposed as one of the main mechanisms responsible for the toxicity of NMs (Fu,
Dionysiou, & Liu, 2014; Kahru, Dubourguier, Blinova, Ivask, & Kasemets, 2008) to several aquatic
Ecotoxicity and Toxicity of Nanomaterials with Potential for Wastewater Treatment Applications
organisms, such as marine phytoplankton (Miller, et al., 2012), freshwater planktonic organisms (K. T.
Kim, Klaine, Cho, Kim, & Kim, 2010; Hongbo Ma, Brennan, & Diamond, 2012a; Hongbo Ma, et al.,
2012b) and benthic organisms (S. Li, Wallis, Diamond, Ma, & Hoff, 2014; S. Li, Wallis, Ma, & Dia-
mond, 2014; Wallis et al., 2014).
Besides metal oxide NMs, several other metal-based materials are being applied to water treatment.
Nano-Zero valent iron (nZVI) has been used effectively for the treatment of toxic contaminants pres-
ent in soil, groundwater and wastewaters (Fu, et al., 2014). The environmental applications of nZVI
has been widely accepted mainly due to the low costs associated and also because the low toxicity of
iron (Crane & Scott, 2012). However, the environmental risks associated with their use are still poorly
understood. For example, Keller et al. (2012) tested the effect of three commercial forms (uncoated,
organic coating, and iron oxide coating) of nZVI to three species of marine phytoplankton (Isochrysis
galbana, Dunaliella tertiolecta and Thalassiosira pseudonana), one species of freshwater phytoplankton
(P. subcapitata), and a freshwater zooplankton species (D. magna) (Keller, Garner, Miller, & Lenihan,
2012). The results showed that nZVI can be toxic to aquatic organisms living either in freshwater streams
or marine environments (Keller, et al., 2012). Another metal-based NMs that has received considerable
attention for applications in water treatment, due to their antibacterial properties, are silver NMs (Q. Li
et al., 2008). However, the biological activity responsible by their antibacterial properties could also
endanger other organisms once discharged into the environment. The ecotoxicity of silver NMs has been
reported to various aquatic organisms, including algae (Miao et al., 2010; Miao et al., 2009; Oukarroum,
et al., 2012), aquatic plants (Gubbins, Batty, & Lead, 2011; S. Kim et al., 2009), aquatic invertebrates
(Asghari, et al., 2012; Nair, et al., 2013) and fish (Chae et al., 2009; George et al., 2014). The toxicity
of nano-Ag is a subject of great debate. While some studies suggested that the release of silver ions
caused the toxicity, other studies related the toxicity not only with silver ions but also with the nano-size
of these particles (Behra et al., 2013). For example, Griffitt et al. (2008) exposed several aquatic organ-
isms (Danio rerio, Daphnia pulex, Ceriodaphnia dubia and Pseudokirchneriella subcapitata) to silver
NMs and AgNO3 (Griffitt, Luo, Gao, Bonzongo, & Barber, 2008). These authors found that during the
exposure the dissolution of nano-Ag was relatively low, so the recorded mortality cannot be attributed
solely to the particle solubilization but also to the nano-Ag particles (Griffitt, et al., 2008). However,
Miao et al. (2009) found that the toxicity of nano-Ag to the marine microalgae (Thalassiosira weisflogii)
was entirely mediated by the dissolution of Ag ions from the NMs (Miao, et al., 2009).
It is recognized that the development and application of nanotechnology can play an important role
in solving or ameliorating issues related to water and wastewater treatment. However we cannot deny
the toxic effects of these NMs and caution should be taken when using NMs for water treatment.
Ecotoxicity of Nanomaterials for the Soil Biota
Once in the soil, NMs can be degraded by several processes (biotic and abiotic), and be transported to
the aquatic compartment through runoff and leaching (Boxall, Tiede, & Chaudhry, 2007). Physical and
chemical characteristics, such as the size of NMs, their chemical composition or their functionalization,
will determine what their fate in the environment (Brar, et al., 2010). Some NMs can be carried over
larger distances before becoming trapped in the soil matrix or they can be immediately adsorb to soil
particles, becoming more immobile (Soni, Naoghare, Saravanadevi, & Pandey, 2015). Additionally, soil
microorganisms may also adsorb or degrade NMs (Wiesner, Lowry, Alvarez, Dionysiou, & Biswas, 2006).
Ecotoxicity and Toxicity of Nanomaterials with Potential for Wastewater Treatment Applications
Table 2. Toxicity effect of NMs towards plants
NMs Size Supports by
Plant Concentration
Observations Reference
ZnO 20±5 Lolium perenne
10 - 1000 mg L-1 Biomass decrease, root tips shrank, root
cells vacuolated or collapsed.
(D. Lin & Xing,
50 Allium cepa
(onion bulbs)
5 - 20 mg L−1 Inhibition of root elongation.
Accumulation in both the cellular and the
chromosomal modules.
(Ghodake, Seo, &
Lee, 2011)
< 100 Triticum
≈ 25 mg L-1 Biomass decrease. (Du et al., 2011)
< 100 Brassica
200 – 1500 mg
Decrease in plant biomass.
Increase in proline content and lipid
(Rao & Shekhawat,
(flax seeds)
0.01 – 100 mg
Inhibition of germination and root biomass. (Clément, Hurel, &
Marmier, 2013)
10, 50 and 100
mg L-1
Seed germination, vegetative development,
photosynthesis and redox balance was not
Wheat roots accumulate NPs with a
primary diameter lower than 140 nm and
the NPs can translocate to the leaves if the
primary size is smaller than 36 nm.
