manufactured nanomaterials: the connection between environmental fate and toxicity
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Manufactured nanomaterials—the connection betweenenvironmental fate and toxicityIzabela Jośko a & Patryk Oleszczuk a
a Institute of Soil Science and Environmental Management, University of Life Sciences inLublin, ul. Leszczyńskiego 7, 20-069, Lublin, PolandAccepted author version posted online: 27 Nov 2012.
To cite this article: Critical Reviews in Environmental Science and Technology (2012): Manufactured nanomaterials—theconnection between environmental fate and toxicity, Critical Reviews in Environmental Science and Technology, DOI:10.1080/10643389.2012.694329
To link to this article: http://dx.doi.org/10.1080/10643389.2012.694329
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Manufactured nanomaterials – the connection between environmental fate and toxicity
Izabela Jośko, Patryk Oleszczuk*
Institute of Soil Science and Environmental Management, University of Life Sciences in Lublin,
ul. Leszczyńskiego 7, 20-069 Lublin, Poland
Correspondence to: [email protected]
Abstract
The intensive development of nanotechnology, evidenced by the enormous number of
nanoproducts, has resulted in nanomaterials being released into the environment, their
occurrence affecting the functioning of ecosystems. The presence of nanoparticles in the
environment brings threats to living organism connected with the exposure to the harmful
activity of nanomaterials. The toxicity of nanomaterials may be considered from a number of
perspectives, starting from the DNA level, and ending with the reaction of the entire organism.
The biological response of organisms depends not only on the primary characteristics of
nanomaterials and those acquired in the process of functionalization, but also on environmental
conditions (pH, ionic strength, natural organic matter, etc.). These environmental conditions then
determine the course of the processes of aggregation and adsorption. The toxicity of
nanomaterials may be rectified by means of the individual predispositions of organisms (e.g.
tolerance to the activity of specific compounds). Nanomaterials’ synergy with and hostility to
other compounds extant in the environment are also of significance. This work provides a review
of the current literature concerning knowledge on the fate of nanomaterials in the environment
with particular attention given to their toxic impact on organisms.
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Keywords: manufactured nanomaterials, environmental behavior, toxicity effects, risk
assessment
1. Introduction
The quality of water or soil is an extremely important issue regardless of the region or the
part of the world. Maintaining the cleanness of those elements of the environment at a high level
provides for proper functioning of ecosystem. However, due to not only industrial but also
everyday human activity the quality of water and soil may be reduced. The use of detergents,
shampoos, pesticides, etc. leads to the contamination of water with biologically-active
compounds. The presence of these contaminants in various elements of the environment creates a
threat to human health and to other living organisms. Of particular concern is the approach to
using new technologies and substances, without previous studies defining their actual impact on
the environment. As the DDT case has shown, such an approach may lead to negative effects,
potentially affecting not just present, but also future, generations.
Nanotechnology is a relatively young field of science, but a dynamically-developing one. Its
area of interest lies in particles with diameters between 1 and 100 nm.1 Nanomaterials, thanks to
their unusual characteristics, including mechanical, electric, optical, and thermal, are more and
more often used in many areas of everyday life, such as medicine, cosmetics, energy, electronics,
and environmental protection.2
Nanomaterials represent a new and non-homogenous group of compounds which may be
created as a result of natural processes, or be a product of human activity. This work focuses on
anthropogenic nanomaterials, due to their unusual characteristics acquired in the course of
formation, which make nanomaterials a new threat to the environment.
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According to predictions, the scale of production of various types of nanomaterials expected
in the years 2011-2020 will total 58 thousand tonnes.3 The expanding fields for the use of
nanoproducts (Figure 1) will most likely result in an increased presence of nanomaterials in all
components of the environment. There are numerous studies pointing to the negative impact of
nanomaterials on living organisms. Pathologic changes start at the DNA level,4,5 which then
bring about modifications to the cell level,6-9 leading to a response from the particular organs10,11
or even organism as a whole12-14 (Figure 2). The response of living organisms exposed to
nanomaterials not only depends on the characteristics of those structures, but may also be
determined by diverse environmental factors, i.e. pH, the presence of organic matter, the ionic
strength, etc.2
The goal of this work was to provide a synthesis of the knowledge from already-conducted
studies concerning the fate of nanomaterials in the environment, particularly focussing the toxic
impact they have on living organisms.
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2. The definition of nanomaterials
While nanometric structures have been known for decades (humic acids, viruses, sootetc.,
which are present in the environment), nanotechnology deals with materials directly created by a
man in the course of industrial processes. The first scientist to describe the concept of
nanoscience was Richard P. Feynman, at a lecture in a session of the American Physical Society
in 1959.15 The term, however, is said to have been coined by Norio Taniguchi from Japan, who
used this term as early as in 1974. In 1980 Eric Drexler popularised nanotechnology among the
public with his book “Engines of Creation. The Coming Era of Nanotechnology”.15
The Royal Society and The Royal Academy of Engineering15 define nanotechnology as a
technology dealing with the design, description, production, and use of structures, devices, and
systems to control shape and size in nanometrics. As the name of this “new” technology
suggests, its basic metrical unit is the nanometre, which equals one billionth of a metre (1 nm =
10-9 m). It is a scale that is equivalent to, say, half the diameter of a DNA helix. One nanometre
is one thousand times smaller than an erythrocyte, and a hundred thousand times smaller than the
diameter of a single human hair.15 Thus, nanomaterials are materials at least one dimension of
which is between 1 and 100 nm.1,16 Nanoparticles, on the other hand, according to various
sources, are materials of two17 or three18 dimensions which are smaller than or equal to 100 nm.
3. The nanomaterials classification and their use
Nanomaterials are a numerous and non-homogenous group of compounds. For the purposes
of classification, these structures are divided according to various criteria. An example
classification of nanomaterials taking into account their genesis and chemical structure is shown
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in Figure 3. There also exists a classification based on the morphology of nanomaterials, which
are characterised by an abundance of forms. They can assume the shape of a sphere, tubes or
triangle. They can be prism- and rod-shaped, etc. The shape of nanomaterials is very significant,
as it can determine their characteristics. For instance, Ag nanoparticles forming a triangular plate
have stronger antibacterial activity than those particles which are spherical or rod-shaped.19 This
will be discussed in more detail further in this paper.
As far as genesis is concerned, nanomaterials are divided into natural and anthropogenic. The
former may be formed as a result of biogenic processes (fulvic and humic acids), geogenic
processes (soot, black carbon), or atmospheric processes (aerosols, sea salt).20,21 We can also
distinguish bionanoparticles, which include viruses, such as tobacco mosaic virus, and proteins,
e.g. ferritin.22
Anthropogenic nanomaterials may be produced in an aware way for a particular use (e.g.
TiO2 nanoparticles in sun creams), or they may be a side effect of human activities (e.g. fuel
combustion and electrical energy generation – soot).21,22
If we take into account the chemical structure of nanomaterials in this classification, we can
distinguish organic and inorganic ones.23,24 This division is most often used in the environmental
context. The first group comprises mainly carbon- based materials, i.e. fullerenes (e.g. C60, C70,
C76) and carbon nanotubes (CTNs). Inorganic nanoparticles are primarily represented by metal
oxides (TiO2, Fe2O3, ZnO, CuO2), metals (Au, Ag), and quantum dots (QDs – CdS, CdSe,
CdTe).20 The use of various nanomaterials in different products is presented in Figure 4.
Fullerenes, which were discovered in 1985, are composed of rings with five or six carbon
atoms, creating a closed system of diverse shapes.25 The most attention to date has been given to
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fullerenes with 60 carbon atoms in a particle (C60). Their shape resembles a football (a regular,
truncated icosahedron) and they are commonly referred to as buckminsterfullerenes.
