Dataset Information

Goethite Hinders Azo Dye Bioreduction by Blocking Terminal Reductive Sites on the Outer Membrane of Shewanella decolorationis S12.

ABSTRACT: Iron (hydr)oxides are the most ubiquitous Fe(III)-containing minerals in the near-surface environments and can regulate organic pollutant biotransformation by participating in bacterial extracellular electron transfer under anaerobic conditions. Mechanisms described so far are based on their redox properties in bacterial extracellular respiration. Here, we find that goethite, a typical iron (hydr)oxide, inhibits the bioreduction of different polar azo dyes by Shewanella decolorationis S12 not through electron competition, but by the contact of its surface Fe(III) with the bacterial outer surface. Through the combined results of attenuated total reflectance (ATR) Fourier transform infrared spectroscopy, two-dimensional correlation spectroscopy, and confocal laser scanning microscope, we found that the outer membrane proteins MtrC and OmcA of strain S12 are key binding sites for goethite surface. Meanwhile, they were identified as the important reductive terminals for azo dyes. These results suggest that goethite may block the terminal reductive sites of azo dyes on the bacterial outer membrane to inhibit their bioreduction. This discovered role of goethite in bioreduction provides new insight into the microbial transformation processes of organic pollutants in iron (hydr)oxide-containing environments.

SUBMITTER: Zhao G

PROVIDER: S-EPMC6604703 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Goethite Hinders Azo Dye Bioreduction by Blocking Terminal Reductive Sites on the Outer Membrane of <i>Shewanella decolorationis</i> S12.

Zhao Gang G Li Enze E Li Jianjun J Liu Feifei F Liu Fei F Xu Meiying M

Frontiers in microbiology 20190625

Iron (hydr)oxides are the most ubiquitous Fe(III)-containing minerals in the near-surface environments and can regulate organic pollutant biotransformation by participating in bacterial extracellular electron transfer under anaerobic conditions. Mechanisms described so far are based on their redox properties in bacterial extracellular respiration. Here, we find that goethite, a typical iron (hydr)oxide, inhibits the bioreduction of different polar azo dyes by <i>Shewanella decolorationis</i> S12 ...[more]

PMID: 31293561

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Project description: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 μm) 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 engineering or synthetic biology if we could picture every unknown node in this pathway.

Project description:The genus Shewanella is well known for its genetic diversity, its outstanding respiratory capacity, and its high potential for bioremediation. Here, a novel strain isolated from sediments of the Indian Ocean was characterized. A 16S rRNA analysis indicated that it belongs to the species Shewanella decolorationis It was named Shewanella decolorationis LDS1. This strain presented an unusual ability to grow efficiently at temperatures from 24°C to 40°C without apparent modifications of its metabolism, as shown by testing respiratory activities or carbon assimilation, and in a wide range of salt concentrations. Moreover, S. decolorationis LDS1 tolerates high chromate concentrations. Indeed, it was able to grow in the presence of 4 mM chromate at 28°C and 3 mM chromate at 40°C. Interestingly, whatever the temperature, when the culture reached the stationary phase, the strain reduced the chromate present in the growth medium. In addition, S. decolorationis LDS1 degrades different toxic dyes, including anthraquinone, triarylmethane, and azo dyes. Thus, compared to Shewanella oneidensis, this strain presented better capacity to cope with various abiotic stresses, particularly at high temperatures. The analysis of genome sequence preliminary data indicated that, in contrast to S. oneidensis and S. decolorationis S12, S. decolorationis LDS1 possesses the phosphorothioate modification machinery that has been described as participating in survival against various abiotic stresses by protecting DNA. We demonstrate that its heterologous production in S. oneidensis allows it to resist higher concentrations of chromate.IMPORTANCEShewanella species have long been described as interesting microorganisms in regard to their ability to reduce many organic and inorganic compounds, including metals. However, members of the Shewanella genus are often depicted as cold-water microorganisms, although their optimal growth temperature usually ranges from 25 to 28°C under laboratory growth conditions. Shewanella decolorationis LDS1 is highly attractive, since its metabolism allows it to develop efficiently at temperatures from 24 to 40°C, conserving its ability to respire alternative substrates and to reduce toxic compounds such as chromate or toxic dyes. Our results clearly indicate that this novel strain has the potential to be a powerful tool for bioremediation and unveil one of the mechanisms involved in its chromate resistance.

Dataset Information

Goethite Hinders Azo Dye Bioreduction by Blocking Terminal Reductive Sites on the Outer Membrane of Shewanella decolorationis S12.

Publications

Goethite Hinders Azo Dye Bioreduction by Blocking Terminal Reductive Sites on the Outer Membrane of <i>Shewanella decolorationis</i> S12.

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