Syntrophy drives the microbial electrochemical oxidation of toluene in a continuous-flow bioelectric well

Microbial electrochemical technologies (MET) are promising for the remediation of groundwater pollutants such as petroleum hydrocarbons (PH). Indeed, MET can provide virtually inexhaustible electron donors or acceptors directly in the subsurface environment. However, the degradation mechanisms linking contaminants removal to electric current flow are still largely unknown, hindering the development of robust design criteria. Here, we analysed the degradation of toluene, a model PH, in a bioelectrochemical reactor known as bioelectric well operated in continuous-flow mode at various influent toluene concentrations. With increasing concentration of toluene, the removal rate increased while the current tended to a plateau, hence the columbic efficiency decreased. Operation at open circuit confirmed that the bioelectrochemical degradation of toluene proceeded via a syntrophic pathway involving cooperation between different microbial populations. First of all, hydrocarbon degraders quickly converted toluene into metabolic intermediates probably by breaking the aromatic ring upon fumarate addition. Subsequently, fermentative bacteria converted these intermediates into volatile fatty acids (VFA) and likely also H2, which were then used as substrates by electroactive microorganisms forming the anodic biofilm. As toluene degradation is faster than subsequent conversion steps, the increase in intermediate concentration could not result in a current increase. This work provides valuable insights on the syntrophic degradation of BTEX, which are essential for the application of microbial electrochemical system to groundwater remediation of petroleum hydrocarbons.

Automated summary

Microbial electrochemical technologies (MET) show promise for groundwater remediation of petroleum hydrocarbons (PH). However, the degradation mechanisms are not well understood. This study analyzed the degradation of toluene, a model PH, in a bioelectrochemical reactor. The results revealed a syntrophic pathway involving different microbial populations for the degradation of toluene. Hydrocarbon degraders converted toluene into metabolic intermediates, which were further converted by fermentative bacteria into volatile fatty acids (VFA) and possibly H2. These compounds were then used as substrates by electroactive microorganisms forming the anodic biofilm. The increase in intermediate concentration did not result in a current increase as toluene degradation was faster.