Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008, China.
Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008, China; University of Chinese Academy of Sciences, Beijing 100049, China.
Sci Total Environ. 2022 Jan 20;805:150324. doi: 10.1016/j.scitotenv.2021.150324. Epub 2021 Sep 14.
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 transfer, respectively. Additions of exogenetic electron mediators of riboflavin, humic acid and potassium ferricyanide accelerated pyrene biodegradation which further verified the critical role of EET in PAH transformation at bacteria-mineral interfaces. These results support the development of clay mineral based advanced bioremediation techniques through regulating the electron transfer processes at the microbe-mineral interfaces by mineral surface modification.
微生物-矿物界面的微生物胞外电子传递（EET）已被报道在污染物生物转化中发挥重要作用。不同的金属通常与有机污染物共存，并固定在矿物表面。然而，对于矿物表面金属离子对有机污染物生物降解的影响及其涉及的电子传递机制知之甚少。为了解决这一知识空白，本研究以芘为模型化合物，利用 Mycobacteria 菌株 NJS-1 研究了金属离子（Na（I）、Ni（II）、Co（II）、Cu（II）和 Fe（III））饱和蒙脱石矿物上多环芳烃的生物降解。此外，还通过电化学方法研究了可能的潜在电子传递机制。结果表明，表面金属离子显著影响了蒙脱石上芘的生物降解，降解效率顺序为 Fe（III）>Na（I）≈Co（II）>Ni（II）≈Cu（II）。生物电化学分析表明，不同金属修饰蒙脱石的电子传递活性（即电子供体能力和电子传递系统活性）不同，与芘生物降解密切相关。Fe（III）修饰极大地刺激了降解酶活性（即过氧化物酶和双加氧酶）和电子传递活性，从而增强了芘的生物降解，这突出了其作为污染物生物修复技术的潜力。细菌胞外蛋白和腐殖质在 EET 过程中发挥重要作用。鉴定出膜结合细胞色素 C 蛋白和胞外核黄素作为负责跨膜和跨细胞外基质电子传递的电子穿梭体。添加外源电子介体核黄素、腐殖酸和铁氰化钾加速了芘的生物降解，进一步验证了 EET 在细菌-矿物界面上多环芳烃转化中的关键作用。这些结果支持通过矿物表面修饰调节微生物-矿物界面的电子传递过程，开发基于粘土矿物的先进生物修复技术。
