ArticlePDF Available

Secondary nanoplastics released from a biodegradable microplastic severely impact freshwater environments

Authors:
Miguel gonzalez pleiter at University of Alcalá
Miguel gonzalez pleiter
Miguel Tamayo Belda at Universidad Autónoma de Madrid
Miguel Tamayo Belda
Gerardo Pulido-Reyes at Universidad Autónoma de Madrid
Gerardo Pulido-Reyes
Georgiana Amariei at University of Alcalá
Georgiana Amariei
Show all 7 authorsHide
Download full-text PDFDownload full-text PDF
Read full-text
Download citation

Abstract

Over the last five decades, plastics production has increased as a consequence of their use in strategic sectors causing damage on aquatic ecosystems. In this context, biodegradable plastics have emerged as an ecological alternative because they are easily degradable in the environment. Despite the recent advances in the field of plastic ecotoxicology, the ecological impact of secondary nanoplastics (nanoplastics resulting from natural degradation of micro and macro plastics) in the environment remains poorly understood. Here, we have investigated the effects of secondary nanoplastics of polyhydroxybutyrate (PHB), a biodegradable plastic, on three representative organisms of aquatic ecosystems. Secondary PHB-nanoplastics were produced from PHB-microplastics by abiotic degradation under environmentally representative conditions. Secondary PHB-nanoplastics induced a significant decrease in cellular growth and altered relevant physiological parameters in all organisms. We investigated whether the observed toxicity was exerted by PHB-nanoplastics themselves or by other abiotic degradation products released from PHB-microplastics. An experiment was run in which PHB-nanoplastics were removed by ultrafiltration; the resulting supernatant was not toxic to the organisms, ruling out the presence of toxic chemicals in the PHB-microplastics. In addition, we have performed a complete physicochemical characterization confirming the presence of secondary PHB-nanoplastics in the 75–200 nm range. All results put together indicated that secondary PHB-nanoplastics released as a consequence of abiotic degradation of PHB-microplastics were harmful for the tested organisms, suggesting that biodegradable plastic does not mean safe for the environment in the case of PHB.
Link to Secondary nanoplastics released from a biodegradable microplastic severely impact freshwater environmen
ts.pdf
Content uploaded by Roberto Rosal
Author content
All content in this area was uploaded by Roberto Rosal on Aug 23, 2024
Content may be subject to copyright.
Link to Secondary nanoplastics released from a biodegradable microplastic severely impact freshwater environmen
ts.pdf
Content uploaded by Roberto Rosal
Author content
All content in this area was uploaded by Roberto Rosal on Aug 21, 2024
Content may be subject to copyright.
Secondary nanoplastics released from a biodegradable
microplastic severely impact freshwater environments
Miguel González-Pleiter1,*, Miguel Tamayo-Belda1, Gerardo Pulido-Reyes1, Georgiana Amariei2, Francisco
Leganés1, Roberto Rosal2 and Francisca Fernández-Piñas1
1 Department of Biology, Faculty of Science, Universidad Autónoma de Madrid, Spain
2 Department of Chemical Engineering, Universidad de Alcalá, E-28871 Alcalá de Henares, Spain
* Corresponding author: mig.gonzalez@uam.es
Abstract
Over the last five decades, plastics production has increased because of their use in strategic sectors causing damage on
aquatic ecosystems. In this context, biodegradable plastics have emerged as an ecological alternative because they are easily
degradable in the environment. Despite the recent advances in the field of plastic ecotoxicology, the ecological impact of
secondary nanoplastics (nanoplastics resulting from natural degradation of micro and macro plastics) in the environment
remains poorly understood. Here, we have investigated the effects of secondary nanoplastics of polyhydroxybutyrate (PHB),
a biodegradable plastic, on three representative organisms of aquatic ecosystems. Secondary PHB-nanoplastics were
produced from PHB-microplastics by abiotic degradation under environmentally representative conditions. Secondary PHB-
nanoplastics induced a significant decrease in cellular growth and altered relevant physiological parameters in all organisms.
