ETH Library
Environmental behavior and
ecotoxicity of engineered
nanoparticles to algae, plants, and
fungi
Journal Article
Author(s):
Navarro, Enrique; Baun, Anders; Behra, Renata; Hartmann, Nanna B.; Filser, Juliane; Miao, Ai-Jun; Quigg, Antonietta; Santschi,
Peter H.; Sigg, Laura
Publication date:
2008
Permanent link:
https://doi.org/10.3929/ethz-b-000081653
Rights / license:
In Copyright - Non-Commercial Use Permitted
Originally published in:
Ecotoxicology 17(5), https://doi.org/10.1007/s10646-008-0214-0
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Environmental behavior and ecotoxicity of engineered
nanoparticles to algae, plants, and fungi
Enrique Navarro Æ Anders Baun Æ Renata Behra Æ Nanna B. Hartmann Æ
Juliane Filser Æ Ai-Jun Miao Æ Antonietta Quigg Æ Peter H. Santschi Æ
Laura Sigg
Accepted: 14 April 2008 / Published online: 7 May 2008
Ó Springer Science+Business Media, LLC 2008
Abstract Developments in nanotechnology are leading to
a rapid proliferation of new materials that are likely to
become a source of engineered nanoparticles (ENPs) to the
environment, where their possible ecotoxicological impacts
remain unknown. The surface properties of ENPs are of
essential importance for their aggregation behavior, and
thus for their mobility in aquatic and terrestrial systems
and for their interactions with algae, plants and, fungi.
Interactions of ENPs with natural organic matter have to be
considered as well, as those will alter the ENPs aggregation
behavior in surface waters or in soils. Cells of plants, algae,
and fungi possess cell walls that constitute a primary site
for interaction and a barrier for the entrance of ENPs.
Mechanisms allowing ENPs to pass through cell walls and
membranes are as yet poorly understood. Inside cells,
ENPs might directly provoke alterations of membranes and
other cell structures and molecules, as well as protective
mechanisms. Indirect effects of ENPs depend on their
chemical and physical properties and may include physical
restraints (clogging effects), solubilization of toxic ENP
compounds, or production of reactive oxygen species.
Many questions regarding the bioavailability of ENPs, their
uptake by algae, plants, and fungi and the toxicity mech-
anisms remain to be elucidated.
Keywords Toxicity Nanoparticles Fullerenes
Carbon nanotubes Carbon black Silver nanoparticles
TiO
2
Organic matter
Introduction
Engineered nanoparticles (ENPs), with sizes smaller than
100 nm in at least one dimension, have received a lot of
attention and concern recently due to their rapidly
increasing applications in various areas of the economy,
such as textiles, electronics, pharmaceutics, cosmetics, and
environmental remediation (Dunphy Guzman et al. 2006b;
The Royal Society & The Royal Academy of Engineering
2004). They are some of the most important products
of nanotechnology, whose benefits and drawbacks are
believed to well exceed those of the industrial revolution.