The second important group of organic nanoparticles is made up of carbon nanotubes
(CNTs). CNTs are fullerene derivatives. They were discovered by Sumio Iijima in 1991.26 CNTs
come in two forms: single-walled carbon nanotubes (SWCNTs) and multi-walled carbon
nanotubes (MWCNTs). MWCNTs are further divided into double-walled carbon nanotubes
(DWCNTs). SWCNTs structurally resemble a cylinder, comprising a single wrapped layer of
graphene, while an MWCNTs are composed of at least two single-walled nanotubes set
concentrically in relation to each other. As MWCNTs feature several SWCNTs, it is assumed
that their physicochemical characteristics are similar to those of SWCNTs.
Based on their structure, CNTs may also be divided into “armchair,” “zigzag” and “chiral”
CNTs.28 Nanotube chirality is one of the factors affecting the value of the band gap, which in
turn determines the conductivity of those materials.26 CNTs may conduct electricity with even
twice the intensity that can be conducted by copper.24 Owing to the structure of CNTs, which
feature C-C covalent bonds, these materials are characterised by high hardness and strength.
CNTs are considered the strongest fibres.24 To illustrate this, the strength of SWCNTs per unit
mass is 460 times higher than that of steel.2
Their characteristic mechanical, thermal, electrical and optical properties allow fullerenes and
CNTs to find widespread use in medicine, electronics, environmental protection, and the energy
sector.25 They are used to produce photovoltaic cells, airplane parts, various types of sensors,
tyres, tennis racquets, and other consumer products.12,26Today, organic nanomaterials are the
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better-known group in comparison to inorganic nanoparticles, which, according to some authors,
constitute a promising object of future research.25
The most common nanoparticles classified as inorganic include metal oxides, metals, and
quantum dots. Among nano metal oxides, those most commonly used are titanium oxide (nTiO2),
zinc oxide (nZnO), cerium oxide (nCeO2), and iron oxides (nFe3O4, nFe2O3). As for metals, the
highest application is found for nano silver (nano Ag), nano gold (nano Au), nano iron (nZVI),
and nano copper (nano Cu).12,20
Owing to their photocatalytic characteristics, nTiO2 and nZnO nanoparticles may be used to
eliminate organic contaminants in various elements of the environment (water, wastewater, soil,
hazardous wastes). As a photocatalyst, nTiO2 can be useful in the degradation of over 3 thousand
organic contaminants, such as nitrobenzene, cyclohexane, tetrachloroethene and more.27,28 These
characteristics carry measurable results, as nTiO2, for example, which is an ingredient in paints
used to cover building facades, leads to their “spontaneous” purification when exposed to
sunlight.11,27 nTiO2 and nZnO have the capability to absorb UV light, which is why they are used
in sun creams and lotions.11 nZnO is also used to produce sensors and photovoltaic cells.23
Among inorganic nanomaterials, nano Ag is the most widely used in consumer products.29
Due to their antibacterial activity, they are an additive to clothes, paints, food packaging,
toothpastes, and detergents. Nano Ag is also used as a protective antibacterial layer in vacuum
cleaners, washing machines and refrigerators.12 The combination of nano Ag with antibiotics
(e.g. vancomycin or amoxicillin) significantly increases their strength.30 Featured in some
fabrics, nano Ag limits the growth of bacteria responsible for unpleasant odours.31 It is relatively
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common to use such fabrics in the production of socks and other clothes, mainly sportswear,
which come into contact with sweat.
Other nanometals are much less used than nano Ag. Nano Au, for example, is used mainly in
medicine, particularly in cancer therapy. It can also be found in electronics and as a catalyst for
chemical reactions.12 Nano Cu is a component of pesticides, fungicides, and coolants, improving
their performance.32 Nano iron (nZVI), owing to its large specific surface area, its characteristic
catalytic features, and high reactivity, is used in the transformation and detoxification of various
pollutions, such as chlorinated solvents, chloroorganic pesticides and polychlorinated
biphenyls.29
Apart from the benefits directly arising from the characteristics of metallic nanomaterials,
their additional advantage is their relatively inexpensive and simple method of production.23,29
The fourth most common group of nanomaterials is quantum dots (QDs). QDs are
semiconductors with a nanocrystal structure, and dimensions between 2 and 10 nm. QDs are
composed of a core, which comprises semimetals or metals (CdSe, InP, CdTe). They can also
feature a shell (ZnS, CdS).32 The external cover protects the internal structure from oxidation,
which would release the metals from the core.33 QDs find application in such fields as medicine,
biology, and electronics.2
Besides the aforementioned nanomaterials, which are the most often purchased, commercial
suppliers also provide more recently developed materials, which are the results of scientific
research at universities. However, their use in commercial products is peripheral, which is why
they are not discussed at length in this work.
4. Potential ways by which the environment can be exposed to nanomaterials
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The size of production and the broad array of applications of nanomaterials have resulted in
the inevitable presence of these structures in the environment. It is estimated that there are
currently over 1000 products using nanomaterials.34 The projected volume of production for the
years 2011-2020 is 58 thousand tonnes. For comparison, in 2004 this quantity was around 2
thousand tonnes.3
The inflow of nanomaterials into various elements of the environment can come from point
sources or area sources. Point sources are the places where nanomaterials and nanoproducts are
produced, landfills, and waste incineration plants, as well as wastewater treatment plants.12 Area
sources are connected with the release of nanomaterials when using products that contain them.
They may be released, for example, when washing clothes which feature nano Ag,31 or when
paints containing TiO2 are washed off building facades by the rain.35 Nanomaterials may also
enter the environment in the course of its remediation (e.g. nZVI).22,36 Nanomaterials are also
used in agrosystems to increase crop production through the stimulation of plant growth or their
protection from pests and diseases.37 nTiO2 may be released to the environment during its
application to leaves to increase the growth of some plants,38 while nano Cu, when using
pesticides with those nanoparticles.
As already mentioned, both during the use of nanomaterials and after, components of
nanoproducts may directly infiltrate elements of the environment. This way may be lengthened,
e.g., through the mediation of a wastewater treatment plants (WWTP). In such conditions the
effectiveness of eliminating nanomaterials determines what then becomes of them. Research
shows, however, that because of nano size of these new materials, WWTP due to the extent of
new pollution, wastewater treatment plants may have limited capabilities for eliminating
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nanomaterials from wastewater.39 For example, TiO2 particles which are larger than 7 µm are
retained during the treatment processes, while smaller (nano) particles are found in sewage
sludge at the level of 5 to 15 µg L-1.40 This suggests that there is a possibility that nanoparticles
may access river waters. Also, as a result of partial elimination during wastewater treatment,
nanoparticles may be present in sewage sludge. It might lead to their transfer to soils as a result
of using sewage sludge as fertiliser.31 During treatment, nanoparticles present in wastewater may
undergo various processes leading to their transformation or altered characteristics. Kim et al.41
have identified nanosized silver sulfide (α-Ag2S) particles in the final stage sewage sludge
materials of a full-scale municipal wastewater treatment plant. Authors suggested that in a
reduced, S-rich environment, such as the sedimentation processes during wastewater treatment,
nanosized silver sulfides are formed from nano Ag. Kaegi et al.42 investigated the behavior of
metallic silver nanoparticles (Ag-NP) in a pilot wastewater treatment plant (WWTP) fed with
municipal wastewater. Transmission electron microscopy (TEM) analyses confirmed that
nanoscale Ag particles were sorbed to wastewater biosolids, both in the sludge and in the
effluent. Most Ag in the sludge and in the effluent was present as Ag2S as was also observed by
Kim et al.41 To date, this is the only research concerning the transformation of nanomaterials in
the course of wastewater treatment. The presence of NPs in wastewater can lead to the efficiency
decrease of the wastewater treatment process. Studies by Zheng et al.43 show that nZnO has a
negative effect on nitrogen and phosphorus removal during the activated sludge process. The
reason for this was the toxicity of nZnO in respect of the microorganisms of activated sludge. As
shown by the above examples, the fate of nanomaterials in the WWTP is a crucial part of the
environmental risk assessment. The wastewater treatment process also creates favorable
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conditions for the transformation of NPs. Due to interaction with other contaminants present in
the treated wastewater, NPs may undergo transformations. Nanomaterials modified in this way
and released into the environment can affect the environment in other ways than unmodified
types of NPs. The problem remains largely unclear, hence it is important to conduct further
research on the presence of nanomaterials in WWTP. It is especially important to understand the
factors responsible for those transformations and the toxicity of the created structures. The focus
should also be focused towards increasing the efficiency in respect of the removal of
nanomaterials from wastewater to reduce their emission into the environment.