(C. Larue et al.,
27±4 Cucumis
0 to 750 mg kg–1 The NPs were translocated without
biotransformation or to the edible part of
cucumber plants.
(Servin et al., 2013)
nZVI ---- Linum
L. (flax)
Lolium perenne
L. (ryegrass)
vulgare L.
0–5000 mg L-1 Inhibitory effects in aqueous suspensions
at 250 mg L-1 and complete inhibition of
germination observed at 1000-2000 mg L-1.
Inhibitory effects observed at 300 mg L-1
in soil.
Complete inhibition observed at 750 and
1500 mg L-1 in sandy soil for flax and
ryegrass, respectively.
(Yehia S. El-Temsah
& Erik J. Joner,
50 - 60 Lactuca sativa
10 and 20 mg L-1 Did not affect lettuce growth and
chlorophyll content
Majumdar, Botez,
Peralta-Videa, &
20 - 30 Lactuca sativa
10 and 20 mg L-1 Affect plant growth, water content, dry
biomass production, and concentration of
several nutrients.
Ag ---- Arabidopsis
(thale cress)
0.2 – 3.0 mg L-1 Inhibition of growth and root elongation.
Decrease photosynthetic pigment content.
Disruption of thylakoid membrane
(Qian et al., 2013)
5 to 25
(average 10)
(mung bean)
0 - 40 mg L-1 The exposure medium influences the
Agar medium:
P. radiates EC50 = 13 mg L-1
S. bicolor EC50 = 26 mg L-1
Soil medium EC50 > 2000 mg kg-1 for both
(W.-M. Lee, Kwak,
& An, 2012)
Ecotoxicity and Toxicity of Nanomaterials with Potential for Wastewater Treatment Applications
NMs used for water and wastewater treatments can enter the terrestrial ecosystem during manufacture/
transport/application or via storage/dump of sludge in landfills or through the use of contaminated sewage
sludge or biosolids for agricultural land fertilization (Brar, et al., 2010; Kiser, Ryu, Jang, Hristovski, &
Westerhoff, 2010). Biosolids are being widely recommended as a cheaper alternative for improving the
fertility of agricultural soils (Antolin, Muro, & Sanchez-Diaz, 2010; Suppan, 2013), while the volumes
to be deposited in landfills are being reduced. In the U.S., more than 60% of biosolids produced each
year are being applied to agricultural lands (Gardea-Torresdey, Rico, & White, 2014). While in Europe
the risks associated with this procedure are being deeply analysed, since NMs as well as other emergent
contaminants can interact and have several impacts on soil organisms (microorganisms, plants and inver-
tebrates). Considering, that soils are essential to the sustainability of ecosystems and for the survival of
the human species (O’Halloran, 2006), it is important to understand how NMs will affect the soil biota
and subsequently soil quality, functions, and services.
Ecotoxicity of Nanomaterials for Plants
Plants are an essential component of terrestrial ecosystems, maintaining the carbon and nitrogen cycling
and are an important food source for humans and other organisms. Further, they are responsible by
many other ecosystem services as soil formation and protection, climate regulation etc. Several recent
data on plants responses to NMs exposure have been gathered and reviewed (Gardea-Torresdey, et al.,
2014; Klaine et al., 2008; K.-E. Li, Chang, Shen, Yaon, & M.H. Siddiqui et al. (eds.), 2015; Y. Ma et
al., 2010; Miralles, Church, & Harris, 2012; Navarro, et al., 2008; Schwab et al., 2015). Table 2 shows
the main toxicity studies of NMs on plants. However, a limited range of plant species has been tested in
nanophytotoxicity studies, and data acquisition is also limited to some NMs.
Seeds germination, biomass production and/or root and shoots elongation have been the main endpoints
used for assessing the effects of NMs on plants (Elgrabli et al., 2008; Stampoulis, Sinha, & White, 2009;
Yang & Watts, 2005) frequently under short exposure periods (Gardea-Torresdey, et al., 2014). Several
studies and reviews also focused on the genotoxic effects, uptake, translocation, bioaccumulation and
biotransformation in food crops (Chen et al., 2015; Kumari, Mukherjee, & Chandrasekaran, 2009; Y.
Ma, et al., 2010; Miralles, et al., 2012; Remédios, Rosário, & Bastos, 2012; Rico, Majumdar, Duarte-
Gardea, Peralta-Videa, & Gardea-Torresdey, 2011; H. Zhu, et al., 2008). However, in the great majority
of studies the plants were exposed to NMs through hydroponic conditions, filter papers or through soils
directly contaminated under laboratorial conditions which do not represent the real route of exposure of
plants, to NMs used for wastewater treatments, which will occur through soils amendments with sludge.
Thus, there is still a vast gap of knowledge that limits our understanding of the long-term risks to plants
(Gardea-Torresdey, et al., 2014; S. Lin et al., 2009).