On one hand, some optimists claim that nanotechnology
can reverse the harm done by industrialization (Borm
2002). On the other hand, in vitro studies, so far, have put a
damper on these claims. Investments in nanotechnology
are thus increasing rapidly worldwide. The total global
investment in nanotechnologies was around $10 billion in
2005 (Harrison 2007) and it is estimated that the annual
value for all nanotechnology-related products will be $1
trillion by 2011–2015 (Roco 2005). Accordingly, the
E. Navarro (&) R. Behra L. Sigg
Swiss Federal Institute of Aquatic Science and Technology
(Eawag), Ueberlandstrasse 133, Dubendorf 8600, Switzerland
e-mail: enrique.navarro@eawag.ch
E. Navarro
Instituto Pirenaico de Ecologı
´
a-CSIC, Avda. Montan
˜
ana 1005,
Zaragoza 50192, Spain
A. Baun N. B. Hartmann
Department of Environment Engineering, Technical University
of Denmark, Bygningstorvet, Building 115, Kongens Lyngby
2800, Denmark
J. Filser
General and Theoretical Ecology (UFT), University of Bremen,
Leobener Strasse, Bremen 28359, Germany
A.-J. Miao A. Quigg P. H. Santschi
Department of Marine Science/Biology, Texas A&M University,
College Station, TX 77843, USA
123
Ecotoxicology (2008) 17:372–386
DOI 10.1007/s10646-008-0214-0
current annual global production of ENPs was on the order
of 10
3
tons in 2004, which is expected to increase further to
10
4
–10
5
tons per year after 2010 (The Royal Society & The
Royal Academy of Engineering 2004). This production
includes ENPs made for use in agricultural applications
(Kuzma and VerHage 2006) and environmental remedia-
tion, such as zero-valent iron (Zhang 2003). However,
because of their widespread use in consumer products, it is
expected that ENPs will find their way into aquatic, ter-
restrial, and atmospheric environments (Nowack and
Bucheli 2007), where their fate and behavior are largely
unknown. The unique properties of ENPs, such as high
specific surface area (Fig. 1), abundant reactive sites on the
surface as a consequence of a large fraction of atoms located
on the exterior rather than in the interior of ENPs, as well as
their mobility, could potentially lead to unexpected health
or environmental hazards (Maynard et al. 2006; Wiesner
et al. 2006). Therefore, organisms, and especially those that
interact strongly with their immediate environment such as
algae, plants, and fungi, are expected to be affected as a
result of their exposure to ENPs. There is a consensus
amongst both proponents and skeptics that the potentially
adverse effects ENPs could have on humans as well as
whole ecosystems need to be widely examined in this early
phase of nanotechnology (Colvin 2003; Dunphy Guzman
et al. 2006b; Nel et al. 2006; Oberdo
¨
rster et al. 2005).
In this review, we examine the environmental behavior
and ecotoxicity of nanoparticles (NPs) to algae, plants,
and fungi. The term NP is used to refer to natural and
unintentionally produced nanoparticles, which often have a
wider distribution of sizes, while the term ENPs is used to
refer to engineered nanoparticles that are designed and
intentionally produced, with generally more narrowly
defined sizes. Sources and behavior of NPs in atmosphere,
soils, and aquatic systems, as the main habitats for algae,
plants, and fungi, are discussed first, then the toxicity of
ENPs. Three key topics are emphasized: (1) sources,
transformations, and fate of nanoparticles (NPs) in the
environment, (2) biotransformations that ENPs can expe-
rience in contact with algae, plants, and fungi, and then the
entrance and fate to these organisms, and (3) the underly-
ing mechanisms of ENPs’ toxicity and their effects on
algae, plants, and fungi, and how these toxic effects might
be transferred through food webs, thus affecting commu-
nities and whole ecosystems. The interaction between these
three areas has been summarized in Fig. 2.
Sources and environmental behavior of NPs
Natural and anthropogenic sources of NPs
NPs are actually not new and have a history as long as that
of the Earth itself. For example, NPs could be produced
during a volcanic eruption through processes like Aiken-
mode nucleation, as a result of simultaneous emission of
substantive nuclei (e.g., sulfuric and nitric acids) (Aiken
1884), and in hydrothermal vent systems (Luther and
Rickard 2005). However, it was not until the appearance of
Particle size (nm)
0 2000 4000 6000 8000 10000
Specific surface area (m
2
kg
-1
)
10
2
10
3
10
4
10
5
10
6
Fig. 1 Relationship between specific surface area (m
2
kg
-1
)ofa
spherical particle and its size (diameter in nm) with a density of
1000 kg m
-3
as an example. Specific surface area increases as
particles become smaller
Sources of NP’s
Ecosystem
Organism
effects
Routes of entrance in the ecosystem
Abiotic interactions
Biotic interactions. Uptake. Routes of
entrance in
the organisms. Intracellular
fate.
