Enhanced microbial reduction of aqueous hexavalent chromium by Shewanella oneidensis MR-1 with biochar as electron shuttle

Highlights

• The conductivity and conjugated O-containing functional groups of BMBCs(ball mill biochar) at higher pyrolysis temperature (≥ 700 °C) were responsible for synergistic effect with MR-1.

• Low electronegative charges of BMBC700 and BMBC800 were more beneficial to the synergistic interaction with MR-1.

• Cr(VI) removal reaction of MR-1 with BMBCs could be classified into two steps-fast reaction and slow reaction.

Abstract

Biochar, carbonaceous material produced from biomass pyrolysis, has been demonstrated to have electron transfer property (associated with redox active groups and multi condensed aromatic moiety), and to be also involved in biogeochemical redox reactions. In this study, the enhanced removal of Cr(VI) by Shewanella oneidensis MR-1(MR-1) in the presence of biochars with different pyrolysis temperatures (300 to 800 °C) was investigated to understand how biochar interacts with Cr(VI) reducing bacteria under anaerobic condition. The promotion effects of biochar (as high as 1.07~1.47 fold) were discovered in this process, of which the synergistic effect of BMBC700(ball milled biochar) and BMBC800 with MR-1 was noticeable, in contrast, the synergistic effect of BMBCs (300–600 °C) with MR-1 was not recognized. The more enhanced removal effect was observed with the increase of BMBC dosage for BMBC700+MR-1 group. The conductivity and conjugated O-containing functional groups of BMBC700 particles themselves has been proposed to become a dominant factor for the synergistic action with this strain. And, the smallest negative Zeta potential of BMBC700 and BMBC800 is thought to favor decreasing the distance from microbe than other BMBCs. The results are expected to provide some technical considerations and scientific insight for the optimization of bioreduction by useful microbes combining with biochar composites to be newly developed.

Introduction

Chromium (Cr), which exists commonly as the type of trivalent chromium [Cr(III)], hexavalent chromium [Cr(VI)], is widely used in various industrial processes, such as electroplating, leather tanning, steelmaking, corrosion control, and wood preservation (Park et al., 2004). Compared to trivalent chromium [Cr(III)](i.e., Cr(OH)₃ and Cr₂O₃), hexavalent chromium [Cr(VI)](CrO₄²⁻, HCrO₄⁻, and Cr₂O₇ ²⁻) shows much higher solubility, mobility, and toxicity, which has been registered as one of priority pollutants due to its negative behavior including carcinogenic, teratogenic and mutagenic properties (Zhong et al., 2017). A large amount of wastewater containing Cr(VI) is still discharged into the environment every year (Ravi and Jabasingh, 2018), and Cr has become one of the most abundant and toxic metals in groundwater worldwide (Dimitroula et al., 2015; Xafenias et al., 2013; Zhang et al., 2020a). There have been several traditional methods proposed to remediate Cr(VI) from wastewater, of which Cr(VI) bioremediation is believed to be most eco-friendly, efficient method because of giving less secondary pollution to environment and relatively low cost(Mohamed et al., 2020; Peng et al., 2015). Shewanella, a typical dissimilatory metal reducing microbe, is capable of reducing Cr(VI) into Cr(III) through a series of EET(extracellular electron transfer) processes by c-Cyts (Wang et al., 2013b), and has been extensively studied on its Cr(VI) reduction (Baaziz et al., 2017; Belchik et al., 2011; Brutinel and Gralnick, 2012; Elias et al., 2008; Han et al., 2017). Considering the involved mechanisms that might be responsible for Cr(VI) reduction by Shewanella, many efforts have been made to improve EET efficiency (Li et al., 2020; Wu et al., 2016).

Biochar, a carbon-rich product of biomass pyrolysis, has received great attention due to its highly porous structure and adsorption capacity as well as redox-activity on various harmful pollutants (e.g. inorganic/organic)(Xu et al., 2020).Recently, biochar has been found to accept/donate several hundred or even thousand micromoles of electrons per gram of biochar, depending on its physic-chemical properties with different feedstock and production conditions (Xu et al., 2020; Zhang et al., 2018).The major moieties of transferring electrons include redox-active surface quinone/hydroquinone groups and the conjugated π-electron system in the condensed polyaromatic carbon ring structures in the carbon matrices (Zhang et al., 2018).

Compared to pristine biochar, mechanical ball milling could increase the activity of materials through improving surface area (Lyu et al., 2017a),reducing the size of particles (Naghdi et al., 2017),and enriching oxygen-containing functional groups (Lyu et al., 2018a).Several studies have reported the effects of ball milling method on the properties and contaminants removal ability of biochar (Huang et al., 2020a; Lyu et al., 2018a). In addition, small biochar particles can easily aggregate with microbes (Gouveia and Pessenda, 2000; Yang et al., 2020) and minerals (Ye et al., 2016).It has been shown that smaller grounded biochar particles exhibited higher rates of microbial Fe(III) reduction compared to larger granulated biochar(Yang et al., 2020; Zhou et al., 2017).Biochar has desirable biocompatibility with Shewanella (Liu et al., 2019; Yang et al., 2020), and evidences have also been accumulated that biochar can act as electron mediator of dissimilatory bacteria (e.g. Shewanella and Geobacter) to enhance anaerobic biotransformation of many kinds of pollutants, offering a promising biological method for soil/wastewater/groundwater remediation (Li et al., 2019; Liu et al., 2020a; Mohamed et al., 2020; Qiao et al., 2018; Wang et al., 2020a; Wu et al., 2020; Xu et al., 2016).

In the microbe-biochar-pollutants system, recent publications have reported the roles of biochar in mediating the microbial reduction of nitrobenzene (Wang et al., 2020a),pentachlorophenol (Yu et al., 2015), but the mechanistic details of the reaction and change characters for microbial Cr(VI) removal in the presence of biochar particles from different pyrolysis temperature are required to further clarify. Whether biochar might exert greater effect on Cr removal with the help of Shewanella would be different to some extent from that of either Shewanella alone or biochar alone. But there has scarcely been seen in the enhancement of Cr removal by Shewanella with the help of biochar but without iron minerals, although there is no evidence that Shewanella strains can use Cr(VI) to grow like iron minerals(RIZLANBENCHEIKH-LATMANI et al., 2007), and that should not be underestimated.

The objective of this research, therefore, was to determine whether the presence of biochar can influence the removal rate and extent of hexavalent chromium by Shewanella oneidensis MR-1, and to understand the mechanism of the microbe-biochar interactions associated with varied pyrolysis temperature of biochar (300 to 800 °C). Firstly, the effect of BMBCs from different pyrolysis temperature as well as its dissolved organic compounds derived from BMBCs on Cr(VI) removal of Shewanella oneidensis MR-1 were evaluated. Then, the cell survival change in the presence of BMBCs during Cr(VI) removal and the characterization of residues after the experiment were also studied. The findings in this study will contribute to supplement and enrich the knowledge on the relationship between biochar and microorganism in the bioreduction of Cr(VI).