Another potential source of nanomaterials in the environment may also be waste containing
used nanomaterials, or exploited products featuring nanoparticles. Used nanoproducts, during
treatment in waste incineration plants, may release nanoparticles into the atmosphere. It is
assumed, however,44 that the atmosphere is exposed to a lower extent to those kind of
contaminants when compared to other elements of the environment, due to its high capacity, and
the relatively short periods (about 10 days) for which the particles smaller than 100 nm stay in
the atmosphere. The recycling process, to which nanoproducts are subjected, is not free from the
risk of “transferring” nanoelements to secondary products, e.g. the nanoparticles present in
textiles may move to paper products.16
It should be clear from the above examples that at every level of a nanoproduct’s “life,”
nanomaterials may infiltrate elements in the environment, posing a threat to living organisms and
human health.
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5. The direct impact of nanomaterials on living organisms
The presence of nanomaterials in the environment exposes living organisms to their activity.
This problem may be considered at cell level or at the level of the entire organism. One of the
key issues analysed in the context of the potential impact of exposing organisms to nanomaterials
is the latter’s capability to infiltrate various types of cells. At cell level, the infiltration of
nanomaterials into the cell may take place in several ways. It was observed45 that prokaryotic
organisms have limited capabilities for absorbing nanoparticles, which, in theory, should protect
them from the toxic impact of some nanomaterials. Eukaryotes, on the other hand, are more
prone to being infiltrated by nanomaterials. In the case of this group of organisms, nanomaterials
may infiltrate into the inside of the cell by means of diffusion through cell membranes,
endocytosis (pinocytosis, phagocytosis, receptor-mediated endocytosis) or adhesion.12,29
In the cell, nanomaterials may interact with individual organelles, which in turn may interfere
with various metabolic processes.6,9,20 Nanomaterials may also be a direct cause of the
deformation of the elements that make up the cell structure, e.g. cytoplasmic membranes.7,46
Modifications to cells result in changes at the organism level, which may take various forms,
such as inflammations, fibrosis, and may even be lethal.20
Nanoparticles may infiltrate the organism by means of oral intake, but also through inhalation
and skin.28,46 After nanoparticles enter the inside of the organism, they are translocated to
individual organs.47 The capability of nanomaterials to penetrate organisms and their mobility in
the organism is varied. For instance, nTiO2 when breathed in, may cause pneumonia and get to
other organs with blood, but the same oxide has no ability to penetrate the skin, so that their
direct contact with the skin poses no actual threat to the organism.48
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Plants are exposed to the transfer of nanomaterials into them mainly through stomata of
leaves and the root system. In addition, nanoparticles may infiltrate into plants in places where
one of the organs has been physically damaged (root, stem, leaf).12 The ability of nanoparticles to
penetrate plant and fungal cells is determined by the size of pores in cell walls, which ranges
from 5 to 20 nm. Nevertheless Navarro et al.49 observed that nanomaterials, when reacting with
elements of the cell wall, may initiate the forming of new, larger pores, thus increasing the
permeability of the cell wall.
5.1 The mechanisms responsible for the toxic activity of nanomaterials
The ways in which nanomaterials exert toxic effects on the environment have not been
conclusively defined yet. In the current literature one may come across two main hypothetical
reasons that would explain the toxic activity of nanomaterials.50 The first hypothesis assumes
that the toxicity of nanomaterials is caused by metal ions released from nanoparticles.50,51 This
toxicity mechanism is called the free ion activity model (FIAM). There is also an extended
version of the FIAM used, termed the biotic ligand model (BLM). BLM takes into account also
the participation of abiotic and biotic ligands.29 The key role in FIAM/BLM hypothesis fulfils
the ion solubility, which is responsible for the release of ions from nanomaterials.52 The toxic
activity then varies, depending on the type of ion. Metal ions may, for example, act as enzyme
inhibitors (e.g. silver ions, which bond with protein thiol groups, thus deactivating enzymes) or
they may interfere with DNA replication.2
The second variant explains the harmful impact of nanomaterials as a result of the production
of reactive oxygen species (ROS). Free radicals may damage any element of the cell and initiate
the production of a greater number of ROS.2
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As an example, generated free radicals oxidise the double bonds of fatty acids in cell
membranes, which increases the permeability of these membranes, making it more possible for
osmotic stress to occur.12 Reactive oxygen species may also bond with enzymes, thus inhibiting
their activity. ROS may modify the DNA helix, thus inducing the degradation of the cell.12 The
large specific surface area of nanomaterials is capable of producing more ROS than it would in
the case of their bulk equivalents.53
Apart from the potential mechanisms behind the toxicity of nanomaterials, which were
mentioned above, there are additional ones – the destruction of cell membranes, the oxidation of
proteins, genotoxicity, and disturbances in the conduction of energy.2
5.2. The biological response of organisms in the presence of nanomaterials
To date there is a lot of data pointing at the detrimental impact of nanomaterials on living
organisms. The toxicity of nanomaterials was found in relation to diverse groups of organisms –
protozoa (e.g. Tetrahymena thermophila),54 bacteria (Escherichia coli),50 fungi (Saccharomyces
cerevisiae),52 crustaceans (Daphnia magna),55 plants and mammals,13,56 as well as people.57
As mentioned earlier, the response of organisms to the presence of nanomaterials may be
varied, starting from changes at DNA level, cell organelles and individual cells and organs, to
disease in or the death of the entire organism. In the course of research, various effects of
nanostructure activity on living organisms were observed.
Bacteria are one of the most commonly-used groups of organisms in toxicological studies of
nanomaterials. The impact of nanomaterials on bacteria may be of a varied nature. The research
conducted by Li et al.50 showed that the exposure of E. coli cells to the activity of nZnO may
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lead to cytoplasmic membrane deformation and osmotic stress. Wang et al.33 when studying
another group of bacteria, Photobacterium phosphoreum, found that there had been a significant
reduction in their luminescence when exposed to QDs present in the solution (CdSe, CdTe, ZnS-
AgInS2). In the case of Pseudomonas chloraphis Dimpka et al.58 observed the inhibition of their
growth due to the activity of nano Ag. The authors observed5960 that inhibition intensity was
affected by the level of exopolysaccharides (EPS) produced by the bacteria. EPS form a
protective layer which prevents the translocation of nanoparticles into the inside of the cell,
while metal ions are able to neutralise them, which results in their absorption by bacteria.59
Another important issue in the context of the toxicity of nanomaterials, taken up by various
researchers, is determining their mutagenic potential. Such assays most often involve Salmonella
typhimurium and E. coli bacteria (the Ames test). Research revealed mutagenic potential caused
by, i.a., TiO2 and ZnO nanoparticles.60 No mutagenic influence of MWCNTs, however, was
observed by Di Sotto et al.61 in relation to the same group of bacteria.
The influence of nanomaterials on bacteria may also express itself in a different way.
Research conducted by Ge et al62 showed that nZnO and nTiO2 may inhibit the activity of soil
bacteria, which was determined on the basis of substrate-induced respiration and total extractable
soil DNA. Besides their impact on activity, nanoparticles may also induce a change in
microorganism species composition.62 The impact of nanoparticles may be varied depending on
their type. With the same concentration (0.5 mg g-1 soil), nZnO exposed higher toxicity to
bacteria than nTiO2.
