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Why 'nano'?
Natural water-borne nanoparticles are ubiquitous. Their very small size, ranging from 1 to 100 nanometers means they are both highly mobile and chemically reactive. Nanoparticles are central in buffering environmental systems, serving the dual role of limiting potentially toxic metal concentrations, while at the same time providing a supply of metals at levels that enables biochemical reactions to take place. 
The term nanoparticle describes a subset of the colloidal range between 1 and 100 nm (Hochella 2002) (Box 1). The distinction is justified partly on their very high specific surface area (Lead & Wilkinson 2006) and partly on their potentially different behavior at this small scale, due to the spatial constraint of electronic properties (in an analogous manner to engineered nanoparticles (Madden et al. 2006)) (Figure 1). As particles transition to smaller and smaller sizes, they become effectively all surface with minimal internal volume, giving rise to their enhanced reactivity (Figure 1).
Figure 1
Generalized trend for size-dependent reactivity change of a material as the particle transitions from macroscopic (bulk-like) to atomic. Reactivity can increase or decrease depending on the material and the chemical reaction involved.
© 2013 Nature Education Adapted from Wigginton et al. (2007). All rights reserved. 
The environmental significance of colloids and nanoparticles resides in their interactions with trace metals (TM), through which they regulate the circulation and bioavailability of TMs in natural waters.
Nanoparticle and colloid types and characteristics
Environmental colloids and nanoparticles can be found in a multitude of compositions and conformations. Much of the environmental pool of colloids consists of the low molecular weight breakdown products of biological decay (humic matter), various fibrillar and mesh-like organic compounds, and minerals generated during the chemical weathering of rocks, principally oxides and oxyhydroxides of iron (Fe), manganese (Mn) and aluminium (Al) and aluminosilicates. 
The most-studied subset of environmental organic matter, the humic substances (HS), are an operationally defined, chemically extracted fraction of the total natural organic carbon pool. Although not completely representative of the natural organic matter (NOM) (Filella 2008), in terms of trace metal binding, extracted HS behave similarly, although not identically, to their natural counterparts and may represent the most functionally significant component of NOM (Tipping 2002).
HS exist both as dispersed material at the lower end of the nano size range (< 5 nm) but can aggregate to form larger structures (often as composites with mineral colloids (e.g., Fe and Mn oxides and aluminosilicates), potentially reaching dimensions outside the nano-range (Stolpe & Hassellöv 2007) (Figure 2).
Figure 2
Representative TEM images from samples of hyperalkaline cave dripwater from Poole’s Cavern, UK. (a) particulate aggregate containing organic matter, aluminosilicates, and Fe oxides (elemental composition from adjacent X-EDS spectrum; Cu peaks in spectrum originate from supporting grid and C peaks originate from grid and analyzed particles), (b and c) globular nanoparticles with diameters between ca. 1 and 5 nm. Image (d) obtained from 1 to 10 nm FlFFF fraction of the same dripwater sample fractionated at a cross-flow of 0.75 mL min-1. Samples prepared by direct ultracentrifugation onto copper TEM grid without pre-concentration following collection/fractionation.
© 2013 Nature Education Adapted from Hartland et al. (2011). All rights reserved.
Figure 3
A typical tapping mode image of a layer developed on a mica sheet after sorption of Suwannee River Humic Acid (SRHA). The line across the image shows the measured transect.
© 2013 Nature Education Adapted from from Gibson et al. (2007). All rights reserved.
The next most abundant organic material found in natural waters consists of the peptides, proteins, peptidoglycans, polysaccharides and similar biomolecules. Polysaccharides have fibrillar or mesh-like configurations, whereas proteins are often globular and differ from HS in that they are ‘fresher,'-that is, less degraded. These types of compounds have the effect of generally increasing the size of nanoparticles and colloids through aggregation (Figure 4), while HS often, but not always, reduce aggregation through charge and/or steric stabilization (Buffle & Leppard 1995). In all environmental systems, metal oxides, especially of iron and manganese, are also important nano-scale phases, if not always in mass terms, then in their ability to bind trace elements (Figure 5).