Nowadays, TiO2 NMs is well known for its great potential for a vast array of applications and also
as a photocatalyst to remove organic pollutants from treated effluents and for several other purifica-
tion technologies (Adesina, 2004; Shahid, McDonagh, Kim, & Ho Shon, 2015). However, the smallest
particles of TiO2 NMs are difficult to extract from water (Shahid, et al., 2015) while on the other hand
the bigger and the heavier aggregates that can be formed during treatments, can easily settle, becoming
part of sediments and sludge. Several studies showed the accumulation of TiO2 NMs in root and leaves
of seedlings of wheat and rapeseed, and also an accumulation of TiO2 NMs in nodules of garden peas
and in trichomes of cucumber (Fan, Huang, Grusak, Huang, & Sherrier, 2014; Camille Larue, Julien
Laurette, et al., 2012; Camille Larue, Giulia Veronesi, et al., 2012; Servin et al., 2012). Even more,
Ecotoxicity and Toxicity of Nanomaterials with Potential for Wastewater Treatment Applications
concerning TiO2 NMs was found accumulated in cucumber fruits (Servin, et al., 2013), does showing
a great potential for trophic transfer. In opposition, several other studies demonstrated that rather than
being bioaccumulated TiO2 NMs have absorbed on the surface of seeds and roots of lettuce, radish and
cucumber (Wu et al., 2012). The main processes contributing for such adsorption were probably the
physical attachment of particles on the rough seed surfaces, electrostatic attractions and hydrophobic
interactions between seeds and NMs aggregates. These authors postulated that seed wax composition
may be a determinant factor in this interaction of NMs with seed coats (X. Hu, Daun, & Scarth, 1994;
H. N. Zhu, Lu, & Abdollahi, 2005).
As far as iron and iron oxide NMs are considered, a study evidenced that nano-Fe3O4 can be uptaken,
translocated, and accumulated within various tissues of pumpkin plants (H. Zhu, et al., 2008).
Phytotoxic effects, as inhibition of shoot growth of ryegrass and barley were also observed at 1000
mg nZVI kg-1 soil (Y.S. El-Temsah & E.J. Joner, 2012). Moreover this iron NMs displayed strong toxic
effect at concentrations above 200 mg L-1 reducing the transpiration and growth of hybrid poplar seedlings
(X. Ma, Gurung, & Deng, 2013). The authors related the phytotoxicity of this NMs with the irregular
aggregates of nanoscale zero-valent iron coating plant roots surface as revealed by transmission electron
microscope (TEM) analysis and, with the internalization of nZVI by poplar root cells as revealed by
scanning transmission electron microscope (STEM) analysis (X. Ma, et al., 2013).
With a more ecological relevant exposure, Chen et al. (2015) evaluated the toxicogenomic responses
of Medicago truncatula growing in soils amended with biosolids containing a mixture of different NMs,
such as Ag, ZnO, and TiO2, and aged for six months (Chen, et al., 2015). The data gathered demonstrated
differential expression of several genes involved in oxidative stress. Further the inhibition in the growth
and nodulation of M. truncatula was observed and it was mainly related with enhanced bioavailability
of Zn ions in the biosolids amended soils (Chen, et al., 2015), thus suggesting that the suspected hazard
of this NMs, persists even when integrated in soil as part of a complex organic matter matrix.
In another study, the effects of NMs (zinc and zinc oxide) on seed germination and root growth of
six higher plant species (radish, rape, ryegrass, lettuce, corn, and cucumber) was investigated and the
results showed that seed germination was affected by nano-Zn on ryegrass and nano-ZnO on corn at
2000 mg L-1. Further, these NMs inhibited the root elongation of tested species (Daohui Lin & Xing,
2007). Similar measurements, in a more recent study showed that the effect of NMs (Ag, Cu, Si, and
ZnO) on Cucurbita pepo (zucchini) on roots elongation was more relevant than the impacts on germina-
tion (Stampoulis, et al., 2009). Also, Wu et al. (2012) investigated the toxicity of various metal oxide
NMs on lettuce, radish and cucumber seeds (Wu, et al., 2012). In this study, only CuO and NiO showed
harmful impacts in germination of all species with calculated EC50s of lettuce: NiO: 28 mg L-1; CuO:
13 mg L-1; radish: NiO: 401 mg L-1; CuO: 398 mg L-1; cucumber: NiO: 175 mg L-1; CuO: 228 mg L-1.
Further, a short term exposures of tomato seeds to nano-NiO resulted in a significant reduction in root
growth and caused oxidative stress (Mohammad Faisal et al., 2013)
In the same way, silver NMs are considered as effective antimicrobial materials for coliform and
pathogen bacteria found in wastewater (Furno et al., 2004; Morones et al., 2005; Tiwari, Behari, & Sen,
2008). These NMs showed a 71% and 57% reduction in zucchini biomass and transpiration, respectively,
after an exposure at 1000 and 500 mg L-1 (Stampoulis, et al., 2009). Ag NMs have also shown effects on
cucumber, lettuce, ryegrass and barley seeds germination (Barrena et al., 2009; Y.S. El-Temsah & E.J.
Joner, 2012). In contrast, these NMs did not show any effect in growth of Phaseolus radiates, and only a
slight inhibition in growth was observed for Sorghum bicolor at a range of concentrations up to 2000 mg
kg-1 in soil (W.-M. Lee, et al., 2012). The same authors proved that the bioavailability of silver ions dis-
Ecotoxicity and Toxicity of Nanomaterials with Potential for Wastewater Treatment Applications
solved from nano-Ag was more reduced in soil than in other tested media. Furthermore, tomato exposure
to nano-Ag resulted in a significantly decreased biomass at concentrations up to 500 mg kg-1 nano-Ag
(U. Song et al., 2013). Kumari et al. (2009) focused on the genotoxic effects of silver nanoparticles on
Allium cepa cells from root and revealed several cytological consequences, namely chromatin bridges
and stickiness (50 ppm concentration of nano-Ag suspended in deionized water), troubled metaphase
(70 ppm) and chromosomal breaks (100 ppm) (Kumari, et al., 2009).
