RESUMO
Although massive studies have investigated the spatiotemporally occurring marine plastisphere, a new microbial ecosystem colonizing the surfaces of plastics, the resulting biofragmentation process and impacts of plastics on biogeochemical cycles remain largely unknown. Here, we leverage synchrotron-based Fourier transform infrared spectromicroscopy (FTIR mapping) and metagenomic sequencing to explore independent marine microcosms amended with petroleum-based polyethylene (PE) and biobased polyhydroxybutyrate (PHB) plastic films. FTIR mapping results demonstrate unequal fragmentation scenarios by which the PE plastic rarely releases oxidized fragments while PHB disintegrates quickly, gradually forming fragments composed of extracellular polymeric substances resembling plastic films. Metagenomic analysis shows the critical role of hydrocarbonoclastic lineages in the biodegradation of the two plastics by the fatty acid degradation pathway, where the PE plastics host different microbial trajectories between the plastisphere (dominated by Alcanivorax) and surrounding seawater. In contrast, the PHB addition demonstrates decreased microbial richness and diversity, consistent community composition (dominated by Phaeobacter and Marinobacter), and apparently stimulated sulfur cycle and denitrification pathways in both the plastisphere and surrounding seawater. Our study gives scientific evidence on the marine biotic processes distinguishing petroleum- and biobased plastics, highlighting marine PHB input exerting straightforward impacts on the water phase and deserving critical management practices.
Assuntos
Plásticos , Polietileno , Biodegradação Ambiental , Água do Mar/microbiologia , Água do Mar/química , Hidroxibutiratos/metabolismo , Poliésteres/químicaRESUMO
The insect Tenebrio molitor exhibits ultrafast efficiency in biodegrading polystyrene (PS). However, the generation and fate of nanoplastics (NPs) in the intestine during plastic biodegradation remain unknown. In this study, we investigated the biodegradation of PS microplastics (MPs) mediated by T. molitor larvae over a 4-week period and confirmed biodegradation by analyzing Δδ13C in the PS before and after biotreatment (-28.37 versus -24.88) as an effective tool. The ·OH radicals, primarily contributed by gut microbiota, and H2O2, primarily produced by the host, both increased after MP digestion. The size distribution of residual MP particles in excrements fluctuated within the micrometer ranges. PS NPs were detected in the intestine but not in the excrements. At the end of Weeks 1, 2, 3, and 4, the concentrations of PS NPs in gut tissues were 3.778, 2.505, 2.087, and 2.853 ng/lava, respectively, while PS NPs in glands were quantified at 0.636, 0.284, and 0.113 ng/lava and eventually fell below the detection limit. The PS NPs in glands remained below the detection limit at the end of Weeks 5 and 6. This indicates that initially, NPs generated in the gut entered glands, then declined gradually and eventually disappeared or possibly biodegraded after Week 4, associated with the elevated plastic-degrading capacities of T. molitor larvae. Our findings unveil rapid synergistic MP biodegradation by the larval host and gut microbiota, as well as the fate of generated NPs, providing new insights into the risks and fate associated with NPs during invertebrate-mediated plastic biodegradation.
Assuntos
Biodegradação Ambiental , Larva , Microplásticos , Poliestirenos , Tenebrio , Animais , Microplásticos/metabolismo , Tenebrio/metabolismo , Larva/metabolismo , Plásticos/metabolismo , Microbioma GastrointestinalRESUMO
The insect Tenebrio molitor possesses an exceptional capacity for ultrafast plastic biodegradation within 1 day of gut retention, but the kinetics remains unknown. Herein, we investigated the biofragmentation and degradation kinetics of different microplastics (MPs), i.e., polyethylene (PE), poly(vinyl chloride) (PVC), and poly(lactic acid) (PLA), in T. molitor larvae. The intestinal reactions contributing to the in vivo MPs biodegradation were concurrently examined by utilizing aggregated-induced emission (AIE) probes. Our findings revealed that the intestinal biofragmentation rates essentially followed the order of PLA > PE > PVC. Notably, all MPs displayed retention effects in the intestine, with PVC requiring the longest duration for complete removal/digestion. The dynamic rate constant of degradable MPs (0.2108 h-1 for PLA) was significantly higher than that of persistent MPs (0.0675 and 0.0501 h-1 for PE and PVC, respectively) during the digestive gut retention. Surprisingly,T. molitor larvae instinctively modulated their internal digestive environment in response to in vivo biodegradation of various MP polymers. Esterase activity and intestinal acidification both significantly increased following MPs ingestion. The highest esterase and acidification levels were observed in the PLA-fed and PVC-fed larvae, respectively. High digestive esterase activity and relatively low acidification levels inT. molitor larvae may, to some extent, contribute to more efficient MPs removal within the plastic-degrading insect. This work provided important understanding of MPs biofragmentation and intestinal responses to in vivo MPs biodegradation in plastic-degrading insects.
