Degradation of BDE-47 in mangrove sediments under alternating anaerobic-aerobic conditions

Journal of Hazardous Materials 378 (2019) 120709

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Degradation of BDE-47 in mangrove sediments under alternating anaerobicaerobic conditions

T

Ying Pana,b, Juan Chenc, Haichao Zhoud, S.G. Cheunga, Nora F.Y. Tama,

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a

Department of Chemistry, City University of Hong Kong, Tat Chee Avenue, Kowloon, Hong Kong Special Administrative Region, PR China College of Oceanography, Hohai University, Xikang Road, Nanjing 210098, PR China c Key Laboratory of Integrated Regulation and Resource Department on Shallow Lakes, Ministry of Education, College of Environment, Hohai University, Xikang Road, Nanjing 210098, PR China d College of Life Sciences and Oceanography, Shenzhen University, Nanhai Avenue, Shenzhen 518060, PR China b

GRAPHICAL ABSTRACT

Debromination and degradation pathways of BDE-47 under alternating anaerobic-aerobic conditions (percentage is the ratio of each product at the end of 40 weeks to the initial spiked BDE-47).

ARTICLE INFO

ABSTRACT

Keywords: Alternating anaerobic-aerobic condition PBDEs OH-PBDEs Microbial degradation

Polybrominated diphenyl ethers (PBDEs) resistant to degradation have significant environmental impacts. Anaerobic reductive debromination and aerobic oxidation of PBDEs by microorganisms are main removal mechanisms during natural attenuation, but previous studies often focused on the process under either aerobic or anaerobic condition leading to unsatisfactory removal. The present study aims to remove PBDEs by employing alternating anaerobicaerobic condition, which is common in inter-tidal mangrove sediments, and elucidate the degradation pathways. During 40-week experiment, BDE-47 reduced with an accumulation of tri-BDEs and di-BDEs as debromination products in all sediments. However, the removal percentages of BDE-47 and the concentrations of debromination congeners varied among flushing regimes. Sediments under less frequent flushing regime (longer duration of aerobic period) had significantly lower concentration and proportion of debromination products, especially BDE-17, than that under more frequent regime (longer anaerobic period). BDE-17 then went through aerobic degradation pathway, as evidenced by the accumulation of its hydroxylation form. Microbial analyses further revealed that less frequent regime favored accumulation of biphenyl dioxygenase gene for aerobic degradation, while more frequent tidal regime promoted growth of dehalogenating bacteria for reductive debromination. This study first time demonstrated that PBDEs in contaminated sediments could be removed under alternating anaerobic-aerobic conditions.

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Corresponding author. E-mail address: [email protected] (N.F.Y. Tam).

https://doi.org/10.1016/j.jhazmat.2019.05.102 Received 24 January 2019; Received in revised form 29 May 2019; Accepted 30 May 2019 Available online 30 May 2019 0304-3894/ © 2019 Elsevier B.V. All rights reserved.

Journal of Hazardous Materials 378 (2019) 120709

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1. Introduction

contaminated sediments. The present study therefore aims to explore the removal efficiency and degradation pathways of BDE-47 in mangrove sediments under different alternating anaerobic-aerobic conditions with various tidal frequencies and durations. BDE-47, a tetra-BDE congener, was chosen as a model PBDE, because it has been widely detected in environment [6,7,23].

Since the introduction of polybrominated diphenyl ethers (PBDEs) to the market in the 1970s, their production and accumulation in the environment have raised worldwide concerns [1]. PBDEs have a tendency to adsorb onto sediments because of their hydrophobic and lipophilic properties, leading to contamination and accumulation in sediments when disposed in the environment [2,3]. In sediments, microbial degradation is the most important mechanism to remove PBDEs. Previous researchers illustrated the microbial degradation rates and pathways of PBDE congeners with different extents of bromination [4,5]. In general, anaerobic microorganisms debrominate highly brominated PBDEs into less brominated ones. A number of dehalorespiring microorganisms such as Dehalococcoides spp. and Dehalogenimonas spp. have been proved to be the two key bacterial groups related to the debromination process of BDE-47 in sediments [6,7]. Dehalococcoides, in particular, was found to be the most important bacterial group in the anaerobic degradation of BDE-47 in mangrove sediments [6]. However, the debromination rate is often slow because functional anaerobic bacteria usually have low abundance and slow metabolism activity in natural environments [8]. On the other hand, aerobic microorganisms oxidize PBDEs into metabolites, such as hydroxylated PBDEs (OHPBDEs), bromophenols, bromocatechols and so on. Among them, the phenolic compounds like phenol, catechol and p-hydroquinone can participate in the tricarboxylic acid cycle [9]. Dioxygenases encoded by biphenyl dioxygenase genes (bph) are key enzymes in catalyzing the aerobic degradation of PBDEs, and 2,3-dihydroxybiphenyl dioxygenase (gene product), among various dioxygenases, plays an important role in ring-cleavage of the less brominated PBDEs [10–12]. However, aerobic microorganisms can only oxidize less brominated PBDEs, such as monoand, to a lesser extent, tri-BDEs, and their aerobic degradation ability weakens with the increasing degree of bromination [13]. How to rapidly and efficiently remove PBDEs from sediments remains an urgent issue that needs to be resolved. Many scientists have proposed the idea of combining anaerobic and aerobic conditions to remove contaminants from sediments, which has been verified in the reduction of polychlorinated biphenyls (PCBs). Evans et al. [14] showed that the efficiency of removing PCBs was enhanced by the combined anaerobic-aerobic treatment (a 19-week anaerobic treatment followed by a 19-week aerobic treatment) in comparison with either anaerobic or aerobic treatment alone. A similar but more detailed transformation process of Aroclor 1260 was also reported showing this contaminant was dehalogenated into less chlorinated PCBs under an anaerobic condition and the products were then degraded during the aerobic treatment [15]. Meggo and Schnoor adopted alternating cycles of flooding and draining to create alternate redox cycles in soil and found that more parent PCBs were reduced than soil not exposed to these cycles [16]. Not only PCBs, the degradation of other halogenated compounds, such as hexachlorobenzene (HCB) [17], tetrabromobisphenol A [18], chlorinated ethylenes (CEs) [19], dichloromethane (DCM) [19] and dichlorodiphenyltrichloroethane (DDT) [20] could also be achieved by alternating anaerobic-aerobic treatment. To our knowledge, only one study reported the removal and degradation of PBDEs under two different tidal regimes in constructed wetland microcosms [21], but the degradation pathways under alternating anaerobic-aerobic conditions were not studied. Mangroves, which are inter-tidal wetlands dominating tropical and subtropical coastlines, receive periodical flooding and draining of tidal water, thus forming cycles of alternating anaerobic-aerobic condition. Vegetation density, evapotranspiration, rainfall, and groundwater also affect flooding and draining, thus causing diverse tidal flushing regimes or patterns within the same mangrove forest. The tidal variation has been reported to range at 3–80 tides per year [22]. It is hypothesized that variations in tidal flushing regimes would generate different durations of anaerobic and aerobic periods, leading to various degrees and even different pathways of PBDE removal and degradation in