Figure 4
Major types of aggregates formed in the three-colloidal component system: fulvic compounds (FC) (or aromatic refractory organic matter) small points; inorganic colloids (IC)- circles; rigid biopolymers -lines. Both FC and polysaccharides can also form gels, which are represented here as grey areas into which IC can be embedded.
© 2013 Nature Education Adapted from Buffle et al. (1998). All rights reserved.
Figure 5
Size distributions for natural soil colloids derived using field flow fractionation inductively coupled plasma mass spectrometry (FFF–ICPMS). In the region of about 5 nm to 10 nm in particle diameter, the UV absorbance signal of the HS is already small (i.e. low concentration), while the Fe and Pb signals show second peaks. The second Fe peak can be interpreted as a second solid, Fe-rich phase present in the sample. On the right, TEM micrographs of the obtained extract are shown.
© 2013 Nature Education Adapted from Hassellov & Kammer (2008). All rights reserved.
The colloidal stability of nanoparticles in the environment
At the circumneutral pH of natural waters (~ pH 7), nanoparticles and colloids typically possess a negative electrostatic surface charge. Indeed, in spite of their original surface potential, nearly all inorganic colloids in natural waters possess a negative surface charge due to HS surface coatings (Tipping & Higgins 1982). Charge differences between particle surfaces (e.g., negative to negative) confer stability through charge repulsion, meaning that nanoparticles and colloids tend to remain dispersed in water, forming a suspension. The surface charge of all particles may be equalized by counter ions, which form a double layer around the particle. 
The Derjaguin and Landau, Verwey and Overbeek (DLVO) theory (Derjaguijn & Landau 1941; Verwey & Overbeek 1948) describes the two opposing forces (exerted through this double layer) that act on nanoparticles that approach one another: the repulsive electrostatic potential VR, created by the ‘halo' of counter ions surrounding each particle, and the sum of attractive forces (van der Waals interactions), VA. Figure 6 shows the combined effect of forces VA and VR.
Figure 6
(a) Combined forces acting on two interacting particles in a low ionic strength medium. (b) Combined forces acting on two interacting particles under high ionic strength conditions. The net force is repulsive at greater distances and becomes attractive only after overcoming a net repulsive force. A means of overcoming this energy barrier is needed before aggregation can take place, e.g. under highly ionic conditions (b) such as in seawater, the double layer becomes compressed.
© 2013 Nature Education All rights reserved.
Under classical DVLO theory, if VA < VR then nanoparticles are considered kinetically stable. In reality the situation is more complex and many non-DLVO forces exist, most notably steric repulsion due to coatings such as HS, where compression of the coatings requires additional energy (Tipping & Higgins 1982). Although traditional DLVO theory can semi-quantitatively predict nanoparticle aggregation and deposition, only by including non-DLVO interactions can a complete understanding of their environmental fate be reached (Petosa et al. 2010).
Nanoparticle mobility in aqueous systems
In general, the mobility of nanoparticles in surface waters is only limited by their colloidal stability. Similarly, in fractured aquifers they can move largely unhindered. However, in subsurface porous media (i.e., alluvial groundwater aquifers) nanoparticle and colloid mobility is more constrained and the movement of nanoparticles is typically predicted using colloid filtration theory (CFT) because of the greater potential for collisions with soil grains (Yao et al. 1971; Lui et al. 2009; Cullen et al. 2010). A variety of phenomena (e.g., Brownian motion, interception, sedimentation, inertia, and hydrodynamic forces) govern the number of collisions with the soil grain (Tufenkji & Elimelech 2004; Nelson & Ginn 2005). Because smaller particles experience a higher degree of random Brownian motion, this is particularly relevant for nanoparticles. A variety of retention mechanisms not considered part of CFT may also be important for the retention of nanoparticles and colloids in porous media (e.g., straining, maximum retention capacity of soil surfaces and soil surface charge heterogeneities).
Figure 7
Role of NPs (large black circles) in the circulation of vital and toxic TMs (small red circles) and their availability to biota (bacteria, algae, fungi etc., green ellipses) in surface waters and porous media.