Besides the effects of metal-based NMs on plants, several studies also concentrated their attention
on impact of carbon nanotubes. Begum, Ikhtiari, & Fugetsu (2014) using 1000 mg L-1 and 2000 mg
L-1 of multi-walled carbon nanotubes showed significant inhibition in shoot elongation, cell death and
electrolyte leakage in red spinach, lettuce, and cucumber, after 15 days of exposure (Begum, Ikhtiari,
& Fugetsu, 2014). Also an effect on root elongation of Cucurbita pepo (zucchini) was recorded (Stam-
poulis, et al., 2009). However, toxicity effects of MWNTs were different between plants species. For
example, red spinach and lettuce were more sensitive than rice and cucumber, while chili, lady’s finger,
and soybean showed slight or no toxic effects after being exposed to these NMs (Begum, et al., 2014).
Several studies showed that plants, and in particular food crops, are sensitive and may be affected by
exposure to NMs. However, the evidences about the entry, transformation and accumulation into the food
chain are limited and the implications on human health/nutrition on terrestrial communities are poorly
understood or even unknown. Preferably, long-term exposures and full life-cycle studies are needed.
Moreover, the future studies need to focus and take into consideration the different factors that may
contribute or ameliorate NMs phytotoxicity like the effect of aging of MNs in soil, the role of different
soil physico-chemical properties in the bioavailability of NMs, the addition of NMs to soils via sludge
amendments or irrigation with treated wastewaters, as well as the interaction of NMs with several other
contaminants, already present in natural soils (e.g. metals, pesticides, PCBs, PAHs, etc.).
Ecotoxicity of NMs for Terrestrial Invertebrates
Most of the studies with terrestrial invertebrates have been made with metal oxide NMs. These studies
have mainly focused in assessing the toxicity of NMs in the avoidance and reproduction of earthworms
as shown in Table 3. Earthworms are widely used in ecotoxicological assessments and were the former
soil organism for which standard protocols were developed. One characteristic that makes interesting
to understand the effect of NMs in these organism is their permanent and direct contact with the soil,
in parallel with their important roles in soil functions (Blouina et al., 2013). Heckmann et al. (2011)
screened the effect of some NMs (Ag-NP, SiO2-NP, TiO2-NP) at a concentration of 1000 mg kg-1
and their corresponding metal salts (AgNO3) and bulk metal oxides in reproduction of the earthworm
Eisenia fetida (Heckmann et al., 2011). Reproduction was affected by some of the NMs tested: nano-Ag
completely inhibited the earthworm reproduction, and nano-TiO2 also affected reproduction.
Hu et al. (2010) evaluated the toxicity of TiO2 and ZnO NMs to the earthworm Eisenia fetida by
measuring the activity of superoxide dismutase (SOD), catalase (CAT), and content of malondialdehyde
(MDA) and DNA damages (C. W. Hu, et al., 2010). TiO2 NMs promoted an increase of the activity
of CAT and the content of MDA at concentrations of 1 g kg-1 and 5 g kg-1, respectively. The same was
not observed for ZnO NMs. The authors observed an increase in the activity of CAT and in the content
of MDA at lowest concentrations, and then a decreasing tendency was observed for the highest con-
centrations. DNA damages were observed in organisms exposed to artificial OECD soil spiked with
ZnO and TiO2 NMs (1 and 5 g kg-1) (C. W. Hu, et al., 2010). Cañas et al. (2011) also observed effects
Ecotoxicity and Toxicity of Nanomaterials with Potential for Wastewater Treatment Applications
Table 3. Characterization and toxicity effect of NMs on terrestrial invertebrate
NMs Size Supported
by the
Particle Size by
DLS (nm)
Concentration Species Endpoint Effect Reference
Ag 3-8 - 1000 mg kg-1 P. pruinosus Avoidance and
feeding activity
EC50 values
of 16.0 mg
(Tourinho, van
Gestel, Jurkschat,
Soares, &
Loureiro, 2015)
Ag 30-50 235±3.73 1000 mg kg-1 E. fetida Effects on
(Heckmann, et
al., 2011)
Ag <100 14-20 0.1 and 0.5 mg L-1 C. elegans Survival,
and gene
(Roh et al., 2009)
Cu 80 419 ± 1.46 1000 mg kg-1 E. fetida Effects on
Affected (Heckmann, et
al., 2011)
TiO210-20 - 1 g kg-1 E. fetida Activity of
Increase (C. W. Hu et al.,
TiO210-20 - 5 g kg-1 E. fetida Content of
Increase (C. W. Hu, et al.,
TiO210-20 - 5 g kg-1 E. fetida DNA damage Observed (C. W. Hu, et al.,
TiO215 350-500
3000 µg g-1 P. scaber Mortality,
weight, and
No effect (Jemec, Drobne,
Remskar, Sepcic,
& Tisler, 2008)
TiO215 350-500
0.1, 1000 and 3000
µg g-1
P. scaber Antioxidant
activities (CAT
and GST)
(Jemec, et al.,
TiO232 - 1000 mg kg-1 E. fetida Effects on
(Cañas et al.,
TiO250 338-917 24-239.6 mg L-1 C. elegans Growth and
LC50 = 80
mg L-1
(Huanhua Wang,
Wick, & Xing,
ZnO 10-20 - >0.5 mg kg-1 E. fetida Activity of
and content of
(C. W. Hu, et al.,
ZnO 10-20 - 5 g kg-1 E. fetida DNA damage Observed (C. W. Hu, et al.,
ZnO 20 478-980 0.4 and 8.1 mg L-1 C. elegans Growth and
Highly toxic
LC50 = 2.2
mg L-1
(Huanhua Wang,
et al., 2009)
ZnO 40-100 - 1000 mg kg-1 E. fetida Effects on
(Cañas, et al.,
ZnO <100 - 750 mg kg-1 E. veneta Effects on
Reduced (Hooper et al.,
continued on following page
Ecotoxicity and Toxicity of Nanomaterials with Potential for Wastewater Treatment Applications
on reproduction of E. fetida exposed to an artificial OECD soil and sand-manure spiked with ZnO and
TiO2 NMs (range of concentrations from 0.1 and 1000 mg kg-1) (Cañas, et al., 2011). ZnO NM at the
highest concentration tested (1000 mg kg-1) significantly inhibited cocoon production in OECD soil.
