Molecular density regulating electron transfer efficiency of S. oneidensis MR-1 mediated roxarsone biotransformation

https://doi.org/10.1016/j.envpol.2020.114370Get rights and content

Highlights

  • Roxarsone stimulated population growth of S. oneidensis MR-1.

  • Roxarsone maximum specific reduction rate decreased with increasing roxarsone.

  • Bacterial electron transfer rate was estimated up to 1.4 × 106 electrons/cell/s.

  • Bacterial electron transfer rate increased with present roxarsone concentration.

Abstract

Efficient extracellular electron transport is a key for sufficient bioremediation of organoarsenic pollutants such as 4-hydroxy-3-nitrobenzenearsonic acid (roxarsone). The related apparent kinetics characteristics are essential for engineering practice of bioremediation activities and for full understanding the environmental fate of roxarsone, yet remains poorly understood. We report, to our knowledge, the first study of the electron transfer characteristics between roxarsone and participating S. oneidensis MR-1. The electron transfer rate during roxarsone biotransformation was estimated up to 3.1 × 106 electrons/cell/s, with its value being clearly associated with the apparent roxarsone concentration. Lowing roxarsone concentration extended the average separation distance between cells and neighboring roxarsone molecules and thereby augmented electric resistance as well as extended cell movement for foraging, thus reduced electron transfer rate. In addition, the presence of roxarsone significantly stimulated population growth of S. oneidensis MR-1 with nearly doubled maximum specific growth rate, albeit with clearly increased lag time, as compared with that of none-roxarsone scenario. These findings provide, at the first time, basic biostoichiometry of S. oneidensis MR-1 induced roxarsone biotransformation, which may shed lights for full understanding of roxarsone transformation process in waste treatment systems that are necessary for engineering practice and/or environmental risks assessment.

Introduction

As an effective organoarsenical feed additive, 4-hydroxy-3-nitrobenzenearsonic acid (roxarsone) has been widely used in poultry industry to promote growth and/or prevent coccidal intestinal parasites for decades (Garbarino et al., 2003; Zhao et al., 2020). Although application of roxarsone has been banned in most developed countries, including China (MARA, 2018), long-term historical extensive application has resulted in a massive accumulation of roxarsone in the environment (Liu et al., 2013; Mangalgiri et al., 2015; Huang et al., 2019). Roxarsone is barely decomposed within animal body, and is usually excreted as its initial form along the manure (Makris et al., 2008; Jiang et al., 2013). Along with the storage or field application of animal waste or direct discharge into the environment, roxarsone can easily enter into soil, surface- or ground-water bodies due to its water-soluble capacity (Silbergeld and Nachman, 2008; Huang et al., 2019). Roxarsone itself is a moderately toxic compound, but it can be converted into higher toxic products upon exposure to the environment, such as trivalent inorganic arsenic or methylarsenicals, and eventually leads to severe environmental and public health risks (Cortinas et al., 2006; Stolz et al., 2007; Chen et al., 2018). In nature, roxarsone can be oxidized, reduced, methylated or dimethylated through numerous physical, chemical and biological interactions, and eventually produce a variety of arsenic compounds (Garbarino et al., 2003; Chen et al., 2016; Oyewumi and Schreiber, 2017). For example, nitro group of roxarsone was observed to be quickly reduced into an amino group in the absence of oxygen, yielding an intermediate product of 3-amino-4-hydroxybenzene arsonic acid (AHBAA) in anaerobic environment (Shi et al., 2014; Liu et al., 2017).