Another group of organisms frequently used in ecotoxicology studies are algae. Wang et al.63
established the toxic activity of nTiO2 and QDs to Chlamydomas reinwardtii. The inhibition of
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the growth of these algae already occurred at QDs concentrations at the level of 1 mg L-1. In the
case of nTiO2, its detrimental impact was seen at a concentration of 10 mg L-1, there was also
toxic influence on other algae (Pseudokirchneriella subcapitata).64 It is presumed that the
inhibiting influence of nanoparticles on algae is caused by the adsorption of nanoparticles on the
surfaces of their cells. This is an obstacle to the inflow of nutrients to these organisms.64 Gong et
al.65 who subjected Chlorella vulgaris algae to the activity of nNiO observed the inhibition of
cell growth. They also noted, however, that living algae accelerate the aggregation of
nanoparticles and the reduction of NiO to metallic Ni, which reduced the detrimental effects of
nNiO. Schwab et al.66 found that, with the same CNT concentrations, the extent of their
influence on green algae Chlorella vulgaris and Pseudokirchneriella subcapitata was varied. The
inhibition of the growth of algae was caused to a greater extent by shading by CNTs, and the
aggregation of CNTs with the green algae cells, than by the type and age of CNTs, or the species
of green algae. The aggregates forming between CNTs and green algae cells reduced the
availability of light to cells.
In tests involving higher plants, there is a division into tests with aquatic and land plants.
Among higher the aquatic plants an important group is duckweeds. In the case of Landoltia
punctata duckweed, exposed to the activity of nCuO, a considerable decrease in the content of
chlorophyl was observed, with nCuO concentration at the level of 1 mg L-1.6 As for Lemna minor
duckweed, which was exposed to the activity of nano Ag, clear inhibition of the plant’s growth
was observed, resulting in the reduction of the frond number and dry weight.67
In assessing the nanoparticles toxicity to land plants, the most frequently-used parameters are
the inhibition of germination and the inhibition of root growth. The negative effect of
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nanoparticles on these two parameters in the long term may lead to the lower production of
edible plants. Yang and Watts13 assessed the impact of nano Al on the growth and development
of corn (Zea mays), soybean (Glycine max), carrot (Brassica oleracea), cucumber (Cucumis
sativus) and cabbage (Brassica oleracea). Additionally, the potential impact of other
contaminants, i.e. phenanthrene, on the toxicity of nano Al was also assessed. It was found that
nano Al containing phenanthrene were characterised by lower toxicity than nano Al not
containing this compound. Probably, the presence of phenanthrene resulted in the elimination of
free radicals from the surface of nano Al, which were responsible for the inhibition of root
growth. The inhibition of germination and root growth in higher plants in the presence of
nanoparticles was also observed in other studies.10,68,69 Lin and Xing68 concluded that in the
presence of nano Zn and nZnO there occurs significant inhibition of germination and root growth
in radish (Raphanus sativus), rape (Brassica napus), ryegrass (Lolium perenne), lettuce (Lactuca
sativa), corn (Zea mays), and cucumber (Cucumis sativus). Lee et al.70 investigated the effects of
four metal oxide nanoparticles, aluminum oxide (nAl2O3), silicon dioxide (nSiO2), magnetite
(nFe3O4), and zinc oxide (nZnO), on the development of Arabidopsis thaliana (Mouse-ear cress).
Among these particles, nZnO was most phytotoxic (the highest inhibition of seed germination
and root growth inhibition), followed by nFe3O4, nSiO2, and nAl2O3, which was not toxic.
Inhibition of seed germination by ZnO depended on particle size, with nanoparticles exerting
higher toxicity than larger (micron-sized) particles at equivalent concentrations. Lopez-Moreno
et al.69 established the toxic impact of nCeO2 on four plant species, alfalfa (Medicago sativa),
corn (Zea mays), cucumber (Cucumis sativus), and tomato (Lycopersicon esculentum). In three
plant species (corn, cucumber, tomato) there was lower germination of seeds at the nCeO2
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concentration of 2000 mg L-1. The impact of nCeO2 on root growth was more varied.
Specifically, in corn and cucumber it was found that nanoparticles stimulate root growth, while
in the case of alfalfa and tomato this growth was inhibited.
Apart from germination and root growth inhibition, the negative impact of nanoparticles on
plants may also appear itself in a different way. Sabo-Attwood et al.10 after 14 days of exposure
to 3.5 nm nano Au observed leaf necrosis of tobacco (Nicotiana xanthi). Kumari et al.8 noted the
cytotoxic influence of nano Ag on Allium cepa onion cells. The authors found an inhibition of
cell divisions in the cells of the root ends of the plant under assessment. It resulted in a reduction,
in the presence of nanoparticles, of the mitotic index from 60% to 27%. Asli and Neumann71
showed a detrimental impact of nTiO2 on corn, which was visible in reduced transpiration and
inhibited leaf growth. The possible cause was interaction of nTiO2 with the cell walls elements,
which posed an obstacle to the transport of water to the cells of the studied plants.
It should be mentioned here that the presence of nanomaterials may also stimulate the growth
and development of plants. This type of phenomenon, called hormesis, was observed in relation
to organic contaminants and heavy metals.72 Hormesis is a dose response phenomenon
characterised by low dose stimulation and high dose inhibition. In the case of plants it is
explained by the possibility of pollution acting as activators of their growth.73 It follows from the
research by Barrena et al.74 that small doses of nano Au had a favourable effect on the
germination of cucumber and lettuce seeds.
Another group of organisms which is widely used in experiments assessing the toxicity of
nanomaterials is crustaceans. Water flea (Daphnia magna), when exposed to nTiO2, showed
limited growth and reduced reproduction. The presence of nanoparticles had a negative impact
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on the assimilation of food by this organism, which should be considered another effect of the
activity of this group of materials.55 Li et al.75 when studying the toxicity of TiO2 and Al2O3
nanoparticles to Ceriodaphnia dubia on the basis of energy budget distribution, observed that
while concentrations of these particles increase, the amount of energy assimilated by these
organisms decreases. The authors claim that it can suggest a higher energy consumption for life
processes by C. dubia in the presence of nanoparticles, as compared to the control conditions.
Wang et al.76 did not observe any toxic impact of nAl2O3 on C. dubia. On the other hand,
subjecting new born Daphnia magna to the activity of C60 resulted in increased mortality among
young organisms over time. Females which were exposed during pregnancy were found unable
to reproduce in the future.77
Amphibians are a group of organisms relatively less often subjected to tests of toxicity in the
context of nanoparticles. Research has shown, however, that this group of organism may undergo
detrimental changes as a result of exposure to nanomaterials. Mouchet et al.78 using Xenopus
laevis (the African clawed frog) as the test organism, found occlusion of the digestive system of
this organism in the presence of MWCNTs. The teratogenic potential of commercially available
nCuO, nTiO2 and nZnO to X. laevis was also evaluated by Bacchetta et al.79 Except for nCuO,
which was found to be weakly embryolethal only at the highest concentration tested, the
nanoparticles did not cause mortality at concentrations up to 500 mg L-1. However, they induced
significant malformation rates, and the gut was observed to be the main target organ. On the
other hand, the research of Nations et al.80 shows the ambivalent nature of nZnO’s activity
towards X. laevis. Namely, the nZnO concentration of 2 mg L-1 resulted in an increase in frog
mortality by 40%. Such a concentration of nanoparticles also caused disturbances in the process
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of the frog metamorphosis. The authors concluded, that at low nZnO concentrations (i.e. 0.125 g
L-1), nanoparticles stimulated the growth and development of X. Laevis.