In sand-manure, cocoon production also decreased with the increase of ZnO NM concentrations. The
authors observe a significant inhibition of cocoon production at 100 and 1000 mg kg-1. ZnO NMs in clay
loam amended with 3% of organic matter reduced in 50% the reproduction of the earthworm E. veneta
at concentrations of 750 mg Zn kg−1 (Hooper, et al., 2011).
Nano zero-valent iron (nZVI) has been considered a great, inexpensive, and environmental friendly
reducing agent, that has been used for remediation of numerous contaminants. However, few works have
reported the effect of nZVI in soils (El-Temsah & Joner, 2013). Same authors tested the effects of nZVI
in the avoidance and reproduction of Eisenia fetida and Lumbricus rubellus in natural and OECD arti-
ficial soils (Yehia S. El-Temsah & Erik J. Joner, 2012). Both species, in different soils, have a tendency
NMs Size Supported
by the
Particle Size by
DLS (nm)
Concentration Species Endpoint Effect Reference
ZnO <200 - 6400 mg kg-1 F. candida Survival No effect (Kool, Ortiz, &
van Gestel, 2011)
ZnO <200 - 1800 mg kg-1 F. candida Reproduction Reduction (Kool, et al.,
nZVI - 178 - 424 >750 mg kg-1 L. rubellus Avoidance OECD soil:
EC50 = 582
mg kg-1
LC50 = 866
mg kg-1
Natural soil:
EC50 = 532
mg kg-1 LC50
= 447 mg
(Yehia S. El-
Temsah & Erik J.
Joner, 2012)
nZVI - 178 - 424 >750 mg kg-1 E. fetida Avoidance OECD soil:
EC50 = 511
mg kg-1
Natural soil:
EC50 = 563
mg kg-1
LC50 = 399
mg kg-1
(Yehia S. El-
Temsah & Erik J.
Joner, 2012)
nZVI - 178 - 424 1000 mg kg-1 L. rubellus
and E. fetida
Reproduction Completely
(Yehia S. El-
Temsah & Erik J.
Joner, 2012)
DWCNT - - 495 mg kg-1 E. veneta Reproduction The
production of
cocoons was
reduced by
EC10 =
37±73 mg
DWNT kg-1
EC50 =
176±150 mg
DWNT kg-1
Krogh, Schaefer,
& Johansen,
Table 3. Continued
Ecotoxicity and Toxicity of Nanomaterials with Potential for Wastewater Treatment Applications
Table 4. Effect of metal and metal oxide nanoparticles on cells in vitro
NMs Size
by the
by Dynamic Light
Scattering (DLS)*
Results Reference
Ag 15 nm n/a C18-4 Cell morphology changes at 10 µg
mL-1. Decrease of cell viability (EC =
8.75 µg mL-1). Increase of membrane
leakage (EC = 2.5 µg mL-1)
Stolle, Hussain,
Schlager, &
Hofmann, 2005)
Ag 7-10 nm n/a HepG2 High toxicity and changes in cell
morphology at higher doses (1.0 µg
(Kawata K.,
Osawa, & Okabe,
with PVP
30-50 nm 121 nm; -21 mV A549 Induction of oxidative stress leading
to cyto/genotoxicity at concentrations
ranging 2.5 µg mL-1 from 10 µg mL-1
(Foldbjerg, Dang,
& Autrup, 2011)
stabilized by
10, 20, 30, 40
and 60 nm
6, 11, 16, 58 and 68 nm,
respectively; -25, -25,
-24, -15 and -16 mV,
Balb/3T3 Smallest NMs (10 nm) lead to highest
bioavailability of Ag ions (EC=0.27
µg mL-1)
(Ivask et al.,
TiO2˂25 nm n/a U-87 and
Induction of cell death on U-87 and
HFF-I cell lines with EC of 30-40 µg
mL-1 and 40 µg mL-1, respectively
(Lai et al., 2008)
TiO2n/a 93.9 nm L929 Reduction of cell viability (≥ 60 µg
mL-1) after 48 h and induction of
oxidative stress at higher concentration
(600 µg mL-1)
(Jin, Zhu, Wang,
& Lu, 2008)
TiO2n/a 124.9 nm; -17.6 mV A431 Decrease of cell viability, production of
ROS and oxidative stress causing DNA
injury and micronucleus formation at
concentrations of 8 and 80 µg mL-1
(Shukla et al.,
TiO2101 - 31.74 mV HAECs and
High expression of adhesion molecules
(VCAM-1 and E-selectin) in HAECs
with endothelium dysfunction at 20
µg mL-1
(Alinovi et al.,
ZnO n/a 165 nm;- 26 mV A431 Genotoxicity effects induced by
oxidative stress with depletion of CAT,
glutathione and SOD at concentration
above 0.008 µg mL-1
(Sharma et al.,
ZnO n/a n/a HL-60 and
Higher toxicity on HL60 (EC= 52.80
µg mL-1) than PBMC cells (741.82 µg
& Manivannan,
ZnO n/a 456.5 nm;
+ 14.4 mV
RAW 264.7
and BEAS-
Cytotoxicity was more pronounced
in RAW 264.7 than in BEAS-2B at
concentrations of 10, 15 and 20 µg
mL-1. DNA damage at doses above 10
µg mL-1
(Ng et al., 2011)
ZnO rod
shape and
ZnO with
n/a 245 and 145 nm,
respectively; + 23.5 and
+ 35 mV, respectively
RAW 264 NMs dissolution is the main cause
of ZnO toxicity. The toxicity can be
attributed to the metabolic perturbation
leading to cell death.
