Temporospatial nano-heterogeneity of self-assembly of extracellular polymeric substances on microplastics and water environmental implications
Graphical Abstract
Aging-caused Nanochemical heterogeneity of MP determined heterogeneity of EPS assembly.
Introduction
Microplastics (MPs) are emerging and ubiquitous particulate pollutants in various aquatic environments from freshwater to ocean (Andrady, 2011) and have been proven to be toxic to many aquatic organisms (Law and Thompson, 2014). MPs can be originally micrometer size or derived from large plastic pieces after mechanical crushing (Luo et al., 2020), long-term natural aging (Potrykus et al., 2021), or biodegradation processes (Auta et al., 2017). Aging significantly modifies the surface properties of MPs such as hydrophobicity (Luo et al., 2022) and this makes their environmental behavior, ecological and toxic effects on aquatic organisms more complicated. For example, MPs are well known as carriers for persistent organic pollutants (POP) and microbial pathogens (Zhang et al., 2019), and provide a venue for the exchange of antibiotic resistance genes (Mammo et al., 2020). The carrier role of MPs is strongly affected by their surface hydrophobicity and interaction with chemical pollutants (Mizukawa et al., 2013). Aging of MPs increases its surface hydrogen bonding, hydrophilicity and specific surface area and thus affect its carrying capacity for pollutants or microbes (Rai et al., 2020).
Extracellular polymeric substances (EPS) from microorganisms, mainly composed of polysaccharides, proteins and related lipid derivatives, are ubiquitous in various water environment (Zhang et al., 2010). In light of this, interaction between MPs and EPS is inevitable in water environments. EPS usually show amphiphilicity due to the presence of amphiphilic proteins and polysaccharides with various functional groups such as carboxyl and amide groups (Pan et al., 2010), they can be spontaneously assembled to solid surface and play significant roles in biofilm formation (Kong et al., 2021). Self-assembly of EPS to solid surface (e.g., MP surface) will significantly modify the surface physicochemical characteristics (e.g., charge and hydrophobicity) and this will further influence subsequent interfacial processes (Galloway et al., 2017). The interaction of EPS with MPs have profound influences on many ecological and environmental processes in aquatic environments, including colonization of microbes as biofilms on MPs, adsorption of pollutants, aggregation of MPs or with other colloids, transport and fate, bioavailability and ecotoxicity of MPs to aquatic organisms (Besseling et al., 2017), and eventually affect the normal operation of aquatic ecosystems (Camacho et al., 2019). For example, once MPs enter the aquatic system, they could be rapidly colonized by biofilms due to formation of EPS microlayers on MP surface (Amaral-Zettler et al., 2020). Its surface adhesion allows to gather more inorganic/organic substances, cause agglomeration, biodegradation, and then change its fate (Rummel et al., 2017). In addition, the adsorption of dissolved organic matter including EPS to MPs may have effects on release of additives in MPs, and affects the bioavailability and transformation in the water environment (Wu et al., 2018). Recently, Junaid and Wang have systematically reviewed the interaction of nanoplastics (NPs) with EPS in the aquatic environment with special reference to eco-corona (biomolecular coating on the nanoparticle surface) formation and associated impacts (Junaid and Wang, 2021).
Although a few studies with focus on the impacts of EPS coating (eco-corona) on MPs/NPs on toxicity of NPs (Fadare et al., 2020, Grassi et al., 2020) have ignited the interest to include eco-corona concept in nanotoxicity test to obtain ecologically rational results, some basic processes and mechanisms of EPS self-assembly to MPs are not well elucidated. To date, little information is available on the spontaneous adsorption (self-assembly) behavior of EPS on MPs in water environments. The self-assembly of EPS to MPs or NPs is a complex process and this cannot be simply viewed as the formation of a uniform molecular layer on the particle surface (Junaid and Wang, 2021). On one hand, EPS are a mixture of a variety of macromolecules with different physicochemical properties. Different components with different adhesion affinity may compete with each other to adhered to MP surface successively. On the other hand, surface of MPs is actually not homogeneous at micrometer scale since additives are physically incorporated into plastic in most cases. The physical heterogeneity of plastic components determines the heterogeneity of surface chemistry, and the latter must have significant impacts on self-assembly of EPS on MP surface. Different components, depending on their affinity to MP surface and micro-scale heterogeneity of MP surface, may be assembled to different sites, and thus form heterogeneous microstructure of the EPS coating. When the plastic surface is aged, the heterogeneity of surface chemistry must be increased and this makes the self-assembly of EPS on MP surface much more complicated. However, what a temporal order of self-assembly of EPS on MP surface follows and how aging degree influence the self-assembly process and nano-heterogeneity of EPS layers on MP surface are still unclear.