RESUMO
It remains unknown whether plastic-biodegrading macroinvertebrates generate microplastics (MPs) and nanoplastics (NPs) during the biodegradation of plastics. In this study, we utilized highly sensitive particle analyzers and pyrolyzer-gas chromatography mass spectrometry (Py-GCMS) to investigate the possibility of generating MPs and NPs in frass during the biodegradation of polystyrene (PS) and low-density polyethylene (LDPE) foams by mealworms (Tenebrio molitor larvae). We also developed a digestive biofragmentation model to predict and unveil the fragmentation process of ingested plastics. The mealworms removed 77.3% of ingested PS and 71.1% of ingested PE over a 6-week test period. Biodegradation of both polymers was verified by the increase in the δ13C signature of residual plastics, changes in molecular weights, and the formation of new oxidative functional groups. MPs accumulated in the frass due to biofragmentation, with residual PS and PE exhibiting the maximum percentage by number at 2.75 and 7.27 µm, respectively. Nevertheless, NPs were not detected using a laser light scattering sizer with a detection limit of 10 nm and Py-GCMS analysis. The digestive biofragmentation model predicted that the ingested PS and PE were progressively size-reduced and rapidly biodegraded, indicating the shorter half-life the smaller plastic particles have. This study allayed concerns regarding the accumulation of NPs by plastic-degrading mealworms and provided critical insights into the factors controlling MP and NP generation during macroinvertebrate-mediated plastic biodegradation.
Assuntos
Poliestirenos , Tenebrio , Animais , Polietileno , Tenebrio/metabolismo , Plásticos , Larva/metabolismo , Biodegradação Ambiental , MicroplásticosRESUMO
This study explored a direct feeding of expanded polystyrene as the sole diet for breeding Tenebrio molitor larvae. Temperature and relative humidity were manipulated to evaluate polystyrene biodegradation efficiency, survival rate, and formation of micro-polystyrene residue. Efficient conditions were at temperature of 25 °C with a humidity of 65 ± 5 %. Comparative metabolomic and metabolic-metabolic network analyses was performed for visualizing detailed pathway. Possibility of forming 4 (p)-hydroxyphenylacetic acid from phenylacetic acid with further conversion to 4-methylphenol, 4-hydroxybenzaldehyde, and 4-hydroxybenzoate could be seen as a side chain route for further biodegrading process. Key species identified in the gut of T. molitor larvae included Citrobacter sp., Serratia marcescens, Klebsiella aerogenes, and Klebsiella oxytoca. Pseudomonas aeruginosa was detected only under an anaerobic condition whereas Acinetobacter sp. was present only under an aerobic condition. These results demonstrate the potential to decrease micro-polystyrene by optimizing breeding conditions and biodegradation process of polystyrene.
Assuntos
Poliestirenos , Tenebrio , Animais , Tenebrio/metabolismo , Biodegradação Ambiental , Larva/metabolismo , Microbioma Gastrointestinal/fisiologia , Bactérias/metabolismoRESUMO
Evidence for plastic degradation by mealworms has been reported. However, little is known about the residual plastics derived from incomplete digestion during mealworm-mediated plastic biodegradation. We herein reveal the residual plastic particles and toxicity produced during mealworm-mediated biodegradation of the three most common microplastics, i.e., polyethylene (PE), polystyrene (PS), and polyvinyl chloride (PVC). All three microplastics are effectively depolymerized and biodegraded. We discover that the PVC-fed mealworms exhibit the lowest survival rate (81.3 ± 1.5%) and the highest body weight reduction (15.1 ± 1.1%) among the experimental groups by the end of the 24-day experiment. We also demonstrate that the residual PVC microplastic particles are more difficult to depurate and excrete for the mealworms compared to the residual PE and PS particles by using laser direct infrared spectrometry. The levels of oxidative stress responses, including reactive oxygen species, antioxidant enzyme activities, and lipid peroxidation, are also highest in the PVC-fed mealworms. Sub-micron microplastics and small microplastics are found in the frass of mealworms fed with PE, PS, and PVC, with the smallest particles detected at diameters of 5.0, 4.0, and 5.9 µm, respectively. Our findings provide insights into the residual microplastics and microplastic-induced stress responses in macroinvertebrates under micro(nano)plastics exposure.
Assuntos
Poliestirenos , Tenebrio , Animais , Poliestirenos/toxicidade , Poliestirenos/metabolismo , Plásticos/toxicidade , Plásticos/metabolismo , Tenebrio/metabolismo , Polietileno/toxicidade , Polietileno/metabolismo , Larva/metabolismo , Microplásticos/toxicidade , Microplásticos/metabolismo , Cloreto de Polivinila/toxicidadeRESUMO
Plastic ingestion has been widely investigated to understand its adverse harms on fauna, but the role of fauna itself in plastic fragmentation has been rarely addressed. Here, we review and discuss the available experimental results on the role of terrestrial and aquatic macrofauna in plastic biofragmentation and degradation. Recent studies have shown how biting, chewing, and stomach contractions of organisms shatter ingested plastic along their digestive tracts. Gut microbial communities can play a role in biodegradation and their composition can shift according to the type of plastic ingested. Shifts in molecular weights, chemical bond forming and breaking, and changes in thermal modification detected in the plastic debris present in the faeces also suggest active biodegradation. A few studies have also shown interactions other than ingestion, such as burrowing, may actively or passively promote physical plastic fragmentation by fauna. We suggest that further investigations into the role of fauna in physical fragmentation and chemical degradation linked to active ingestion and gut associated microbiota metabolism, respectively, should be conducted to better evaluate the impact of these mechanisms on the release of micro- and nano-plastic in the environment. Knowledge on macrofauna other than marine invertebrates and terrestrial soil dwelling invertebrates is particularly lacking, as well as focus on broader types of plastic polymers.