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

Feifei Liu,Fei Liu,Gang Zhao,Jianjun Li,Meiying Xu,Enze Li

doi:10.3389/fmicb.2019.01452

Feifei Liu, Fei Liu + Show 4 more

Open Access

https://doi.org/10.3389/fmicb.2019.01452

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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.

Highlights

Under anaerobic conditions, various organic pollutants such as azo dyes and halogenated hydrocarbons can be reduced by acting as electron acceptors in bacterial anaerobic respiration (Schwarz et al, 2012; Venkidusamy et al, 2016; Xu et al, 2019)
The first-order reduction rate constants of methyl orange and methyl red were 0.28 and 0.39 h−1, respectively, showing no difference from the goethite-free treatments. These results suggested that goethite-surface Fe(III) inhibited the bioreduction of azo dyes by the contact with bacterial cells, rather than serving as a competitive electron acceptor
This study presents evidence that goethite does not act as a competitive electron acceptor to hinder azo dye bioreduction and suggests a novel mechanism that the contact of insoluble ironoxide particles with bacterial outer membrane can affect the bioreduction process

Summary

Introduction

Various organic pollutants such as azo dyes and halogenated hydrocarbons can be reduced by acting as electron acceptors in bacterial anaerobic respiration (Schwarz et al, 2012; Venkidusamy et al, 2016; Xu et al, 2019). In organisms capable of extracellular electron transport such as Shewanella and Geobacter, the hemeproteins on the bacterial outer membrane had shown high affinity to iron (hydr)oxide surface (Xiong et al, 2006; Sheng et al, 2016) They are the terminal proteins of the electron transport chain that transports electrons from the cell to the extracellular electron receptors such as soluble Fe ions and high polar organics (Ross et al, 2009; Liu et al, 2017). For Shewanella decolorationis strain S12, no Fe(OH) reduction was detected after 7 days incubation, but its efficiency in azo dye decolorization reached 97.6% after 7 h (Xu et al, 2007) It remains unknown whether the contact of the hemeproteins with Fe(III) on the surface of iron (hydr)oxide will affect the electron transfer from these terminal reductive proteins to organic compounds. The effects of this behavior on extracellular electron transfer are essential for understanding microbial reduction of organic pollutants in iron-rich environments

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