Do pyrene and Kandelia obovata improve removal of BDE-209 in mangrove soils?

Chemosphere 240 (2020) 124873

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Do pyrene and Kandelia obovata improve removal of BDE-209 in mangrove soils? Ruili Li a, *, Huan Ding a, Meixian Guo b, Xiaoxue Shen a, Qijie Zan c, d a

School of Environment and Energy, Shenzhen Graduate School of Peking University, Shenzhen, 518055, Guangdong, China Nanshan Second Experimental School, Shenzhen, 518053, China c College of Life Sciences and Oceanography, Shenzhen University, Shenzhen, 518060, China d Guangdong Neilingding Futian National Nature Reserve, Shenzhen, 518000, China b

h i g h l i g h t s

g r a p h i c a l a b s t r a c t


BDE-209 uptake and debromination in K. obovata root is limited in affecting soil BDE-209 removal.
Pyrene addition improved removal of BDE-209 in contaminated soil without K. obovata planting.
K. obovata planting improved removal of BDE-209 in contaminated soil with/without pyrene addition.
Microbial community responses for BDE-209 removal caused by pyrene and K. obovata were different.

a r t i c l e i n f o

a b s t r a c t

Article history: Received 20 December 2018 Received in revised form 7 September 2019 Accepted 14 September 2019 Available online 14 September 2019

Combined pollution caused by polybrominated diphenyl ethers (PBDEs) and polycyclic aromatic hydrocarbons (PAHs) in mangrove wetlands is serious, with their remediation to be been paid more and more attention. However, little is known about the combined impact of PAHs and mangrove species on removal of PBDEs in contaminated soils. In this study, BDE-209 and pyrene were selected and a 9 months experiment was conducted to explore how BDE-209 removal in contaminated soil varied with pyrene addition and Kandelia obovata planting, and to clarify corresponding microbial responses. Results showed that BDE-209 removals in soil induced by pyrene addition or K. obovata planting were significant and stable after 6 months, with the lowest levels of BDE-209 in combined pyrene addition with K. obovata planting. Unexpected, root uptake of BDE-209 in K. obovata was limited for BDE-209 removal in soil, which was verified by lower total amount of BDE-209 bioaccumulated in K. obovata's root. In soil without K. obovata planting, BDE-209 removal caused by pyrene addition coexisted with changed bacterial abundance at phylum Planctomycetes and Chloroflexi, class Planctomycetacia, and genus Blastopirellula. K. obovata-induced removal of BDE-209 in soil may be related to bacterial enrichment in phylum Proteobacteria, class Gammaproteobacteria and genus Ilumatobacter, Gaiella. Thus, in BDE-209 contaminated soil, microbial community responses induced by pyrene addition and K. obovata planting were different at phylum, class and genus levels. This is the first study demonstrating that pyrene addition and K. obovata planting could improve BDE-209 removal, and differently affected the corresponding responses of microbial communities. © 2019 Elsevier Ltd. All rights reserved.

Handling Editor: Chang-Ping Yu Keywords: Polybrominated diphenyl ethers Polycyclic aromatic hydrocarbons Kandelia obovata Dissipation Microbial community response

* Corresponding author. E-mail address: [email protected] (R. Li). https://doi.org/10.1016/j.chemosphere.2019.124873 0045-6535/© 2019 Elsevier Ltd. All rights reserved.

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R. Li et al. / Chemosphere 240 (2020) 124873

