Adaptive Responses of Shewanella decolorationis to the Toxic Organic Extracellular Electron Acceptor in Anaerobic Respiration

Bacterial anaerobic respiration using extracellular electron acceptor plays a predominant role in global biogeochemical cycles. However, the bacterial adaptive mechanisms to the toxic organic pollutant as the extracellular electron acceptor during anaerobic respiration is not clear, which limits us to optimize the strategies for the bioremediation of contaminated environment. Here, we report the physiological characteristics and the global gene expression of an ecologically successful bacterium Shewanella decolorationis S12 when using a typical toxic organic pollutant, amaranth, as the extracellular electron acceptor. Our results revealed that filamentous shift (the cells stretched to fiber-like shapes as long as 18 µm) occurred under amaranth stress. Persistent stress led to higher filamentous cell rate and decolorization ability in subcultural cells compared with parental strains. Additionally, the expression of genes involved in cell division, chemotaxi system, energy conservation, damage repair, and material transport in filamentous cells were significantly stimulated. The detailed roles of some genes with significantly elevated expressions in filamentous cells were identified by site-directed mutagenesis, such as the outer membrane porin genes ompA and ompW, the cytochrome C genes arpC and arpD, the global regulatory factor gene rpoS and methyl-accepting chemotaxis proteins genes SHD_2793 and SHD_0015. Finally, a conceptual model was proposed to help deepen our insights into both the bacterial survival strategy when toxic organics were present, and the mechanisms in which these toxic organics were biodegraded as the extracellular electron acceptors. Overall design: mRNA profiles of the normal (exposed to azo dye for 0.5h) and filamentous (exposed to azo dye for 8h) cells of Shewanella decoloriationis S12 were generated by deep sequencing, in triplicate, using Illumina Hiseq 2000.