2. Materials and methods 2.1. Sediment collection and experimental setup In this experiment, bulk samples of surface sediment (0–5 cm) were collected from the middle part of a mature mangrove forest in Mai Po, Hong Kong. The stock solution of BDE-47 dissolved in acetone was added into a small portion (about 100 g) of freeze-dried mangrove sediments and mixed thoroughly. After the solvent evaporated, the BDE47-spiked freeze-dried sediments were added to a large lot of fresh sediments and mixed homogeneously to obtain sediments with an initial contamination level of 1 μg g−1 freeze-dried weight (dw). This initial value aimed to simulate PBDE levels in severely contaminated areas in South China [23]. Such addition and mixing process to prepare artificially contaminated sediments were used in previous studies and did not have any significant influence on the indigenous microorganisms [5,24]. The actual concentrations of BDE-47 in the contaminated sediments were also determined and the measured initial concentrations were 1.02 ± 0.02 μg g-1. These artificially contaminated sediments were immediately used without aging for monitoring the entire degradation pathways of BDE-47. Microcosms were set up in polyvinyl chloride baskets (15 cm × 15 cm × 10 cm), and each basket was prepadded with two layers of nylon cloth (400 mesh) to prevent any leakage of sediment particles. Each basket filled with approximately 1 kg of contaminated sediment was subject to flooding and draining of tidal water by submerging the basket into a bucket containing artificial seawater at a salinity of 15 psu under high tide, and removing it from the bucket for exposure to air at low tide. Three tidal flushing regimes with different high and low tides were prepared, that is, (i) 1-day high tide and 1-day low tide (1:1d), (ii) 1-week high tide and 1-week low tide (1:1w), and (iii) 2-week high tide and 2-week low tide (2:2w). The 1:1d group was similar to the real tidal flushing regime in Hong Kong and was mostly adopted in previous studies conducted in laboratory or greenhouse [5,24]. The 1:1w and 2:2w groups were chosen to produce alternating anaerobic-aerobic conditions with different frequencies and durations. Sterilized controls, with sediment autoclaved at 121 °C for 1 h on two consecutive days prior to the spike of BDE-47 (1 μg g-1 dw), were also set up for each tidal flushing regime to monitor any abiotic loss or degradation of BDE-47. Sodium azide (NaN3) (200 mg L−1) was added into the tidal water biweekly to inhibit microbial activity in sterilized controls. Each treatment or control was prepared in triplicate. The entire experiment lasted for 40 weeks, and at weeks 0, 8, 16, 28, and 40, about 25 g of sediment samples was collected from each microcosm using a plastic hollow tube and homogenized prior to analysis. Each sediment sample was divided into three portions, 0.5 g was immediately stored in −20 °C for DNA extraction, 15 g was freeze-dried for the analysis of PBDEs, OH-PBDEs, and the rest was air-dried for the determination of sediment properties. 2.2. Analyses of sediment properties The redox potential (Eh) of sediment was measured at a depth of 3 cm below the surface in situ at a time interval of 3 or 4 days for the first 12 weeks using a hand-held combination meter (TPS WP-81, Australia). The Eh of sediments were also recorded at each sampling time. Sediment pH was determined using a digital pH meter (Thermo Electron Corporation, USA) after mixing air-dried sediment with double distilled water (ddH2O) at a ratio of 1:5 (w/v). The concentrations of total Kjeldahl nitrogen (TKN) and total phosphorus (TP) in sediment 2

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were measured by the flow injection analyzer (Lachat QuikChem Method 8000, USA) after digestion with concentrated sulfuric acid (H2SO4) at 390 °C for 4 h. Total organic carbon (TOC) was determined using the standard sulfuric acid-potassium dichromate oxidation method according to Wen et al [25]. The physico-chemical properties of sediment at the beginning of the study were listed in table S1 in Supplementary information. 2.3. Analyses of PBDEs and OH-PBDEs The extraction, purification and instrumental quantification procedures for PBDEs and OH-PBDEs were according to Chen et al. [5] and Gao et al. [26], respectively. In brief, the sample was extracted with an ASE 200 accelerated solvent extraction system (Dionex, Sunnyvale, CA, USA) and analyzed by GC–MS with a 30 m HP-5 fused silica capillary column (0.25 mm i.d. and 0.25 μm film thickness) in a negative chemical ionization (for PBDEs) or electron-impact ionization (for OHPBDEs) mode. More details were provided in the Supplementary information. The complete debromination product, i.e. diphenyl ether, was not determined, as its parent PBDE congeners, mono-BDEs, were not detected during the entire experiment. The quality control and recovery were performed by a matrix-spike recovery test as described by Zhu et al [24]. The recoveries of BDE-7, -8, -17, -28 and -47 in sediment were close to 90%, while the recoveries of target OH-PBDE congeners ranged from 82% to 105%. All the reported concentrations of PBDE and OH-PBDE congeners were not corrected by the recovery rate.