1. Introduction Mangroves, with characteristics of high productivity and organic carbon accumulation, are susceptible to various persistent organic pollutants (POPs) (Li et al., 2014; Wanapaisan et al., 2018). Polybrominated diphenyl ethers (PBDEs) and polycyclic aromatic hydrocarbons (PAHs) are two kinds of POPs commonly detected in environment, which have been detected in mangrove wetlands in and out of China, such as mainland China (Wu et al., 2017), Hong Kong SAR of China (Zhu et al., 2014a), Korea (Moon et al., 2012), India (Pozo et al., 2017), Senegal (Bodin et al., 2011), Argentina (Tombesi et al., 2017) and USA (Damseaux et al., 2017). PBDEs, additive flame retardants, could bound to soil and atmospheric fine particles, and transfer into organisms through food chains and food webs due to their highly lipophilic and hydrophobic characteristics (Kelly et al., 2008; Babalola and Adeyi, 2018; Chen et al., 2019). PAHs, mutagenic/carcinogenic compounds containing two or more benzene rings, are tolerant to microbial degradation in anaerobic/ reductive soil, which lead to adverse effect on ecosystem (Toyama et al., 2011) and human health (Geier et al., 2018). Generally, the biodegradation of PBDEs mainly focused on anaerobic and aerobic processes with different microbial communities to be responsible for their debromination (Yang et al., 2015, 2017). Furthermore, the dissipations of PBDEs would be affected by their combination with other factors (such as carbon sources, electron acceptors, surfactants, inducers, and vitamin B12, etc), which would affect bacterial communities to alter their dissipation process and potential damage (Jeelani et al., 2017; Li et al., 2018; Zhao et al., 2018). The application of yeast extract in sewage sludge could improve dissipation of PBDEs with 10e15.7% (Stiborova et al., 2015). Surfactant b-cyclodextrin is a feasible choice for phytoremediation of combined Cd/BDE-209 contaminated soil with Solanum nigrum planting (Li et al., 2018). On the other hand, soil microorganisms would be directly related to biogeochemical processes, and could respond rapidly to various contaminants (Bayen, 2012; Liu et al., 2015). The dissipation of lower PBDE congeners in soil is closely related to microorganism activities, with Pseudomonas stutzeri and Pseudomonas putida strain TZ-1 to utilize BDE-47 as carbon and energy source for their growth (Zhang et al., 2013; Xin et al., 2014). Previous studies have shown that wastewater-borne PBDEs and PAHs could be immobilized in the iron plaque on mangrove's root surface, with lesser accumulation into plant tissues (Pi et al., 2016, 2017). The toxicity and suppression of PBDEs and PAHs on mangrove plant species are also reported (Wang et al., 2014a; Farzana and Tam, 2018). The improved BDE-209 removal by K. obovata planting may also be related to that plant root could release various organic compounds to provide potential carbon source or energy for the growth of rhizosphere microorganisms (Tesar et al., 2002). Rhizosphere was a dynamic interface between plant and soil, where various invertebrates and microorganisms would affect plant growth and biogeochemical cycling (McNear, 2013; Philippot et al., 2013). While, there are still some questions remain to be ambiguous: Can PAHs addition and mangrove planting improve removal of PBDEs in mangrove soils? The corresponding microbial response in soil is not clear. In fact, the multiple components of PBDEs and PAHs make it difficult to explore the function of PAHs in PBDEs dissipation (Wang et al., 2015; Pi et al., 2016). In this study, BDE-209, pyrene and Kandelia obovata was selected to explore the impact of pyrene addition and K. obovata planting on dissipation and debromination of BDE-209 in mangrove soil. We also identified the responses of bacterial communities which would contribute to the microbial ecology of in situ bioremediation of BDE-209. It is hypothesized that pyrene addition and K. obovata planting would improve dissipation of BDE-209 in

mangrove sediment, with special microbial activities. Generally, BDE-209 is predominant commercial deca-BDE, with greater accumulation than lower-brominated BDE congeners in soil (Li et al., 2015a). Pyrene, a class of organic compounds, polyaromatic hydrocarbons with carcinogenic potential, has often been used as model compound in biodegradation of PAHs (Rostami et al., 2016; Qiu et al., 2018; Wanapaisan et al., 2018), and has been detected in mangrove wetlands (Li et al., 2014; Qiu et al., 2018). K. obovata is adapted to various environmental conditions, and could produce strong rhizosphere effect due to its well-developed root system (Wang et al., 2014b; Li et al., 2015b). 2. Material and methods 2.1. Experimental setup and sampling Mature propagules of K. obovata (18e20 cm height), were provided by Quanzhou Tong Qing Mangrove Technology Co. Ltd, China. The soil was collected from mangrove wetland in Sai Keng, Hong Kong China with slight human disturbance and contamination (Tam et al., 2001; Farzana et al., 2017). The basic information of soils were as follows: pH, 7.43; TN, 0.76 g kg1; TC, 2.28 g kg1; Sand, 74.2%; Silt, 14.1%; Clay, 11.7%. In this study, the background concentration of BDE-209 in treated soil was 40 mg g1, and other debrominated BDE congeners were not detected. In this study, soil treatments included: (1) single BDE-209-soil with 40 mg g1 BDE209 addition; (2) BDE-209þpyrene-soil with 40 mg g1 BDE-209 and 10 mg g1 pyrene addition. Pyrene was provided by Chem Service Inc., USA, and pyrene-treated soils were prepared as follows: 600 g dry soil was spiked with 0.6 g pyrene dissolved in acetone, then mixed thoroughly and placed in fume hood to evaporate the solvent for 12 h. Then, the soil was homogeneously mixed with 59.4 kg dry soil to obtain 10 mg g1 pyrene-treated soil. The concentrations of BDE-209 and pyrene were aimed to simulate environmental pollution in some severely contaminated areas (Pruell et al., 1990; Sun et al., 2013; Li et al., 2014). For the planted treatments, 2-year-old seedlings of K. obovata (about 20 cm height) were previously grown in greenhouse with 800e1400 mmol m2s1 photosynthetic active, 20e29.5  C, and 60e80% relative humidity. The 2-year old seedlings has high survival after transplanting. The culture time last for one week to make seedlings to be acclimated to the contaminated soils. All the seedlings were irrigated with deionized water to avoid water loss caused by evaporation if necessary. A mangrove tide-tank system with 6 PVC tanks was applied in this study. The tide-tank system was composed of tank, storage container, pump, control valve, and the computer control system (Chu et al., 2000; Tam et al., 2009; Ke et al., 2011). Each PVC tank (1 m length  0.5 m width  0.3 m depth) filled with 20 kg treated soil was divided longitudinally into two identical compartments by a plastic board. The plastic boards did not completely separate the tank and there was movement of water between the compartments. In this study, the effect of water movement on mixing treatments was limited, because BDE-209 was mixed with soil and the hydrophilicity of BDE-209 is very low. In each tank, one compartment was planted with 10 K. obovata, and the other one was kept unplanted. Thus, the experiment treatments were divided into four treatment groups as follows (each with three replicates): (1) unplanted with BDE-209 addition (NP þ B treatment); (2) K. obovata planting with BDE-209 addition (Ko þ B treatment); (3) unplanted with BDE-209 and pyrene addition (NP þ BP treatment); (4) K. obovata planting with BDE-209 and pyrene addition (Ko þ BP treatment). There were 3 replicates in every treatment. Thus, 30 seedlings were transplanted into the single BDE-209 treatments, and combined BDE-209 and pyrene treatments, respectively. In this

