Elsevier

Water Research

Volume 201, 1 August 2021, 117319
Water Research

Review
Interaction of nanoplastics with extracellular polymeric substances (EPS) in the aquatic environment: A special reference to eco-corona formation and associated impacts

https://doi.org/10.1016/j.watres.2021.117319Get rights and content

Highlights

  • Eco-corona formation on NPs can alter their identity, properties, and bioreactivity.

  • Integration of techniques is required to fully understand eco-corona formation on NPs.

  • Characteristics of NPs, EPS, and medium can influence eco-corona formation.

  • Eco-corona formation affects the toxicity of NPs to aquatic organisms.

  • Extensive field studies are required to decipher eco-corona mediated impacts of NPs.

Abstract

Nanoplastics (NPs) are plastic particles with sizes ranging between 1 and 1000 nm, exhibiting exceptional qualities such as large surface area, lightweight, durability; therefore, are widely used in cosmetics, paints, electronics, etc. NPs are inevitability released into the aquatic environment where they tend to interact with both, the extracellular polymeric substances (EPS) and other fractions of natural organic matter (NOM), respectively secreted by organisms (e.g., DNA, proteins, and carbohydrates) and degradation byproducts of organic materials (e.g., humic acid and fulvic acid) fluxed into the water bodies. These biomolecules robustly encapsulate NPs to develop an eco-corona layer that alters not only the physicochemical properties but also the fate, bioreactivity, and ecological impacts of NPs. Therefore, this review summarized the documented studies highlighting the eco-corona formation on NPs and associated ecological implications in the aquatic environment. After presenting the precise background information on the occurrence of NPs and EPS in the aquatic environment, we demonstrated the basic difference between eco-corona and bio-corona formation. The reviewed studies showed that the eco-corona formed on NPs have varying sizes and composition, mainly depending on the properties of parent biomolecules, characteristics of NPs, and physicochemical parameters of the aquatic environment. Further, the potential methods for characterization and quantification of eco-corona and its composition have been also highlighted. Moreover, the ecological implications (both toxic and non-toxic) of eco-corona formation on NPs in marine and freshwater environments have been also summarized. Last but not the least, challenges and future research directions are also given, e.g., conducting field studies on eco-corona formation in the aquatic environment, optimizing methods for its characterization and quantification, and considering eco-corona concept in the future toxicity studies on NPs. Finally, understanding eco-corona formation will be critical to unveil the complex NP interactions occurring in natural aquatic systems.

Introduction

Plastics are abundantly used in various fields owing to their unique properties such as low cost, lightweight, durability, and portability. Due to the high market demand, a gradual increase in global plastic manufacturing has been observed since the 1960s with the recent production of 360 million tons in 2018 (PlasticsEurope 2019). However, unregulated consumption and improper disposal of plastics have resulted in their ubiquitous accumulation in every corner of the globe, which researchers describe as “living in the plasticene” (Alimi et al. 2018, Rochman et al. 2013). The recent plastic load in surface waters of the open ocean is estimated as high as 10,000–40,000 tons; therefore, plastics are considered as one of the major components of marine litter (Cózar et al. 2014, Law et al. 2010). In the natural environment, plastic debris and microplastics (MPs) will break down into miniature particles termed nanoplastics (NPs), through various processes such as hydrolysis, biodegradation, photodegradation, and mechanical abrasion (Lambert and Wagner 2016). Moreover, NPs are also released inevitably into the environment from products that contain manufactured nano-sized particles for various biomedical applications and consumer products (Koelmans et al. 2017). The occurrence and accumulation of NPs in the aquatic environment have raised alarming concerns due to their known hazardous impacts on aquatic organisms (Gaylarde et al. 2020). Although studies on the occurrence of NPs in the aquatic environment are elusive yet, they have been reported in water samples from the North Atlantic Subtropical Gyre (Ter Halle et al. 2017) and in surface snow from the Austrian Alps (Materić et al. 2020). Recent in vivo studies have demonstrated that NPs can induce physiological (Wang et al. 2021a) and behavioral alterations (Mattsson et al. 2015), embryotoxicity (Eliso et al. 2020), reproductive abnormalities (Sarasamma et al. 2020), transgenerational impacts (Liu et al. 2020), and immunotoxicity (Greven et al. 2016) in aquatic organisms.

