Different performance of pyrene biodegradation on metal-modified montmorillonite: Role of surface metal ions from a bioelectrochemical perspective

Microbial extracellular electron transfer (EET) at microbe-mineral interface has been reported to play a significant role in pollutant biotransformation. Different metals often co-exist with organic pollutants and are immobilized on mineral surfaces. However, little is known about the influence of mineral surface metal ions on organic pollutant biodegradation and the involved electron transfer mechanism. To address this knowledge gap, pyrene was used as a model compound to investigate the biodegradation of polycyclic aromatic hydrocarbon on montmorillonite mineral saturated with metal ions (Na(I), Ni(II), Co(II), Cu(II) and Fe(III)) by Mycobacteria strain NJS-1. Further, the possible underlying electron transfer mechanism by electrochemical approaches was investigated. The results show that pyrene biodegradation on montmorillonite was markedly influenced by surface metal ions, with degradation efficiency following the order Fe(III) > Na(I) Co(II) > Ni(II) Cu(II). Bioelectrochemical analysis showed that electron transfer activities (i.e., electron donating capacity and electron transport system activity) varied in different metal-modified montmorillonites and were closely related to pyrene biodegradation. Fe(III) modification greatly stimulated degrading enzyme activities (i.e., peroxidase and dioxygenase) and electron transfer activities resulting in enhanced pyrene biodegradation, which highlights its potential as a technique for pollutant bioremediation. The bacterial extracellular protein and humic substances played important roles in EET processes. Membrane-bound cytochrome C protein and extracellular riboflavin were identified as the electron shuttles responsible for transmembrane and cross extracellular matrix electron

Automated summary

Microbial extracellular electron transfer (EET) at microbe-mineral interface plays a significant role in pollutant biotransformation, with different metal ions on mineral surfaces influencing organic pollutant biodegradation. Fe(III) modification in montmorillonite significantly stimulated degrading enzyme and electron transfer activities, leading to enhanced pyrene biodegradation and highlighting its potential for pollutant bioremediation. Bacterial extracellular proteins and humic substances are important in EET processes, with membrane-bound cytochrome C protein and extracellular riboflavin identified as key electron shuttles.