Genomic and transcriptomic insights into Achromobacter-Sphingobium co-colonization within polycyclic aromatic...

Efficient and complete biodegradation of polycyclic aromatic hydrocarbons (PAHs), which are persistent and genotoxic petroleum hydrocarbon pollutants, is often considered to require the cooperative activities of multiple bacterial groups, and bacterial (meta)genomic investigations of PAH-exposed ecosystems have contributed to elucidating such interactions. In this study, two bacterial isolates representing dominant genera within a PAH-grown soil bacterial consortium, Achromobacter xylosoxidans strain KK8 and Sphingobium barthaii strain KK22, were utilized as model organisms to investigate the relationship between these bacterial genera during PAH biodegradation. Strain KK8 has previously been characterized as incapable of biodegrading PAHs; thus, Achromobacter in the consortium appears to grow under metabolic dependence on PAH biodegradation products (i.e. salicylic acid) provided by the pioneer PAH-degrading Sphingobium. This metabolic relationship was evidenced through complete genome sequencing and functional gene analysis of strain KK8 conducted in the present study. To further elucidate potential interactions between Achromobacter and Sphingobium, cell-free filtrate-exchange experiments were performed using these isolates, revealing that strain KK8 exhibited a significantly shortened growth lag phase in the presence of the filtrate of strain KK22. Subsequent transcriptomic profiling of strain KK8 indicated that exposure to the Sphingobium filtrate up-regulated functional genes likely associated with Achromobacter colonization, including genes involved in biofilm formation (pga genes) or cell division (fts genes). Enhanced biofilm formation of strain KK8 in response to strain KK22 filtrate was additionally evidenced by biofilm assays. Taken together, these results suggest that the high abundance of Achromobacter within the consortium may be stimulated by Sphingobium when they are present together, potentially via extracellular signalling molecule(s). As the co-occurrence of Achromobacter and Sphingobium has been repeatedly documented in PAH-degrading bacterial communities, elucidating the mechanisms underlying their specific interspecies co-colonization during PAH biodegradation shall be valuable for the future biotechnological applications utilizing these bacteria.