In higher order organisms, the presence of nanoparticles may induce changes in gene
expression. This type of response to the presence of nano Ag in an aquatic environment was
observed by Chae et al.81 to Oryzias latipes (Japanese medaka). The research by Blirgen et al.82
on Carassius carassius (Crucian carp) and Perca fluviatilis (Eurasian perch) shows that nano Ag
may be toxic to the olfaction, which results in the reduced ability to seek food, reproduce, and
protect against predators. Wang et al.14 observed the impact of nTiO2 on the reproduction of
Danio rerio (Zebrafish). After 13 weeks of exposure to nanoparticles an almost 30% reduction
was noted in the amount of D. rerio eggs produced. Reproductive toxicity in the presence of
nTiO2 may be a result of the direct impact of nanoparticles on roe, or indirect, by disrupting
vitellogenesis.
With regard to mammals, experiments most often involve mice and rats. Similar to lower-
order organisms, here the negative impact of nanoparticles was also observed. Mice exposed to
nZnO experienced spleen damage and pancreatitis.83 The exposure of this organism to nTiO2
nanoparticles caused liver and heart damage.11 Rats subjected to nCeO2 inhalation had those
nanoparticles present in their lungs, which resulted in inflammation.84
Determining the impact of nanomaterials on human health is mainly based on model studies
using susceptible animals (mice, rats, hamsters). The potential toxicity of nanomaterials to
humans is also determined on the basis of similarity with other harmful compounds (e.g. asbestos
to CNTs). Research on the toxicity of nanomaterials to humans that would prove their
detrimental effect on human health is still scarce.85
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As shown earlier the response of organisms to the activity of nanoparticles may vary
depending on the organism. Similarly, the extent of toxic impact is varied, depending on the type
of nanoparticles. Numerous studies show that the response of organisms to the activity of various
nanomaterials assumes various scales of intensity. Adams et al.86 when studying the antibacterial
characteristics of selected nano metal oxides (nZnO, nTiO2, nSiO2) in relation to gram-positive
B. subtilis and gram-negative E. coli bacteria, noted the highest susceptibility of bacteria to
nZnO, then nTiO2, and finally to nSiO2. The case was similar with algae (Pseudokirchneriella
subcapitata)87 and protozoa (Tetrahymena thermophila)54 for which nZnO showed higher
toxicity in comparison to nCuO. In Wang et al.’s research33 a varied toxicity of QDs to
bioluminescent bacteria was also noted in the following order - CdSe>CdTe>ZnS-AgInS. The
authors explain the varied toxicity of the tested materials with the nature of ions present in the
structures of the QDs studied. Cadmium, selenium, and tellurium ions are characterised by a
higher toxicity than silver, zinc, and indium ions.33 A study by Galloway et al.88 showed the toxic
activity of nTiO2 on lugworm Arenicola marina, while SWCNTs did not have harmful effects.
The varied impact of metal oxides was also observed in the case of other organisms, the already-
mentioned X. laevis. X. laevis exposed to metal oxides showed varied symptoms depending on
the type of nanoparticles. The presence of nCuO and nZnO in the concentration of 10 g L-1
caused inhibition in the organism growth, causing developmental malformations of the guts and
spleen. It was observed, however, that the extent of the detrimental impact in the case of nZnO
was considerably higher than for nCuO. Other nanoparticles tested in the quoted study (nTiO2
and nFe2O3) did not exhibit toxicity to X. laevis.89
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6. Bioaccumulation of nanoparticles by biota
Apart from the impact of nanomaterials on living organisms, which is found in their direct
toxic activity, there is a threat of their bioaccumulation in the successive level of the food
chain.20,29 On the one hand this may lead to harmful effects being delayed in time, and on the
other, it may accumulate the pollution load in successive organisms. As a result of this process,
the concentration of nanoparticles may increase to a level that shows a clear detrimental impact.
Numerous studies prove that nanomaterials accumulate in the tissues of living organisms. A wide
range of such research has been conducted on the earthworm - Eisenia fetida. It is no
coincidence that these organisms have become the object of numerous toxicology studies in the
context of trophic transfer. E. fetida, by feeding on organic matter, is one of the level in the
detritus food chain, which makes it a kind of link between the environment and higher-order
consumers.38
Accumulation of a wide range of nanomaterials (e.g. nano Au,90 nano Ag,91 nTiO2 and
nZnO,92 QDs93 as well as fullerenes94) has been shown by many researchers. Furthermore, the
studies carried out by Hu et al.92 showed that besides the bioaccumulation of nTiO2 and nZnO,
these nanoparticles in the concentration higher than 1 g kg-1 of soil may have a harmful impact
on E. fetida. Some of the effects observed were the inhibition of cellulose activity, damage to
mitochondria and DNA, and oxidative stress. The research on the bioaccumulation of
nanomaterials should also be focused on indentifying in which parts of the organism they
concentrate. Lin and Xing95 observed that nZnO after uptake by roots of ryegrass is not
translocated to the aerial part of the plant, as proved by the low translocation factor (TF<0,02).
Therefore, if the aerial part of the plant is the only one “utilised”, then there is no real risk of
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nZnO finding its way into the trophic transfer. Research shows96 that the extent of
bioaccumulation may depend on the nanomaterial’s properties. This is supported by Coutris et
al.,96 whose research involved an assessment of the bioaccumulation of nano Co and nano Ag by
E. fetida. After a 4-week period of exposure the worms assimilated with food 69% of nano Co
and only 0.4% of nano Ag. Also the rate of the removal of nanoparticles differed between these
nanoparticles. In particular, nano Ag was fairly rapidly excreted from the organism, while
following a 4-month period E. fetida excreted only 32% of the cobalt they received from their
organisms. The authors96 suggested that this was caused by the higher solubility of cobalt
nanoparticles, and, therefore, increased Co ion release, the high concentration of which was
found in the blood and the digestive tract of earthworm. In the study carried out by Domingos et
al.93 Chlamydomonas reinhardtii (green alga) was exposed to either a soluble Cd salt or QD at
similar concentrations of total Cd. QD were shown to be taken up by the cells and to provoke
unique biological effects. Whole transcriptome screening using RNA-Seq analysis showed that
the free Cd and the QD had distinctly different biological effects. Pipan-Tkalec et al.97
investigated the activity of Zn from various sources (unmodified nano ZnO, ZnO macropowders,
and the ZnCl2 solution) on the Porcellio scaber isopod. The results obtained by the authors
showed that the level of bioaccumulation of these compounds is not only determined by the
source of the Zn, but also by the solubility of these nanoparticles. Zhu et al.98 observed
significant bioaccumulation of nTiO2 in D. magna which was associated with the slow excretion
of nanoparticles from the organism resulted in difficulties in absorbing food, which then led to
malnutrition. Petersen et al.99 did not find significant bioaccumulation, either in MWCNTs or in
MWCNT with polyetheyleneimine in E. fetida, perhaps due to nanomaterials being excreted
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from the organisms in a relatively short time. The problem of the accumulation of nanomaterials
is inherently instrumental in forecasting the dangers connected with the presence of the said
nanomaterials in the environment. Nanomaterials accumulated in organisms may be a
“secondary” source of contamination. After excretion from the organism, or upon their perishing,
the nanomaterials may continue to pose danger to the environment. So far, this aspect has not
been addressed in the studies. It is also important to note the fact that nanomaterials accumulated
by an organism can undergo various transformations while inside that organism, e.g. react with
the building materials of cells. The studies show100 that nano-Ag capped by bacterial
extracellular proteins become stabilized, which can potentially cause higher levels of toxicity in
the environment.
As stated above, bioaccumulation may also be connected with the risk of increasing the
concentration of nanoparticles, transferred to successive level in the food chain called
biomagnification. Judy et al.101 observed an increased in nano Au (with diameters of 5, 10, 15
nm) concentration by trophic transfer from Nicotiana tabacum L. cv Xanthi (producer) to
tobacco hornworm Manduca sexta (consumer). The extent of the bioaccumulation of nano Au in
the tissues of tobacco hornworms was significantly affected by the size of the nanoparticles. The
highest bioaccumulation was found with nano Au of 10 nm in diameter, then 15 nm, and 5 nm.