(Triboulet et al.,
continued on following page
Ecotoxicity and Toxicity of Nanomaterials with Potential for Wastewater Treatment Applications
Figure 1. Schematic representation of NMs effects at cellular level caused by oxidative stress generation
NMs Size
by the
by Dynamic Light
Scattering (DLS)*
Results Reference
SPIONs and
coated with
n/a 158, 195, 41.2, 44.9,
199 and 262 nm.
L929 Increase of cell viability by increasing
the concentration of iron salts. Coated
NMs showed less toxicity events
Simchi, Milani,
& Stroeve, 2009)
Fe3O4n/a 174 nm A549 Decrease of cell viability, changes
in cell morphology, gluathione
depletion, induction of ROS and lipid
peroxidation at cell exposed to10, 25
and 50 µg mL1
(Dwivedi et al.,
*measured in distilled water. C18-4: Mouse spermatogonial stem cells; HepG2: human hepatocarcinoma cells; PVP: Poly vinylalcohol;
A549: Human lung adenocarcinoma epithelial cells; Balb/3T3: Mouse embryonic fibroblast cells; U-87: Human glioblastoma cells; HFF-I:
Human Foreskin Fibroblasts; L929: Mouse fibroblasts; A431: human epithelial carcinoma cells;; HAECs: Human aortic endothelial cells;
HUVECs: Human umbilical vein endothelial cells; VCAM-1: Vascular cell adhesion molecule 1; SOD: Superoxide dismutase; HL-60:
Human myeloblastic leukemia cells; PBMC: Peripheral blood mononuclear cells; RAW 264.7: Mouse macrophage cells; BEAS-2B: Human
bronchial epithelial cells; SPIOs: Superparamagnetic iron oxide nanoparticles; PVA: Polyvinyl alcohol;
n/a: not available;
Table 4. Continued
Ecotoxicity and Toxicity of Nanomaterials with Potential for Wastewater Treatment Applications
to prefer soils with the lowest concentrations of nZVI (≤ 500 mg kg-1). The EC50 values determined for
avoidance were 582 mg kg-1 and 532 mg kg-1 for L. rubellus in OECD and natural soil, respectively. For
E. fetida they determined an EC50 value of 511 mg kg-1 in OECD soil, and of 563 mg kg-1 for natural
soil. The same authors reported LC50 values for L. rubellus (866 mg kg-1 in OECD soil and 447 mg kg-1
in natural soil). For E. fetida they only determined a LC50 of 399 mg kg-1 in natural soil, after 14 days
of exposure. The reproduction of both species was completely inhibited in all the concentrations tested,
up to 1000 mg kg-1. This study showed that nZVI can have serious harmful effects for the behaviour
and reproduction of earthworms at high concentrations, which could be attained if this NM is directly
applied to soils, for remediation purposes.
Considering non-metallic NMs, Scott-Fordsmand et al. (2008) observed the toxic effects of double-
walled carbon nanotubes (DWCNT) in the earthworm Eisenia veneta. The production of cocoons was
reduced by 60% at 495 mg DWNT kg-1 (Scott-Fordsmand, et al., 2008). These authors reported an EC10
of 37±73 mg DWNT kg-1 and EC50 of 176±150 mg DWNT kg-1 for the reproduction of this species.
Regarding other soil invertebrates, nano-TiO2 at concentrations of 3000 µg g-1 did not caused effects
on mortality, weight or feeding behaviour of the isopod Parcellio scaber (Jemec, et al., 2008). However,
sub-lethal effects on antioxidant enzymes activities (CAT and glutathione-S-transferase – (GST)) were
recorded for exposure concentrations of 0.1, 1000 and 3000 µg TiO2 g-1 (Jemec, et al., 2008).
Roh et al. (2009) assessed the toxicity of silver NMs for Caenorhabditis elegans by assessing survival,
growth, reproduction and gene expression endpoints (Roh, et al., 2009). They concluded that Ag NMs
(0.1 and 0.5 mg L-1) were considerably toxic to C. elegans, mainly affecting reproduction potential. These
authors also concluded that the sod-3 and daf-12 genes may have been associated with the reproduc-
tive failure induced by Ag NMs in these organisms and that oxidative stress had an important role in
the mechanism of toxicity of Ag NMs. Tourinho et al. (2015) also observed that Ag NMs affected the
avoidance behaviour (EC50 values of 16.0 mg kg-1) and the feeding activity of the isopod P. pruinosus
(Tourinho, et al., 2015).
The survival of collembolans F. candida was not affected by ZnO NMs at concentrations up to 6400
mg Zn kg-1
DW (Kool, et al., 2011). The authors also concluded that nano-ZnO contributed to a reduction
of springtails reproduction for concentrations below 1800 mg Zn kg-1 in natural LUFA soil. Ma et al.