The rapidly emerging technique Atomic force microscopy-based infrared spectroscopy (AFM-IR) has provided chemical analysis and compositional mapping with spatially nanoscale resolution (Dazzi and Prater, 2017). The AFM-IR technique has unique advantages of high sensitivity, nano-level spatial resolution and the ability to detect functional groups, nanomechanical and nanothermal information. It has been proven to be an ideal cutting-edge instrument in the field of MPs.
In this study, taking the PP plastics with different aging degree as exemplified MP surfaces, we take advantage of the AFM-IR technique to get deep insight into the self-assembly sequence of EPS components on PP MP surface and nanostructure characteristics of the assembled EPS layers. The heterogeneity of nanochemistry and nanomechanics of MP surface before and after self-assembly of EPS was addressed. The self-assembly succession of major EPS components, proteins and polysaccharides, was discussed. The relationship between nano-heterogeneity of MP surface properties and the nanoscale structure and texture of the assembled EPS on MP with different aging degree was also elaborated based on analysis of IR nanospectroscopical images. Our study not only provided important insight into nanoscale self-assembly mechanisms of EPS onto MP surface and also is of great importance for scientific evaluation of environmental behavior, transport and fate, ecotoxicity, and effects of MPs on other pollutants and cycling of nutrients in the aquatic environment.
Section snippets
Materials
Polypropylene (PP) was the source of activated carbon packaging, purchased from Beijing Zhongou Purui Technology Co., Ltd., China. The aerobic activated sludge was collected in a municipal sewage treatment plant located in Hangzhou, China. The fresh sludge was sampled directly and used for the extraction of extracellular polymers (EPS).
Preparation of PP fragments
The PP film samples were obtained from market. The PP film suffered one-year naturally aging on the window-ledge, and the same PP film newly produced, were used
Nanochemical heterogeneity induced by aging
One year of natural aging caused obvious change of the PP MP surface. The aged surface become rougher with many debris (Fig. 1a, b). The water contact angle of fresh and aged PP MP surface was shown in Fig. S1. The maximum contact angle of the fresh sample was 115.9 ± 6.35°, obviously larger than that of the aged sample (94.6 ± 1.18°), indicating that the surface of the aged sample was hydrophilic while the fresh surface was relatively hydrophobic.
The increased hydrophilicity of MP surface
Conclusions
This study investigated the temporospatial heterogeneity of self-assembly of EPS onto MPs with different aging degree using the cutting-edge AFM-IR technique. It was found one year of natural aging of MPs led to high degree fragmentation physically and chemically at nano scale. Self-assembly of EPS to MPs was significantly influenced by EPS components and aging degree of plastic surface. The polysaccharides were assembled to PP MP surface faster than the proteins. Initially, polysaccharides and
Environmental implications
This study showed that components of EPS can be spontaneously and successively assembled to MP surface with nanoscale spatial hetereogeneity, which depends on nanochemical heterogeneity induced by natural aging. These findings are of importance for understanding the environmental behavior of MPs and its impact on some key ecological and environmental processes. Self-assembly of EPS to MP surface forms eco-corona of MPs and this will significantly influence the aggregation, settlement and
CRediT authorship contribution statement
Shuyan Xu: Investigation, Writing- Original draft preparation, Caiqin Wang: Supervision, Pengfeng Zhu: Investigation, Daoyong Zhang: Funding acquisition, Resources, Supervision, Xiangliang Pan: Conceptualization, Supervision, Methodology, Writing- Reviewing and Editing.
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.
Acknowledgements
This work was supported by the National Natural Science Foundation of China (U1703243).
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