Unraveling the mechanism of interaction: accelerated phenanthrene degradation and rhizosphere biofilm/iron plaque formation influenced by phenolic root exudates

Abstract

Phenolic root exudates (PREs) secreted by wetland plants facilitate the accumulation of iron in the rhizosphere, potentially providing the essential active iron required for the generation of enzymes that degrade polycyclic aromatic hydrocarbon, thereby enhancing their biodegradation. However, the underlying mechanisms involved are yet to be elucidated. This study focuses on phenanthrene (PHE), a typical polycyclic aromatic hydrocarbon pollutant, utilizing representative PREs from wetland plants, including p-hydroxybenzoic, p-coumaric, caffeic, and ferulic acids. Using hydroponic experiments, 16S rRNA sequencing, and multiple characterization techniques, we aimed to elucidate the interaction mechanism between the accelerated degradation of PHE and the formation of rhizosphere biofilm/iron plaque influenced by PREs. Although all four types of PREs altered the biofilm composition and promoted the formation of iron plaque on the root surface, only caffeic acid, possessing a similar structure to the intermediate metabolite of PHE (catechol), could accelerate the PHE degradation rate. Caffeic acid, notable for its catechol structure, plays a significant role in enhancing PHE degradation through two main mechanisms: (a) it directly boosts PHE co-metabolism by fostering the growth of PHE-degrading bacteria, specifically Burkholderiaceae, and by facilitating the production of the key metabolic enzyme catechol 1,2-dioxygenase (C12O) and (b) it indirectly supports PHE biodegradation by promoting iron plaque formation on root surfaces, thereby enriching free iron for efficient microbial synthesis of C12O, a crucial factor in PHE decomposition.

Keywords: Biofilm; Co-metabolic degradation; Iron plaque; Phenanthrene; Phenolic root exudates; Rhizosphere microenvironment.