(2009) also reported the low toxicity (for behaviour, lethality, and reproduction endpoints) of nano-ZnO
to C. elegans (H. Ma, Bertsch, Glenn, Kabengi, & Williams, 2009). In opposition, Wang et al. (2009),
testing particles with a bigger size, observed that uncoated ZnO (a range of concentrations from 0.4 and
8.1 mg L-1) was highly toxic to C. elegans larvae (LC50 of 2.2 mg L-1) (Huanhua Wang, et al., 2009).
These authors also showed the toxicity of TiO2 (24 – 239.6 mg L-1) that inhibited the growth and espe-
cially the reproductive capability of C. elegans (LC50 of 80 mg L-1).
Although few studies available suggest that NMs will affect soil invertebrates, but such effects will
occur only at concentrations that could be attained with cumulative applications of sewage sludge on
soils. Thus in the future studies, will be crucial to obtain more data about the toxicity of other NMs,
for a wide range of soil invertebrates; to perceive the indirect effects of NMs in soil communities and
their population interactions, as well as gain new insights in trans-generational effects in invertebrate
populations, submitted to cumulative exposures to low levels of NMs.
Ecotoxicity and Toxicity of Nanomaterials with Potential for Wastewater Treatment Applications
In Vitro Toxicity Studies of NMs Using Cell Culture Lines
The impact of NMs at the cellular level has been widely investigated. Almost all the toxicity tests with
cell lines were conducted to perceive the mechanisms of toxicity of the contaminants. Table 4 lists the
in vitro toxicity studies with different cell lines, evaluating NMs with potential for wastewater treat-
ment. According to the Table 4, the effect of NMS on biological systems can be related not only to
their physicochemical features (size, surface charge, morphology, solubility) (Donaldson, Stone, Tran,
Kreyling, & Borm, 2004) but also with the type of cell line used in vitro toxicity assays, which is se-
lected depending on the expected entry pathways of the NMs (lung, skin, intestine or liver) in the body
(Oberdörster et al., 2002).
The cell viability studies can be performed by a battery of standard toxicological assays, including
AlamarBlue (AB), MTT (3-(4,5-dimethyl-2-thiazolyl)-2,5-diphenyl-2H-tetrazolium bromide), neutral red
(to evaluate the dye uptake) and lactate dehydrogenase (LDH) (to evaluate the damage of cell membrane
due to the release of LDH) methods already reported in several studies and reviews (Ahamed, Akhtar,
Alhadlaq, Khan, & Alrokayan, 2015; Andreani et al., 2014; Asare et al., 2012; Doktorovova, Souto, &
Silva, 2014). Many other more extensive NMs cytotoxicity assays can be conducted to evaluate DNA
damages (comet assay), DNA damage and apoptosis (flow cytometry), detection of oxidative stress
(ROS production and alteration in antioxidant enzymes level), lipid peroxidation (thiobarbituric acidic
method-TBA) and inflammation (enzyme-linked immunosorbant assay- ELISA) (Lewinski, Colvin, &
Drezek, 2008).
Similarly to ecotoxicological test organisms and according to data reported the toxicity of most tested
NMs to cell lines can be related with the induction of oxidative stress (Figure 1). ROS including the
superoxide anion, hydrogen peroxide and hydroxyl radicals, can accumulate in the cells leading to severe
cellular injuries, including membrane lipid peroxidation and protein and DNA damages. The cellular
defense mechanisms against ROS can include non-enzymatic antioxidants (e.g. α-tocopherols, carotens,
ubiquinone), as well as enzymatic scavengers, such as, SOD, CAT, glutathione peroxidase (GPx) and
GST enzymes (Franco, Sánchez-Olea, Reyes-Reyes, & Panayiotidis, 2009).
Several studies claim that the use of ultrafine nano-TiO2, one of the most used NMs for wastewater
treatment applications, can lead to severe cytotoxicity when exposed to UV irradiation. However, they
are considered safe materials in the absence of photoactivation (Peters, Unger, Kirkpatrick, Gatti, &
Monari, 2004). In contrast, several other studies showed that nano-TiO2 (10 and 20 nm) at 10 µg mL-1
can lead to lipid peroxidation, DNA damage and increase of nitric oxide and hydrogen peroxide levels
in human bronchial epithelial cells (BEAS-2B) (Gurr, Wang, Chen, & Jan, 2005). This NMs has also
induced significant apoptotic events in Syrian hamster embryo fibroblasts cells at 1.0 µg mL-1 (Q. Rahman
et al., 2002), decreased the intracellular level of reduced glutathione (GSH) and activated caspase-3 and
chromatin condensation at concentrations above 5 µg mL-1 leading to the apoptosis in BEAS-2B cells
(E.-J. Park et al., 2008). According to García et al. (2014), nano-TiO2 was also able to induce oxidative
stress effects on glial cells associated with an increase of GPx activity. CAT and SOD activities, which
were not able to prevent lipid peroxidation and mitochondrial damage at 20 µg mL-1 (Huerta-García et
al., 2014).
Induction of cell toxicity by Ag NMs was also shown in different cell lines (AshaRani, Low Kah Mun,
Hande, & Valiyaveettil, 2009; Hackenberg et al., 2011; Y.-H. Lee et al., 2014; E.-J. Park, Yi, Kim, Choi,
& Park, 2010; M. V. D. Z. Park et al., 2011). Evaluation of the cytotoxicity of nano-Ag was conducted on
dermal noncancerous (HaCat) and cervical cancer (HeLa) cell lines demonstrated the induction of high
Ecotoxicity and Toxicity of Nanomaterials with Potential for Wastewater Treatment Applications
levels of oxidative stress, glutathione depletion and cell membrane damage with subsequent apoptosis.