In the majority of the model research performed to date on simple trophic chains, although
trophic transfer of nanomaterials was confirmed, no biomagnification was observed. For
example, Zhu et al.98 did not observe this phenomenon when they studied the trophic transfer of
nTiO2 from Daphnia magna (crustaceans) to Danio rerio (zebrafish). An explanation suggested
by the authors is the rapid removal of nTiO2 from the organism of D. magna. The research
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carried out by Holbrook et al.102 involving the transport of QDs within the following trophic
chain – E. coli (bacteria)-Tetrahymena pyriformis (ciliate)-Brachionus calyciflorus (rotifer) –
also showed the absence of biomagnification.
Some authors suggest29 that metal nanoparticles may be more available to higher-order
consumers, when compared to direct exposure. For example, metallic nanoparticles adsorbed on
the surface of the gastrointestinal epithelium may be covered with surfactants secreted by
digestive glands, which facilitates the assimilation of these nanoparticles by higher-order
consumers.29 Living organisms also have the ability to modify the characteristics of the
nanomaterials assimilated. In the experiment by Roberts et al.103 D. magna accumulated
SWCNTs covered by lysophophatidylcholine (LPC-SWCNTs) with food. Digesting of the LPC
covering changes the solubility of SWCNTs, which after excreting from the organism, may be
toxic to other aquatic organisms.
7. Factors affect nanomaterial toxicity
The difficulty in assessing the risk connected with the presence of nanomaterials in the
environment is caused by the complexity of factors determining their harmful activity. The
toxicity of nanomaterials is a combination of their properties, environmental conditions, and the
already-mentioned natural tolerance of living organisms to the presence of these structures.21
7.1. Properties of nanomaterials and their toxicity
It follows from numerous studies that the same compounds in the nano scale display a higher
toxicity than their bulk equivalents.104 There are, however, contrary opinions on this issue. The
authors87,105 who did not find size-dependent toxicity towards various organisms, see size as the
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factor that triggers the domino effect, i.e. determines the physico-chemical and biological
properties of nanomaterials. These properties, in turn, determine the behaviour of these
compounds in the environment and their potential toxicity. The nano size of compounds entails a
higher specific surface area than is the case in their bulk equivalents. The consequences of a
higher surface-area-to-volume ratio include changes in the in the physico-chemical and optical
properties, as well as changes in nanomaterial reactivity.24 The smaller the particles of metal
oxides or metal, the more susceptible they are to oxidation and dissolution, which may also
determine their toxic activity.24,105 Size may also be treated as a barrier which prevents
penetration by nanomaterials of organisms or organs. E. coli bacteria cells exposed to silver
nanoparticles of medium size of about 21 nm, absorbed only those particles with a diameter of
less than 5 nm.106
A significant parameter that potentially affects the characteristics of nanomaterials is also
shape, which, up to some extent, may contribute to the threats connected with their use. Studies
by Hsiao and Huang107 on the cytotoxicity of nZnO showed that at longer exposures rod-shaped
particles display a higher toxicity than sphere-shaped particles. Also the experiments by Peng et
al.108 performed on Thalassiosira pseudonana, confirm this observation.
7.2. Nanomaterials aggregation and deposition
The mobility of nanoparticles in the environment is controlled by their aggregation and
deposition rates. The susceptibility of nanomaterials to aggregation results in the decreased
mobility of these structures, thus limiting bioavailability, and thereby the toxic effects exerted on
organisms.22,35,108 Aggregation intensity is negatively correlated with particle size.20 The smaller
the size/diameter of nanoparticles, the higher their “eagerness” to undergo aggregation.
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Furthermore, aggregation affects other characteristics of nanomaterials, such as reactivity and
mobility in the environment. For example, aggregates composed of lead sulphide nanoparticles
are characterised by lower solubility due to the limited availability of the surface of those
compounds which form conglomerates.109 It should then be assumed that their impact on
organisms will be lower than that of non-aggregated particles. Limiting the surface area also
reduces the number of occurrences of contaminants potentially adsorbed by nanoparticles.21,110
The course of the aggregation of nanomaterials is affected by such factors as:111-114 pH, ionic
strength, the presence of organic matter and surfactants, salinity, and the type of cations present
in the solution. The aggregation of nanoparticles is negatively correlated with pH. Saleh et al.111
suppose that the decreased aggregation of MWNTs, which progresses as pH increases, is caused
by the dissociation of surface functional groups in MWCNTs. An increase in ionic strength
decreases the repulsive force between particles, which, in turn, is conducive to their
aggregation.114 The presence in the solution of monovalent and divalent cations favours the
aggregation process of nanomaterials. The critical coagulation concentration (CCC) may be used
to measure their influence on the aggregation process. The CCC values for mono- and divalent
cations differs considerably. Saleh et al.111 stated that in the case of MWCNT aggregation, CCC
for NaCl, CaCl2, and MgCl2 was 25 mM, 2.6 mM, and 1.5 mM, respectively. Chen and
Elimelech,115 when studying the kinetics of C60 aggregation, observed an even greater difference
in CCC between monovalent (NaCl – 120 mM) and divalent (CaCl2 - 4.8 mM) cations.
In uncontrolled conditions that exist in the environment it is possible for heteroaggregation to
occur. Heteroaggregation involves the forming of aggregates of nanoparticles with compounds of
a different nature, such as NOM, clay, and microorganisms. The interactions between
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nanoparticles and NOM have a positive impact on the stability of the solution. As due to -
type bonds, fractions of organic matter such as humic acids, are adsorbed on the surface of
MWCNT, which prevents homoaggregation. Nanoparticle conglomerates with bacteria, besides
limiting aggregation, may also lead to the dispersion of the already-formed aggregates.109
Heteroaggregation may positively influence the mobility of nanomaterials. For example, clay,
which forms conglomerates with nZVI is conducive to their transport.109
Complex aggregates formed of nanoparticles become heavier, which facilitates their
deposition because of gravity. Deposited nanoparticle aggregates are less toxic in comparison to
their dispersed forms due to limited mobility. However, the deposition of aggregates does not
eliminate the threat of their continued activity. As a result of changing environmental conditions,
conglomerates may become dispersed, thus “recovering” their toxicity potential.109
7.3. Effect of organic matter on nanomaterials toxicity
The presence of natural organic matter (NOM), composed of thousands of organic
compounds (e.g. organic acids, sugars and other carbohydrates, cellulosic materials, alginate,
proteins, lipids, etc.), in all natural aqueous matrices has a profound effect on the charge balance
of the NPs, and thus on their mobility, deposition behavior as well as toxicity. As mentioned
earlier, NOM positively affects the stability of nanomaterials. For example, MWCNTs achieved
a greater stability in the presence of NOM than they did with surfactants.109 The adsorption of
NOM on the surface of nanomaterials brings about a change in the surface charge and an
increase in repulsive forces between nanoparticles. This leads to the limited availability of
nanomaterials to living organisms. Chen et al.116 recorded a significant decrease in the toxicity of
nZVI in relation to E. coli and B. subtilis in the presence of NOM. The studies has shown that
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NOM influences the reduction of adhesion between nanoparticles and bacteria cells. Also Van
Hoecke et al.117 observed reduced toxicity of nCeO2 in the presence of NOM in the case of
Pseudokirchneriella subcapitata. Authors attribute the reduced toxicity to the lower
bioavailability for algae of nanoparticles covered with NOM. Edgington et al.118 on the other
hand, noted an increase in MWCNT toxicity to D. magna in the presence of NOM during 96
hours of exposure. The authors suggest that the increased toxicity was caused by obstructing the
digestive tract of D. magna by the ingested complex NOM-MWCNTs.
