Insights into plastic biodegradation: community composition and functional capabilities of the superworm (Zophobas morio) microbiome in styrofoam feeding trials

Abstract

Plastics are inexpensive and widely used organic polymers, but their high durability hinders biodegradation. Polystyrene, including extruded polystyrene also known as styrofoam, is among the most commonly produced plastics worldwide and is recalcitrant to microbial degradation. In this study, we assessed changes in the gut microbiome of superworms (Zophobas morio) reared on bran, polystyrene, or under starvation conditions over a three weeks’ time period. Superworms on all diets were able to complete their life cycle to pupae and imago, although superworms reared on polystyrene had minimal weight gains, resulting in lower pupation rates. The change in microbial gut communities from baseline differed considerably between diet groups, with polystyrene and starvation groups characterized by a loss of microbial diversity and the presence of opportunistic pathogens. Inferred microbial functions enriched in the polystyrene group included transposon movements, membrane restructuring, and adaptations to oxidative stress. We detected several encoded enzymes with reported polystyrene and styrene degradation abilities, supporting previous reports of polystyrene degrading bacteria in the superworm gut. By recovering metagenome-assembled genomes (MAGs) we linked phylogeny and functions and identified genera including Pseudomonas, Rhodococcus and Corynebacterium, that possess genes associated with polystyrene degradation. In conclusion, our results provide the first metagenomic insights into the metabolic pathways used by the gut microbiome of superworms to degrade polystyrene. Our results also confirm that superworms can survive on polystyrene feed, however, this diet has considerable negative impacts on host gut microbiome diversity and health.Impact StatementIncreasing plastic pollution is a major environmental problem, and a recently proposed way to counteract this trend is to embrace a circular economy, in which used materials are recycled, rather than disposed of. An important step to facilitate this process is to invent new approaches for upcycling of plastic waste to desirable consumer products. Microbial plastic degradation and conversion is likely to play a considerable part in shaping a circular economy, by engineering microbes or their enzymes to bio-upcycle plastic waste. A first step towards actualizing this goal is to identify microbes that can degrade polystyrene and to investigate the enzymes and pathways involved. Our study represents the first metagenomic analysis of an insect gut microbiome on a polystyrene diet. It identifies bacteria with polystyrene and styrene degrading abilities, and infers enzymes and pathways involved in these reactions. Therefore, our results contribute towards understanding microbial polystyrene degradation and will provide a base for future investigations into microbial upcycling of plastic waste.

Analysis of the influence of polystyrene microplastics and their derivatives on the DNA of human colon epithelial cells HT29 with the comet assay

“…After many years of thinking about plastics as a very durable and problematic element in environment, we could notice a rising amount of information about enzymes, microorganisms or even a higher organism like worms (of course with their microbiota) which could utilise plastics. 13,30 So, if we know that microbiota could interact with MPS particles, the presence of dyes and re retardant additives weakens the structure of PS, and MPs are a perfect vector of xenobiotics into our body, maybe we should start to focus on MPs more intensively? We shouldn't underestimate this 'small' 5-6% of DNA damage which we observed in the comet assay.…”

Biodegradation of Expanded and Extruded Polystyrene with Different Diets by Using Zophobas atratus Larvae (Coleoptera: Tenebrionidae)

“…Klebsiella sp. acts mutualistic relationship with insect hosts by digesting food in the gut and providing nutrients to the host (Sun et al, 2022). Besides, Machona et al (2022) mentioned that Klebsiella sp.…”

Chemistry must respond to the crisis of transgression of planetary boundaries

“…They have become ubiquitous in the environment, even in deep-ocean and polar regions (microplastics have now been observed 62 in fresh snow in the Antarctic), and have been identified as a major threat to ecological niches such as coral as well as to overall environmental stability. Chemists need to take a comprehensive, Earth-system approach to the design, production and fate of plastics to eliminate this environmental hazard, including through attention to biodegradation, 63 recapture and reuse/recycling of plastic materials in green chemistry and circular processes, including strategies and processes for depolymerization. 64 …”