Quorum sensing system effectively enhances DegU-mediated degradation of pyrethroids by Bacillus subtilis

The contamination of the natural environment is a growing concern that threatens all life forms, including microorganisms. Bacteria protect themselves by initiating quorum sensing (QS), a bacterial cell-cell communication, to generate adaptive responses to these pollutants. Bacillus subtilis has a typical QS ComQXPA system that regulates the phosphorylation of the transcription factor DegU (DegU-P), and thus can mediate the expression of various downstream genes under different stress conditions. Herein, we found that cesB, a gene of Bacillus subtilis 168, plays a key role in pyrethroid degradation, and cesB-mediated degradation could be enhanced by coordinating with the ComX communication system. Using β-cypermethrin (β-CP) as a paradigm, we demonstrated that DegU-P increased upon exposure to β-CP, thus facilitating β-CP degradation by binding to the upstream regulatory regions of cesB, leading to the activation of the expression of cesB. Further, we showed that the expression of different levels of phosphorylated DegU in a degU deletion strain resulted in varying degrees of β-CP degradation efficiency, with phosphorylated DegUH12L achieving 78.39% degradation efficiency on the first day, surpassing the 56.27% degradation efficiency in the wild type strain. Consequently, based on the conserved regulatory mechanism of ComQXPA system, we propose that DegU-P-dependent regulation serves as a conserved defense mechanism owing to its ability to fine-tune the expression of genes involved in the degradation of pollutants upon exposure to different pesticides.