Fig. 1. Variation in redox potential in sediments with indigenous living microorganisms under different tidal flushing regimes during 28 days to represent a complete cycle of 2:2w flushing regime (mean and standard deviation values of three replicates are shown; at each time point, different letters indicate significant differences among three tidal flushing regimes at p ≤ 0.05 according to one-way ANOVA; 1:1d: 1-day high tide and 1-day low tide; 1:1w: 1-week high tide and 1-week low tide; 2:2w: 2-week high tide and 2-week low tide).

(reaching −100 mV) and a similar Eh at the end of draining period (increasing to 320 mV) (Fig. 1). The duration of 28 days reflected one complete cycle of the 2:2w flushing regime and two cycles of 1:1w regime. Fig. S1 depicted Eh values of sediments at the end of weeks 8, 16, 28 and 40. Sediments under 1:1d flushing regime always had lower Eh value than that under 1:1w and 2:2w flushing regimes, while no significant difference was detected between sediments under the latter two flushing regimes. The pH value of the sediments under the three flushing regimes across the entire experiment was around 6 and was comparable with that of the initial value of 6.2 at week 0 (Fig. 2A). No significant changes were found in the concentration of TOC in sediments with indigenous living microorganisms in the first 16 weeks, but decreased significantly thereafter, especially in sediments under 1:1w and 2:2w flushing regimes (Fig. 2B). At the end of the 40-week experiment, sediments under the 2:2w regime had the lowest TOC concentration. This result indicated that a longer duration of aerobic period enhanced the decomposition of organic carbon in sediments. Similarly, TKN also decreased slightly from weeks 16 to 40, and the lowest value was detected in 2:2w regime at the end of the 40-week experiment (Fig. 2C). The concentration of TP did not show any significant change during the entire experimental period, and no significant difference was found among tidal flushing regimes (Fig. 2D). The temporal changes of TOC and TKN in sterilized control treatments were not measured in this study. It is because sediments were sterilized and NaN3 was added to these sediments during the incubation to inhibit the microbial process. As the metabolism of TOC and TKN is mainly controlled by microorganisms, the temporal changes of TOC and TKN in sterilized control treatments should be minimal without any microbes or microbial activity.

2.4. Microbial analysis Total DNA was extracted from 0.5 g of fresh sediment using the FastDNA SPIN kit for Soil (MP Biomedicals, USA), following the manufacturer's instruction. The copy numbers of total bacterial, Dehalococcoides spp. and Dehalogenimonas spp. 16S rRNA gene were determined using quantitative real-time polymerase chain reaction (qPCR), with the primers and conditions as described in table S2 in Supplementary information. The bphC gene copy number was quantified with a forward primer 5'-GTCGGACATCATTGACATCCAG-3' and a reverse primer 5'-AAGGCGTAGCCCACATCG-3' [27], and the amplifying condition was the same as that for Dehalococcoides spp. 16S rRNA gene. 2.5. Statistical analysis The mean and standard deviations (SD) of three replicates of all parameters, including concentrations of sediment properties, PBDEs, OH-PBDEs, and gene copy numbers of each sample were calculated. A parametric one-way analysis of variance (ANOVA) was performed using the SPSS 11.5 software (USA) to test any difference in each parameter among the tidal flushing regimes at each sampling time at P < 0.05. 3. Results 3.1. Changes in sediment physico-chemical properties Changes in redox potential (Eh) of sediment samples with indigenous living microorganisms from weeks 8 to 12 (28 days) clearly reflected the effect of tidal flushing regimes (Fig. 1). For 1:1d flushing regime, Eh was maintained at around −200 mV and did not show any significant change between high and low tides, probably due to the frequent alternating flooding-draining process. Different from 1:1d tidal regime, Eh for 1:1w flushing regime decreased to about −50 mV during flooding period (7-day high tide) but increased to around 310 mV during draining period (7-day low tide). This pattern repeated well during the next flushing regime of 7-day high tide followed by 7-day low tide (Fig. 1). The trend for 2:2w flushing regime was similar to that for 1:1w but with an even lower Eh at the end of flooding period

3.2. PBDEs in sediments under different tidal flushing regimes At the end of the 40-week experiment, abiotic losses of BDE-47 in sterilized controls under 1:1d, 1:1w, and 2:2w regimes were 19.4%, 20.8%, and 20.8%, respectively (Fig. 3A), and no debromination products were detected. On the contrary, sediments with indigenous living microorganisms exhibited a significant reduction of BDE-47 (Fig. 3B). The removal under 1:1d flushing regime was 73.2%, greater than that under 1:1w regime (55.5%), and 2:2w regime had the lowest removal percentage (47.5%). The concentrations of daughter PBDE congeners, particularly tri- and di-BDEs, increased with time, and such increasing 3

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Fig. 2. Temporal changes in pH (A), total organic carbon (TOC) (B), total Kjeldahl nitrogen (TKN) (C), and total phosphorus (TP) (D) in sediments with indigenous living microorganisms under different tidal flushing regimes during the 40-week experiment (mean and standard deviation values of three replicates are shown; at each time point, different letters indicate significant differences among three tidal flushing regimes at p ≤ 0.05 according to one-way ANOVA; ns: not significant; 1:1d: 1day high tide and 1-day low tide; 1:1w: 1-week high tide and 1-week low tide; 2:2w: 2-week high tide and 2-week low tide).

trend was consistent with decreases in the parent congener, BDE-47 (Fig. 3B; Table 1). At the end of week 8, tri- and di-BDEs were found in all sediment samples, with similar concentrations and percentages among tidal regimes (Fig. S2; Table 1). However, congener profiles of PBDEs in sediments started to show differences among three tidal flushing regimes from week 16 onwards, with higher concentrations and proportions of debromination products such as BDE-17 in 1:1d than in 1:1w and 2:2w flushing regimes, especially at the end of weeks 16 and 28 (Fig. S2; Table 1). The concentration and proportion of other debromination products, such as BDE-28, -8 and -7, also exhibited a similar temporal pattern as BDE-17, with higher concentration and proportion found in 1:1d than in the 1:1w and 2:2w tidal flushing regimes. Among the tri-BDE congeners, BDE-17 had significantly higher concentration than BDE-28.

