Stimulatory and inhibitory effects of metals on 1,4-dioxane degradation by four different 1,4-dioxane-degrading bacteria
Introduction
The ether 1,4-dioxane has been used mainly as a solvent for extraction and as a detergent in chemicals manufacturing. It is also formed as a by-product in the production of ethylene oxide, ethylene glycol, and detergents. 1,4-Dioxane is a suspected human carcinogen, and can persist in aquatic environments due to its stable physicochemical properties (Zhang et al., 2017). Thus, 1,4-dioxane is a contaminant of emerging concern in aquatic environments.
During the last two decades, bacterial strains capable of degrading 1,4-dioxane as a sole carbon and energy source have been isolated from various environments (Inoue et al., 2016; Zhang et al., 2017; Li et al., 2018; Yamamoto et al., 2018c), and found to be distributed even in non-contaminated environments (Sei et al., 2010; He et al., 2018). As a result, biological treatment using 1,4-dioxane-degrading bacteria have been studied extensively as a promising strategy to treat and remediate 1,4-dioxane-contaminated waters (Zhang et al., 2017; Deng et al., 2018; Myers et al., 2018; Yamamoto et al., 2018b).
Biodegradation pathways of 1,4-dioxane have been proposed through the identification of degradation intermediates (Zhang et al., 2017). The common rate-limiting step in proposed biodegradation pathways is the initial oxidation of the carbon atom adjacent to the oxygen atom, namely 2-hydroxylation, which precedes the cleavage of the high-energy C–O bond of the cyclic ether structure (Li et al., 2017). This oxidation is catalyzed by soluble di-iron monooxygenases (SDIMOs) (Masuda et al., 2012; Inoue et al., 2016; He et al., 2017). 1,4-Dioxane-catalyzable SDIMOs are distributed over the six groups of SDIMOs currently recognized, although strains capable of metabolizing 1,4-dioxane are limited to group-5 and group-6 (He et al., 2017). Despite the increasing number of studies aimed at clarifying the diversity of 1,4-dioxane-catabolizing SDIMOs, their enzymatic characterization remains limited.
The enzymatic activity for 1,4-dioxane degradation can be affected by co-occurring compounds. Tetrahydrofuran (THF), a structural analog of 1,4-dioxane, is a well-known primary substrate for cometabolic 1,4-dioxane degradation (Zenker et al., 2000; Mahendra and Alvarez-Cohen, 2006; Sun et al., 2011; Sei et al., 2013b; Inoue et al., 2016). Competitive inhibition of 1,4-dioxane degradation by other analogous cyclic ethers has also been confirmed in previous studies (Inoue et al., 2018; Yamamoto et al., 2018a). Furthermore, chlorinated volatile organic compounds such as 1,1-dichloroethylene, cis-1,2-dichloroethene, and trichloroethene—which are major co-contaminants with 1,4-dioxane in groundwater—have been proven to inhibit 1,4-dioxane biodegradation via complex mechanisms including competition and impairment of degradative enzymes (i.e., SDIMO), the suppression of degradative gene expression, and via negative effects on other cellular activities in 1,4-dioxane-degrading bacteria (Mahendra et al., 2013; Zhang et al., 2016; Deng et al., 2018). In contrast, the effects of metals on 1,4-dioxane biodegradation and associated enzymes have been rarely studied. To our knowledge, only Pornwongthong et al. (2014) have examined the inhibitory effects of Cd(II), Cu(II), Ni(II), and Zn(II) on 1,4-dioxane degradation by Pseudonocardia dioxanivorans CB1190, in which the initial hydroxylation of 1,4-dioxane is catalyzed by THF monooxygenase (Thm) categorized under the group-5 SDIMOs. Due to the possible co-occurrence with 1,4-dioxane in industrial wastewaters and natural environments, the potential impacts of various metals on 1,4-dioxane biodegradation requires further research. In particular, given the diversity in the taxonomy of degrading bacteria (Inoue et al., 2016; Zhang et al., 2017; Li et al., 2018) and in 1,4-dioxane-catalyzable SDIMOs (He et al., 2017), further study of different 1,4-dioxane-degrading bacteria is urgently needed.
This study aimed to evaluate the effects of various metals on the initial oxidation of 1,4-dioxane by different 1,4-dioxane-degrading bacterial strains. Eight metal ions, including those reported to inhibit 1,4-dioxane degradation by P. dioxanivorans CB1190 (Pornwongthong et al., 2014), were used as the test metals. Four 1,4-dioxane-degrading bacterial strains belonging to Mycobacterium, Pseudonocardia, and Rhodococcus were used as the test strains, because most of known 1,4-dioxane-degrading bacteria capable of growing on 1,4-dioxane belong to these three genera (Inoue et al., 2016; Zhang et al., 2017; Li et al., 2018; Yamamoto et al., 2018c). The test strains had been confirmed to possess group-5 or group-6 SDIMOs depending on the strain. The study aimed to improve current understanding of the enzymatic aspects of 1,4-dioxane biodegradation to help identify the promising strains and design the overall system for effective biotreatment/bioremediation of 1,4-dioxane-contaminated waters.
Section snippets
Bacterial strains and culture conditions
The following four bacterial strains capable of degrading 1,4-dioxane as the sole carbon source were used in this study: (i) Mycobacterium sp. D6 (Sei et al., 2013a); (ii) Pseudonocardia sp. D17 (Sei et al., 2013a); (iii) Pseudonocardia sp. N23 (Yamamoto et al., 2018c); and (iv) Rhodococcus aetherivorans JCM 14343 (Goodfellow et al., 2004; Inoue et al., 2016). Mycobacterium sp. D6 and R. aetherivorans JCM 14343 possess inducible 1,4-dioxane degradation enzymes, while Pseudonocardia sp. D17 and
Screening of the effects of metals on 1,4-dioxane degradation
To screen the metals that enhance or suppress 1,4-dioxane degradation by Pseudonocardia sp. D17, Pseudonocardia sp. N23, Mycobacterium sp. D6, and R. aetherivorans JCM 14343, 1,4-dioxane degradation experiments were conducted with and without the addition of 2 mg-metal/L of each of the eight test metals (Fig. 1). The concentration of 1,4-dioxane in the abiotic controls without inoculation and test metal addition showed slight decreasing trends throughout of the test periods due to
Discussion
Soluble di-iron monooxygenases (SDIMOs), which are involved in the initial oxidation of 1,4-dioxane, are a family of multicomponent enzymes consisting of three or four components (an oxygenase, a reductase, and a coupling protein in most cases, with an additional ferredoxin in several cases), and contain a di-iron center at the active site (Leahy et al., 2003; Thiemer et al., 2003; Holmes and Coleman, 2008). Transition metals act as cofactors in the catalytic site of SDIMOs, and are essential
Declaration of interest
None.
CRediT authorship contribution statement
Daisuke Inoue: Conceptualization, Methodology, Formal analysis, Data curation, Writing - original draft, Writing - review & editing, Visualization, Funding acquisition. Tsubasa Tsunoda: Methodology, Investigation. Kazuko Sawada: Investigation, Writing - review & editing, Resources, Writing - review & editing, Supervision. Norifumi Yamamoto: Resources, Writing - review & editing, Funding acquisition. Michihiko Ike: Writing - review & editing, Supervision, Project administration, Funding
Acknowledgements
This study was supported by the Adaptable and Seamless Technology Transfer Program through Target-driven R&D (A-STEP) of the Japan Science and Technology Agency [grant number AS2715159U] and the Kurita Water and Environment Foundation [grant number 16K024].
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