Interplay Between Superworm and its Gut Microbiome in Facilitating Polyethylene Biodegradation by Host Transcriptomic Analysis: Insights from Xenobiotic Metabolism

Abstract Plastics are a serious cause of environmental pollution, and microplastics pose a threat to human health. To solve this problem, the plastic-degrading mechanism of insect larvae is being investigated. Symbiosis between insect larvae and microorganisms plays a crucial role in this process. The aim of this study was to examine the metabolic pathways involved in polyethylene metabolism, the interaction between the host and microorganisms, and the role of superworms in promoting plastic degradation in polyethylene-fed superworms. Through host transcriptomic analysis, we identified 429 up-regulated and 777 down-regulated genes and analyzed their functions using the Kyoto Encyclopedia of Genes and Genomes and Gene Ontology databases. We found that insect larvae and their gut microbiomes interacted in two ways to enhance their polyethylene degradation ability. First, polyethylene metabolites activate the lipid metabolism pathway in insects, promoting the synthesis of carboxylic ester hydrolases and accelerating polyethylene degradation. Second, strains that degrade polyethylene cause infection in the host, which activates the immune response and generates reactive oxygen species (ROS). ROS are critical for insect immune responses and for the initial oxidation of polyethylene. As polyethylene degradation is promoted, polyethylene-degrading strains become dominant, and this interaction is strengthened. Furthermore, we suggest for the first time that xenobiotic metabolism is critical for polyethylene metabolism in superworm guts. In particular, enzymes involved in xenobiotic metabolism phase 2, such as glutathione S-transferase and uridine diphosphate glycosyltransferase, convert lipophilic plastic degradation intermediates into water-soluble forms and promote polyethylene degradation.