Sediments under 1:1w and 2:2w tidal flushing regimes had higher concentrations of OH-PBDEs than that under 1:1d regime. Such concentration differences among tidal flushing regimes became even larger at the end of week 40, with the concentration in 2:2w doubling that in 1:1d regime (Table 2). Among all OH-PBDEs, 4′-OH-BDE17 was the most dominant hydroxylated congener, and its proportion increased from 27.7% at the end of week 8 to 77.1% at the end of week 40 (average value of three tidal flushing regimes) (Fig. S3). The percentage of 4′-OH-BDE17 in sediments under 2:2w flushing regime was significantly higher than that in sediments under other regimes (Fig. S3; Table 2). The average proportion of meta- plus para-substituted OHPBDEs, including 3-OH-BDE47, 5-OH-BDE47, and 4′-OH-BDE17, in all sediment samples collected at four sampling times was ≥ 80%, much higher than that of ortho-substituted OH-PBDEs, namely, 6-OH-BDE47, 2′-OH-BDE28, and 6′-OH-BDE17 (≤ 20%) (Fig. S3). Very low concentrations of 3-OH-BDE47, 5-OH-BDE47, and 6-OHBDE47 were found in sterilized controls at the end of 40 weeks, the average values, 0.77, 1.16, and 0.45 ng g−1 dw, respectively, were significantly lower than that in sediments with indigenous living microorganisms. The composition profiles of OH-PBDEs in sterilized controls were similar among three tidal flushing regimes (Fig. S4).

3.3. OH-PBDEs in sediments under different tidal flushing regimes In sediments with indigenous living microorganisms, five OH-PBDE congeners, namely, 3-OH-BDE47, 5-OH-BDE47, 6-OH-BDE47, 2′-OHBDE28, and 4′-OH-BDE17, were detected at the end of week 8, and another congener, 6′-OH-BDE17, was detected from week 28 onwards (Fig. S3; Table 2). Total concentrations of all OH-PBDE congeners (∑OH-PBDEs) in sediments with indigenous living microorganisms increased rapidly with time, especially from week 8 onwards, but the extent of the increase depended on tidal flushing regime (Table 2).

3.4. Mass balance calculation of BDE-47 in different tidal flushing regimes Percentages of residual parent BDE-47, its debromination products Fig. 3. Removal curves of BDE-47 in sterilized sediments (A) and sediments with indigenous living microorganisms (B) under different tidal flushing regimes during the 40-week experiment (mean and standard deviation values of three replicates are shown; at each time point, different letters indicate significant differences among three tidal flushing regimes at p ≤ 0.05 according to one-way ANOVA; ns: not significant; 1:1d: 1-day high tide and 1-day low tide; 1:1w: 1-week high tide and 1-week low tide; 2:2w: 2-week high tide and 2-week low tide). 4

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Table 1 Concentrations of five PBDE congeners (BDE-47, BDE-28, BDE-17, BDE-8, and BDE-7) and their total (∑PBDEs) (ng g−1 dw) in sediments with indigenous living microorganisms under different tidal flushing regimes at weeks 8, 16, 28, and 40 (mean and standard deviation values of three replicates are shown; at the same sampling time, the values of each PBDE congener followed by different letters indicate significant differences among three tidal flushing regimes at p ≤ 0.05 according to one-way ANOVA; ND: not detected; 1:1d: 1-day high tide and 1-day low tide; 1:1w: 1-week high tide and 1-week low tide; 2:2w: 2-week high tide and 2week low tide). Time

Tidal flushing regime

BDE-47

Week 8

1:1d 1:1w 2:2w 1:1d 1:1w 2:2w 1:1d 1:1w 2:2w 1:1d 1:1w 2:2w

812.7 860.4 863.9 742.5 837.2 800.4 423.6 630.7 679.6 271.6 451.4 532.8

Week 16 Week 28 Week 40

± ± ± ± ± ± ± ± ± ± ± ±

33.8a 39.9a 28.3a 12.8a 40.1b 6.9b 21.7a 16.9b 11.8c 27.9a 14.1b 14.4c

BDE-28

BDE-17

BDE-8

BDE-7

∑PBDEs

3.6 3.3 3.4 5.9 3.8 3.2 7.0 4.8 3.9 5.3 3.8 2.4

68.5 ± 1.8a 66.2 ± 3.6a 63.7 ± 1.3a 140.8 ± 6.1c 84.8 ± 7.8b 72.4 ± 4.6a 145.1 ± 3.4b 119.1 ± 8.1a 114.2 ± 7.3a 198.4 ± 8.4b 143.8 ± 9.7a 150.2 ± 2.9a

ND ND ND 10.8 ± 0.4b 8.3 ± 0.2a 8.0 ± 0.2a 20.8 ± 1.3b 10.4 ± 0.2a 9.5 ± 0.3a 26.7 ± 3.5c 8.9 ± 2.8b 2.9 ± 0.5a

10.2 ± 0.1a 10.0 ± 0.2a 10.0 ± 0.1a 14.3 ± 0.2b 9.9 ± 0.4a 9.4 ± 0.3a 26.3 ± 1.1b 13.6 ± 0.6a 12.5 ± 0.6a 16.0 ± 2.2b 10.8 ± 3.0a 9.4 ± 1.3a

895.1 939.9 940.9 914.3 943.9 893.5 622.8 778.7 819.8 518.1 618.8 697.7

± ± ± ± ± ± ± ± ± ± ± ±

0.2a 0.2a 0.1a 0.1c 0.3b 0.2a 0.3c 0.1b 0.1a 0.5c 0.5b 0.2a

(de-PBDEs) and hydroxylation products (OH-PBDEs) in sediments and tidal waters with/without living microorganisms at the end of 40-week experiment are shown in Table 3. In sterilized controls, most BDE-47 (around 80%) still remained in sediments, and very low percentage of BDE-47 (< 1%) was found in tidal waters or transformed into OHPBDEs (< 1%) (Table 3). In sediments with living microorganisms, percentages of de-PBDEs under three tidal flushing regimes accounted for 24.68%, 16.49% and 16.25%, respectively, while percentages of OH-PBDEs only accounted for 1–2.3% of the initial concentration of BDE-47 in sediments (Table 3). In tidal waters flooded and drained from sediments with living microorganisms, very low percentages of BDE-47 and de-PBDEs (all < 1%) were detected, and OH-PBDEs were below detection limits (Table 3). Loss of the spiked BDE-47 in sterilized controls ranged from 18.37 to 19.67%, lower than that in the corresponding non-sterilized sediments with living microorganisms, and the maximum value (47.36%) was found in 1:1d flushing regime (Table 3).

