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

Abstract

Bacterial anaerobic respiration using an extracellular electron acceptor plays a predominant role in global biogeochemical cycles. However, the mechanisms of bacterial adaptation to the toxic organic pollutant as the extracellular electron acceptor during anaerobic respiration are not clear, which limits our ability to optimize the strategies for the bioremediation of a 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 m) occurred under amaranth stress. Persistent stress led to a higher filamentous cell rate and decolorization ability in subcultural cells compared to parental strains. In addition, the expression of genes involved in cell division, the chemotaxis system, energy conservation, damage repair, and material transport in filamentous cells was significantly stimulated. The detailed roles of some genes with significantly elevated expressions in filamentous cells, such as the outer membrane porin genes ompA and ompW, the cytochrome c genes arpC and arpD, the global regulatory factor gene rpoS, and the methyl-accepting chemotaxis proteins genes SHD_2793 and SHD_0015, were identified by site-directed mutagenesis. 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 by which these toxic organics were biodegraded as the extracellular electron acceptors. IMPORTANCE Keeping toxic organic pollutants (TOPs) in tolerable levels is a huge challenge for bacteria in extremely unfavorable environments since TOPs could serve as energy substitutes but also as survival stresses when they are beyond some thresholds. This study focused on the underlying adaptive mechanisms of ecologically successful bacterium Shewanella decolorationis S12 when exposed to amaranth, a typical toxic organic pollutant, as the extracellular electron acceptor. Our results suggest that filamentous shift is a flexible and valid way to solve the dilemma between the energy resource and toxic stress. Filamentous cells regulate gene expression to enhance their degradation and detoxification capabilities, resulting in a strong viability. These novel adaptive responses to TOPs are believed to be an evolutionary achievement to succeed in harsh habitats and thus have great potential to be applied to environment

Genome analysis to decipher syntrophy in the bacterial consortium ‘SCP’ for azo dye degradation

“…When the microbial cells encounter a chemical stimulus like dyes, these respond by altering physiology in multifarious ways. The previous reports on transcriptome analysis of the azo-dye respiring or degrading strains have revealed that dyes induce the expressions of genes associated with chemotaxis, signal transduction, motility, DNA and protein damage repair, and oxidative stress [ 65 ]. Based on this, a meticulous inspection of the ORFs encoding several critical proteins dedicated to these functions was conducted (Additional files 10 , 11 , 12 , 13 , 14 and 15 ), and a model for the mechanism of dye co-metabolism was hypothesized (Fig.…”

Lack of Periplasmic Non-heme Protein SorA Increases Shewanella decolorationis Current Generation

“…S. decolorationis S12 was isolated from the activated sludge of a textile-wastewater treatment plant (Xu et al, 2005). S12 mutants and complemented strains were constructed using the methods described previously (Fang et al, 2019). Escherichia coli and S. decolorationis strains were cultured aerobically in LB medium at 37 and 30 • C, respectively.…”

“…Plasmid pHGM01 was used to construct the mutant strains with Ap r , Gm r , Cm r , and att-based suicide vector. Plasmid pHG102 was used to construct the complemented strains with Km r and the S. oneidensis arcA promoter vector (Fang et al, 2019). Gentamycin (15 µg/mL), ampicillin (50 µg/mL), or 2,6-diaminopimelic acid (30 µM) were added to the medium as necessary.…”

“…Ferric ion concentration was determined by ferrozine assay (Lovley and Phillips, 1987). The absorption value of azo dye amaranth was analyzed by UV/Vis spectrophotometer at 520 nm (Fang et al, 2019).…”

“…Strains and plasmids used in this study.WM3064Host for pir-dependent plasmids and donor strain for conjugation; dapAFang et al, 2019 …”