Degradation of pyrene at high concentrations in sediment and the implications for the microbiome in microbial electrochemical systems

Abstract

The polycyclic aromatic hydrocarbons (PAHs) frequently accumulate in sediments, particularly those near industrial sites. The efficacy of microbial electrochemical systems (MESs) in electricity generation and PAHs degradation is intricately linked to the microbiome's response to high contaminant levels. Metabolomics and metagenomics were applied to elucidate the impact of a high pyrene concentration on the functional structure and metabolic dynamics of sediment microbiomes within MES. In sediment with a high pyrene concentration, both the electrical output of MES and efficiency of their microbiomes in degrading organic substrates and pyrene were markedly reduced. These conditions were associated with the enrichment of PAH-degrading microorganisms, such as Hydrogenophaga and Flavobacterium. Analyses of metabolites and genetic profiles revealed that metabolic pathways were primarily influenced in MES exposed to low pyrene concentrations whereas fewer metabolic pathways were activated in MES exposed to high concentrations; instead, pathways representing functions critical for microbial survival and communication were activated as well. According to enzymatic analyses, low pyrene levels promoted carbohydrate metabolism by sediment microorganisms, whereas high levels had an inhibitory effect. An examination of electron transport enzymes revealed that intracellular electron transfer was facilitated by both low and high concentrations. However, high levels impeded enzymes associated with outer membrane electron transfer, hindering electron movement from intracellular to extracellular electron acceptors and thus negatively affecting the electrical output of MES. Our study provides crucial theoretical insight and mechanistic understanding for addressing the challenges that may be encountered when MES are used to treat pyrene-contaminated sediment near industrial sites.