± ± ± ± ± ± ± ± ± ± ± ±

13.5a 43.2a 6.6a 35.9a 48.1a 25.9a 22.3a 13.4b 3.8c 35.1a 3.9b 14.4c

gene copies of Dehalogenimonas spp. in sediments under 1:1d and 1:1w regimes were maintained at the same level (Fig. S5). The temporal trend of the two bacterial groups appeared to follow changes in air temperature (Fig. S5). During the entire experimental period, gene copies of the two dehalogenating bacteria in sediments under 1:1d flushing regime were significantly higher than those under 1:1w or 2:2w flushing regimes. At the end of the 40-week experiment, gene copies of Dehalococcoides spp. and Dehalogenimonas spp. in sediments under 1:1d flushing regime were 6.3 and 5.9 × 107 g−1dw, respectively. The copy number of bphC gene in sediments under three flushing regimes decreased slightly within the first 16 weeks, increased dramatically to the highest value at week 28, and then decreased again toward the end of the experiment (Fig. S5). Temporal trends in the abundance of bphC gene in all sediments also followed changes in air temperature (Fig. S5). Sediments under 1:1w and 2:2w flushing regimes had higher copy numbers of bphC gene than that under 1:1d flushing regime, especially at weeks 28 and 40, corresponding to the higher concentrations of OH-PBDEs. At week 40, the bphC gene copy numbers in sediments under 1:1w and 2:2w flushing regimes were 10.7 and 12.1 × 107 g−1dw, respectively, higher than that under 1:1d flushing regime at 6.9 × 107 g−1dw.

3.5. Abundances of dehalogenating bacteria and bphC gene Temporal changes in 16S rRNA gene copies of dehalogenating bacteria, Dehalococcoides spp. and Dehalogenimonas spp., were comparable during the entire experiment (Figs. 4A,B; S5). Gene copies of the two bacterial groups decreased during the first 16 weeks and then increased rapidly to the highest level at the end of 28 weeks (Figs. 4A,B; S5). At weeks 28–40, gene copies of Dehalococcoides spp. in sediments under three regimes showed slight decreases, similar to those of Dehalogenimonas spp. in sediments under 2:2w tidal flushing regime, and

4. Discussion Both anaerobic debromination and aerobic metabolism can remove PBDEs, depending on the type of PBDE congener and the environmental

Table 2 Concentrations of six OH-PBDE congeners (3-OH-BDE47, 5-OH-BDE47, 6-OH-BDE47, 2′-OH-BDE28, 4′-OH-BDE17, and 6′-OH-BDE17) and their total (∑OH-PBDEs) (ng g−1 dw) in sediments with indigenous living microorganisms under different tidal flushing regimes at weeks 8, 16, 28, and 40 (mean and standard deviation values of three replicates are shown; at the same sampling time, the values of each OH-PBDE congener followed by different letters indicate significant differences among three tidal flushing regimes at p ≤ 0.05 according to one-way ANOVA; ND: not detected; 1:1d: 1-day high tide and 1-day low tide; 1:1w: 1-week high tide and 1-week low tide; 2:2w: 2-week high tide and 2-week low tide). Time

Tidal flushing regime

6'-OH-BDE17

2'-OH-BDE28

4'-OH-BDE17

6-OH-BDE47

5-OH-BDE47

3-OH-BDE47

∑OH-PBDEs

Week 8

1:1d 1:1w 2:2w 1:1d 1:1w 2:2w 1:1d 1:1w 2:2w 1:1d 1:1w 2:2w

ND ND ND ND ND ND 0.02 0.03 0.03 0.05 0.06 0.06

0.07 0.11 0.08 0.08 0.09 0.07 0.14 0.19 0.17 0.23 0.24 0.21

0.50 ± 0.01a 0.53 ± 0.14a 0.73 ± 0.15a 1.59 ± 0.02a 2.92 ± 0.57b 4.16 ± 0.56c 5.75 ± 0.31a 7.49 ± 0.16b 11.41 ± 0.79c 6.43 ± 0.26a 20.17 ± 0.48b 17.90 ± 2.31b

0.26 0.36 0.39 0.31 0.43 0.43 0.85 0.85 0.68 0.45 0.67 0.65

0.53 0.76 0.61 0.79 0.83 0.64 2.80 1.93 1.18 1.64 1.64 1.24

0.38 0.62 0.45 0.39 0.47 0.37 2.27 1.64 0.86 1.25 1.35 1.38

1.74 ± 0.06a 2.38 ± 0.21b 2.26 ± 0.19b 3.17 ± 0.11a 4.74 ± 0.69b 5.67 ± 0.71b 11.83 ± 1.68a 12.13 ± 0.44b 14.32 ± 1.05b 10.05 ± 0.35a 24.12 ± 0.81b 21.45 ± 2.58b

Week 16 Week 28 Week 40

± ± ± ± ± ±

0.005a 0.008a 0.005a 0.003a 0.007a 0.006a

± ± ± ± ± ± ± ± ± ± ± ±

0.03a 0.02a 0.01a 0.004a 0.01a 0.005a 0.02a 0.03a 0.02a 0.02a 0.02a 0.02a

5

± ± ± ± ± ± ± ± ± ± ± ±

0.05a 0.02b 0.01b 0.003a 0.01b 0.01b 0.02b 0.01b 0.01a 0.01a 0.02b 0.02b

± ± ± ± ± ± ± ± ± ± ± ±

0.03a 0.04c 0.01b 0.06b 0.04b 0.07a 0.21c 0.12b 0.06a 0.01b 0.10b 0.07a

± ± ± ± ± ± ± ± ± ± ± ±

0.02a 0.03c 0.01b 0.01a 0.05a 0.05a 0.11c 0.11b 0.17a 0.05a 0.16a 0.16a

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Table 3 Percentages of BDE-47, its debromination products (de-PBDEs) and hydroxylation products (OH-PBDEs) in sediments and tidal waters of different treatments at the end of 40-week experiment (% = concentration of BDE-47 or de-PBDEs or OH-PBDEs / initial concentration of BDE-47 × 100%; ND: not detected; for each treatment, loss = 1 - % of BDE-47 - % of de-PBDEs - % of OH-PBDEs in both sediments and tidal water; different letters in each row indicate significant differences among different treatments at p ≤ 0.05 according to one-way ANOVA). Sterilized control

