Polar Marine Microbial Communities as Reservoirs of Polyester Degrading Enzymes

Abstract

Background: Polyethylene terephthalate (PET) is one of the most widely used plastics and a major contributor to marine pollution. While the diversity of PET hydrolases (PETases), which degrade PET into mono(2-hydroxyethyl) terephthalate (MHET), terephthalate (TPA) and ethylene glycol, has been documented in temperate and tropical waters, their potential presence in polar oceans remains unascertained. Results: Here, we systematically screened polar and non-polar marine metagenomes using Hidden Markov models (HMM) generated using experimentally validated PETases. We identified >680 putative PETase-like sequences, with Antarctic and Arctic candidates enriched in high-fidelity motifs associated with PETase-like activity. Phylogenetic and structural analyses defined a high-confidence PETase-like clade comprising both Type I and Type II enzymes, differing in thermostability-related features and PET-binding motifs. Experimental assays confirmed polyesterase activity in 5/9 candidates from this clade, including polar-derived variants active at 14-25{degrees}C. Downstream enzymes for PET consumption were also widespread, detecting 209 putative MHET hydrolases and 442 TPA-catabolyzing enzymes. Further, we reconstructed 112 metagenome-assembled genomes (MAGs) carrying at least one enzyme of the PET degradation pathway, 89 of them carrying a PETase-like gene. Notably, 15 MAGs encoded multiple PETase-like enzymes, nine of them from polar datasets, and one polar MAG harbored a complete PETase-MHETase-TPA pathway, suggesting the genomic potential for a fully integrated degradation potential in cold-adapted taxa. Conclusions: Together, these results demonstrate that polar oceans act as previously overlooked reservoirs of taxonomically and functionally diverse plastic-degrading enzymes. The enrichment of PETase-like enzymes and downstream pathways in polar microbial communities expands the global biogeography of plastic biodegradation and highlights cold-active enzymes as promising candidates for developing low-temperature plastic bioremediation strategies.