Superior performance of natural electron shuttles over a synthetic analogue in promoting electrogenic hydrocarbon degradation in contaminated soil

Abstract

The application of microbial electrochemical system (MES) is limited by the slow rate of extracellular electron transfer in soil remediation. In this study, we evaluated the effects of shuttles, including anthraquinone-2,6-disulfonic acid disodium salt (AQDS), phenazine (PHE), and L-cysteine (CYS) on electricity generation, petroleum hydrocarbon degradation, and the microbial community in a soil MES. The results demonstrated that PHE and CYS enhanced the electron transfer flux by 30% and 22%, respectively, with 10%–18% higher than AQDS. Notably, CYS treatment resulted in the highest removal of petroleum hydrocarbons with a 152% increase which was 164% more than AQDS treatment, and specific degradation selectivity towards benzo[a]pyrene and long-chain alkanes. The addition of glucose as a cosubstrate universally increased the voltage output, confirming carbon source availability as a key limiting factor for electron transfer. Biological analysis revealed that electron shuttle addition reshaped the soil bacterial community structure and increased network complexity. Essentially, PHE not only functioned as an electron shuttle to promote cytochrome c expression but also stimulated Pseudomonas to overexpress endogenous phenazine compounds via quorum sensing. CYS served as both a sulphur source and a redox mediator, significantly increasing NAD(H) levels, and enriching electroactive bacteria with hydrocarbon degradation capability, such as Marinobacter and Clostridium. These findings clarify the potential of quinone- and cysteine-shuttles in pollutant degradation, providing an enhancement strategy for soil remediation.

Graphical abstract

Keywords

Soil remediation / Petroleum hydrocarbon degradation / Electrochemical system / Electron shuttles / Microbial community

Highlight

	● Phenazine and L-cysteine boosted electron transfer flux by 22%–30% in soil, outperforming AQDS.
	● Removal of TPHs improved by 152%, especially for benzo[a]pyrene and long-chain alkanes.
	● Availability of carbon source was identified as a bottleneck for extracellular electron transfer.
	● Exogenous shuttles stimulated the biosynthesis of endogenous PCA and PYO.
	● Enhancement of electron transport enriched electrogenic hydrocarbon degraders.

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