Synergy between fungi and bacteria promotes polycyclic aromatic hydrocarbon cometabolism in lignin-amended soil

Abstract

Lignin enhanced biodegradation of polycyclic aromatic hydrocarbons (PAHs) in soil, but collaboration among soil microorganisms during this process remains poorly understood. Here we explored the relations between microbial communities and PAH transformation in soil microcosms amended with lignin. Mineralization of the four-ring benzo(a)anthracene (BaA), which was selected as a model, was determined by using an isotope-labeled tracer. The eukaryotic inhibitor cycloheximide and redox mediator ABTS were used to validate the fungal role, while microbial communities were monitored by amplicon sequencing. The results demonstrated that lignin significantly promoted BaA mineralization to CO2, which was inhibited and enhanced by cycloheximide and ABTS, respectively. Together with the increased abundance of Basidiomycota, these observations suggested an essential contribution of fungi to BaA biodegradation, which possibly through a ligninolytic enzyme-mediated pathway. The enrichment of Methylophilaceae and Sphingomonadaceae supported bacterial utilization of methyl and aryl groups derived from lignin, implicating cometabolic BaA degradation. Co-occurrence network analysis revealed increased interactions between fungi and bacteria, suggesting they played synergistic roles in the transformation of lignin and BaA. Collectively, these findings demonstrate the importance of synergy between fungi and bacteria in PAH transformation, and further suggest that the modulation of microbial interplay may ameliorate soil bioremediation with natural materials such as lignin.