Besides plastic entities, natural organic matter (NOM) is also ubiquitously present in the aquatic environment, comprised of complex assemblies of heterogeneous organic compounds with significantly varying composition and molecular weight (Wang et al. 2015). NOM can be categorized into autochthonous and allochthonous compounds, respectively released inside the water body and formed outside and then transported into the water body (Docter et al. 2015b). The autochthonous NOM is an assembly of biomolecules, released by organisms after in situ reduction, and it accounts for a significant proportion of organic macromolecules in the aquatic ecosystem (Wilkinson and Lead 2007). Among autochthonous NOM, the extracellular polymeric substances (EPS) are the main and important constituents, secreted by aquatic organisms as metabolic byproducts in response to stress or for habitat adaptations (Gutierrez et al. 2013). Recent studies showed that not only microbes (bacteria, algae, etc.) but invertebrates (e.g., Daphnia magna) also release EPS that are mainly comprised of high molecular weight polysaccharides and to a lesser extent also contained proteins, nucleic acid, and lipids (Delattre et al. 2016, Nasser and Lynch 2016). For example, Daphnia magna secretes EPS in the form of proteins in the freshwater environment, which can adsorb on NPs surface, altering their size and identity, and serve as signaling factors, assisting them to interact efficiently with cellular recognition receptors (Nasser and Lynch 2016).

Marine water bodies are dynamic, usually rich in EPS secreted by organisms; therefore exhibiting higher chances of interaction between NPs and EPS (Corsi et al. 2020). For instance, a variety of EPS are released by marine diatoms either in response to an environmental stimulus or as a mandatory step in their basal metabolism (Grassi et al. 2020). The composition of marine EPS is diverse, comprising biomolecules of various sizes and molecular weight, spanning from amino acids to protein peptides and polysaccharides that give rise to macromolecular entities and also contribute to the overall complexity of the marine ecosystem (Grassi et al. 2020). Due to high protein content, marine EPS usually facilitate aggregates formation and serve as the active storage sites with strong adaptive properties to uptake new materials. Therefore, EPS aggregates can stabilize the extracellular enzymes that result in the induction of protein repository through the digestion process; hence, enhancing the protein accumulation in the ecosystem (Flemming et al. 2016). Hazardous materials (plastics, dispersant, and oil) and environmental stresses (nutrient limitation and variations in the light exposure) can alter the protein to carbohydrate (P/C) ratio of EPS (Bacosa et al. 2018, Kamalanathan et al. 2019, Shiu et al. 2020b). This change in the P/C ratio can alter the adsorptive properties, quenching potential, and physical hindrance of EPS for hazardous particles; therefore, regulates their effective quantity reaching aquatic organisms (Nichols et al. 2005). Further, the aggregation behavior, stickiness and hydrophobicity can also regulate the key properties of EPS; affecting the interactions of aquatic organisms with plastic particles that ultimately play important role in the transport and fate of NPs in the environment (Chiu et al. 2019, Santschi et al. 2020). More information on the cellular biosynthesis, fate. and interactive properties of EPS in the aquatic environment is provided in text S1 and S2 of the supplementary information.

Among allochthonous NOM, humic acid (HA), fulvic acid (FA), and humin are the most common compounds that are degradation byproducts of organic materials (Gutierrez et al. 2018). They are also originated as byproducts of bacterial metabolism and through different oxidation processes in the environment (Lynch et al. 2014, Wang et al. 2015). HA and FA are mainly present in the aquatic environment while humin is mainly present in the terrestrial environment due to its insolubility in the aquatic phase (IHSS 2007). Owing to the heterogeneous functional groups (covalently linked phenolic rings), HA can easily interact with NPs through hydrophobic interactions in the aquatic environment (Szabó et al. 2017, Winkler and Ghosh 2018). Conversely, FA is more water-soluble due to deprotonation of its functional groups (hydroxyl and carboxyl groups), higher oxygen content, and low molecular weight (Schellekens et al. 2017). In seawater, NOM is usually comprised of elevated concentrations of HA and FA, excreted products, metabolic waste, and exuded polysaccharides, proteins, and lipids, which lead to the formation of complex and geographically diverse polymeric mixtures (Gibson et al. 2007).