We investigated whether the observed toxicity was exerted by PHB-nanoplastics themselves or by other abiotic degradation
products released from PHB-microplastics. An experiment was run in which PHB-nanoplastics were removed by
ultrafiltration; the resulting supernatant was not toxic to the organisms, ruling out the presence of toxic chemicals in the PHB-
microplastics. In addition, we have performed a complete physicochemical characterization confirming the presence of
secondary PHB-nanoplastics in the 75–200 nm range. All results put together indicated that secondary PHB-nanoplastics
released because of the abiotic degradation of PHB-microplastics were harmful for the tested organisms, suggesting that
biodegradable plastic does not mean safe for the environment in the case of PHB.
https://doi.org/10.1039/C8EN01427B
This article is part of the themed collection: Environmental Science: Nano Recent HOT Articles
https://pubs.rsc.org/en/journals/articlecollectionlanding?sercode=en&themeid=280a89ca-3eed-4abe-
ae65-c856206f6c3c
Article selected by the Editors in Chief of Environmental Science journals:
For some reason, RG believes this postprint is protected by RSC copyright, but this is
not the case. You can download the full text from the links below:
Link to full text
https://rosal.web.uah.es/publications/Secondary%20nanoplastics%20released%20from%20a%20biodegradable%
20microplastic%20severely%20impact%20freshwater%20environments.pdf
... Despite compostability claims, PLA may not completely degrade in realistic environmental conditions, particularly aquatic systems [86,87]. Although PLA and PHB may disintegrate faster than petroleum-based plastics, they still pose significant risks to exposed biota, such as inducing down-regulation of stress, detoxification, skeletogenic, and developmental genes in sea-urchins [88], inhibiting growth in cyanobacteria [89], and causing digestive constraints on amphipods [90]. This study demonstrates that MPs originating from purportedly biodegradable polymers, widely adopted as alternatives to traditional plastics, contaminate aquatic biota. ...
Microplastic in bivalves of an urbanized Brazilian estuary: Human modification, population density and vegetation influence
Article
  • Nov 2024
  • J HAZARD MATER
Microplastics (MPs) global ubiquitously affects particularly coastal regions under significant anthropogenic pressures, where there are limited monitoring efforts. Bivalves are valuable sentinels of MPs contamination. This investigation determined MP contamination in oysters, clams, and mussels at Santos-São Vicente, a heavily urbanized estuary in Brazil, focusing on socio-environmental predictors, spatial distribution, and interspecies variations. Elevated MPs levels were linked to higher human modification (β = 0.5747, p = 0.0223) and reduced population density (β = -8.918e-06, p = 0.0443), regardless of vegetation cover (p > 0.05). Such a negative connection between population density and MP contamination occurred due to the significant presence of industrial and port activities, leading to high MP discharges despite a low population. The simultaneous presence of the three species at specific sites is an intrinsic limitation for broad spatial studies, depending on their environmental availability. Despite higher concentrations in clams, mussels and oysters also exhibited spatial variations in MP concentrations, serving as suitable sentinels. The central and left segments of the estuary displayed elevated MP concentrations, consistent with a well-known contamination gradient. Clams accumulated more MPs (1.97 ± 1.37 [0.00 – 5.55] particles.g-1 ) than mussels (0.72 ± 1.07 [0.00 – 7.74] particles.g-1 ) and oysters (0.70 ± 1.03 [0.00 – 7.70] particles.g-1 ), suggesting higher bioavailability in sediments than the water column. MPs found across all species were predominantly smaller (<1,000 µm), fragments or fibers, and colorless. These discoveries lay a groundwork for prospective global investigations by linking MPs concentrations to socio-environmental predictors, contributing to the development of local mitigation measures and global discussions.
View
... On the contrary, the potential negative effects of P3HB degradation products on terrestrial or freshwater organisms are well recognized (González-Pleiter et al. 2019). In addition, the P3HB degradation product such as 3-hydroxybutyric acid (3-HB) has been reported to play a significant signaling role in the global regulation processes of eukaryotic cells (Puchalska and Crawford 2017). ...
