Extracellular pollutant degradation feedback regulates intracellular electron transfer process of exoelectrogens: Strategy and mechanism

Abstract

Exoelectrogens possess extraordinary degradation ability to various pollutants through extracellular electron transfer (EET). Compared with extracellular electron release process, intracellular electron transfer network is not yet fully recognized. Especially, controversy remains regarding the role of CymA, an essential electron-transfer hub of Shewanella oneidensis MR-1, in EET process. In this study, we thoroughly surveyed the intracellular transfer strategies during EET through dye decolorization. Loss of CymA severely impaired the reduction ability of S. oneidensis MR-1 to methyl orange (MO), but hardly affected the decolorization of aniline blue (AB). Complement of cymA fully restored the MO decolorization ability of ΔcymA mutant. The contribution of CymA to extracellular decolorization was subjected to MO concentrations. The defect in the decolorization ability of ΔcymA mutant was not evident at low MO concentration, but severe at high MO concentration. Further investigation revealed that EET rate determined the significance of CymA in the extracellular bioremediation by S. oneidensis MR-1. Coupled with MO concentrations increasing from 15 to 120 mg/L, the initial electron transfer rates of S. oneidensis MR-1 increased accordingly from 2.69 × 104 to 11.21 × 104 electrons CFU−1 s−1, which led to a gradual increase of the dependencyCymA. Thus, we first revealed that extracellular degradation performance could feedback regulate the intracellular electron transfer process of S. oneidensis MR-1. This work is helpful to fully understand the complex EET process of exoelectrogens and facilitates the application of exoelectrogens in bioremediation of environmental pollutants.