Natural and anthropogenic sources of NP’s
Population, community,
ecosystem
NP’s effects on organisms
Transfer of the effe
cts. Environmental
relevance. Risk assessment
Environmental
effects on NP
Fig. 2 The logical chain of events accounting for the toxicity of NP
starts with the sources of NPs and their entrance routes into the
ecosystem. Then, the NPs will experience abiotic interactions because
the conditions prevailing in the different atmospheric, aquatic and
terrestrial environments, leading to physical and chemical alterations
(graphically represented as changes at the NPs’ surface). These
alterations will greatly determine the fate of the NPs in the
environment and thus their bioavailability to organisms. Once in
the proximity of organisms, interactions might occur at biological
interfaces, resulting in the entrance of NPs into these organisms. Once
inside the organisms, NPs may cause various toxic effects and might
be transferred through food webs, thus affecting communities and
ecosystems
Nanoparticles, plants, algae, and fungi 373
123
internal combustion engines, power plants, and extensive
burning of fossil fuels with the advent of the industrial
revolution that their amounts increased significantly and
became a potential risk to the environment (Biswas and Wu
2005). With a foreseeable further development of nano-
technology, there will be a substantial increase in the
production and release of ENPs.
Therefore, NPs can be produced either intentionally, as
ENPs, or unintentionally, with the latter including natural
sources such as aerosols from volcanic eruptions, forest
fires, pollen fragments, and viruses as well as anthropo-
genic sources such as power plants, vehicles, coal
combustion, frying, and welding, and include nanoparticles
such as soot, black or elemental carbon. In aquatic systems,
NPs include metal sulfide nanoclusters emanating from
hydrothermal systems (Luther and Rickard 2005). At the
same time, the physicochemical properties may be differ-
ent for the NPs from different sources, which may further
affect NPs’ interactions with organisms, although their
toxicity is found to be mainly size or surface area depen-
dent (Nel et al. 2006). NPs from unintentional sources are
mostly polydisperse/heterogeneous, containing sulfide,
sulfate, nitrate, ammonium, organic carbon, elemental
carbon, and trace metals, and have irregular shapes,
whereas ENPs are monodisperse/homogeneous and regu-
larly shaped (Sioutas et al. 2005).
Although a budget for NPs in the atmosphere, soils, and
aquatic systems is currently lacking, it is conceivable that a
significant amount of NPs from an increasing range of
applications will find their way into these environments,
where plants, algae, and fungi live. Besides direct emission
into the atmosphere or photochemical formation therein,
ENPs, as they are used in sunscreens, detergents, paints,
printer inks, or tires, can also enter the environment
through accidental spills during their production and
transportation, wear and tear, and the final disposal of the
ENP-containing products. In particular, there are certain
types of ENPs that are made for the purpose of environ-
mental remediation, such as dechlorination of groundwater
pollutants and reclamation of land lost to forest fires
(Masciangioli and Zhang 2003; Waychunas et al. 2005;
Yue and Economy 2005; Zhang 2003). A lifecycle
assessment of the release of ENPs into the environment is
thus imperative for the establishment and implementation
of effective and protective regulatory policy.
NP behavior and fate in the atmosphere
NPs in the atmospheric environment may come from either
point/stationary or nonpoint/mobile sources. A portion of
these NPs are directly emitted from combustion sources.
Others are formed through nucleation and condensation
processes of the hot supersaturated vapors when being
cooled to ambient temperature. Furthermore, chemical
reactions in the atmosphere may lead to chemical species
with very low saturation vapor pressures, which will finally
produce particles by nucleation (Biswas and Wu 2005;
Friedlander and Pui 2004; Sioutas et al. 2005). During
the course of gas to particle conversion (nucleation) in
the latter two processes, the gaseous molecules are first
combined into ultrafine nuclei (3–20 nm) through binary
water-sulfuric acid, ternary water-sulfuric acid-ammonia,
or ion-induced nucleation (Kulmala 2003; Kulmala et al.