Effect of stabilized organic amendments on biodegradability of poly-3-hydroxybutyrate, soil biological properties, and plant biomass
Article
Full-text available
  • Sep 2024
Poly-3-hydroxybutyrate (P3HB) is a biodegradable polymer with a potential extensive use in agriculture. However, while P3HB biodegradation boosts microbial enzyme activity, it significantly reduces plant biomass due to nutrient competition. In this study, we test the hypothesis that these detrimental effects can be mitigated though the co-application of nutrient-rich organic amendments, such as compost and digestate. A pot experiment with lettuce ( Lactuca sativa ), grown in soil amended with P3HB lone or combined with either compost or digestate. Six variants were tested: Control, Compost, Compost + P3HB, Digestate, Digestate + P3HB, and P3HB alone. We evaluated degradation of the P3HB polymer, biological soil properties, and both the dry and fresh biomass of the lettuce. We observed that adding P3HB alone enhanced dehydrogenase and urease activities, as well as all types of respiration, except for L-arginine-induced respiration. However, it strongly and negatively affected the biomass of lettuce (both aboveground and root). The strong adverse effects of P3HB on plant growth were also observed when compost was co-applied, although this combination enhanced all enzyme activities except for suppressed β -glucosidase. Conversely, co-applying digestate with P3HB alleviated the negative effect of P3HB on both the dry and fresh biomass together lettuce. Additionally, this combination increased the activity of several enzymes (dehydrogenase, arylsulfatase, N -acetyl- β - D -glucosaminidase, urease), and enhanced all types of respiration, except for L -arginine-induced respiration. The use of biodegradable plastics in agriculture is on rise, but it may be compromised, because their biodegradation my negatively impact plant growth. The results showed that co-application of digestate is an effective solution to alleviate these effects, while co-application of compost failed. Generally, organic amendments seem to be an option to alleviate the negative effects of bioplastics biodegradation, and offers options how to handle the treatment of waste bioplastics or their residues, but further investigation is needed to understand the underlaying mechanisms involved. Graphical Abstract
View
View
View
View
Micropollutants in Environment: Sources, Ecotoxicity, and Strategies for Remediation
Chapter
  • Oct 2024
Micropollutants are burgeoning threats to the environment and human health. Several micro-scaled chemical contaminants like pharmaceutical products, textile dyes, antibiotics, pesticides, and microplastics are regularly released into the environment and invade the food chain. Humans can directly inhale these micropollutants or ingest via food media. Many of such micropollutants fuel adverse health issues in both animals and humans. Essential information regarding micropollutants is maintained in several databases like The German Centre for Micropollutants, EU Pesticide Database, and Pesticide Properties Database. Certain micropollutants mimic steroid hormones and promote cancer development. In addition, micropollutants having allergic potential favor the onset of pulmonary illnesses like acute respiratory distress syndrome. Microparticles of pesticides are readily absorbed inside tissues and disrupt redox homeostasis and immune cascades. Several measures have been implemented to degrade micropollutants in drinking water to limit unintentional exposure. Approaches involving physicochemical, biological, and advanced oxidation processes are being implemented to degrade micropollutants in the environment. However,further advancements in such treatment measures are warranted for more efficient removal of micropollutants from the environment. Keywords: Micropollutants, pesticides, antibiotics, environmental contaminants
View
View
View
View
View
Age-dependent survival, stress defense, and AMPK in Daphnia pulex after short-term exposure to a polystyrene nanoplastic
Article
Full-text available
  • Oct 2019
  • AQUAT TOXICOL
The widespread occurrence and accumulation of micro- and nanoplastics in aquatic environments has become a growing global concern. Generally, natural aquatic populations are characterized by a variety of multi-structured age groups, for which physiological and biochemical responses typically differ. The freshwater cladoceran, Daphnia pulex, is a model species used extensively in environmental monitoring studies and ecotoxicology testing. Here, the effects of a polystyrene nanoplastic on the physiological changes (i.e., survival) and expression levels of stress defense genes (i.e., those encoding antioxidant-mediated and heat shock proteins) in this freshwater flea were measured. Results from acute bioassays were used to determine the respective nanoplastic LC50 values for five age groups (1-, 4-, 7-, 14- and 21-day-old individuals): the obtained values for the 1- and 21day-old D. pulex groups were similar (i.e., not significantly different). The expression levels