7.4. The functionalization of nanoparticles
Apart from their characteristic properties, typical of nanomaterials, they are subjected to
functionalization. This process aims at adding functional groups, which change the properties of
the nanomaterials, adapting them to a particular purpose. Thus the functionalization of
nanoparticles through changes in their properties influences their mobility in the environment,
and indirectly also their toxicity.
Susceptibility to aggregation lowers the ”use value" of nanomaterials, as it decreases their
specific surface area and limits their mobility. In order to prevent this phenomenon,
nanomaterials are often covered with surfactants. As a result of this procedure the surface charge
and repulsive forces between particles increase.109 This limits the aggregation of nanoparticles,
thus prolonging the effectiveness of their operation. For example, in order to prevent nZVI
aggregation, their surface is covered with carboxymethylcellulose (CMC).119
In order to increase the reactivity of nanoparticles, e.g. nZVI are combined with noble metals
such as Pd, Ni, Pt, Ag. Research shows that the resulting structures, called bimetals, can fix
pollutants faster than any of their bare equivalents.120
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The issue of the functionalization of nanomaterials, especially of CNTs, by the addition of
functional groups, is widely analysed.121-123 The modification of CNTs surface with the
hydrophilic groups (-OH, -COOH, O3) may occur spontaneously in the environment, changing
the properties of nanomaterials. Adsorption of hydrophobic organic compounds (atrazine,
phenanthrene, lindane) by MWCNTs functionalized with –OH groups was lower than in the case
of nanomaterials with the original structure.121 Chen et al.122 also observed a decrease of atrazine
adsorption by functionalized MWCNTs with different oxygen content. The phenomenon of the
lower ability to adsorb HOCs of functionalized CNTs has not been fully explained. The most
common hypothesis is the reduction of hydrophobic reactions as one of the main machanisms of
the sorption of hydrophobic organic compounds by CNTs. However, as research shows,123 the
sorption of nitrobenzene by MWCNTs was higher than of toluene and benzene, even though they
were more hydrophobic compared to nitrobenzene.123 The reduction in adsorption capability of
CNTs as an effect of the functionalization is also explained by the decrease in the number of
active sites which are potentially available to the pollutants.121 Functionalization of CNTs by
adding hydrophilic groups makes them less useful adsorbents for water remediation.
All these ”improvements” of nanoparticles leading to the increase in their functionality as
mentioned earlier, simultaneously make nanoparticles become more mobile, which can increase
their toxic activity. For example, surface-modified gold nanoparticles which have been covered
with peptides are more easily adsorbed by cells.124 Because of the hydrophilic functional groups,
CNTs easily dispergate and became more accessible to organisms. For example, in the algae
Dunaliella tertiolecta exposed to functionalized CNTs growth inhibition was observed, probably
as a result of the disturbance of the photosynthesis process.125
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However, the functionalization of nanoparticles can also have a positive effect. Xiu et al.126
investigated the effect of bare and coated nZVI with olefin maleic acid copolymer (a common
approach to enhance its mobility in aquifers) on tceA and vcrA gene expression in
Dehalococcoides spp. Both tceA and vcrA were significantly down-regulated after 72-h
exposure to bare-NZVI. However, coating NZVI with copolymer overcame this significant
inhibitory effect. nSiO2 covered with a layer of aluminium is also characterised by a lower
toxicity to Pseudokirchneriella subcapitata than nanoparticles without the addition of
aluminium.127
7.5. The other environmental factors
The toxic effect of nanomaterials is also influenced by environmental factors. The influence
of these factors can vary significantly. On one hand they can reduce the negative effects caused
by nanomaterials, on the other, they can intensify them. The presence of NOM, ionic strength
and pH, as mentioned earlier, influence the processes of aggregation and adsorption, which
determine the bioavailability and toxicity of nanomaterials.
The natural constituents present in the environment (e.g. salts) can increase the aggregation
of CNTs, reducing their harmful activity.128 ZnO nanoparticles, in the presence of silica,
commonly present in the environment, are becoming less soluble, therefore less available to
living organisms.44 A significant influence on the toxic effect of nanomaterials may also be
caused by the access of light. Lee et al.70 stated that in favourable lighting conditions the toxicity
of QDs towards D. magna may be increased. The decisive factor in respect of the immunity of
organisms to the activity of nanomaterials may also be the availability of nutritional
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substances.46,105 As research shows46 the supply of nutritional substances increased the tolerance
of E. coli to the toxic activity of nZnO.
The influence of the matrix (water, soil, sediments, sewage sludge) is not insignificant for the
toxicity of nanomaterials. In the end it is these elements of the environment that the nanoparticles
will find their way to. On the one hand the mobility and toxicity of nanoparticles may vary under
the influence of properties of a given matrix, on the other the presence of nanomaterials may to a
certain extent determine its properties. This issue is relatively new and studied to a small extent.
The physical, chemical or biological properties of the matrix can significantly determine the
toxicity of nanomaterials, affecting their mobility or bioavailability. So far the only sparse
research shows that the prescence of CNTs depending on the type of sewage sludge can increase
or decrease its phytotoxicity.129 The authors suggest that the positive influence of the CNTs is a
result of binding pollutants present in sewage sludge, which earlier had a negative influence on
plants. Chung et al.130 investigated the short-term effect of MWCNTs on the activity and biomass
of microorganisms inhabiting two different soil types (sandy and loamy). The authors established
varied influence of CNTs, depending on the type of soil in the case of almost all the tested
parameters.
7.6. The synergistic and antagonistic activity of nanoparticles with other contaminants
Nanomaterials as adsorbents may be treated ambivalently. On one hand they exhibit higher
efficiency of adsorption of pollutants than the other commonly-used adsorbents, i.a. active
carbon.131 On the other hand the well-developed adsorption properties of nanomaterials may be
the factor which intensify their toxic activity. Nanomaterials turn out to be useful as the
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adsorbents of a wide range of pollutants: dioxins,20 dyes,132 PAH,99,133 and trihalomethanes
(THMs).134 The pollutants adsorbed by nanoparticles can permeate to the environment and create
problems which have not been identified so far. It can be assumed that in such conditions,
nanoparticles can play the role of a carrier of organic pollutants transferring not only pollutants
adsorbed in the environment (from site to site) but also making bioaccumulation of such
pollutants by the organisms easier. In the environment, the pollutants adsorbed, can be resistant
to biological decomposition. However, in the variable environmental conditions or in an
organism, such pollutants can be gradually released which may lead to environmental pollution,
illness or death of the organism concerned.135 Reduction of toxicity in presence of carbon-based
nanomaterials is related to their high adsorption capacity towards many contaminants. The
adsorption of pollutants by carbon-based nanomaterials significantly reduces their bioavailability
and therefore also the toxic activity of pollutants to the organisms.136 Park et al.137 stated that the
bioavailability of 17-ethinylestradiol (EE2) to D. rerio was reduced by the increasing
concentration of nC60, and the bioavailability of EE2 decreased further after aging 28 d with
nC60.