BDE-47 De-PBDEs OH-PBDEs Loss

Sediment Tidal water Sediment Tidal water Sediment Tidal water

Non-sterilized groups

1:1d

1:1w

2:2w

1:1d

1:1w

2:2w

80.73%d 0.61%c ND ND 0.29%c ND 18.37%a

80.26%d 0.63%c ND ND 0.24%b ND 18.87%a

79.29%d 0.65%c ND ND 0.19%a ND 19.87%a

26.76%a 0.29%a 24.28%b 0.32%a 0.99%d ND 47.36%d

44.48%b 0.43%b 16.49%a 0.19%b 2.38%e ND 36.03%c

52.5%c 0.45%b 16.25%a 0.19%b 2.11%e ND 28.5%b

Fig. 4. Relative abundances of Dehalococcoides spp. (A) and Dehalogenimonas spp. (B) 16S rRNA genes in sediments with indigenous living microorganisms under different tidal flushing regimes during the 40-week experiment (% = copy numbers of dehalorespiring bacterial 16S rRNA gene/ copy numbers of total bacterial 16S rRNA gene; mean and standard deviation values of three replicates are shown; at each time point, different letters indicate significant differences among three tidal flushing regimes at p ≤ 0.05 according to one-way ANOVA; ns: not significant; 1:1d: 1day high tide and 1-day low tide; 1:1w: 1-week high tide and 1-week low tide; 2:2w: 2-week high tide and 2-week low tide).

condition. The typical highly brominated PBDE congeners like nonaand deca-BDEs can only go through anaerobic debromination [28,29], whereas less brominated congeners, such as mono- through tri-BDE congeners, can undergo aerobic metabolism [30,31]. Zhu et al. [32] reported that BDE-47 in mangrove sediments could debrominate within three months under a strict anaerobic condition but did not show any significant change under a pure aerobic condition. Although this reductive debromination process could remove the parent PBDEs from contaminated sediments, the debromination congeners produced could induce secondary contamination. In most of the observed systems reported in literature, only anaerobic process without an effective aerobic degradation would result in incomplete debromination. However, Ding et al. [33] found that D. mccartyi-containing microbial consortia, ANAS195, could completely debrominate penta-BDE mixtures to diphenyl ether through reductive debromination. The importance of aerobic and anaerobic processes, and the alternation of these two processes for complete debromination and removal of PBDEs, especially PBDEs with high bromine number, deserve more in-depth research. In the present study, BDE-47 was first debrominated to less brominated congeners (tri- and di-BDEs) and followed by aerobic degradation under alternating anaerobic-aerobic conditions. However, only a low concentration of hydroxylated BDE-47 was detected in the present study, indicating the difficulty in hydroxylating BDE-47 in mangrove sediments even under alternating anaerobic-aerobic conditions. The high molecular size and hydrophobicity of BDE-47 decreased its susceptibility to hydroxylation and hindered the subsequent attack by aerobic enzymes [13]. The position of bromine atoms also affects the aerobic degradation reaction. For example, PBDE congeners with orthosubstitution are usually more difficult to degrade than the congeners with meta- or para- substitution presumably because of the steric hindrance of the responsible dioxygenase [34]. As BDE-47 has two orthosubstitutions with bromine atoms, the aerobic degradation may be difficult to occur. The high total organic matter content in mangrove

sediments also retained PBDEs in sediments and reduced their bioavailability to microorganisms, leading to the difficulty in degrading PBDEs aerobically in mangrove sediments [32]. On the other hand, debromination products of BDE-47 (tri-BDE and di-BDE congeners) generated during the anaerobic period of alternating anaerobic-aerobic conditions such as under 2:2w and 1:1w tidal regimes could be further mineralized to hydroxylated metabolites through the aerobic process. Although three OH-BDE47 metabolites were detected without firstly undergoing reductive debromination, the concentrations of OH-BDE47 were much lower than that of OH-BDE17 despite the concentration of BDE-47 was much higher than that of BDE-17. These suggested that the hydroxylation ability of microorganisms decreased with increases in the bromination extent of PBDEs. Moreover, the higher concentration of OH-PBDEs, especially 4′-OH-BDE17, detected in 2:2w and 1:1w than in 1:1d flushing regime confirmed the hydroxylation process under alternating anaerobic-aerobic conditions. Hydroxylated PBDEs could be produced naturally by marine algae and other microorganisms, or via biological/abiotic hydroxylation of PBDEs [35,36]. Wang et al. [37] reported that ortho-substituted OHPBDEs were the main natural occurring compounds and were dominant in environmental matrices and biotic samples, although some orthosubstituted OH-PBDEs were also detected in plants and animals exposed to PBDEs. Meta- and para-substituted OH-PBDEs mainly resulted from the biotransformation of PBDEs in contaminated environments, with only a small proportion occurring naturally in environmental matrices [38,39]. In the present study, the proportions of meta- plus para-substituted OH-PBDEs were much higher than those of ortho-substituted OH-PBDEs, indicating the important contribution of metabolic biotransformation to the occurrence of OH-PBDEs in sediments. These findings provide further evidence for the biotransformation of debromination products to OH-PBDEs in mangrove sediments under alternating anaerobic-aerobic conditions. The formation of hydroxylated PBDEs catalyzed by dioxygenases was an initial step of PBDE aerobic 6

