Degradation of high pyrene concentration in sediment and its implications to microbiome in microbial electrochemical system

Polycyclic aromatic hydrocarbons (PAHs), such as pyrene, frequently accumulate in sediment, particularly near industrial sites. Concentration can reach several hundred milligrams per kilogram of dry sediment. The efficacy of microbial electrochemical systems (MES) in electricity generation and degradation of PAHs is intricately linked to the microbiome's response to these high contaminant levels. This study leverages metabolomics and metagenomics to elucidate the impact of elevated pyrene concentration on the functional structure and metabolic dynamics of sediment microbiomes within MES.In sediment with high pyrene concentration pollution, the electrical output and degradation efficiency of MES for organic substrates and pyrene were markedly reduced. Specific microorganisms, such as Hydrogenophaga and Flavobacterium, known for PAHs degradation, were selectively enriched under these conditions. Analysis of metabolites and genetic profiles revealed that high pyrene levels lead to a more focused yet extensive alteration of metabolic pathways, encompassing not just metabolic functions but also aspects critical for microbial survival and communication. In contrast, low pyrene concentration primarily influenced metabolic pathways. Enzymatic analysis indicated that low pyrene levels promoted carbohydrate metabolism by sediment microorganisms, whereas high levels exerted an inhibitory effect. Furthermore, at higher pyrene concentration, PAH-degrading microorganisms showed increased activity and tolerance to pyrene toxicity. Examination of electron transport enzymes revealed that both low and high pyrene concentration could facilitate intracellular electron transfer and potentially serve as a partial carbon source. However, high pyrene levels impeded enzymes associated with outer membrane electron transfer, hindering electron movement from intracellular to extracellular electron acceptors, negatively affecting the electrical output of MES.Through metabolomic and metagenomic analysis, this study offers theoretical insights and mechanistic understanding crucial for addressing the challenges faced by MES in treating pyrene-contaminated sediment near industrial sites.