of genes encoding key stress defense enzymes and proteins—SOD, CAT, GST, GPx, HSP70, and HSP90—were influenced by the nanoplastic in all the age groups, but not in the same way for each. Significant differences were observed among all age groups in their expression of the gene encoding the energy-sensing enzyme AMPK (adenosine monophosphate-activated protein kinase) α, β, and γ following exposure to the nanoplastic. Moreover, the expression of AMPK α was significantly increased in the 1-, 7-, and 21-day-old individuals exposed to nanoplastic relative to the control group. Together, these results indicate that age in D. pulex affects the sensitivity of its individuals to pollution from this nanoplastic, primarily via alterations to vital physiological and biochemical processes, such as cellular energy homeostasis and oxidation, which were demonstrated in vivo. We speculate that such agerelated effects may extend to other nanoplastics and forms of pollution in D. pulex and perhaps similar marine organisms.
View
Mechanism of toxic action of cationic G5 and G7 PAMAM dendrimers in the cyanobacterium Anabaena sp. PCC7120
Article
Full-text available
  • Jan 2019
Nowadays, nanomaterials are extensively used worldwide in many different fields and their potentially serious effects in aquatic ecosystems have become a global concern. In this study, we have investigated the effect of two nanometric manufactured polymers, high-generation cationic G5 and G7 poly(amidoamine) dendrimers, in a prokaryotic primary producer of aquatic ecosystems, the filamentous cyanobacterium Anabaena sp. PCC7120. Dendrimers significantly decreased the growth of the cyanobacterium and they induced morphological alterations both at the filaments and single cell level. Furthermore, the exposure to dendrimers induced significant alteration in several physiological parameters of the cyanobacterium: intracellular reactive oxygen species overproduction, damage in membrane integrity, membrane potential alterations, increase of metabolic activity, acidification of intracellular pH, oxidative DNA damage and alteration of intracellular free Ca2+ homeostasis. Dendrimers also induced alterations in the photosynthesis of Anabaena: decrease in oxygen evolution and in PSII activity, alteration in different photochemical events and in chlorophyll a content. Moreover, both dendrimers were internalized into cyanobacterial cells. In conclusion, high-generation cationic dendrimers exhibited high toxicity towards Anabaena severely affecting several physiological, morphological and photosynthetic parameters.
View
Leachate From Expanded Polystyrene Cups Is Toxic to Aquatic Invertebrates (Ceriodaphnia dubia)
Article
Full-text available
  • Feb 2018
Expanded polystyrene (EPS) products and their associated chemicals (e.g., styrenes) are widespread in the marine environment. As a consequence, bans on their use for single-use packaging materials are being proposed in several municipalities. To better understand how science can inform decision-making, we looked at the available scientific literature about contamination and effects and conducted experiments to measure chemical leachate from polystyrene products and toxicity from the leachate. We conducted leaching experiments with common food matrices (water, soup broth, gravy, black coffee and coffee with cream and sugar) at relevant temperatures (70 and 95°C) that are consumed in or with several polystyrene products (coffee cup lids, polystyrene stir sticks, polystyrene spoons, EPS cups, EPS bowls, and EPS takeout containers). We analyzed each sample for styrene, ethylbenzene, toluene, benzene, meta- and para- xylene, isopropylbenzene, and isopropyltoluene—chemicals associated with polystyrene products. To determine whether the leachates are toxic, we conducted chronic toxicity tests, measuring survival and reproductive output in Ceriodaphnia dubia. Toxicity tests included nine treatments: seven concentrations of ethylbenzene, EPS cup leachate and a negative control. Overall, we found that temperature has a significant effect on leaching. We only detected leachates in trials conducted at higher temperature −95°C. Ethylbenzene was the only target analyte with final concentrations above the method limit of detection, and was present in the greatest concentrations in EPS and with soup broth. Measurable concentrations of ethylbenzene in the leachate ranged from 1.3 to 3.4 μg/L. In toxicity tests, the calculated LC50 for ethylbenzene was 14 mg/L and the calculated LC20 was 210 μg/L. For the treatment exposed to the EPS cup leachate, mortality was 40%—four times greater than the negative control. Finally, there was no significant difference (p = 0.17) between reproductive output for any treatment with ethylbenzene, but there was a significant reduction (p = 0.01) in reproductive output for the treatment exposed to the EPS leachate compared to the negative control. Thus, although the target analyte ethylbenzene was not toxic at concentrations detected in the leachate, significant adverse effects were detected in the whole EPS cup leachate sample.