© 2013 Nature Education Adapted from Buffle & Leppard (1995). All rights reserved.
Trace metal binding in nano-metal complexes
The importance of nanoparticles (over colloids in general) lies in their ability to bind large amounts of TMs, which impacts the bioavailability of vital and toxic metals in natural waters. The principles that govern these binding reactions are thought to be similar regardless of the size and chemistry of the colloids and typically occur via inner-sphere, e.g. covalent bonding, complexation reactions with surface functional groups (Box 2).
Inner-sphere complexation between metal ions and common metal oxides, which also occurs for HS and other colloids, has been shown to be the predominant mechanism of adsorption (Bargar et al. 1997; Alcacio et al. 2001) and can be conceptualized as of the type in Equation 1, where complexation of the metal ion (Mz+) follows deprotonation of a hydroxyl group (S-OH) at the aquatic particle surface:
(1) S-OH(aq) + Mz+(aq) ↔ S-OM(aq) + H+(aq)
Edge site valence and additional surface protons are omitted for convenience.
By definition, metals in inner-sphere complexes are more strongly bound, and therefore are less labile (Box 3) than metals in outer-sphere complexes (ion pairs), with implications for metal bioavailability and ecotoxicity.
Metal binding by HS-containing nanoparticles and colloids is affected by their polyfunctionality (resulting from the presence of metal binding sites with different chemical nature) and their polyelectrolyte character (resulting from the presence of a large density of charge due to numerous dissociable sites) (Box 4). The relative importance of each of these factors depends on ambient conditions such as salt concentration, type of ions in the medium, and pH, which ultimately influence the inter- and intra-particle interactions as well as metal to HS ratio (Tipping 2001). Much less is known about metal binding by other non-humic organic nano-sized components, despite being present in large proportion within flocs and biofilms (Flemming & Wingender 2001) in freshwaters (up to 25% of DOM; Wilkinson et al. 1997) and in marine systems (up to 80% of DOM; Verdugo et al. 2004).
The ecological significance of nanoparticles
Biological availability is defined as "the extent of absorption of a substance by a living organism" (Nordberg et al. 2010). Because of the interaction of TMs with other constituents of the aquatic system (such as nanoparticles), only a fraction of the total mass of TM present interacts with organisms, and therefore, the remainder is unavailable as either a nutrient or toxin unless directly absorbed prior to dissociation. Nanoparticles and colloids regulate TM bioavailability by influencing TM speciation and other processes at the organism - environment interface (Figure 8).
Figure 8
Processes at organism-environment interface determining TM bioavailability. In this case, TM represents free trace metal and NP a nanoparticle, TM-NP is the TM bound to nanoparticle. Different chemical forms are transported from the medium to the vicinity of the organisms; during transport, TM complexes (e.g., with nanoparticles) can dissociate/associate; chemical species can adsorb to the protective layer of organisms (e.g., mucus or cell walls) and cellular membranes, then cross cell membranes by different mechanisms. Depending on the nature of the TM, organism and its environment, any of the processes shown above could be rate-limiting. If the transport of TM across the cellular membrane limits the overall process of metal transport into the cell, bio-responses to both essential and toxic elements can be related to any species of metal in the state of equilibrium, including metal bound to the receptor sites on the organisms - the biotic ligand model (Slaveykova & Wilkinson 2005); or free metal ions in the solution - the free ion activity model (Campbell 1995). Under the conditions of nutrient limitation or in biofilms where mass transport is the limiting factor (Buffle et al. 2009), TM complexes are expected to contribute to the bioavailability depending on their mobility and lability.
© 2013 Nature Education All rights reserved.
In general, colloids reduce TM bioavailability by decreasing the freely available fraction of TMs to cross the cellular membrane of an organism. Indeed, colloids of different composition have been shown to limit the bioavailability (and detrimental effects) of toxic metals (e.g., Ag, Cd, Cu, Ni and Pb) to various organisms, including bacteria, fungi, phytoplankton, daphnia and fish, in direct proportion to the free metal ion concentrations (Slaveykova & Wilkinson 2005).