2004). Then the size of these nuclei will increase due to the
condensation of organic or inorganic vapors on the nuclei,
with a growth rate of 1–20 nm h
-1
; the nucleation rate
of particles with a diameter of 3 nm lies between 0.01 and
10
5
particles cm
-3
s
-1
. The size distribution of the newly
formed particles is mainly determined by processes such as
condensation/evaporation and dilution, while coagulation
and deposition play minor roles (Zhang and Wexler 2004).
Therefore, any environmental or meteorological factors
(temperature, relative humidity, atmospheric turbulence,
etc.) that are involved in these processes may affect the
NPs’ concentration in the atmosphere. For example, Chang
et al. (2004) found that samples taken at different com-
bustion and exhaust temperatures showed higher particle
number concentrations at 645°K than at 450°K. Thus it is
expected that the exposure of organisms to ENPs will be
strongly determined by the environmental conditions
prevailing in each ecosystem.
Although there is a lack of knowledge about the fraction
of NPs from each of the formation processes mentioned
above, emission inventories suggest that motor vehicles are
the primary sources of fine and ultrafine (nano)particles in
the atmosphere (Schauer et al. 1996; Shi et al. 2001). As
the importance of traffic emission sources and the poten-
tially high transportability of NPs in the air, a lot of work
has been carried out to determine the concentration and
size distribution of ultrafine particles near highways (Hinds
1999). Both spatial and temporal variations of these
parameters have been observed. The particle concentration
was mostly found to decrease exponentially with down-
wind distance from the freeway due to atmospheric
dispersion and coagulation (Zhu et al. 2002a, b). In these
studies, the measured particle size ranged from 7 to 300 nm
with particle number concentration mostly accounted for
by 10–20 nm particles, and the particle concentration
decreased from 2 9 10
5
on the freeway to 5 9 10
4
parti-
cles cm
-3
300 m downwind. One exception is from the
work of Morawska et al. (1999), who did not observe
statistically significant differences in fine particle number
concentrations for distances up to 200 m away from the
road. At the same time there is also a diurnal variation
of the concentration of NPs in the atmosphere, which
is mainly determined by two counteracting processes:
374 E. Navarro et al.
123
reduced temperature may increase particle emissions, while
lower traffic may reduce it. Zhu et al. (2006) found that
particle number concentration measured 30 m downwind
from the freeway was 80% of the previous daytime mea-
surements (e.g., 1.5 9 10
5
versus 1.1 9 10
5
particles cm
-3
).
Similarly, higher particle concentrations were observed in
winter, as a result of lower temperatures and smaller extent
of dilution (Jeong et al. 2004; Stanier et al. 2004). Jeong
et al. (2004) measured the ultrafine particles (10–500 nm)
in Rochester, New York, USA from December 2001 to
December 2002. More than 70% of the total measured
number concentration was associated with 11–50 nm
ultrafine particles with a concentration of about 7000 par-
ticles cm
-3
in winter and 4000 particles cm
-3
in summer.
Although a recent study evaluating the aerosol generation
during the handling of ENPs such as carbon nanotubes
showed an insignificant release (Maynard et al. 2004), it
remains unknown to what extent ENPs may contribute
to the ultrafine (nano)particles in the atmosphere, while
their behavior might be similar to natural ones of similar
size.
Aggregation, deposition, and mobility of NPs and ENPs
in aquatic systems
The surface properties of NPs are one of the most important
factors that govern their stability and mobility as colloidal
suspensions or their aggregation into larger particles and
deposition in aquatic systems. The stability of NPs as col-
loidal suspensions governs their mobility in aquatic
systems. Stable colloidal suspensions of NPs are a pre-
requisite for efficient interactions of NPs with algae, which
may lead to uptake or toxic effects. In soils, the mobility of
NPs in pore water is an essential condition for interactions
with plant roots or fungi hyphae. Therefore, the surface
properties of various NPs have to be briefly discussed. Due
to the complexity of the surfaces of natural NPs, we focus in
this review mainly on the surface properties of ENPs.
