Exogenous quorum sensing signal enhances central energy metabolism to fuel biofilm formation and denitrification on microplastics

Microplastics (MPs) are known to host dense microbial biofilms and form the plastisphere, which serve as significant sites for various biogeochemical processes, including nitrogen transformation. The communication within these complex microbial communities is facilitated by quorum sensing (QS) signals. However, how this inter-bacteria signal crosstalk impacts the colonization and function of key microbes, such as denitrifiers, remains inadequately elucidated. This research delves into the impact of the external signaling molecule N-3-oxododecanoyl-L-homoserine lactone (C12-oxo-HSL) on biofilm development and denitrification processes by the model bacterium Paracoccus denitrificans (P. denitrificans) on microplastic surfaces. Treatment with 10 μM C12-oxo-HSL increased biofilm biomass 2.67-fold and nitrate removal rates 2.61-fold relative to controls, while planktonic biomass remained comparable to or lower than untreated samples, refuting the hypothesis that increased biofilm mass merely reflects accelerated planktonic growth. Transcriptomic analysis unveiled a sophisticated regulatory network. C12-oxo-HSL not only stimulated the expression of genes involved in initial adhesion and motility but also orchestrated a substantial upregulation of key energy metabolism pathways, including glycolysis, the tricarboxylic acid (TCA) cycle, and oxidative phosphorylation. Metabolic upregulation likely increased ATP availability for the augmented production of extracellular polymeric substances, ultimately leading to the formation of a more resilient and efficient biofilm structure. Our findings suggest a potential energy-centric mechanism where exogenous AHLs prime the cellular bioenergetic status to support the structural and functional demands of plastisphere colonization. This highlights the pivotal role of signal-mediated resource allocation in shaping the biogeochemical impact of microplastic pollution.