R. Li et al. / Chemosphere 240 (2020) 124873

study, the experimental design did not include control of sediment without BDE-209 contamination, and the primary focus was to compare the effect of different treatments (BP, Ko) on BDE-209 removal. The depth of soil in tanks was about 5 cm. During the whole experiment, all tanks were flooded as one tidal cycle every day (12 h high tide/12 h low tide). At high tides, artificial seawater (1.5% salinity, mixing commercial sea salts with tap water) in storage container was pumped into tank with 5 cm water depth. At low tides, the seawater was drained off into the storage container to expose the soil. The artificial seawater was supplied with some tap water if necessary to avoid water loss caused by evaporation. Every four weeks, the seawater in storage container was replaced with fresh artificial seawater. At the start of this experiment (0 month), sediment and K. obovata root were analyzed for the background concentrations of BDE-209 in this study. At 3, 6, and 9 months of the experiment, soil samples (0e5 cm depth) and root samples were collected randomly. In each compartment without K. obovate planting, three sediment samples were collected, with three sediment samples and three root samples collected in compartments with K. obovata planting. Totally, 36 soil samples and 18 root samples were collected. All the samples were freeze-dried to constant weight for PBDEs determination (Alpha 2e4 LSC basic, Germany).

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(0.8 mL), 2.5 mM dNTPs (2 mL), 5  FastPfu Buffer (4 mL) and template DNA (10 ng). The reaction was repeated three times. The A xyPrep DNA Gel Extraction Kit (Axygen Biosciences, Union City, CA, USA) was applied to purify the resulted PCR products. Based on an Illumina MiSeq platform (Illumina, San Diego, USA), the amplicons were pooled in equimolar and paired-end sequenced. All raw reads in this study have been deposited in Sequence Read Archive database (PRJNA491800). Raw FASTQ files in this study were qualityfiltered by Trimmomatic. Furthermore, FLASH software was used to merge raw FASTQ files according to Chen et al. (2018a). In this study, UPARSE (version 7.1) was used to cluster operational taxonomic units (OTUs) with 97% similarity cutoff. UCHIME was used to identify and remove chimeric sequences. With confidence threshold of 70%, RDP Classifier algorithm against the Silva (SSU123) 16S rRNA was used to analyze the taxonomy of 16S rRNA gene sequence (Zhong et al., 2017). In order to evaluate the complexity of different bacterial communities, QIME was performed to obtain a-diversity indices (observed species, Chao 1, Shannon and Simpson) using Mothur software. Principal coordinate analysis (PCoA) was also performed to display differences in bacterial community compositions among soils based on the unweighted UniFrac metric. 2.4. Statistical analysis