Metallic ENPs are usually coated with inorganic or
organic compounds, such as citrate, cysteine, carbonate or
surfactants such as sodium dodecyl sulfate to maintain the
stability of the colloidal suspension (Mafune et al. 2000).
Therefore, surface properties of ENPs in aqueous suspen-
sions are strongly dependent on the composition of these
coatings, which typically results, at neutral pH, in a neg-
ative charge of the ENPs, which then results in their
stabilization with respect to aggregation (Mafune et al.
2000; Mandal et al. 2001; Munro et al. 1995). Surface
properties of metal oxide NPs are also determined by their
acidity constants and zero-point of charge (Giammar et al.
2007; Hristovski et al. 2007; Kormann et al. 1991; Schin-
dler and Stumm 1987). For example, TiO
2
ENPs are
expected to be positively charged at pH \ 6 and negatively
charged at pH [ 7 (Dunphy Guzman et al. 2006b; Ridley
et al. 2006), whereas SiO
2
particles are generally negatively
charged, as their zero-point of charge is located at around
pH 2 (Hiemstra et al. 1996). Furthermore, some elemental
metal NPs may have similar surface properties to their
oxidized counterparts, as their surfaces are mostly coated by
a layer of passivating oxide (Nurmi et al. 2005). Nonme-
tallic ENPs such as carbon nanotubes and fullerenes have
hydrophobic surfaces and are not readily dissolved in water.
These ENPs may be solubilized by functionalization with
polar groups at their surfaces. Otherwise, the surfaces of
hydrophobic carbon nanotubes are likely to interact pref-
erentially with hydrophobic or amphiphilic compounds.
Particle aggregation and deposition are closely related
phenomena (Wiesner et al. 2006). Aggregation describes
the interaction between two mobile objects, whereas
deposition refers to the attachment of a mobile particle to
an immobile phase (e.g., collector) (Elimelech and Omelia
1990). The limited research that has been carried out on
ENP aggregation and deposition suggests that prior prin-
ciples on colloidal transport in aqueous media (i.e.,
Smoluchovsky’s equations and DLVO theory) may still
apply to ENPs, except that the Brønsted concept needs to
be applied for supersmall NPs (\ 10 nm) (Brant et al.
2005; Derjaguin and Landau 1941; Kallay and Zalac 2002;
Lecoanet et al. 2004; Lecoanet and Wiesner 2004;
Smoluchowski 1917; Verwey and Overbeek 1948).
According to these theories, particle deposition/aggrega-
tion kinetics can be defined as a two-step process of
particle transport followed by attachment (Elimelech and
Omelia 1990). The transport of colloidal particles (1 nm to
1 lm) is determined by convection, diffusion (Brownian
motion), as well as external forces, whereas attachment
onto other particles/surfaces is controlled by the colloidal
interaction forces at short distances of operation.
The deposition/aggregation process is determined by the
NPs’ surface properties, which are mainly dependent on
parameters such as temperature, ionic strength, pH, particle
concentration and size, etc. (Dunphy Guzman et al. 2006a;
Elimelech and Omelia 1990; Filella and Buffle 1993;
Kretzschmar and Sticher 1997; Lecoanet et al. 2004). For
example, an increase in the ionic strength compresses the
electric double layer, thus decreasing the electrostatic repul-
sion between two objects with the same charge. The energy
barrier will then decrease and the attachment probability
becomes closer to unity. However, other forces may be
involved in the deposition/aggregation process, such as steric
repulsion/attraction, hydration effects, hydrophobic interac-
tions, magnetic attraction, or the charge may be
heterogeneously distributed on the particle surface (Metcalfe
et al. 2006), all of which can further complicate the interac-
tions and remain to be examined. In addition, NPs’ association
with either natural organic matter (NOM) (Buffle et al. 1998)
Nanoparticles, plants, algae, and fungi 375
123
