Biodegradation of components from an oxidized polyethylene by a Rhodococcus strain isolated from the gut of Atlantic salmon

ABSTRACT Polyethylene (PE) is the most produced synthetic polymer and, consequently, a major source of microplastic waste accumulating globally. Exposure to photo- and thermo-oxidative conditions in the environment can promote PE degradation into carbonyl-containing compounds, hydrocarbons, and low-molecular-weight PE (LMWPE). In both marine and freshwater ecosystems, fish, including Atlantic salmon, can ingest PE and its derivatives, creating opportunities for interactions with their gut microbes. Here, we investigated the capacity of a bacterial isolate from the salmon gut, Rhodococcus sp002259485 strain ASF-10, to grow on an LMWPE model substrate for partially depolymerized and oxidized PE. Comparative genomic analyses showed that ASF-10 has a smaller genome than other Rhodococcus species yet retains conserved functions, including those related to utilization of medium- and long-chain hydrocarbons. In-depth characterization of the substrate following growth with ASF-10 confirmed depletion of alkanes and 2-ketones deriving from LMWPE, whereas the polymeric component remained unchanged. Proteomic analysis identified multiple enzymes likely involved in the degradation of LMWPE derivatives, including an alkane 1-monooxygenase and cytochrome P450 hydroxylases, as well as proteins for the production of biofilm and a surfactant that may enhance accessibility to the substrate. The bacterium was detected as metabolically active in a metatranscriptomic data set derived from freshwater-reared salmon. Collectively, our findings advance the understanding of the ecology and enzymatic mechanisms underlying the utilization of medium- to long-chain alkanes and oxidized variants thereof, that resemble molecules that can occur from abiotic PE degradation, by a fish gut-associated microbe. This metabolic capacity could be harnessed to develop sustainable strategies for bioremediation of LMWPE derivatives. IMPORTANCE The widespread presence of plastics in marine and freshwater environments has raised concerns due to their toxicity when ingested by fish. Microbial mechanisms driving the breakdown of microplastic components, such as low-molecular-weight polyethylene (LMWPE) and derivatives, in gut systems remain poorly understood. This study reveals how a bacterium isolated from the gut of salmon, Rhodococcus sp002259485 strain ASF-10, metabolizes alkanes and oxidized variants thereof that can result from abiotic PE decomposition. We identified key enzymes that are potentially involved in this process, as well as in the production of biofilm and surfactants that may facilitate access to the substrate. Besides extending the knowledge of the enzymatic basis for the degradation of PE derivatives in gut-associated microbes from aquatic organisms, our results provide a framework that couples advanced compositional characterization of the substrate with omics techniques, offering valuable insight to support future studies aimed at unequivocally identifying microbes and their enzymes implicated in the transformation of PE derivatives.