2.2. Determination of PBDEs In this study, the freeze-dried samples were firstly ground into powder, and then homogenized, and sieved by 0.5 mm stainless steel sieve. The sample preparation and extraction, as well as instrumental analysis were described previously (Pan et al., 2018; Chai et al., 2019). In brief, PBDEs in samples were extracted by an accelerated solvent extractor (ASE200) purchased from Dionex (USA), an EPA approved technique under Method 3545A. The measurement of PBDEs was conducted with a 6890 N gas chromatograph (Agilent Technologies, Avondale, PA, USA) equipped with an Agilent 5975 mass spectrometer (GC.MS). In this study, an HP-5 fused silica capillary column (15 m  0.25 mm i. d., 0.25 mm film thickness) was used to separate the eight PBDE congeners in this study. Ion fragments (m/z) 79 and 81 (Br) was monitored to quantify all PBDE congeners, and m/z 79, 81, 487 and 489 for BDE209 were monitored to quantify BDE-209. The surrogate stand PCB209, was quantified by monitoring m/z 464, 487 and 500. In this study, the mixed standard included BDE-28, -47, 99, 100, 154, 153, 183, and 209, and were purchased from AccuStandard (USA). The mean recoveries (n ¼ 3) for all PBDE congeners ranged from 83.5% to 113.6%. 2.3. Molecular analyses At 6 months of the experiment, soil samples from all treatments were collected for analyzing microbial community. In each little tank, three soil samples (0e5 cm depth) were collected randomly to from one composite sample, with 12 soil samples to be collected in all 12 little tanks totally. In this study, OMEGA-soil DNA Kit (Omega Bio-tek, U.S.A) was used to extract microbial DNA from soil samples. Then, the Illumina MiSeq analysis was conducted. The bacteria 16S rRNA gene were amplified with primers 515F (50 GTGCCAGCMGCCGCGG-30 ) and 806R (50 -GGACTACHVGGGTWTCTAAT-30 ) (Walters et al., 2016). The PCR reactions were carried out as follows: Firstly, 3 min denaturation with 95  C; Secondly, 27 cycles of 30 s with 95  C; Thirdly, 30s annealing with 55  C; Fourthly, 45s elongation with 72  C, and Finally, 10 min extension with 72  C. In this study, PCR reactions were conducted in 20 mL mixed solution: FastPfu Polymerase (0.4 mL), 5 mM each primer

In this study, all data were expressed as the mean value ± standard deviation of three replicates. For the data of BDE209 concentrations in soil and root, one-way ANOVA was used to test the significance of BDE-209 with experiment time. Student's ttest was performed to evaluate the significance of BDE-209 in roots between Ko þ B and Ko þ BP treatments. The microbiological data were analyzed on the free online platform of Majorbio I-Sanger Cloud Platform (www.i-sanger.com). One-way ANOVA was used to test the significance of a-diversity indices in sediment among different treatments at 6 months of the experiment. 3. Results 3.1. Residual BDE-209 in soil From 0 to 6 months, the concentrations of BDE-209 in soil reduced significantly with increasing treatment time (P < 0.05), except for NP þ B treatment (Fig. 1). From 6 to 9 months, no significant changes of concentrations of BDE-209 were detected with increasing treatment time (P > 0.05). At 6 months, the concentrations of BDE-209 in NP þ BP were lower than that in NP þ B treatment (P < 0.05), with lower BDE-209 in K. obovata planting treatments compared to unplanted treatments (P < 0.05). The lowest concentration of BDE-209 was detected in Ko þ BP treatment. In Table 1, total amounts of BDE-209 in soil were calculated based on BDE-209 concentrations and corresponding dry weights of soil. In all treatments, total amounts of BDE-209 in soils reduced with increasing treatment time, leading to increased removal percentages of BDE-209 in soils (Table 1). 3.2. BDE-209 in K. obovata root In Fig. 2, the concentrations of BDE-209 in K. obovata root increased significantly with increasing treatment time (P < 0.05); in Ko þ BP treatment, level of BDE-209 accumulated in K. obovata root was higher than that in NP þ BP treatment at 9 months (P < 0.01). In Table 1, total amounts of BDE-209 in root were calculated based on BDE-209 concentrations and corresponding dry weights of root biomass. The improved total amounts of BDE-209 in K. obovata root were detected in Ko þ B and Ko þ BP treatments, which rose up to

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Fig. 1. Concentrations of BDE-209 in soils with different treatments. NP þ B, unplanted with BDE-209; Ko þ B, K. obovata with BDE-209; NP þ BP, unplanted with BDE-209 and pyrene; Ko þ BP, K. obovata with BDE-209 and pyrene. At the same experiment time, different lowercase letters indicate significant differences among four treatments at P < 0.05. In the same treatment, different capital letters indicate significant differences during the whole experiment at P < 0.05.

