Integrative genomic and transcriptomic analyses reveal marine Actinomycetota adaptations for hydrocarbon degradation

Marine oil pollution poses critical ecological challenges, necessitating innovative and sustainable bioremediation strategies. This study provides a comprehensive multi-omics investigation into a synthetic coastal marine consortium comprising four strains belonging to Actinomycetota, including Rhodococcus sp. strain 1Y, Gordonia sp. strain BP1o, and two Janibacter indicus strains isolated from hydrocarbon-contaminated sediments. Genomic analysis identified multiple orthologous gene clusters associated with hydrocarbon degradation, encompassing pathways such as alkB, cyp and nah. Rhodococcus sp. strain 1Y exhibited the highest number of these hydrocarbon-degradation gene clusters, highlighting its robust genetic potential and versatility in metabolizing diverse hydrocarbons. Secondary metabolite analysis identified stress-related biosynthetic pathways, including ectoine and siderophore production, supporting hydrocarbon solubilization and enzymatic activity. In a medium containing a mixture of phenanthrene and hexadecane (50 mg/L each) as the sole source of carbon, the consortium demonstrated rapid hydrocarbon degradation, with nearly complete degradation of hexadecane (reduced to 2.76 %) and partial degradation of phenanthrene (reduced to 36.56 %) by Day 12. Transcriptomic profiling across time points revealed dynamic shifts in gene expression, with 502 differentially expressed genes between Day 3 and Day 12, of which 487 were downregulated, enriched in pathways associated with xenobiotics biodegradation, lipid metabolism, and membrane transport. Functional annotations highlighted the transcriptional activation of metabolic pathways enabling hydrocarbon uptake, breakdown, and stress adaptation. This integrated approach connects genomic potential with functional performance, emphasizing the metabolic versatility and ecological resilience of Actinomycetota for oil-spill bioremediation. These findings advance our understanding of microbial hydrocarbon degradation and offer actionable insights for developing eco-friendly remediation strategies.