Biodegradation of polyethylene terephthalate by Tenebrio molitor: Insights for polymer chain size, gut metabolome and host genes

• Published in: Journal of hazardous materials 2024-03, Vol.465, p.133446, Article 133446
• Main Authors: He, Lei, Yang, Shan-Shan, Ding, Jie, Chen, Cheng-Xin, Yang, Fan, He, Zhi-Li, Pang, Ji-Wei, Peng, Bo-Yu, Zhang, Yalei, Xing, De-Feng, Ren, Nan-Qi, Wu, Wei-Min
• Format: Article
• Language: English
• Subjects: Animals; Biodegradation; Biodegradation, Environmental; Gut microbiome; Host transcriptome; Larva - metabolism; Metabolome; Plastics - metabolism; Polyethylene - metabolism; Polyethylene terephthalate; Polyethylene Terephthalates - metabolism; Polymers; Polystyrenes - metabolism; Tenebrio - metabolism; Tenebrio - microbiology; Tenebrio molitor
• ISSN: 0304-3894; 1873-3336; 1873-3336
• DOI: 10.1016/j.jhazmat.2024.133446

Polyethylene terephthalate (PET or polyester) is a commonly used plastic and also contributes to the majority of plastic wastes. Mealworms (Tenebrio molitor larvae) are capable of biodegrading major plastic polymers but their degrading ability for PET has not been characterized based on polymer chain size molecular size, gut microbiome, metabolome and transcriptome. We verified biodegradation of commercial PET by T. molitor larvae in a previous report. Here, we reported that biodegradation of commercial PET (Mw 29.43 kDa) was further confirmed by using the δ13C signature as an indication of bioreaction, which was increased from − 27.50‰ to − 26.05‰. Under antibiotic suppression of gut microbes, the PET was still depolymerized, indicating that the host digestive enzymes could degrade PET independently. Biodegradation of high purity PET with low, medium, and high molecular weights (MW), i.e., Mw values of 1.10, 27.10, and 63.50 kDa with crystallinity 53.66%, 33.43%, and 4.25%, respectively, showed a mass reduction of > 95%, 86%, and 74% via broad depolymerization. Microbiome analyses indicated that PET diets shifted gut microbiota to three distinct structures, depending on the low, medium, and high MW. Metagenome sequencing, transcriptomic, and metabolic analyses indicated symbiotic biodegradation of PET by the host and gut microbiota. After PET was fed, the host’s genes encoding degradation enzymes were upregulated, including genes encoding oxidizing, hydrolyzing, and non-specific CYP450 enzymes. Gut bacterial genes for biodegrading intermediates and nitrogen fixation also upregulated. The multiple-functional metabolic pathways for PET biodegradation ensured rapid biodegradation resulting in a half-life of PET less than 4 h with less negative impact by PET MW and crystallinity. [Display omitted] •High-crystallinity PET biodegradation was confirmed by testing change of δ13C.•Depolymerization is independent of gut microbes.•Polymer molecular size influences degradation rates.•Gut microbiomes synergistically biodegrade intermediates and provide nitrogen sources.•Upregulation of host genes for PET depolymerization and metabolism.