Table 1 Total amounts of BDE-209 in soil (mg) and K. obovata root (mg) with different treatments. Soil (removal percentage, %)

Month Month Month Month

0 3 6 9

K. obovata root

NP þ B

Ko þ B

NP þ BP

Ko þ BP

Ko þ B

Ko þ BP

756.0 723.1 640.4 581.9

756.0 509.5 446.4 428.3

757.4 601.6 487.8 478.9

744.4 579.0 403.5 373.1

1.01 71.5 90.6 94.2

1.01 65.2 93.2 115.4

(0%) (4.3%) (15.3%) (23.0%)

(0%) (32.6%) (41.0%) (43.4%)

(0%) (20.6%) (35.6%) (36.8%)

(0%) (22.2%) (45.8%) (49.9%)

Total amounts of BDE-209 in soil/root were calculated based on BDE-209 concentrations and corresponding dry weights of soil and root biomass. Removal percentage (%)¼(initial spiked concentration of BDE-209 - residual concentration of BDE-209)/initial spiked concentration of BDE-209  100%. NP þ B, no planted with BDE-209; Ko þ B, K. obovata with BDE-209; NP þ BP, no planted with BDE-209 and pyrene; Ko þ BP, K. obovata with BDE-209 and pyrene.

In Ko þ BP or Ko þ B treatment, both concentration and percentage of BDE-100 and -154 in root were higher than that in soil, respectively (Fig. 3C and D). 3.4. Bacterial community diversities

Fig. 2. Concentrations of BDE-209 in K. obovata roots with different treatments. Ko þ B, K. obovata with BDE-209; Ko þ BP, K. obovata with BDE-209 and pyrene. In the same treatment, different capital letters indicate significant differences during the whole experiment at P < 0.05. At the same experiment time, ** indicate significant differences between Ko þ B and Ko þ BP treatments at P < 0.01 according to Student's t-test. ns, not significant.

94.2 and 115.4 mg at 9 months, respectively (Table 1).

3.3. Debromination of BDE-209 in soil and K. obovata root At 6 months, BDE-28, -47, 99, 100, 153, 154, and 183 were all detected in both soil and K. obovata root, with significantly lower concentrations than that of BDE-209 (Fig. 3A and B). The concentrations of total de-PBDEs in K. obovata root were higher than that in soil, regardless of Ko þ B or Ko þ BP treatment (Fig. 3C).

At 6 months, bacterial community diversity and composition in soil were analyzed by 16S rRNA Illumina sequencing. The basic information about the total 12 soil samples was as follows: domain 1, kingdom 1, phylum 45, class 125, order 277, family 493, genus 872, species 1529, OTU 5498. In Table 2, the observed species in Ko þ B treatment were significantly higher than that in NP þ B treatment (P < 0.05). Furthermore, significantly higher Chao1 and Shannon indices were detected in Ko þ B compared to Ko þ BP and NP þ B treatments (P < 0.05). 3.5. Bacterial community structure In Fig. 4, UniFrac-based PCoA revealed that pyrene addition changed bacterial community structures between Ko þ B and Ko þ BP treatments, with no separation between NP þ B and NP þ BP along PC1 (30.09% of the variance) and PC2 (14.17% of the variance), respectively. K. obovata planting significantly affected bacterial community structures, which was verified by separation between NP þ B and Ko þ B treatments, as well as NP þ BP and Ko þ BP treatments. Fig. 5 showed bacterial abundances at phylum, class and genus among different treatments. As for improved BDE-209 dissipation, bacterial abundance at phylum Planctomycetes, Chloroflexi, class Plactomycetacia, and genus Blastopirellula in NP þ BP treatment

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Fig. 3. Concentrations and percentages of BDE congeners with (A and B) and without BDE-209 (C and D) in soils and K. obovata roots at 6 months of the experiment. Ko þ B, K. obovata with BDE-209; Ko þ BP, K. obovata with BDE-209 and pyrene.

Table 2 Microbial-a-diversity indices in sediments at 6 months of the experiment. Treatments

Observed species

Chao 1

Shannon

Simpson

NP þ B Ko þ B NP þ BP Ko þ BP

994 ± 13b 1048 ± 21a 962 ± 14b 1017 ± 55 ab

1270 ± 26b 1357 ± 13a 1214 ± 12b 1213 ± 52b

5.16 ± 0.10b 5.36 ± 0.04a 5.12 ± 0.03b 5.07 ± 0.01b

0.019 ± 0.003a 0.019 ± 0.002a 0.019 ± 0.002a 0.016 ± 0.001a

NP þ B, no planted with BDE-209; Ko þ B, K. obovata with BDE-209; NP þ BP, no planted with BDE-209 and pyrene; Ko þ BP, K. obovata with BDE-209 and pyrene. For each index, different lowercase indicates significant differences with different treatments at P < 0.05 according to one-way ANOVA.