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oxidation. These hydroxylated PBDEs would then go through a further oxidation process to become bromophenols, bromocatechols, bromide ions, and so on [28]. In a human liver microsome study, 5-OH-BDE47 was the direct hydroxylation product of BDE-47, which could be further degraded into 2,4-dibromophenol (2,4-DBP) by P450 2B6, one human recombinant P450 enzyme involved in the oxidative biotransformation of BDE-47 [40]. In the present study, the higher concentration of 5-OHBDE47 in sediments with more frequent tidal treatment than that with less frequent tidal regimes might be related to redox potential, the more negative redox potential in former sediments might inhibit the further degradation of 5-OH-BDE47. However, it is not clear whether 4'-OHBDE17 will go through further oxidative metabolism under aerobic condition. More experiments should be carried out on the production and degradation rates of different hydroxylated metabolites, particularly 5-OH-BDE47 and 4’-OH-BDE17, to illuminate their metabolism and kinetics in sediments. Because of the limitation of measuring methods, these degradation products were not determined in the present study. The limitations are as follows. First, the concentration of OH-PBDEs was low and the degradation products of OH-PBDEs was probably lower, so it was difficult to detect the degradation products using GC-MS. Second, previous studies found that OH-PBDEs could further be degraded into brominated phenol and brominated catechols [13], but standards of these products were not commercially available. Without standards, it was unable to quantify the degradation products of OH-PBDEs. A more sensitive measuring method should be developed in future to detect all possible degradation intermediates and to elucidate the complete pathway of BDE-47 under all flushing regimes, especially those under alternating anaerobic-aerobic conditions. Microorganisms are the key players in the transformation of PBDEs in sediments. Zanaroli et al. [29] reported that anaerobic bacteria could couple the reductive debromination of PBDEs to energy conservation using halogenated compounds as electron acceptors, generating less or none brominated congeners under an anaerobic condition. This halorespiring mechanism usually occurs under an anaerobic condition because the usual electron acceptor O2 is depleted and the halogenated compounds can act as alternate electron acceptors [41]. Dehalococcoides and Dehalogenimonas are two typical halorespiring bacterial genera. They have been used to evaluate or predict the potential of sediments to remove halogenated compounds under an anaerobic condition [6,7,42]. In the present study, higher abundances of Dehalococcoides spp. and Dehalogenimonas spp. were detected in sediments under 1:1d regime than under the other regimes, suggesting their association with the removal of BDE-47 through an anaerobic pathway. Nevertheless, there was no direct evidence to support a causal link between bacterial abundance and PBDE removal efficiency, and more research is needed to elucidate such link. Statistical tests showed that significant differences in the absolute abundances of Dehalococcoides spp. and Dehalogenimonas spp. among different tidal regimes. However, their number differences were not considerable in magnitude among different regimes. This might be due to that organohalide respiring bacteria were typically minor populations and difficult to enrich [43], so the magnitude of changes during the experiment might not be considerable. Some researchers proposed only the presence of these organohalide respiring bacteria was insufficient to indicate their metabolic activities [43], and it is better to measure the activity of PBDE reductive dehalogenases enzymes. However, the same study also pointed that the identification of PBDEs reductive dehalogenases is impeded by the co-metabolic nature of PBDEs and the marginal cell yield of PBDE debrominating populations in most mixed cultures and isolates. On the other hand, qPCR is a very sensitive molecular technique and has been widely used in identifying and quantifying specific bacterial populations in microcosm experiments [5–8]. At present, measuring the abundance of organohalide respiring bacteria using qPCR technique is still one of the most feasible and appropriate methods to link their metabolic activities in microcosm experiments even though there are some limitations. For aerobic degradation of PBDEs, different types of dioxygenases

encoded by biphenyl dioxygenase genes (bph) have been reported. For example, 1,2-dioxygenase and 2,3-dioxygenase in an aerobic bacterial strain, Rhodococcus jostii RHA1, can catalyze the initial hydroxylation step of less brominated PBDE congeners, and phenol hydroxylase and catechol 1,2-dioxygenase are responsible for the downstream degradation processes [13]. In the present study, bphC gene was selected to characterizing and quantifying the potential aerobic PBDE degraders. A significantly higher abundance of bphC gene was detected in sediments under 2:2w regime than under other regimes, coinciding with our hypothesis that a more aerobic environment was more favorable to aerobic degradation activities, thus explaining the higher concentrations of OH-PBDEs in sediments under 2:2w regime. As bphC gene only encodes 2,3-dihydroxybiphenyl dioxygenase responsible for the ringcleavage of the less brominated PBDEs, other types of bph genes such as bphA gene encoding biphenyl dioxygenase that is responsible for the initial hydroxylation step of the less brominated PBDE congeners [13] should also be analyzed in future. This will enhance our understanding of the aerobic degradation mechanisms of PBDEs. The dynamics of the bphC gene, as well as the two bacterial groups, followed the changes in air temperature, revealing the significant effect of temperature on the abundance of microorganisms and microbial activity. More, the three treatments at each time point in the present study were under the same temperature, so the effect of tidal flushing on gene copy numbers at each time point should not be influenced by temperature changes. Overall, the loss of BDE-47 was less than 50% in this study, possibly due to the short cultivation time which was 40 weeks. It has been reported that the growth rate of functional bacteria and associated degradation activity were slow [43]. More research should be conducted to further enhance the removal of PBDEs. The OH-PBDE metabolites accumulated in sediments regardless of the tidal regime, although more OH-PBDE metabolites were detected in sediments with less frequent tidal regime than that with more frequent regimes. The OH-PBDEs are more potent for some endpoints such as endocrine disruption than PBDEs, causing the secondary contamination, which is still an inevitable issue in removing PBDEs either by anaerobic debromination or aerobic hydroxylation or both pathways. Not only tidal frequency, the timing and shift between alternating anaerobic and aerobic conditions are also important parameters affecting the degradation of BDE-47. One possible way to reduce such accumulation is to completely debrominate PBDEs to less-brominated products before exposing to aerobic conditions [14,15]. Previous studies have shown that sequential anoxic-oxic treatment could be an effective strategy to remove halogenated compounds from soil or groundwater [15,44]. On the other hand, Liu et al. [18] proved that tetrabromobisphenol A (TBBPA), the most commonly used brominated flame retardants, were effectively debrominated to bisphenol A (BPA) during the anoxic incubation which was then degraded rapidly during the subsequent oxic incubation, however, the residues of TBBPA bound with soil organic matter under the anoxic condition were released during the subsequent oxic condition, indicating that the sequential anoxic-oxic incubation approach might not completely remove TBBPA from environmental matrices. The researchers suggested that multiple cycles of anoxic-oxic conditions, i.e., repeatedly alternating anaerobic-aerobic conditions, might help resolve the issue of bound residues and enhance the degradation efficiency of these pollutants compared to only one cycle of sequential anaerobicaerobic conditions. More studies on the duration of anaerobic and aerobic conditions, as well as multiple cycles of alternation between these two conditions, should be performed in future to reveal the degradation kinetics of BDE-47 under different anaerobic-aerobic conditions and to identify the most appropriate way in removing PBDEs. 5. Conclusions In this study, tidal flushing regimes produced different redox conditions in mangrove sediments, affecting the anaerobic debromination and aerobic degradation processes of PBDEs. A constant anaerobic 7

