Deciphering the coordinated strategy between enzymatic aromatic-ring cleavage and metabolic remodeling for efficient...

Petroleum pollution represents a severe and persistent threat to aquatic ecosystems and human health. Microbial bioremediation offers an environmentally sustainable solution, yet the diversity of highly efficient degraders is limited, and the systemic molecular mechanisms underlying their adaptation to complex petroleum mixtures remain poorly understood. This study isolated a novel and highly efficient petroleum-degrading bacterium, Vagococcus fluvialis LH1, from oil-contaminated soil. Response surface methodology optimized its degradation conditions to 29.5 °C, 1.8 % salinity, pH 6.88, and 4.9 % (v/v) inoculum size. Under these conditions, strain LH1 degraded 63.73 % of 2 % (v/v) crude oil within 28 days, with particularly high removal (68.86 %) of aromatic hydrocarbons. Integrated multi-omics analyses revealed the molecular basis for its efficiency. Whole-genome sequencing identified key aromatic-ring cleavage genes (e.g., catE, mhpC, pcaD), and their functional roles were corroborated by the metabolomic detection of corresponding ring-cleavage products. Transcriptomic and metabolomic profiling showed that LH1 remodels its central metabolism under petroleum stress: it activates oxidative phosphorylation to meet elevated energy demands and redirects L‑glutamine flux to reconfigure nitrogen metabolism, thereby prioritizing degradation over growth. This is a coordinated strategy that couples enzymatic ring‑opening with global metabolic remodeling. Notably, the strain retained high degradation activity in genuine seawater, demonstrating its strong potential for in‑situ marine oil-spill remediation. Our study provides novel multi‑omics insights into the systematic metabolic adaptation of petroleum‑degrading bacteria and offers a promising microbial resource, together with a mechanistic foundation for developing efficient bioremediation strategies.