Plastisphere on microplastics: In situ assays in an estuarine environment

https://doi.org/10.1016/j.jhazmat.2022.129737Get rights and content

Highlights

  • Pathogenic bacteria were identified on the Ny and PS-microplastic surfaces.

  • Superficial weathering and leaching of TiO2 from Ny Microplastics were evidenced.

  • The crystallinity of Ny-microplastics decreased during the assay.

  • High Cr, Mn, and Zn levels were detected on the microplastic surface biofilms.

Abstract

In this study, the influence of the plastisphere on metals accumulation and weathering processes of polystyrene (PSMPs) and nylon microplastics (NyMPs) in polluted waters during a 129 day-assay were studied. MPs were characterized through scanning electron microscopy (SEM) with Energy dispersive X-ray (EDX), X-ray diffraction (XRD), attenuated total reflectance Fourier transformed infrared (ATR-FTIR) spectroscopy, contact angle, and thermogravimetric analysis (TGA). Also Cr, Mn, Zn, Cd, Pb, and Cu in the plastisphere on MPs were analyzed during the assay. Potentially pathogenic Vibrio, Escherichia coli, and Pseudomonas spp. were abundant in both MPs. Ascomycota fungi (Phona s.l., Alternaria sp., Penicillium sp., and Cladosporium sp.), and yeast, were also identified. NyMPs and PSMPs exhibited a decrease in the contact angle and increased their weights. SEM/EDX showed weathering signs, like surface cracks and pits, and leaching TiO2 pigments from NyMPs after 42 days. XRD displayed a notorious decrease in NyMPs crystallinity, which could alter its interaction with external contaminants. Heavy metal accumulation on the plastisphere formed on each type of MPs increased over the exposure time. After 129 days of immersion, metals concentrations in the plastisphere on MPs were in the following order Cr ˃ Mn ˃ Zn ˃ Cu ˃ Pb ˃ Cd, demonstrating how the biofilm facilitates metal mobilization. The results of this study lead to a better understanding of the impact of marine plastic debris as vectors of pathogens and heavy metals in coastal environments.

Introduction

Plastics are used for several purposes, making our life easier; however, the excessive use of these materials has generated large volumes of waste in the environment. Plastic waste after long-term exposure to environmental conditions such as mechanical abrasion, wind effects, ultraviolet radiation, chemical actions, and biodegradation (Wang et al., 2017, Paul-Pont et al., 2018, Kumar et al., 2021) breaks down into small pieces (micro/nanoplastics). The presence of microplastics (MPs, plastic pieces smaller than 5 mm) and nanoplastics (PNPs, particles smaller than 1 µm), around the world is a critical issue of great concern because they are degradation-resistant and have the ability to absorb, accumulate, and transport other contaminants and pathogenic organisms present in the environment (Thompson, 2015, Pizarro-Ortega et al., 2022; Forero López et al., 2022). Furthermore, the presence of MPs/PNPs has been reported in aquatic, terrestrial, and air environments and in the organisms that inhabit them (Horton et al., 2017, Gasperi et al., 2018, Guo et al., 2020, Ocean, 2020). These plastic particles pose an ecological and toxicological threat (Sussarellu et al., 2016, Bhagat et al., 2020, Payton et al., 2020) because they can release additives (Deng et al., 2018, Luo et al., 2020) therefore, impacting on organisms causing cellular damage through oxidative stress, reduced fertility and alteration of their metabolism, among others (Cole et al., 2015, Sussarellu et al., 2016, Payton et al., 2020). Moreover, within the ecological ones, MPs as a substrate, may favor the growth of some microbiological species, generating critical changes in the food chains as well as in the phenology and survival of some species (Nava and Leoni, 2021; Lear et al., 2021; Li et al., 2021).

Like any material that enters aquatic environments, MPs rapidly become biofouled, i.e., colonized by living organisms that accumulate over time. These organisms are microbial communities (biofilms) composed of diverse bacteria, single-celled algae, diatoms, fungi, and protozoa (Rummel et al., 2017, Miao et al., 2021, Kalčíková and Bundschuh, 2021). The plastisphere is the term used to mention the microbial biofilms associated with plastics or MPs (Zettler et al., 2013). These microorganisms that form the plastisphere, develop on the surface and sometimes even inside plastics depending on the structure of the polymer (Kettner et al., 2017, Amaral-Zettler et al., 2020). The prokaryotic and eukaryotic groups that live in plastic biofilms can also include pathogenic (Kirstein et al., 2016, Amaral-Zettler et al., 2020) or hydrocarbon-degrading organisms (Delacuvellerie et al., 2019, Oberbeckmann and Labrenz, 2020, Zhang et al., 2021). In recent years, the potential hazards of microbial communities from biofilms on MPs surface have received increasing attention. Some studies have shown that MPs surfaces are enriched with certain pathogenic bacteria (Kirstein et al., 2016, Wu et al., 2019), such as Vibrio and Pseudomonas, and could also be a reservoir for faecal indicator organisms, such as E. coli.