were higher than that in NP þ B treatment. Bacterial abundance at phylum Proteobacteria, class Gammaproteobacteria, and genus Ilumatobacter and Gaiella in Ko þ B and Ko þ BP were higher than that in NP þ B and NP þ BP treatments, respectively. 4. Discussion

Fig. 4. Principal co-ordinates analysis showing the differences in bacterial community in NP þ B, Ko þ B, NP þ BP and Ko þ BP treatments at 6 months of the experiment. NP þ B, unplanted with BDE-209; Ko þ B, K. obovata with BDE-209; NP þ BP, unplanted with BDE-209 and pyrene; Ko þ BP, K. obovata with BDE-209 and pyrene.

4.1. Removal of BDE-209 in soil Generally, debromination of PBDEs under anaerobic conditions is a slow process due to their long LD50 (Tokarz et al., 2008b; Shih et al., 2012; Zhu et al., 2014a). Plant uptake and PBDEs biodegradation in rhizosphere are two important processes in controlling fate of PBDEs in soil (Zhu et al., 2014b; Chen et al., 2017). Planting of xerophytes and aquatic plant species could improve BDE-209 removal in soil (He et al., 2015, He and Chi, 2016). In this study, BDE-209 removal in NP þ B and Ko þ B treatments rose up to 15.3% and 41.0% at 6 months, higher than previous report about BDE-209

removal (about 5% after 7 months) in mangrove soils (5 mg g1 BDE-209) with mangrove planting, regardless of K. obovate and Avicennia mamrina (Zhu et al., 2014b). This indicated that BDE-209 adapted process in this study might improve the capacity of microbial debromination on soil BDE-209, being consisted with anaerobic debromination of PBDEs in river sediment (Huang et al., 2014). K. obovata planting improved BDE-209 removal in soil after 6 months, which coexisted with increasing BDE-209 accumulation in K. obovata root (Figs. 1 and 2). Thus, K. obovata planting was useful

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Fig. 5. Taxonomic distributions at phylum (A) and class (B) levels, as well as heat map showing differences in relative abundances of genera (C) in the soils at 6 months of the experiment. In Fig. C, the colors represent the changes of relative abundance according to the color-coded column on the down right of figure. The top 10 phyla, 19 class, and 20 genera were indicated. NP þ B, unplanted with BDE-209; Ko þ B, K. obovata with BDE-209; NP þ BP, unplanted with BDE-209 and pyrene; Ko þ BP, K. obovata with BDE-209 and pyrene. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)

in phytoremediation application for BDE-209 contamination remediation. The underlying mechanism may be related to that root could secret various small molecular organic acids into surrounding environment (Wang et al., 2014c; Jiang et al., 2017), change the rhizosphere microenvironment and microbial activity, and affect the biodegradation of BDE-209. Based on the total amount of BDE-209 accumulated in soil, the function of plant uptake might be limited because the total amount of BDE-209 removal due to accumulation in root was lower than 1% of BDE209 in soil (Table 1), which was in accordance with the results of Zhu et al. (2014b) and Chen et al. (2017). In this study, pyrene addition improved BDE-209 degradation in soil after 6 months regardless of K. obovata planting or not. Up to now, there has been no reasonable explanation for the impact of pyrene addition on BDE-209 dissipation in mangrove soil. The degradation of BDE-209 could be promoted after moderate addition of carbon sources, such as phenol, toluene and biphenyl (Lu et al., 2013). Thus, we suggested that the improved function of pyrene addition on BDE-209 degradation in soil might be similar to that of alternative carbon sources, with co-metabolism for many persistent and toxic pollutants (Gu, 2016). The suggestion could be, at least partly, verified by the loss of pyrene with increasing BDE-209 removal in soil (Fig. S1). The degradation of PAHs was relatively easier in the environment compared to PBDEs, and could be improved by various soil amendments, including biochar, gravel sludge, and iron oxides (Wawra et al., 2018). BDE-209 could be transformed into lower brominated PBDEs, and then be degraded by microbes in soil (Tokarz et al., 2008a,b; Liu et al., 2011). In this study, lower brominated BDE congeners were detected in soil and K. obovata root at 6 months (Fig. 3), suggesting metabolic debromination of BDE-209 in the root-soil system. The

