Dual-directional regulation of extracellular respiration in Shewanella oneidensis for intelligently treating multi-nuclide contamination

Abstract

Radionuclide contamination has become a global environmental concern due to the high mobility and toxicity of certain isotopes. Bioreduction mediated by electrochemically active bacteria (EAB) with unique extracellular electron transfer (EET) capability is recognized as a promising approach for nuclear waste treatment. However, it is difficult to achieve bidirectional regulation of EET pathway through traditional genetic manipulation, limiting the bioremediation application of EAB. Here, we designed and optimized a novel Esa quorum sensing (EQS) system for highly efficient gene expression and interleaved cellular functional output. By promoting dimethyl sulfoxide reductase at low cell density and increasing the synthesis of electron conductive complex and flavins at high cell density, the EQS system dynamically switched the extracellular respiratory pathway of Shewanella oneidensis MR-1 according to cell density. The engineered strain exhibited precise switching and substantial improvement in the extracellular remediation of multiple nuclides, sequentially increasing the reduction of iodine IO₃^- and uranium U(VI) by 2.51- and 2.05-fold compared with the control, respectively. Furthermore, a mobile bacterial biofilm material was fabricated for collecting uranium precipitates coupled with U(VI) reduction. This work clearly demonstrates that EQS system contributes to the bidirectional regulation of EET pathway in EAB, providing an effective and refined strategy for bioremediation of multi-nuclide contamination.

Keywords: Bidirectional dynamic regulation; Electrochemically active bacteria; Extracellular electron transfer; Nuclide contamination; Quorum sensing.