Changes in syntrophic microbial communities, EPS matrix, and gene-expression patterns in biofilm anode in response to silver nanoparticles exposure

Abstract

Understanding the toxic effect of silver nanoparticles (AgNPs) on various biological wastewater treatment systems is of significant interest to researchers. In recent years, microbial electrochemical technologies have opened up new opportunities for bioenergy and chemicals production from organic wastewater. However, the effects of AgNPs on microbial electrochemical systems are yet to be understood fully. Notably, no studies have investigated the impact of AgNPs on a microbial electrochemical system fed with a complex fermentable substrate. Here, we investigated the impact of AgNPs (50 mg/L) exposure to a biofilm anode in a microbial electrolysis cell (MEC) fed with glucose. The volumetric current density was 29 ± 2.0 A/m3 before the AgNPs exposure, which decreased to 20 ± 2.2 A/m3 after AgNPs exposure. The biofilms produced more extracellular polymeric substances (EPS) to cope with the AgNPs exposure, while carbohydrate to protein ratio in EPS considerably increased from 0.4 to 0.7. Scanning electron microscope (SEM) imaging also confirmed the marked excretion of EPS, forming a thick layer covering the anode biofilms after AgNPs injection. Transmission electron microscope (TEM) imaging showed that AgNPs still penetrated some microbial cells, which could explain the deterioration of MEC performance after AgNPs exposure. The relative expression level of the quorum signalling gene (LuxR) increased by 30%. Microbial community analyses suggested that various fermentative bacterial species (e.g., Bacteroides, Synergistaceae_vadinCA02, Dysgonomonas, etc.) were susceptible to AgNPs toxicity, which led to the disruption of their syntrophic partnership with electroactive bacteria. The abundance of some specific electroactive bacteria (e.g., Geobacter species) also decreased. Moreover, decreased relative expressions of various extracellular electron transfer associated genes (omcB, omcC, omcE, omcZ, omcS, and pilA) were observed. However, the members of family Enterobacteriaceae, known to perform a dual function of fermentation and anodic respiration, became dominant after biofilm anode exposed to AgNPs. Thus, EPS extraction provided partial protection against AgNPs exposure.