Assessing the impact of soil microbial fuel cells on atrazine removal in soil

Widespread pesticide use in agriculture is a major source of soil pollution, driving biodiversity loss and posing serious threads to human health. The recalcitrant nature of most of these pesticides demands for effective remediation strategies. In this study, we assess the ability of soil microbial fuel cell (SMFC) technology to bioremediate soil polluted by the model pesticide atrazine. To elucidate the degradation mechanism and consequently define effective implementation strategies, we provide the first comprehensive investigation of the SMFC performance, in which the monitoring of the electrochemical performance of the system is combined with Quadrupole Time-of-Flight (QTOF) mass spectrometry and microbial analyses. Our results show that, while both SMFC and natural attenuation lead to a reduction on atrazine levels, the SMFC modulates the activity of different microbial pathways. As a result, atrazine degradation by natural attenuation leads to high levels of deisoproylatrazine (DIPA), a very toxic degradation metabolite, while DIPA levels in soil treated by SMFC remain comparatively low. The beta diversity and differential abundance analyses revealed how the microbial community evolves over time in the SMFCs degrading atrazine, demonstrating the enrichment of electroactive taxa on the anode, and the enrichment of a mixture of electroactive and atrazine-degrading taxa at the cathode. The detection and taxonomic classification of peripheral atrazine degrading genes, atzA, atzB and atzC, was carried out in combination with the differential abundance analysis. Results revealed that these genes are likely harboured by members of the order Rhizobiales enriched at the cathode, thus promoting atrazine degradation via the conversion of hydroxyatrazine (HA) into N-isopropylammelide (NIPA), as confirmed by mass spectrometry data. Overall, the comprehensive approach adopted in this work, provides fundamental insights into the degradation pathways of atrazine in soil by SMFC technology, which is critical for practical applications, thus suggesting an effective approach to advance research in the field.