View
Analysis, Occurrence, and Degradation of Microplastics in the Aqueous Environment
Chapter
Full-text available
  • Jan 2018
Synthetic polymers are one of the most significant pollutants in the aquatic environment. Most research focused on small plastic particles, so-called microplastics (particle size, 1–5,000 μm). Compared to macroplastics, the small size complicates their determination in environmental samples and demands for more sophisticated analytical approaches. The detection methods of microplastics reported in the past are highly diverse. This chapter summarizes different strategies for the sampling of water and sediment and sample treatments, including the separation of plastic particles and removal of natural debris that are necessary prior the identification of microplastics. Moreover, the techniques used for the identification of plastics particles are presented in this chapter.
View
Microplastic-Associated Biofilms: A Comparison of Freshwater and Marine Environments
Chapter
Full-text available
  • Jan 2018
Microplastics (<5 mm particles) occur within both engineered and natural freshwater ecosystems, including wastewater treatment plants, lakes, rivers, and estuaries. While a significant proportion of microplastic pollution is likely sequestered within freshwater environments, these habitats also constitute an important conduit of microscopic polymer particles to oceans worldwide. The quantity of aquatic microplastic waste is predicted to dramatically increase over the next decade, but the fate and biological implications of this pollution are still poorly understood. A growing body of research has aimed to characterize the formation, composition, and spatiotemporal distribution of microplastic-associated (“plastisphere”) microbial biofilms. Plastisphere microorganisms have been suggested to play significant roles in pathogen transfer, modulation of particle buoyancy, and biodegradation of plastic polymers and co-contaminants, yet investigation of these topics within freshwater environments is at a very early stage. Here, what is known about marine plastisphere assemblages is systematically compared with up-to-date findings from freshwater habitats. Through analysis of key differences and likely commonalities between environments, we discuss how an integrated view of these fields of research will enhance our knowledge of the complex behavior and ecological impacts of microplastic pollutants.
View
Age-dependent survival, stress defense, and AMPK in Daphnia pulex after short-term exposure to a polystyrene nanoplastic
Article
  • Aug 2018
  • AQUAT TOXICOL
The widespread occurrence and accumulation of micro- and nanoplastics in aquatic environments has become a growing global concern. Generally, natural aquatic populations are characterized by a variety of multi-structured age groups, for which physiological and biochemical responses typically differ. The freshwater cladoceran, Daphnia pulex, is a model species used extensively in environmental monitoring studies and ecotoxicology testing. Here, the effects of a polystyrene nanoplastic on the physiological changes (i.e., survival) and expression levels of stress defense genes (i.e., antioxidant-mediated and heat shock proteins) in this freshwater flea were measured. Results from the acute bioassays were used to determine the respective nanoplastic LC50 values for five age groups (1-, 4-, 7-, 14- and 21-day-old individuals): the obtained values for the 1- and 21-day-old D. pulex groups were similar (i.e., not significantly different). The gene expression levels of key stress defense enzymes and proteins—SOD, CAT, GSTD, GPx, HSP70, and HSP90—were influenced by the nanoplastic in all the age groups, but not in the same way for each. Significant differences were observed among all age groups in their expression of energy-sensing enzyme AMPK (adenosine monophosphate-activated protein kinase) α, β, and γ following exposure to the nanoplastic. Moreover, the expression of AMPK α was significantly increased in the 1-, 7-, and 21-day-old individuals exposed to nanoplastic relative to the control group. Together, these results indicate that age in D. pulex affects the sensitivity of its individuals to pollution from this nanoplastic, primarily via alterations to vital physiological and biochemical processes, such as cellular energy homeostasis and oxidation, which were demonstrated in vivo. We speculate that such age-related effects may extend to other nanoplastics and forms of pollution in D. pulex and perhaps similar marine organisms.