However, HeLa cells demonstrated to be more sensitive upon nano-Ag exposure (lethal dose (LD) of 6.9
µg mL-1) in comparison to HaCat cells (29 µg mL-1) after 79 h with AB assay. This difference between
the two cell lines was attributed to different capacities of antioxidant defense mechanisms (Mukherjee,
O’Claonadh, Casey, & Chambers, 2012). Some studies have also demonstrated that the oxidative damage
caused by nanoparticulate systems can be driven by the release of the metal ions. For instance, Beer et al.
(2012), observed that a synergic effect between silver ions and nano-Ag contributed for toxicity events
at lower concentrations of Ag+ ions (≤ 2.6%) in A549 cells (Beer, Foldbjerg, Hayashi, Sutherland, &
Autrup, 2012). However, Kim et al. (2009) studied the toxicity of nano-Ag and Ag+ (AgNO3 source) ions
using HepG2 cell line. The authors using a cation exchange treatment showed that nano-Ag produces
low concentration of Ag ions and thus, the cytotoxicity and genotoxicity effects observed were induced
by nano-Ag per se and not by silver ions (S. Kim, et al., 2009).
The cytotoxicity of nano-ZnO has also been investigated in several studies using different cells as
shown in Table 1. In some studies, the toxicity of nano-ZnO was ascribed to the release of Zn+2 ions
from the NMs (George et al., 2010). According to Xia et al. (2008), the toxicity of nano-ZnO on RAW
264 and BEAS-2B cells was also likely dependent on the release of dissolved Zn ions (Xia et al., 2008).
However, Sharma et al. (2012), demonstrated that nano-ZnO per se induced mitochondrial apoptosis
mediated by ROS generation in HepG2 cells at 14 µg mL-1 (Sharma, Anderson, & Dhawan, 2012). The
authors evaluated the supernatant from the incubation of nano-ZnO in cell culture medium and observed
no cytotoxic events. Also, they evaluated the effect of a free Zn ions source (ZnCl2) and again no cell
toxicity was detectable, suggesting that the Zn ions release did not contribute to the toxicity effects on
HepG2 cell line.
The oxidative stress induced by nano-ZnO even a low concentration (2.5 µg mL-1), was also showed by
Guo et al. (2013) in rat retinal ganglion cells (RGC-5 cells), since ROS overproduction in cells leaded to
apoptotic events (Guo et al., 2013). Another interesting study, conducted by Kumar et al. (2015), showed
that the surface modification of nano-ZnO using reduced glutathione (GSH) and curcumin decreased
the oxidative stress in human embryonic kidney cells (HEK-293) (Kumar et al., 2015).
The application of iron NMs for wastewater treatment has been recently reviewed by Xu et al. (2012).
The cellular mechanism underlying ROS production and oxidative stress induced by iron NMs in cell
culture lines were exhaustively discussed (Enrico Burello & Wortha, 2011; Keenan, Goth-Goldstein,
Lucas, & Sedlak, 2009). Dwivedi et al. (2014) using A 549 cells, showed that nano-Fe3O4 induced cell
morphological changes and production of intracellular ROS (23, 46 and 82% of control for 10, 25 and
50 µg mL-1, respectively) leading to lipid peroxidation (15, 32 and 91% of untreated cells for 10, 25 and
50 µg mL-1, respectively) and depletion of glutathione at 10 µg mL-1 (Dwivedi, et al., 2014).
A systematic study conducted by Naqvi et al. (2010) indicated that highest concentrations of super-
paramagnetic iron oxide nanoparticles (SPIONs) (above 100 µg mL-1) in murine macrophage cells (J774)
resulted in elevated ROS production and cell death (Naqvi et al., 2010). Also, the cytotoxicity effects
following iron oxide NMs exposures were associated with ROS generation and oxidative stress which
resulted in the formation of actin stress fiber in Porcine aortic endothelial cells (PAEC) at concentration
of 0.5 mg mL-1 (Buyukhatipoglu & Clyne, 2011).
Similarly to what was previously described for nano-ZnO above, the surface modification of Fe3O4
NMs showed that the coating of NMs with silica shell reduced the generation of ROS on A549 and HeLa
cells due to the reduction of the free iron ions release (Malvindi et al., 2014). In summary, available
data indicates that NMs with potential for wastewater treatment may also have risks on human health,
Ecotoxicity and Toxicity of Nanomaterials with Potential for Wastewater Treatment Applications
as they can be cytotoxic to different human cell lines, representing different exposure pathways. It was
also demonstrated that surface modifications of some of these NMs, or the combination with others may
mitigate their effects on cells. Thus, in the future, more research is needed to perceive if such modifi-
cations also benefit the capability of NMs to remove organic and inorganic contaminants from water.
In recent years, the design and application of NMs on the industry are widely increasing due to their
great potential for the society and the economy. Water treatment is an attractive area for the application
of advanced nanotechnology based solutions in order to develop new and functional materials to capture
different contaminants. Although there are great advances with the use of nanotechnology, environmental
and health effects associated to MNs are attracting considerable concern in the scientific community
and in the society
Studies to predict the mechanism toxicity of NMs on environmental species and in cell culture lines
in vitro are important to guarantee their safety for ecosystems and human health. For this purpose, the
collaboration between industry and academy is crucial to provide robust basis and information about the
mechanisms of action of NMs, in order to support new and safe developments in NMs that are designed
for being intentionally applied in the environment.
The authors wish to acknowledge FCT (Fundação para Ciência e Tecnologia) under the reference SFRH/
BD/94902/2013 (Doctoral grant for Gavina, A.C.)
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