Nanoparticles and colloids may also alter TM bioavailability by decreasing the mass transport towards the organism surface and lability of the associated TM. Under diffusion-limited conditions the bioavailable metal is proportional to the diffusion coefficients of the complexes and their lability (Buffle et al. 2009). Exceptions to this rule include where metallic nanoparticles (and TM-NP complexes) are an additional source of TMs for filter feeders (e.g., clams, mussels and oysters) (Luoma & Rainbow, 2005) and organisms with endocytotic capability (i.e., absorb molecules such as proteins by engulfing them) (Simkiss & Taylor 1995).
Given the large proportion of TMs bound to nanoparticles and colloids in surface waters (Lead & Wilkinson 2006), they are expected to mitigate the detrimental effects of toxic trace elements by generally decreasing their bioavailability. In addition, by regulating the bioavailability of micronutrients (Cu, Co, Fe, Mn, Mo, Ni and Zn) used in enzymatic processes (Morel & Price 2003), NPs could affect the phytoplankton biomass and diversity in the ocean and lakes (Morel & Price 2003; Sterner et al. 2004; Boyd & Ellwood 2010). Such alteration could have profound consequences for the biogeochemical cycles of C, N, Fe as well as for food-web interactions, as phytoplankton is responsible for more than 40% of the primary productivity on Earth and represents the base of the aquatic food chain. For example, the mass flux of Fe in the form of nano-clusters delivered by icebergs in the Southern Ocean has been shown to be comparable to Aeolian inputs (Raiswell et al. 2008). Changes in the mass flux of nano-Fe in response to climate changes may be an important negative feedback to warming in the Antarctic region.
Conclusion: environmental nanoparticles and geosystems
Nanogeoscience is perhaps the ultimate research frontier in geosystems. Natural nanoparticles are of central importance in the earth system: in global biogeochemical cycles, weathering, metal binding and transport, bioavailability and ecotoxicity. Furthermore, the influence of nanoparticles on the bioavailability of both nutrient and toxic elements has been a factor in the evolution and development of higher organisms, potentially buffering environmental systems against change (Tipping 2001). It is interesting therefore that manufactured nanoparticles are a focus of concern given that they are present in much lower amounts than their natural counterparts. The reason for this is that manufactured nanoparticles are made of specific structures and chemistries, as distinct from those found in nature, for which organisms may not have appropriate defense mechanisms.
Glossary
oxides: Minerals in which the oxide anion (O2-) is bonded to one or more metal ions
oxyhydroxides: A mixed oxide and hydroxide mineral
aluminosilicates: Minerals composed of aluminium, silicon, and oxygen, plus counter-cations
humic substances: Major components of the natural organic matter (NOM) in soil and water as well as in geologic deposits
natural organic Matter (NOM): the natural organic material present waters including both humic and non-humic fractions
aggregation: Formation of clusters in a colloidal suspension and is the most frequent mechanism of colloid destabilization in surface waters
steric: Referring to steric stabilization of a colloidal suspension by polymer-covered surfaces (e.g. NOM) or in solutions containing non-adsorbing polymer can modulate interparticle forces, producing an additional steric repulsive force
circumneutral: Having a pH between 6.5 and 7.5
electrostatic: The electric force that a particle exerts on another particle
double layer: Also called an electrical double layer (EDL), is a structure that appears on the surface of an object when it is exposed to a fluid
adsorption: Here refers to the adhesion of ions to a surface
bioavailability: The degree and rate at which a substance is absorbed into a living system
covalent: A chemical bond that involves the sharing of electron pairs between atoms
complexation: A coordination complex or metal complex, consisting of a metallic ion, surrounded by an array of bound molecules or anions
functional groups: Collections of atoms in a molecule that participate in characteristic reactions (e.g. metal coordination)
ecotoxicity: The potential for chemical stressors to affect ecosystems
endocytotic: Entry of a substance into a cell without passing through the cell membrane
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