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, yet 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 (HGT). 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 (TPA) and methylated MHET (MMHET). Together, these findings demonstrate how cooperation and competition within consortia facilitate targeted gene exchange, enabling emergent plastic biodegradation in natural microbial communities. IMPORTANCE Environmental plastic degradation is rarely accomplished by a single organism, yet the microbial mechanisms enabling community-level PET plastic breakdown remain poorly understood. This study shows that a bacterial consortium isolated from crude petroleum-contaminated beaches biodegrades PET through exaptation of ancestral hydrocarbon pathways, metabolic division of labor, and targeted gene exchange rather than specialized PET-specific metabolic pathways. Pseudomonas strains initiate PET cleavage, while stress-tolerant Bacillus strains persist long enough to clear inhibitory intermediates and enable downstream aromatic and diol metabolism. PET degradation is observed to be an emergent property of ecological interactions and distant evolutionary history. These findings provide a community-level model for understanding how natural microbial communities may adapt to novel anthropogenic substrates such as synthetic polymers, sustaining prolonged biodegradation.