total concentration of debrominated BDE congeners was higher in root than that in soil, similar to results obtained by Deng et al. (2016) who found higher PBDEs uptake in roots of seven aquatic plant species. In the same treatment, the concentrations of BDE100, and -154 in roots were higher than that in the soils, implying that they might be adsorbed by K. obovata root and/or further metabolic debromination of PBDEs probably take place in the plants (Huang et al., 2010). On the other hand, pyrene addition improved concentrations of BDE-100 and -154 in root, indicating that pyrene might improve debromination of BDE-209 in K. obovata root, or improve the uptake of low brominated PBDEs degraded by bacteria in the rhizosphere. BDE-209 mainly accumulated in roots, with less to be transferred up to the aboveground parts (Chen et al., 2015; Deng et al., 2016). In this study, BDE-209 removal in soil could not completely explained by root uptake of BDE-209 and its’ debromination in K. obovata root, because BDE-209 removal in soil was higher than the sum of root uptake of BDE-209 and the total debromination BDE in root (Table 1). In this study, the roles of biotic and abiotic factors were not separated, and the abiotic losses caused by photodegradation, volatilization, as well as leaching might be non-ignorable, which needs more evidence to verify. 4.2. Dynamics of microbial communities The mutual influences of potentially toxic organic pollutants on soil remediation mainly included changing biomass of soil biota, altering the structure and composition of biological cells, and transforming the production and activities of secretion (Ye et al., 2017). In this study, the diversity and composition of soil microbial community of experiment were explored at 6 months, when the dissipation of BDE-209 was relatively stable during the whole

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experiment. Previous studies have shown that debromination of PBDEs is important in affecting microbial community structure in soil, with higher brominated BDE congeners to be more pronounced in affecting microbial community structure compared to lower brominated BDE congeners (Ma et al., 2016; Zhao et al., 2018). Planting could change the structure and composition of bacterial community and improve microbial degradation on various organic contaminants (such as PCB, PAH and PBDEs, etc.), compared to the non-degradable heavy metals (Li et al., 2011; Passatore et al., 2014; Chen et al., 2017). In this study, K. obovata planting significantly affected microbial communities in BDE-209 contaminated soil without pyrene addition, which could be verified by higher observed species, Chao 1 and Shannon, as well as different bacterial community structures (Table 1, Fig. 4A). Furthermore, K. obovata planting changed bacterial abundance at phylum Proteobacteria, class Gammaproteobacteria and genus illumatobacter, Gaiella, indicating their importance in dissipation process of BDE-209 (Fig. 5). Generally, the abundant genes for biodegradation made Proteobacteria to be potential in removing POPs, such as perfluorooctanoic acid, creosote, and BDE-153, (Fang et al., 2014; Sun et al., 2016; Pan et al., 2018). In Figs. 1 and 5, pyrene addition improved BDE-209 removal in soil without K. obovata planting, which coexisted with increasing bacterial abundance at phylum Planctomycetes, Chloroflexi, class Planctomycetacia, and genus Blastopirellula, demonstrating different pressure on bacterial communities. Generally, many bacterial species at phylum Chloroflex were involved in biodegradation of organic pollutants (Maphosa et al., 2010; Chen et al., 2018b). Chen et al. (2017) reported pressure on soil bacterial of phylum Chloroflex in BDE-47 contaminated soil (Chen et al., 2017). Nevertheless, our results were at odds with previous studies that some important functional groups for reductive dehalogenation were not detected, such as genera Dehalobacter, Dehalococcides, Dehalogenimonas, Desulfitobacterium, Geobacter and Sulfurospirillum (Zanaroli et al., 2015; Chen et al., 2018c), which may be due to the different biogeochemical conditions in soil-water system, such as particulates, redox reactions and bioturbation (Middelburg and Levin, 2009; Chan et al., 2014). Generally, the life strategies or ecological traits of bacterial from one taxon were different from the other taxa (Philippot et al., 2010). Higher bacterial taxa may not share similar ecological coherence which is up to the ecological question and the level of taxonomic rank. Furthermore, in the same taxon, it is also hard to rely the phylogenetic identities and microbe abundance to their activities and ecological roles based on the diverse physiologies of microorganisms (Chan et al., 2014). In this study, the changes of microbial community composition and structure provided insights into the ecological implications of pyrene addition and K. obovata planting on removal of BDE-209 according to functional changes of microbial communities. Though similar promoting functions of pyrene addition or K. obovata planting were detected in removal of BDE209 in soil, the corresponding responses of microbial communities were different at phylum, class and genus levels, deserving further investigation. 5. Conclusion The effects of pyrene addition and K. obovata planting on removal of BDE-209 in mangrove soil are explored through 9 months-lasting experiment. After 6 months, BDE-209 removals caused by pyrene addition or K. obovata planting were significant and stable, with the highest removal of BDE-209 to be detected in pyrene treatment with K. obovata planting. Plant uptake and debromination of BDE-209 in K. obovata root were limited in