The possible syngergistic or antagonistic interactions between nanomaterials and different
contaminants are presented in Table 1. A fundamental role in the toxic response to nanoparticles-
other contaminants is played by the properties of the contaminants. This mechanism has not been
fully explained yet. For example Baun et al.138 observed a significant reduction in the toxicity of
pentachlorophenol in the presence of fullerenes, while in case of phenanthrene an increase of
bioaccumulation and toxicity of this compound to D. manga was noted. A similar diversity, but
pertaining to other compounds, was observed by Brausch et al.139 The increase in acute toxicity
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to D. magna in presence of fullerenes was noted in the case of bifenthrin, while fullerenes did
not affect the toxicity of tributyl phosphate.139 The potential acute toxicity of the interaction
between nTiO2 (50 and 120 nm) and lead acetate (PbAC) in adult mice was investigated by
Zhang et al.140 There were no significant changes of the body weight coefficients of liver, kidney
and brain. However, the results of liver function and nephrotoxicity examination revealed that
there were serious damages to liver and kidney between the group treated with the mix
suspension and the one with TiO2. Authors stated that PbAC may increase the acute toxicity of
TiO2 nanoparticle in some degree with is probably related to oxidative damages.140 Wang et al.141
studied the combined toxicological effect of TiO2 nanoparticles and As(V) in relation to the
Ceriodaphnia dubia crustacean. Arsenic is a highly toxic contaminant found in groundwater in
many regions in the world. Results showed that in the presence of low concentrations of nTiO2,
the toxicity of As(V) increased significantly. The toxicity of nano-Al2O3, inorganic As(V), and a
combination of both to C. dubia as the model organisms was also examined.76 nAl2O3 particles
alone did not have significant toxic effect on C. dubia. However, nAl2O3 particles significantly
enhanced the toxicity of As(V). Kim et al.142 examined the effect of a combination of soluble Cu
and surface-modified SWCNTs on D. magna. The toxicity of the SWCNTs–Cu mixture was
determined to be additive. The addition of nontoxic concentration of SWNTs enhanced the
uptake and toxicity of Cu. Greater amounts of Cu were shown to accumulate in D. magna upon
addition of 0.5 and 1.0 mg L-1 SWNTs. Unfortunately there are still few studies that would
determine the synergic or antagonistic effects of nanoparticles and other common contaminants.
Nanomaterials can nevertheless play the role of carriers of adsorbed contaminants and act as
a “Trojan Horse”, i.e. the adsorbed compounds get through to the inside of the cell along with
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nanomaterials, where they can undergo desorption. Oleszczuk et al.135 noted that changes in
environmental conditions (e.g. pH) increased the desorption rate of two pharmaceuticals
(oxytetracycline and carbamazepine), which may have subsequently resulted in potential health
and environmental risks. In the simulation model of gastrointestinal fluid composed of pepsin
and bile salts, the rapid (in less than an hour) desorption of phenanthrene was observed from
CNTs.143 This experiment shows that bioparticles occurring in living organisms and participating
in digestive processes may support the release of pollutions from CNTs, thus inducing their
direct influence on the host organism. The research carried out by Wild and Jones144 showed that
CNTs pierce plant cells. CNTs play the role of a nanometric channel which allow contaminants
(in this case phenanthrene) to get inside to plant cell.
It is also worth emphasising that, apart from the direct impact of nanoparticles on toxicity in
relation to various groups of organisms, the influence of nanomaterials may also be indirect. One
trophic link remaining under toxic effect can influence all the components of biocenosis through
the restriction of feeding. Numerous studies have shown the toxic influence of nanomaterials on
the microbial community of rivers145 and soils.146 Having a toxic effect on the soil micro-
organisms, the nanomaterials can lower their enzymatic activity, which affects the nutrient
cycling. MWCNTs applied to the soil in the dose of 5000 µg∙g-1 significantly reduced enzymatic
activity and microbial biomass130. As a result, soil conditions change, which negatively
influences the growth and development of plants and impede the functions of the organisms
present in the soil. The strong sorption properties of nanomaterials (CNTs), which is one of their
positive qualities that is used for adsorption of contaminants, may also reduce the availability of
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the nutrients to plants.23Nanomaterials may interact with e.g. soil nutrients, thus limiting their
availability to plants or microorganisms.24
7.7. The predispositions of living organisms
Complementing the final biological response of organisms exposed to nanomaterials is their
natural tolerance to the presence of released compounds. For example, S. cerevisiae yeast is
characterised by high immunity to the activity of Zn2+ ions, which are released from nZnO.52 The
age of organisms may also predispose them to greater susceptibility to the toxicity of
nanomaterials. Van der Ploeg et al.147 exposed Lumbricus rubellus earthworms to the activity of
fullerenes. This experiment showed that juveniles are more susceptible to the harmful effects of
those nanomaterials than adult earthworms. Chen et al.56 established that the toxicity of nano Cu
to mice, and the intensity of toxic symptoms, also depended on gender. Namely, male specimens
were more susceptible to pathologic changes in organs (kidneys, spleen, liver) than female
specimens.
8. Conclusion
Today, nanotechnology is one of the most promising branch of science, which is evidenced
by the growing numbers of nanoproduct purchasers. Therefore, it should be expected that
nanoparticles will soon become a serious pollutant. The manufactured nanomaterials carry a risk
of toxicity to living organisms, due to their different chemical composition in comparison to
natural materials, and also due to their peculiar characteristics, which are “designed” with
specific applications in mind. Furthermore, the volume of the production of nanomaterials is
conducive to the propagation of those compounds in the environment, increasing the possibility
of living organisms coming into contact with nanomaterials.
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Nanomaterials absorbed by living organisms are translocated to various organs, where they
display toxic activity at cell level, the mechanism of which has not been conclusively
determined. The two dominant hypotheses as to the reasons for this phenomenon assume the
specific toxicity of ions released from nanomaterials and the production of reactive oxygen
species by those structures.
The final response of organisms exposed to nanomaterials is, apart from the peculiar
properties of the latter, is also determined by environmental conditions, and the natural tolerance
of organisms to the nanomaterials activity. That is why the assessment of the potential threat that
arises from the presence of manufactured nanomaterials in the environment must take into
account the above components. On the basis of the available literature it should be assumed that
a relatively poorly-studied problem, with prospects for further research, in the field of
nanoparticles, is defining the interaction of nanoparticles with other pollutants and the impact of
this type of structures on mobility and toxicity in relation to various groups of organisms.
Another important direction for research is undoubtedly determining the influence of the matrix
(soil, sewage sludge) on the mobility, bioavailability, and toxicity of nanoparticles, as well as the
influence of nanoparticles on the characteristics of the matrix.
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(Lumbricus rubellus) and implications for population dynamics. Environ. Pollut., 159,
198-203.
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Table 1. Syngergistic or antagonistic effect of different nanomaterials with organic and inorganic
contaminants
Nanomaterials Compounds Organisms Effect Effect
Fullerene (C60) 17-ethinylestradiol
(EE2)
Danio rerio + Bioavailability of 17-ethinylestradiol (EE2) to zebrafish (
rerio) was reduced in presence of C
Fullerene (C60) pentachlorophenol Daphnia magna + Decrease toxicity of pentachlorophenol
Fullerene (C60) phenanthrene Daphnia magna Increase toxicity of pentachlorophenol
Fullerene (C60) bifenthrin Daphnia magna Increase acute toxicity of bifenthrin
SWCNTs Cu Daphnia magna SWNTs enhanced the uptake and toxicity of Cu
nTiO2 As (V) Ceriodaphnia dubia The toxicity of As (V) increased significantly
nAl2O3 As (V) Ceriodaphnia dubia nAl2O3 enhanced the toxicity of As (V)
nTiO2 lead acetate mice Possibile accumulation of Ti and Pb in liver, kidney and brain
nTiO2 Cd Cyprinus carpio (carp) nTiO2 enhanced accumulation of Cd in carp
+ positive, negative effect
FIGURES CAPTION
Figure 1. Estimated global production of various nanomaterials (tonnes per year) in 2020
(soruce: Royal Society and Royal Academy of Engineering Report, 2004)
Figure 2. The impact of the nanomaterials on the living organism
Figure 3. Classification of nanoparticles (NPs)
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Figure 4. Contribution of nanomaterials in different commercial products in year 2008 (source:
Consumer Products Inventory)
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Figure 1. Estimated global production of various nanomaterials (tonnes per year) in 2020
(soruce:Royal Society and Royal Academy of Engineering Report, 2004)
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Figure 2. The impact of the nanomaterials on the living organism
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Figure 3.Classification of nanoparticles (NPs)
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Figure 4.Contribution of nanomaterials in different commercial products in year 2008 (source:
Consumer Products Inventory)
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