Abstract

Anaerobic biodegradation of aromatic compounds under sulfate-reducing conditions is important to marine sediments. Sulfate respiration by a single bacterial strain and syntrophic metabolism by a syntrophic bacterial consortium are primary strategies for sulfate-dependent biodegradation of aromatic compounds. The objective of this study was to investigate the potential of conductive iron oxides to facilitate the degradation of aromatic compounds under sulfate-reducing conditions in marine sediments, using benzoate as a model aromatic compound. Here, in anaerobic incubations of sediments from the Pearl River Estuary, the addition of hematite or magnetite (20 mM as Fe atom) enhanced the rates of sulfate-dependent benzoate degradation by 81.8 and 91.5%, respectively, compared with control incubations without iron oxides. Further experiments demonstrated that the rate of sulfate-dependent benzoate degradation accelerated with increased magnetite concentration (5, 10, and 20 mM). The detection of acetate as an intermediate product implied syntrophic benzoate degradation pathway, which was also supported by the abundance of putative acetate- or/and H2-utilizing sulfate reducers from microbial community analysis. Microbial reduction of iron oxides under sulfate-reducing conditions only accounted for 2–11% of electrons produced by benzoate oxidation, thus the stimulatory effect of conductive iron oxides on sulfate-dependent benzoate degradation was not mainly due to an increased pool of terminal electron acceptors. The enhanced rates of syntrophic benzoate degradation by the presence of conductive iron oxides probably resulted from the establishment of a direct interspecies electron transfer (DIET) between syntrophic partners. In the presence of magnetite, Bacteroidetes and Desulfobulbaceae with potential function of extracellular electron transfer might be involved in syntrophic benzoate degradation. Results from this study will contribute to the development of new strategies for in situ bioremediation of anaerobic sediments contaminated with aromatic compounds, and provide a new perspective for the natural attenuation of aromatic compounds in iron-rich marine sediments.

Highlights

  • Aromatic compounds comprise numerous environmental pollutants and their removal often relies on microbial degradation (Cao et al, 2009)

  • Using sediment from Pearl River Estuary as microbial inocula, the present study demonstrated that the supplementation ofconductive iron oxides, magnetite or hematite, accelerated the rate of benzoate degradation under sulfate-reducing conditions

  • The detection of acetate, along with microbial analysis implied that syntrophic dependence was essential to benzoate degradation under sulfate-reducing conditions

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Summary

Introduction

Aromatic compounds comprise numerous environmental pollutants and their removal often relies on microbial degradation (Cao et al, 2009). Most contaminated subsurface environments are anaerobic, microbial degradation of aromatic compounds, such as BTEX (benzene, toluene, ethylbenzene, and xylene) or PAH (polycyclic aromatic hydrocarbons), have been observed under nitrate-reducing, Fe(III)-reducing, sulfatereducing, and methanogenic conditions (Fuchs et al, 2011; Ghattas et al, 2017; Muller et al, 2017; Varjani et al, 2017). This might be the main mechanism in the natural attenuation of aromatic compounds in natural environments, and the supplementation of alternative electron acceptors has been considered as an attractive strategy for bioremediation of sites contaminated with aromatic compounds (Perelo, 2010; Ghattas et al, 2017; Hou et al, 2018; Guo et al, 2019). The degradation of aromatic hydrocarbons has been inhibited by suppressing the activity of sulfate-reducing microorganisms or depleting the presence of sulfate in sediments (Lovley et al, 1995). Rothermich et al (2002) demonstrated biodegradation of in situ pools of aromatic hydrocarbons in petroleum-contaminated marine sediments under sulfatereducing conditions, and suggested that microbial sulfate reduction was the main driving force responsible for the self-purification capacity of contaminated harbor sediments

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