As previously mentioned, MPs/PNPs can absorb, accumulate, and transport other pollutants present in the aquatic environment (Tang et al., 2020, Tang et al., 2021, Wang et al., 2017; Gao et al., 2021b; Liu et al., 2022; Xie et al., 2022). Moreover, it has also been evidenced that the plastisphere formed on the plastic surface and the weathering degree plays an important role in the sorption processes between plastic particles and pollutants such as heavy metals (Richard et al., 2019; Gao et al., 2021b; Liu et al., 2022; Wu et al., 2022). Likewise, laboratory studies have also demonstrated that the physicochemical variables (e.g., salinity, organic matter dissolved, pH), chemical speciation of metal ions, type of polymer and its physicochemical properties (e.g., polarity, functional groups, specific surface area, and crystallinity), affect MPs sorption behavior (Tang et al., 2020, Tang et al., 2021; Li et al., 2022). However, the nature of the multiple sorption mechanisms that occur on MPs surface and in the microparticle body is still unclear (Binda et al., 2021).

Furthermore, most publications have studied the growth of biofilm and the influence of the plastisphere on the accumulation of heavy metals as well as the weathering process of MPs under laboratory conditions (e.g., Gao et al., 2021a; Li et al., 2022; Wu et al., 2022). However, few studies have been performed in situ. This is mainly due to the multiple factors that may affect the results and can’t be controlled. For example, weather and the physico-chemical variables constantly change, making natural environments dynamic and complex. Anyway, in situ experiments help better understand the magnitude of microplastic pollution on the environment. They provide a more accurate and complete overview of the influence of all-environmental variables on the sorption behavior and aging of MPs in the presence of other pollutants. Among the few publications with in situ experiments,researchers have studied the growth of biofilm and the composition of the microbial community on the surface of MPs. It is also of great interest its possible impact on the biogeochemical cycles (e.g., phosphorus, nitrogen and carbon) (Arias-Andres et al., 2018, Chen et al., 2020, Deng et al., 2021), and accumulation and speciation distribution of heavy metals on polystyrene (Richards et al., 2019; Xie et al., 2022). However, the influence of biofilm growth on the heavy metal accumulation in MPs and how the presence of biofilm affects their aging in estuarine environments has not been studied yet. Under this context, the goals of the present study are: 1) to conduct in situ assays to analyze changes in the formation of the plastisphere as well as the structural and chemical changes in MPs (polystyrene and nylon) submerged in marine waters from the Bahía Blanca Estuary for 129 days, 2) analyze metals adsorbed on MPs and 3) analyze the surrounding water through their physicochemical characteristics.

Section snippets

Study Area

The in situ assays were conducted during Summer-Autumn (129 days, January-June 2021) in The Bahía Blanca Estuary (BBE) (38°55.5′10.52″ S; 62°03′20.75″ W) situated in the Southwestern Atlantic Ocean, Buenos Aires province (Argentina) (Fig. S1.). It is a highly polluted estuary with several chemical and petrochemical industries, sewage discharges, and intense marine traffic (Fernández Severini et al., 2018). However, it is also a Natural Reserve with emblematic species of ecological importance as

Environmental variables

It has been demonstrated that the sorption behavior of MPs in the water column mainly depends upon the physicochemical variables (e.g., pH, temperature, DOM, and salinity), the nature and intrinsic properties of polymers as well as the presence of pollutants such as heavy metals and organic contaminants, among others (Tang et al., 2020, Binda et al., 2021; Forero López et al., 2022). In this way, Fig. S2 (Supl. Material) shows how the temporal distribution of pH, salinity, DO, SPM, TPC, TPN,

Conclusion

The present contribution comprised an unprecedented multidisciplinary approach to study weathering in two types of MPs (Ny and PS), and heavy metal accumulation in their plastisphere, formed during 129 days of immersion, in a polluted estuarine environment. During the assay, pathogenic microorganisms such as Vibrio spp., Pseudomonas spp. and E. coli abounded in both types of MPs that acted as dispersal vectors of these pathogens in moving estuarine waters.

Heavy metals such as Cr and Cd

Environmental implication

The manuscript is of environmental relevance because it studies the presence of hazardous materials like microplastics and heavy metals in a marine ecosystem and their interactions with microorganisms of human health implications. Microplastics produce several impacts on the environment and one of them is the formation of the plastisphere: microorganisms that colonize plastics. This study showed that MPs surfaces acted as new niches for heterotrophic microorganisms like pathogenic bacteria and

CRediT authorship contribution statement

A.D. Forero-López: Conceptualization, Data curation, Formal analysis, Investigation, Visualization, Methodology, Supervision, Writing – original draft, Formal Analysis, Writing – review & editing. L.I. Brugnoni: Methodology, Resources, Writing – original draft, Visualization, Writing – reviewing & editing. B. Abasto: Methodology, Writing – original draft, Writing – review & editing. G.N. Rimondino: Conceptualization, Data curation, Formal analysis, Methodology, Writing – original draft, Writing

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

We thank Prof. Madeleine Raño for correcting the manuscript in English language. Also, we thank Prof. Dr. María Virginia Bianchinotti for helping us with fungi taxonomy. This study was supported by PICT 2019–2241 (FONCYT, Argentina) granted to Dr. Melisa Fernández-Severini, and PGI UNS 24/Q109 granted to Dr. Carla Spetter.

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