View
Distribution of Microplastics and Nanoplastics in Aquatic Ecosystems and Their Impacts on Aquatic Organisms, with Emphasis on Microalgae
Chapter
  • Jun 2018
Plastics, with their many useful physical and chemical properties, are widely used in various industries and activities of daily living. Yet, the insidious effects of plastics, particularly long-term effects on aquatic organisms, are not properly understood. Plastics have been shown to degrade to micro- and nanosize particles known as microplastics and nanoplastics, respectively. These minute particles have been shown to cause various adverse effects on aquatic organisms, ranging from growth inhibition, developmental delay and altered feeding behaviour in aquatic animals to decrease of photosynthetic efficiency and induction of oxidative stress in microalgae. This review paper covers the distribution of microplastics and nanoplastics in aquatic ecosystems, focusing on their effects on microalgae as well as co-toxicity of microplastics and nanoplastics with other pollutants. Besides that, this review paper also discusses future research directions which could be taken to gain a better understanding of the impacts of microplastics and nanoplastics on aquatic ecosystems.
View
View
Current opinion: What is a nanoplastic?
Article
  • Jan 2018
  • ENVIRON POLLUT
Abstract With the large amount of attention being given to microplastics in the environment, several researchers have begun to consider the fragmentation of plastics down to lower scales (i.e., the sub-micrometer scale). The term “nanoplastics” is still under debate, and different studies have set the upper size limit at either 1000 nm or 100 nm. The aim of the present work is to propose a definition of nanoplastics, based on our recently published and unpublished research definition of nanoplastics. We define nanoplastics as particles unintentionally produced (i.e. from the degradation and the manufacturing of the plastic objects) and presenting a colloidal behavior, within the size range from 1 to 1000 nm.
View
Microplastics in freshwater systems: A review on occurrence, environmental effects, and methods for microplastics detection
Article
  • Dec 2017
  • WATER RES
Defined as plastic debris of size less than 5mm, microplastics have become emerging contaminants in recent years with increasing plastic production and poor management of plastic waste. Though freshwater environment is often closely connected to microplastics origins and acts as the pathway of microplastics transferring to oceans, limited studies have focused on freshwater bodies when compared with marine studies. The significance of assessing microplastics contamination in freshwater systems has been observed recently because of its prevalent occurrence (even in drinking water) and high abundance in this environment. Since the environmental effects can include adsorption of persistent organic pollutant, bioaccumulation and bacteria transfer media, a more comprehensive understanding of microplastics in freshwater systems is necessary. However, at current stage, the fact remains that no standardized method has been established for effective quantification and identification of microplastics. In addition, the difficulty to apply analytical methods in marine researches to freshwater samples was observed because these miroplastics usually have smaller sizes. Therefore, it is unlikely to reveal microplastics contamination levels in reality and compare results from different sources. These technical difficulties should be solved as the first priority to understand the distribution and nature of microplastics in surrounding freshwater environments and provide following studies on environmental behavior with practical support. Given these facts, we first briefly evaluate the occurrence and sources of microplastics in freshwater environment from literature and present the possible environmental behavior of microplastics which are associated with health concerns. Then, we highlighted sampling and identification methods for detecting microplastics in freshwater environment from existing studies to reveal the current research status. Robust and reliable methods are of urgent need to be developed and more studies on monitoring microplastics in freshwaters should be conducted. Only with sufficient knowledge of microplastics distribution can academic institutions, stake-holders and government take appropriate actions to address microplastics contamination.
View