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affecting removal of BDE-209 in mangrove soil. In soil without K. obovata planting, pyrene-induced BDE-209 removal coexisted with improved bacterial abundance at phylum Planctomycetes, Chloroflexi, class Planctomycetacia, and genus Blastopirellula. BDE209 removal caused by K. obovata planting may be related with bacterial enrichment at phylum Proteobacteria, class Gammaproteobacteria and genus Ilumatobacter, Gaiella. Thus, both pyrene addition and K. obovata planting could improve removal of BDE209 in soil. Bacterial community responses caused by pyrene addition and K. obovata planting were different, regardless of phylum, class or genus levels. More research about functional change of bacterial community at genetic level should be conducted to explore the microbial ecology for field bioremediation. Acknowledgements This work was financially supported by the Program of Science and Technology of Shenzhen (JSGG20170413103811649, JCYJ20170818090224745), the Program of Marine Science and Technology of Guangdong Province (Study on ecological investigation and protection patterns of typical coastal Mangroves in Guangdong Province), Special fund of State Key Joint Laboratory of Environment Simulation and Pollution Control(18K05ESPCP), and Shenzhen Municipal Development and Reform Commission (Discipline construction of watershed ecological engineering). Ruili Li is responsible for the operation of this research and writing this article. Huan Ding, Meixian Guo, Xiaoxue Shen and Qijie Zan provide a lot of help in operation of this research. Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi.org/10.1016/j.chemosphere.2019.124873. References Babalola, B.A., Adeyi, A.A., 2018. Levels, dietary intake and risk of polybrominated diphenyl ethers (PBDEs) in foods commonly consumed in Nigeria. Food Chem. 265, 78e84. Bayen, S., 2012. Occurrence, bioavailability and toxic effects of trace metals and organic contaminants in mangrove ecosystems: a review. Environ. Int. 48, 84e101. Bodin, N., N'Gom Ka, R., Le Loc'h, F., Raffray, J., Budzinski, H., Peluhet, L., Tito de Morais, L., 2011. Are exploited mangrove molluscs exposed to persistent organic pollutant contamination in Senegal, west Africa? Chemosphere 84, 318e327. Chai, M.W., Li, R.L., Shi, C., Shen, X.X., Li, R.Y., Zan, Q.J., 2019. Contamination of polybrominated diphenyl ethers (PBDEs) in urban mangroves of Southern China. Sci. Total Environ. 646, 390e399. Chan, Y.K., Li, A., Gopalakrishnan, S., Shin, P.K.S., Wu, R.S.S., Pointing, S.B., Chiu, J.M.Y., 2014. Interactive effects of hypoxia and polybrominated diphenyl ethers (PBDEs) on microbial community assembly in surface marine sediments. Mar. Pollut. Bull. 85, 400e409. Chen, J., Zhou, H.C., Wang, C., Zhu, C.Q., Tam, N.F.Y., 2015. 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, 84e92. Chen, J., Wang, C., Shen, Z.J., Gao, G.F., Zheng, H.L., 2017. Insight into the long-term effect of mangrove species on removal of polybrominated diphenyl ethers (PBDEs) from BDE-47 contaminated sediments. Sci. Total Environ. 575, 390e399. Chen, Y.J., Wu, H., Wu, S.D., Lu, N., Wang, Y.T., Liu, H.N., Dong, L., Liu, T.T., Shen, X.Z., 2018a. Parasutterella, in association with irritable bowel syndrome and intestinal chronic inflammation. J. Gastroenterol. Hepatol. 33, 1844e1852. Chen, J., Wang, C., Pan, Y., Farzana, S.S., Tam, N.F.Y., 2018b. Biochar accelerates microbial reductive debromination of 2,2’,4,4’-tetrabromodiphenyl ether (BDE-47) in anaerobic mangrove sediments. J. Hazard Mater. 341, 177e186. Chen, J., Wang, P.F., Wang, C., Liu, J.J., Gao, H., Wang, X., 2018c. Spatial distribution and diversity of organohalide-respiring bacteria and their relationships with polybrominated diphenyl ether concentration in Taihu Lake sediments. Environ. Pollut. 232, 200e211. Chen, Y.Y., Chen, Y.J., Zhang, Y.H., Li, R.J., Chen, W., Yan, S.C., Qi, Z.H., Chen, Z.F., Cai, Z.W., 2019. Determination of HFRs and OPFRs in PM2.5 by ultrasonicassisted extraction combined with multi-segment column purification and GC-MS/MS. Talanta 194, 320e328.

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