A novel FadL family outer membrane transporter is involved in the uptake of polycyclic aromatic hydrocarbons

Gram-negative bacteria play a pivotal role in the bioremediation of persistent organic pollutants, such as polycyclic aromatic hydrocarbons (PAHs). Because the outer membrane (OM) of these bacteria hinders the direct permeation of hydrophobic substances into the cells, trans-OM proteins are required for the uptake of PAHs. However, neither the characteristics of PAH transporters nor the specific transport mechanism has been well interpreted. In this study, we revealed the participation of a novel FadL family transporter, PadL, in the biodegradation of the representative PAH phenanthrene in Novosphingobium pentaromativorans US6-1, an efficient PAH-degrading bacterium. PadL facilitates the cross-OM transport of phenanthrene, thus upregulating the expression of the gene ahdA1e that is critical to the PAH catabolism. We then showed that hydrophobic amino acid residues in the substrate binding pockets of PadL are essential for the binding of PAHs, such as phenanthrene and benzo[a]pyrene. PadL homologs commonly exist in most of the PAH-degrading species from Sphingomonas and Novosphingobium. The characterization of PadL provided in this study holds significant potential for improving the PAH biodegradation efficiency.

Importance: Persistent organic pollutants, including polycyclic aromatic hydrocarbons (PAHs), pose serious threats to human health, and biodegradation has been applied as an efficient strategy for PAH removal. However, due to the high hydrophobicity of PAHs, their uptake is hindered by the bacterial outer membrane, restraining degradation efficiency. The present study reveals the critical roles of a novel FadL family protein (PadL) in the biodegradation of PAHs. PadL specifically transports PAHs such as phenanthrene and benzo[a]pyrene and PadL homologs generally exist in PAH-degrading bacteria of Sphingomonas and Novosphingobium. Our findings fill the knowledge gap in the bacterial trans-membrane uptake process of PAHs and provide a future direction for enhancing the bacterial PAH bioremediation capacity.