A multi-OMIC characterisation of biodegradation and microbial community succession within the PET plastisphere

Abstract

Background Plastics now pollute marine environments across the globe. On entering these environments, plastics are rapidly colonised by a diverse community of microorganisms termed the plastisphere. Members of the plastisphere have a myriad of diverse functions typically found in any biofilm but, additionally, a number of marine plastisphere studies have claimed the presence of plastic-biodegrading organisms, although with little mechanistic verification. Here, we obtained a microbial community from marine plastic debris and analysed the community succession across 6 weeks of incubation with different polyethylene terephthalate (PET) products as the sole carbon source, and further characterised the mechanisms involved in PET degradation by two bacterial isolates from the plastisphere. Results We found that all communities differed significantly from the inoculum and were dominated by Gammaproteobacteria, i.e. Alteromonadaceae and Thalassospiraceae at early time points, Alcanivoraceae at later time points and Vibrionaceae throughout. The large number of encoded enzymes involved in PET degradation found in predicted metagenomes and the observation of polymer oxidation by FTIR analyses both suggested PET degradation was occurring. However, we were unable to detect intermediates of PET hydrolysis with metabolomic analyses, which may be attributed to their rapid depletion by the complex community. To further confirm the PET biodegrading potential within the plastisphere of marine plastic debris, we used a combined proteogenomic and metabolomic approach to characterise amorphous PET degradation by two novel marine isolates, Thioclava sp. BHET1 and Bacillus sp. BHET2. The identification of PET hydrolytic intermediates by metabolomics confirmed that both isolates were able to degrade PET. High-throughput proteomics revealed that whilst Thioclava sp. BHET1 used the degradation pathway identified in terrestrial environment counterparts, these were absent in Bacillus sp. BHET2, indicating that either the enzymes used by this bacterium share little homology with those characterised previously, or that this bacterium uses a novel pathway for PET degradation. Conclusions Overall, the results of our multi-OMIC characterisation of PET degradation provide a significant step forwards in our understanding of marine plastic degradation by bacterial isolates and communities and evidences the biodegrading potential extant in the plastisphere of marine plastic debris.

Microbial biodegradation of plastics: Challenges, opportunities, and a critical perspective

“…BHET2 and Bacillus sp. BHET2 and the presence of PET hydrolytic intermediates confirmed their degradation ability (Wright et al, 2021). The exploration of microbial communities through metagenomics could serve as a great tool for mining novel enzymes and genes involved Fig.…”

Living in a bottle: Bacteria from sediment‐associated Mediterranean waste and potential growth on polyethylene terephthalate

“…Specifically, Idiomarina has been recently reported to possibly assist in the formation of biofilms on the surface of PET particles, although it showed no significant PET degradation (Gao & Sun, 2021). On the contrary, although there is no previous report on the ability of Bacillus algicola (which showed double CFU count when incubated with PET) to degrade plastic polymers, other species and strains within the genus have been described as degraders of polystyrene, polypropylene, polyethylene, and PET microplastic particles (Auta et al, 2017; Wright, Bosch, et al, 2021) as well as polyvinyl chloride (Giacomucci et al, 2019). Finally, the yeast Rhodotorula evergladensis , which showed a tiny increase in growth on PET in our study, has been previously reported to degrade plasticizers (Gartshore et al, 2003).…”

Plastisphere community assemblage of aquatic environment: plastic-microbe interaction, role in degradation and characterization technologies

“…Microplastic serves as an excellent substratum for biofilm attachment as they adsorb essential nutrients and organic matter from the surrounding environment to support microbial growth. Usually, the microbes colonize the plastics within 24 h [179] depending on several environmental factors, which significantly influence the microbial composition of the plastisphere [74]. The fluorescence microscopy (FM) and scanning electron microscopy (SEM) recognize the microbial association in the biofilm [47,89,92,206,207] (Table 3).…”