An Intracellular Sensing and Signal Transduction System That Regulates the Metabolism of Polycyclic Aromatic Hydrocarbons in Bacteria

Many bacteria utilize polycyclic aromatic hydrocarbon (PAH) as carbon and energy sources for growth. These bacteria play an important role in the amelioration of PAH pollution in various environments. However, it is unclear how bacteria sense PAHs and how PAH degradation pathways are regulated via signal transduction. Here, we investigated these mechanisms in Cycloclasticus, a ubiquitous PAH-degrading bacterium in marine environments. We identified the key genes involved in intracellular PAH sensing, signal transduction, and the differential regulation of degradation pathways for each PAH examined. Our results showed that PAHs bind specifically to a diguanylate cyclase PdgC, leading to the generation of cyclic dimeric GMP (c-di-GMP), which subsequently binds to two CRP/FNR family regulators, DPR-1 and DPR-2. c-di-GMP activates the transcription of DPR-1 and DPR-2 to positively regulate degradation pathways specific to pyrene and phenanthrene/naphthalene, respectively. This is the first report of an intracellular signal transduction pathway associated with PAH degradation in bacteria. Our results improve our understanding of the intracellular responses to PAHs. The existence of the identified genes in other bacteria indicates that the strategy described here is widely used by other PAH-degrading bacteria. IMPORTANCE Polycyclic aromatic hydrocarbons (PAHs) are widely distributed and have been found indoors, in the atmosphere, in terrestrial soils, in marine waters and sediments, and even in outer space. Bacteria degrade PAHs via degradation pathways. PAH signal sensing and transduction, as well as the regulation of PAH degradation pathways, are crucial for bacterial PAH biodegradation. However, prior to this study, these processes were poorly known. This study employed multiple molecular approaches to better understand the regulatory networks controlling PAH metabolism in bacteria. This report illustrates, for the first time, PAH-specific intracellular sensing, signal transduction, and metabolic regulatory pathways. Our results will help to increase our understanding of the hydrocarbon-metabolism regulatory network as well as the regulatory intricacies that control microbial biodegradation of organic matter. These key data should be considered to improve the rational design and efficiency of recombinant biodegradable, bacterial biosensors, and biocatalysts in modern green chemistry.