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Nano-sized plastics (NPLs, size < 100 nm) are characterized by a very small size and high reactivity, allowing them to interact with diverse phytoplankton species. The processes governing the interactions of NPLs with phytoplankton cells include absorption onto cell, penetration into cells via endocytosis or physical damage, and the obstruction of substance and energy exchange with the surrounding medium. Upon association with the cells, elevated concentrations of NPLs can reduce phytoplankton growth and photosynthesis, trigger overproduction of reactive oxygen species and damages, as well as alter cellular metabolic activity. NPLs can influence toxin production by cyanobacteria and release of extracellular polymeric substances by different phytoplankton species. Conversely, phytoplankton species can modulate NPL fate by secreting biomolecules that form an eco-corona around the NPLs, as well as taking part in the NPLs biotransformation.
Plastic particles are considered as nanomaterials if at least half of them, in an unbound state or as an aggregate or an agglomerate state, have at least one dimension ranging from 1 to 100 nm [1]. As the usage of diverse plastic materials continues to expand, the accumulation of plastic waste is on the rise. Consequently, the presence of nanoplastics (NPLs) in the environment is increasing [2][3][4] together with the concerns regarding the possible environmental implications of NPLs [5][6]. Indeed, NPLs, originating from various primary or secondary sources, represent the least explored facet of plastic pollution [5][6]. In environmental settings, diverse plastic debris can release a large amount of NPLs through various physical and chemical degradation pathways, as previously reviewed [7]. The concentrations of NPLs in the environment have not yet been measured due to the constraints of current analytical methodologies. Multi-media model estimations provide average concentrations of NPLs in surface water of 280 µg L−1 [8]. More recently, NPLs’ abundance has been estimated to be in the range 0.3–488 μg L−1 in freshwaters, which are higher than those for marine environments (2.7–67 μg L−1) [9]. These concentrations are generally lower as compared to the predicted no-effect concentrations (PNECs) derived from probabilistic species sensitivity distributions, resulting in values of 99 μg L−1 and 72 μg L−1 for freshwater and marine datasets [10]. They are also below the estimated hazard concentration affecting 5% of the species (HC5) of 410 μg L−1 for marine plankton for two types of materials, polymethylmethacrylate (PMMA) and polystyrene (PS) [11], as well as HC5 for NPLs with a size of 50 nm in freshwater, 187.9 (8.0–2978.3) μg L−1 [12]. Nevertheless, some hotspots of NPLs pollution can be of risk for aquatic organisms, including phytoplankton. Consequently, considerable attention has been paid to the bioaccumulation of NPLs and their adverse effects within higher trophic levels [9]. Recent insigths into their accumulation within aquatic organisms have highlighted numerous challenges [13]. The accumulation of NPLs in aquatic organisms has been shown to lead to detrimental effects on various freshwater organisms [4][5][6][7][9][1][14][15][16][17][18][19][20]. These effects include oxidative stress and damage, inflammation, altered development, reduced growth, energy and movement, genotoxicity, etc., as recently reviewed in references [9][16][19][21][22][23][24]. Modifying factors, such as particle characteristics, concentration, size, exposure duration, and co-factors like presence of other organic or inorganic contaminants, food availability, species, development stage, and environmental conditions were extensively discussed in references [16][22][24][25]. However, there is a scarcity of scientific evidences regarding the interactions and possible impacts of NPLs on phytoplankton species.
Figure 1. Key processes governing the interactions of the NPLs and phytoplankton cells.
Indeed, both amidine and carboxyl - functionalized polystyrene NPLs (PS-COOH) were found to adsorb onto the marine diatom Dunaliella tertiolecta. However, only amidine PS NPLs triggered the inhibition of algal growth, displaying an effective concentration for 50% of the algal population (EC50) of 12.97 μg mL−1 [28]. In another study, fluorescent-blue 50 nm amino - modified polystyrene NPLs (PS-NH2) adhered to the diatom Chaetoceros neogracile, leading to impairment of the photosynthetic machinery and an overproduction of reactive oxygen species (ROS) at both low (0.05 μg mL−1) and high (5 μg mL−1) exposure concentrations [29]. The adsorption onto the cells of green alga Pseudokirchneriella subcapitata was significantly higher for neutral and positively charged PS-NH2 NPLs at a concentration of 100 mg L−1. Conversely, negatively charged PS-COOH NPLs displayed minimal adsorption onto the algal cell wall [30]. These examples highlight the important role of the surface charge of NPL particles and the specificity of interactions with different algal species. The rapid adsorption and/or absorption of PS NPLs onto/in diatom Phaeodactylum tricornutum was evidenced through an observed increase in cell complexity, size and microalgae fluorescence induced by 100 nm fluoresbrite [31]. Fluorescent 51 nm PS NPLs attached to and penetrated the outer layer of green alga Chlamydomonas reinhardtii during cell division [32]. In a recent study involving metal - doped PS NPLs, it was demonstrated that more than 60% of Fe-PS or Eu-PS NPLs remained associated with algal cells of P. subcapitata after 72 hours [33]. A recent study uncovered that fluorescent aggregation - induced emission fluorogens-incorporated nanoparticles (AIE-NPs) of sizes 40, 70, and 85 nm were internally taken up via clathrin - dependent endocytosis in C. reinhardtii, while the 140 nm AIE-NPs remained surface-bound [34]. Notably, the authors highlighted the importance of endocytosis, algal cell membrane permeability, and the thickness of extracellular polymeric substances (EPS) and their cell cycle dependence in the uptake of AIE-NPs [34].
Phytoplankton species could influence the NPLs fate in the aquatic environment and thus their impact via release of biomolecules such as extracellular polymeric substance and via cellular transformations. Recent reviews have shed light on how phytoplankton can influence the fate and biological availability of NPLs by excreting diverse EPS, leading to the formation of the eco-corona [58][59]. Studies indicate that EPS produced by the marine phytoplankton play a role in forming an eco-corona arround various NPLs, thereby influencing their reactivity [58]. For example, the EPS derived from the diatom P. tricornutum, containing proteins with molecular weight ranging from 30 to 100 kDa along with high molecular weight carbohydrates, formed an eco-corona on 60 nm-sized PS-COOH NPLs, effectively reducing NPLs’ aggregation [60]. However, when EPS from P. tricornutum, Ankistrodesmus angustus, and Amphora sp. interacted with 23 nm PS NPLs, it led to the formation of gel-like micrometer aggregates, which was presumably driven by hydrophobic interactions [61]. The formation of the eco-corona has been found to depend on NPLs size, charges, and incubation duration [58]. Alginate, used as a model polysaccharide, formed an eco-corona on amidine functionalized PS NPLs, altering the surface charge, although aggregation was minimal [62][63]. Furthermore, aminated, carboxylated and plain NPLs aged in EPS reduced the oxidative stress and mitigated toxic effects in the marine alga Chlorella sp. [64].
Overall, the accumulating evidences obtained from model NPLs demonstrated that these particles interact with phytoplanktonic organisms, potentially causing harm when present in concentrations significantly higher than those typically found in aquatic environments. However, further investigations are indispensible to understand the intricate interplays between phytoplankton species and more realistic nanoplastic materials, such as secondary NPLs and aged NPLs, at concentrations closer to those anticipated in aquatic settings. Enhanced and quantitative understanding of the fundamental processes governing the interactions between NPLs and phytoplankton species is pivotal for a comprehensive grasp of their potential impacts on aquatic ecosystems. Notably, phytoplankton play a critical role in global elemental cycling, contributing to nearly half of the global primary production, and occupies a foundational position at the base of aquatic food chains.