Biodegradation of high-molecular-weight polycyclic aromatic hydrocarbons by a novel species of the genus Devosia isolated from the deep-sea region of the Kermadec Trench

Polycyclic aromatic hydrocarbons (PAHs) are categorized as persistent organic pollutants due to their high toxicity and environmental persistence. In this study, a deep-sea bacterium, designed Naph2^T, was isolated from the sediments of the Kermadec Trench using PAH-enriched cultures. A comparative analysis of Overall Genome Relatedness Indices (OGRI) values between Naph2^T and closely related strains within the genus <i>Devosia</i> indicated that the isolate represents a novel species, designated as <i>Devosia polycyclovorans</i> sp. nov. (type strain Naph2^T = MCCC 1K09447^T). This conclusion is further supported by physiological and biochemical analyses. Naph2^T exhibited the ability to degrade high-molecular-weight PAHs such as pyrene and benzo[a]pyrene, a feature not previously reported for any strain within the genus <i>Devosia</i>. The degradation degree of Naph2^T for pyrene and benzo[a]pyrene reached 58 and 48% at a concentration of 300 mg/L and 200 mg/L, respectively, in 5 days. Genomic analysis revealed key genes associated with PAH degradation, including aromatic ring-hydroxylating dioxygenase (RHD), <i>nagAa</i>, and downstream gene clusters such as <i>pht</i>, <i>pob</i>, and <i>pca</i>. Comparative genomic studies showed that Naph2^T harbors a greater number of PAH degradation genes than other species within the <i>Devosia</i> genus, demonstrate that it may have acquired these capabilities through horizontal gene transfer. Transcriptome data revealed significant upregulation of <i>pcaG</i> and <i>pcaH</i>, which encode enzymes involved in the degradation of 3,4-dihydroxybenzoic acid, a downstream intermediate of polycyclic aromatic hydrocarbon metabolism. These findings not only provide novel insights into the ecological roles of the genus <i>Devosia</i>, but also highlight the potential of this new species for PAH bioremediation applications.