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condition was formed under the 1:1d flushing regime and favored the growth of Dehalococcoides spp. and Dehalogenimonas spp., leading to reductive debromination of highly brominated BDE-47. Conversely, the 1:1w and 2:2w tidal flushing regimes generated alternating anaerobicaerobic conditions and supported both anaerobic debromination and aerobic degradation mechanisms. The longer aerobic periods generated under these two flushing regimes induced a higher abundance of the bphC gene than those under the 1:1d flushing regime. The debromination products, such as BDE-17, generated from debromination could then be hydroxylated aerobically and become 4’-OH-BDE17, the predominant hydroxylation congener. The alternating anaerobic-aerobic condition could be a promising in situ natural attenuation strategy to achieve the removal of PBDEs. Further investigation should be conducted to optimize this strategy to achieve the effective bioremediation of PBDE-contaminated sediments, without generating secondary contamination.

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Acknowledgments The work described in this paper was financially supported by the Research Fund from the National Key Research and Development Program of China (2017YFC0506102), the National Natural Science Foundation of China (41576086, 41876090), the Innovation of Science Technology Commission of Shenzhen Municipality (JCYJ20170818092901989), and Hong Kong RGC GRF fund (Project No. 11301717). We thank Dr. Patrick Lee (School of Energy and Environment, City University of Hong Kong, Hong Kong) for his help in microbial analysis and Prof. Michael Lam (Department of Chemistry, City University of Hong Kong, Hong Kong) for his assistance in quantification of OH-PBDEs. Appendix A. Supplementary data Supplementary material related to this article can be found, in the online version, at doi:https://doi.org/10.1016/j.jhazmat.2019.05.102. References [1] X. Zhu, J.Z. Beiyuan, A.Y.Y. Lau, S.S. Chen, D.C.W. Tsang, N.J.D. Graham, D.H. Lin, J.T. Sun, Y.H. Pan, X. Yang, X.D. Li, Sorption, mobility, and bioavailability of PBDEs in the agricultural soils: roles of co-existing metals, dissolved organic matter, and fertilizers, Sci. Total Environ. 619–620 (2018) 1153–1162. [2] M. Iqbal, J.H. Syed, A. Katsoyiannis, R.N. Malik, A. Farooqi, A. Butt, J. Li, G. Zhang, A. Cincinelli, K.C. Jones, Legacy and emerging flame retardants (FRs) in the freshwater ecosystem: a review, Environ. Res. 152 (2017) 26–42. [3] G. Yu, Q.W. Bu, Z.G. Cao, X.M. Du, J. Xia, M. Wu, J. Huang, Brominated flame retardants (BFRs): a review on environmental contamination in China, Chemosphere 150 (2016) 479–490. [4] M.A. Ramirez-Elias, R. Ferrera-Cerrato, A. Alarcon, J.J. Almaraz, G. RamirezValverde, L.E. de-Bashan, F.J. Esparza-Garcia, O. Garcia-Barradas, Identification of culturable microbial functional groups isolated from the rhizosphere of four species of mangroves and their biotechnological potential, Appl. Soil Ecol. 82 (2014) 1–10. [5] J. Chen, H.C. Zhou, C. Wang, C.Q. Zhu, N.F.Y. Tam, Short-term enhancement effect of nitrogen addition on microbial degradation and plant uptake of polybrominated diphenyl ethers (PBDEs) in contaminated mangrove soil, J. Hazard. Mater. 300 (2015) 84–92. [6] Y. Pan, J. Chen, H.C. Zhou, S. Farzana, N.F.Y. Tam, Vertical distribution of dehalogenating bacteria in mangrove sediment and their potential to remove polybrominated diphenyl ether contamination, Mar. Pollut. Bull. 2 (2017) 1055–1062. [7] J. Chen, P.F. Wang, C. Wang, J.J. Liu, H. Gao, X. Wang, Spatial distribution and diversity of organohalide-respiring bacteria and their relationships with polybrominated diphenyl ether concentration in Taihu Lake sediments, Environ. Pollut. 232 (2018) 200–211. [8] C. Shin, P.L. McCarty, J. Kim, J. Bae, Pilot-scale temperate-climate treatment of domestic wastewater with a staged anaerobic fluidized membrane bioreactor (SAFMBR), Bioresour. Technol. 159 (2014) 95–103. [9] Y. Lv, Z. Zhang, Y. Chen, Y. Hu, A novel three-stage hybrid nano bimetallic reduction/oxidation/biodegradation treatment for remediation of 2,2′4,4′-tetrabromodiphenyl ether, Chem. Eng. J. 289 (2016) 382–390. [10] K.R. Robrock, W.W. Mohn, L.D. Eltis, L. Alvarez-Cohen, Biphenyl and ethylbenzene dioxygenases of Rhodococcus jostii RHA1 transform PBDEs, Biotechnol. Bioeng. 108 (2011) 313–321. [11] L.F. Jiang, C.L. Luo, D.Y. Zhang, M.K. Song, Y.T. Sun, G. Zhang, Biphenyl-metabolizing microbial community and a functional operon revealed in e-waste-

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