Ancestral hydrocarbon metabolism enables PET degradation by a natural bacterial consortium.

Abstract

Plastic biodegradation in natural environments is increasingly recognized as a multi-organism process; however, the mechanisms enabling coordinated depolymerization and metabolism of polyethylene terephthalate (PET) remain poorly understood. Previously, we demonstrated that a full consortium containing three Pseudomonas and two Bacillus strains isolated from hydrocarbon-rich coastal soils of Galveston Bay, Texas, can synergistically depolymerize PET plastic and utilize it as a sole carbon source, a capacity not observed in individual isolates. In this report, using integrated comparative genomics, proteomics, and chemical analyses, we show that PET degradation in this system reflects exaptation of hydrocarbon metabolism, reinforced by metabolic division of labor. Within this naturally occurring consortium, Bacillus strains persist under environmental stress, establish biofilms, and perform essential secondary hydrolysis, while Pseudomonas strains catabolize aromatic monomers and buffer oxidative stress. Genes supporting these functions are enriched within the accessory genomes of the consortium strains, indicating consortium-enriched horizontal gene transfer. In addition to the canonical two-step hydrolytic pathway well documented in PET biodegradation, we identify a secondary methylation- and redox-associated process, mechanisms where the full consortium acts on the oligomer mono(2-hydroxyethyl) terephthalate (MHET), yielding nearly complete conversion to terephthalic acid and methylated MHET. Together, these findings support a model in which PET degradation is driven by pre-existing hydrocarbon metabolic traits distributed across the native consortium, particularly stress-response and redox pathways, aromatic catabolism, and alcohol catabolism.

Importance: Environmental plastic degradation is rarely accomplished by a single organism; however, the microbial mechanisms enabling community-level polyethylene terephthalate (PET) plastic breakdown remain poorly understood. This study shows that a bacterial consortium isolated from crude petroleum-contaminated coastal soils degrades PET by coordinating older hydrocarbon, aromatic, stress-response, and redox-associated metabolisms rather than by acquiring a dedicated PET pathway. Predicted horizontal gene transfer events were linked mainly to survival, biofilm formation, and metabolic flexibility, not PET depolymerization itself. These findings shift the focus from searching for single PET-degrading organisms toward understanding how microbial communities combine pre-existing metabolic tools to process synthetic polymers and manage the chemical stress created during biodegradation.