Recently, the interactions among NPs and ecosystem components (eco-nano interface) have gained increasing attention. In the aquatic environment, NOM (mainly EPS) inevitability interacts with both primary and secondary NPs and compete for hydrophobic surfaces (Grassi et al. 2020). The EPS-NP interaction is driven by several intrinsic and extrinsic factors through various forces such as steric hindrance, electrostatic and hydrophobic bonds, which largely depend on the properties of NPs (e.g., size, concentration, and surface functionalization,), EPS (e.g., charge, concentration, and functional groups), and medium (e.g., pH, salinity, and ionic strength)(Philippe and Schaumann 2014). Therefore, these interactions can regulate the colloidal behavior of NPs by provoking additional electrosteric stabilization or inducing destabilization by enhancing bridging mechanisms in aquatic environment. Further, such interfaces not only influence the bioavailability and biological impacts of NPs but also change their environmental fate, distribution, and transportation by modifying their sinking or floating behavior (Nasser et al. 2020). Importantly, the impacts of bio-nano interactions have been extensively studied for nanoparticles in terms of their internalization potential and ultimately changed toxicity potential both with in vivo and in vitro models (Kihara et al. 2020, Lin et al. 2017, Pulido-Reyes et al. 2017), albeit studies on eco-nano interface are elusive yet.

The interaction of NPs with the totality of NOM (especially EPS) can lead to the development of diverse biomolecular coating on the surface of NPs, collectively known as eco-corona (Lynch et al. 2014). The suspension of NPs with EPS in the aquatic environment can result in tightly coated layers on the surface of NPs or develop a composite network embedding individual NP particles, turning into aggregates (Grassi et al. 2020). Moreover, the dispersion of NPs in the aquatic environment confers some degree of polydispersity resulting in their complex interactions with EPS. The EPS-NP interaction in natural water is a complex process and this cannot be simply viewed as the formation of aggregates or a uniform molecular layer on the particle surface. The adsorption of EPS on NPs can portray a competing phenomenon in the aquatic environment, where aggregates can be formed due to high salinity, while the development of eco-corona can disrupt this process (Wang et al. 2021b).

Although the studies highlighting eco-corona formation on NPs in the natural environment are in their infancy stage, the impacts of eco-corona in altering the properties and toxicity of NPs have been highlighted in recent studies (Fadare et al. 2020, Grassi et al. 2020, Saavedra et al. 2019). Further, the inclusion of the eco-corona concept in nanotoxicity testing is highly encouraged to obtain ecologically rational results (Nasser et al. 2020). Interestingly, recent studies on the ecological effects of NPs mediated eco-corona showed contrasting results, e.g., the formation of eco-corona increased the uptake of NPs and enhanced their toxicity to Daphnia magna (Nasser and Lynch 2016); meanwhile, the protective role of eco-corona against NPs’ toxicity to Daphnia magna has been also reported (Saavedra et al. 2019). Similarly, the eco-corona formation increased the cell viability and reduced the oxidative stress and membrane permeability in marine algae Chlorella sp. (Natarajan et al. 2020). These studies showed that our knowledge of the eco-corona formation on NPs and associated ecological impacts in the aquatic environment is still not comprehensive (Fadare et al. 2020). Therefore, to gain a sufficiently broad knowledge and solve eco-corona riddles, huge datasets are required for many different combinations of NPs and EPS and their potential interactions. Hence, this review collates the knowledge on the documented studies regarding the eco-corona formation on NPs and associated implications in the aquatic environment with the following objectives: (1) presenting precise background information on the sources and occurrence of NPs and EPS and the basic difference between eco-corona and bio-corona formation, (2) providing potential methods for characterization and quantification of eco-corona and its composition, (3) highlighting factors affecting the eco-corona formation such as characteristics of NPs, properties of biomolecules, and physicochemical characteristics of the aquatic environment, (4) elucidating change in ecological implications of NPs mediated by eco-corona (both toxic and non-toxic), and (5) summarizing the existing challenges and future research directions regarding eco-corona formation on NPs in the aquatic environment.

This systematic review was compiled in compliance with principles recommended in the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) method (Moher et al. 2010). More details on the implementation steps of the PRISMA method are shown in Text S3 of the supplementary information.