Shewanella species are widely distributed in nature, including soil, sedimentary, freshwater and marine environments (Heidelberg et al., 2002; Harris et al., 2010), and they are capable of utilizing a variety of electron acceptors for anaerobic respiration and thus have attracted massive attention especially in biotechnology applications (Bretschger et al., 2007). Numerous respiration pathways of Shewanella oneidensis MR-1 and their underlying mechanisms at the presence of various electron donors have been reported (Liang et al., 2014; Zhang et al., 2015). For example, S. oneidensis MR-1 was able to utilize roxarsone as a sole terminal electron acceptor during its anaerobic respiration, and enabled roxarsone transformation (Chen et al., 2016, 2018). Meanwhile, as a dissimilative iron-reducing bacterium, S. oneidensis MR-1 is able to reduce Fe(Ⅲ) into Fe(Ⅱ) in the presence of both Fe(Ⅲ) and roxarsone, with the formed Fe(Ⅱ) capable of transmitting electrons to roxarsone and thereby, conspire to stimulate roxarsone transformation (Chen et al., 2016). The yielded byproduct of roxarsone transformation (e.g., AHBAA) can be either adsorbed and immobilized or to be further biodegraded into inorganic arsenics (Liang et al., 2014; Liu et al., 2017), adding uncertainty to environmental- and public-health risks (Cortinas et al., 2006; Shi et al., 2014). During these transformation processes, one molecular roxarsone receives six electrons from bacterial cells or electron donors to form a primary byproduct of AHBAA (Stolz et al., 2007), whereby efficient extracellular electron transport is a key for sufficient reduction of roxarsone. Shewanella species have evolved various strategies of extracellular electron transport, including direct electron transfer using multiheme cytochromes (Bretschger et al., 2007; McLean et al. 2010) or via conductive nanowires (Reguera et al., 2005; Zacharoff and EI-Naggar, 2017), as well as using soluble shuttle-mediators that transfer electrons between cells and acceptors (Marsili et al., 2008; Wu et al., 2014). Harris et al. (2010) have shown that S. oneidensis MR-1 cells tended to stay on (or in close proximity to) a redox active surface (that served as electron acceptors) to facilitate extracellular electron transport. A recent study showed that nanowires existed as extensions of the outer membrane and periplasm of a S. oneidensis MR-1 cell, which associating with localized multiheme cytochromes MtrC and OmcA enhanced extracellular electron transport (Pirbadian et al., 2014). Notwithstanding the importance of the metal-reducing bacterium S. oneidensis MR-1 for the transformation and potentially bioremediation of the abandoned roxarsone in nature, the electron transfer characteristics between roxarsone and partnering bacterial cells are poorly understood, which are essential for full understanding the biotransformation process and environmental fate of roxarsone in nature or in waste treatment systems. In this study, we investigated the electron transfer performance of S. oneidensis MR-1 induced roxarsone transformation in a model aqueous system, and quantified the kinetics characteristics of both roxarsone transformation and the participating bacterial population growth.

Section snippets

Material and methods

The study is a reanalysis of raw data from an earlier research (Chen et al., 2016), focusing on the extracellular electron transfer characteristics between the target toxicant, roxarsone, and the bacterium, S. oneidensis MR-1, as well as bacterial growth kinetics, which are essential for full understanding of bacteria mediated roxarsone (bio)transformation process and engineering practices. The experimental material and setup, as well as the analytical methods are identical to (and can be

Bacterial population growth kinetics at the presence of roxarsone

Simulation results revealed that the logistic model was capable of mimicking bacterial population growth kinetics for all scenarios (Fig. 1), evidenced by high values of the coefficient of determination (R2 > 0.9376), as shown in Table 1. The maximum specific growth rate of S. oneidensis MR-1 under 0.10 mmol/l of roxarsone was estimated doubled (1.02 h−1) as compared to that of none-roxarsone scenario (0.49 h−1), associating with significantly amplified (nearly by half) maximum population. It

Conclusions

The electron transfer characteristics between roxarsone and the closely associated partnering S. oneidensis MR-1 cells were investigated by linking the biostoichiometry and kinetics of roxarsone biotransformation and bacterial population growth in an aqueous system. The apparent electron transfer rate between a S. oneidensis MR-1 cell and the closely-surrounding roxarsone molecules was estimated up to 3.1 × 106 electrons/cell/s, which was in good agreement with recently reported literature

CRediT authorship contribution statement

Gang Wang: Conceptualization, Investigation, Methodology, Writing - review & editing. Neng Han: Investigation, Writing - original draft. Li Liu: Writing - review & editing. Zhengchen Ke: Investigation. Baoguo Li: Writing - review & editing. Guowei Chen: Conceptualization, Writing - review & editing.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgement

The authors thank Drs. Yuanpei Luo and Yan Jin for helpful scientific comments, and acknowledge the financial supports of the National Natural Science Foundation of China (41877412, 41401265), the Scholarship of the ‘National Thousand (Young) Talents Program’ of China, and the Chinese Universities Scientific Fund (2019TC067).

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