Combined transcriptome and metabolome analysis reveal the dual catabolic pathways of naphthalene in Pseudomonas putida ND6

Microorganisms stand as the most effective mediators for degradation, utilization/mineralization of polycyclic aromatic hydrocarbons (PAHs), serving as vital restorers of polluted environment. Transcriptome and metabolome analysis are crucial for pinpointing differentially expressed genes (DEGs) and differentially accumulated metabolites (DAMs) under varying conditions, thereby providing a new understanding of genes or pathways involved in PAHs degradation. Pseudomonas putida ND6 is a remarkably proficient naphthalene-degrading bacterium, harboring two substantial plasmids named pND6–1 and pND6–2. Specifically, plasmid pND6–1 carries the genes responsible for naphthalene degradation. Conversely, the genes pertinent to conjugation transfer reside on plasmid pND6–2. In this work, transcriptome and metabolome analysis of naphthalene degrading strain P. putida ND6 grown on naphthalene and glucose was performed. A total of 1503 significant DEGs were found, of which 696 were up-regulated and 807 were down-regulated, participating in diverse metabolic pathways. Functional analysis of these DEGs and DAMs revealed that naphthalene exposure subjected strain ND6 cells to stressful condition, disrupting a range of primary metabolisms, including citrate cycle, protein synthesis (transcription and translation) and DNA replication. Furthermore, strain ND6 employs dual catechol metabolic pathways during naphthalene degradation, recognized as ortho- and meta-pathway. Notably, the up-regulated expression of ortho-pathway encoding genes was significantly higher than that of meta-pathway, suggesting that ortho-pathway is more effective than meta-pathway in degrading catechol in strain ND6. Additionally, curing of the pND6–2 plasmid had no significant impact on naphthalene degradation, highlighting the stability advantage of naphthalene degradation gene in strain ND6. This study provides compelling evidence for the preference and regulation of naphthalene-degrading pathways in strain ND6, ensuring effective and efficient biodegradation.