Section snippets

Sources, fate and implications of nanoplastics in the aquatic environment

Generally, NPs are defined as plastic particles with a size between 1 nm and 1000 nm (Gigault et al. 2018); however, some studies have suggested a maximum size of 100 nm (Besseling et al. 2019). Conventional wastewater treatment plants (WWTPs) are not designed to remove NPs from the wastewater, inevitably releasing them to aquatic resources (Kihara et al. 2020). Important sources and processes involved in the generation and formation of NPs in the aquatic environment are presented in Fig. 1.

Eco-corona vs. bio-corona formation: the basic concept

The term “environmental- or eco-corona” is defined as an environmentally acquired encapsulation of synthetic particles (plastic or non-plastic) by biomolecules such as proteins, carbohydrates, etc. (Baalousha et al. 2018, Grassi et al. 2020). This paradigm has been recently translated from “protein- or bio-corona, which is the robust coating of nanomaterials (NMs) with a layer of biomolecules upon entering into an in vivo biological environment (Cedervall et al. 2007). After entering into the

Eco-corona formation on nanoplastics in the aquatic environment

Recently, multiple studies highlighted the eco-corona formation on NPs under laboratory conditions, mediated by organism secreted EPS (proteins, carbohydrates, etc.) or through artificially added NOM (HA, FA, and alginate) in aquatic mediums. However, studies demonstrating this phenomenon in natural waters are elusive yet. A summary of recent studies elucidating the eco-corona formation on NPs in the presence of freshwater and marine organisms is given in Table 1.

Regarding freshwater scenarios,

Potential methods for eco-corona measurement in the aquatic environment

Potential techniques for the identification and quantification of eco-corona formation on NPs and their composition in the aquatic environment are presented in Fig. 3. Several factors are involved in eco-corona formation on NPs in the aquatic environment (section 6). The impact of size, composition, biological and physicochemical properties of eco-corona is largely unknown yet (Natarajan et al. 2020). However, it is well defined that biogenic aggregates in the aquatic environment exhibit unique

Factors affecting eco-corona formation on nanoplastics

Studies are still elusive that highlighted specific influencing factors involved in eco-corona formation on NPs in the aquatic environment (Shiu et al. 2020a). Generally, three main elements can describe the interaction between NPs and biomolecules in the aquatic environment: (1) the size, aging, and surface properties of NPs, (2) the physicochemical characteristics of the aquatic environment, and (3) the levels, composition and functional properties of biomolecules (Fig. 4, Table 1 & 2).

Ecological implications of eco-corona formation in the aquatic environment

Recent studies showed that EPS or biomolecules encapsulate NPs in the aquatic environment and modify their physicochemical properties, bioreactivity, and transportation through eco-corona formation (Alimi et al. 2018, Galloway 2015, Pulido-Reyes et al. 2017). Therefore, eco-corona can influence the environmental fate and bioavailability of NPs and ultimately change their ecological impacts (toxic and non-toxic) in the aquatic environment (Fadare et al. 2020, Nasser et al. 2020,

Clarifying the role of nanoplastic properties

It is still challenging to understand the role of NP properties in the formation of eco-corona and how those properties influence the interactions among NPs and EPS. So far, the reviewed studies employed PS as model NPs with selected functional groups (COOH-, NH2-), surface charges, and sizes to decipher their interactions with EPS under laboratory conditions. In the natural aquatic environment, primary and secondary NPs are more heterogeneous, exhibiting various polymer type, composition,

Conclusion

This review summarized the documented studies highlighting the eco-corona formation on NPs and associated ecological implications in the aquatic environment. In the aquatic environment, NPs are encapsulated by eco-corona, comprised of secreted biomolecules including DNA, proteins, and carbohydrates, as well as of allochthonous compounds such as HA and FA. The eco-corona formation is influenced by various factors such as characteristics of NPs, properties of EPS, and physicochemical parameters

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

This study was funded by the National Key Research and Development Program of China (2018YFD0900604), Guangdong Province Universities and Colleges Pearl River Scholar Funded Scheme (2018), the National Natural Science Foundation of China (42077364), and Key Research Projects of Universities in Guangdong Province (2019KZDXM003 and 2020KZDZX1040).

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