Science of the Total Environment 613–614 (2018) 644–652
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Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv
Changes in microbial community during removal of BDE-153 in four types of aquatic sediments Ying Pan a,b, Juan Chen c, Haichao Zhou b,d,e, Nora F.Y. Tam a,b,⁎ a
Department of Chemistry, City University of Hong Kong, Tat Chee Avenue, Kowloon, Hong Kong, China State Key Laboratory in Marine Pollution, City University of Hong Kong, Tat Chee Avenue, Kowloon, Hong Kong, China Key Laboratory of Integrated Regulation and Resource Department on Shallow Lakes, Ministry of Education, College of Environment, Hohai University, Xikang Road, Nanjing 210098, China d Futian-CityU Mangrove R&D Centre, City University of Hong Kong, Tat Chee Avenue, Kowloon, Hong Kong, China e College of Life Sciences and Oceanography, Shenzhen University, Nanhai Avenue, 518060, China b c
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
• Phylum Proteobacteria correlated with BDE-153 removal rates in aquatic sediments • BDE-153 did not change sediment microbial α-diversity within 150 days. • BDE-153 altered microbial composition in saline but not freshwater sediments. • BDE-52 exerted a significant effect on the microbial community composition. • Salinity also affected the microbial composition, irrespective of PBDE pollution.
a r t i c l e
i n f o
Article history: Received 2 August 2017 Received in revised form 13 September 2017 Accepted 13 September 2017 Available online xxxx Editor: Jay Gan Keywords: PBDEs Microbial community Anaerobic removal Aquatic sediment
a b s t r a c t Indigenous microorganisms in sediments could degrade polybrominated diphenyl ethers (PBDEs), but how the microbial communities respond to PBDEs was seldom reported. The effect of BDE-153, a common congener in aquatic environments, on the microbial communities in four types of aquatic sediments was evaluated during the 150 days' incubation under an anaerobic condition. The intrinsic potential to remove BDE-153 varied significantly among four sediment types, and the removal rates of mangrove, mudflat, marine and freshwater sediments were 0.013, 0.013, 0.011, and 0.009 day−1, respectively. The observed microbial species, Simpson, Shannon, and Chao1 indices in all sediments were rather stable and were not changed significantly by BDE153 amendment. However, BDE-153 amendment altered the microbial community compositions in three saline sediments at the end of the incubation period. Distance-based multivariate multiple regression analysis revealed that salinity, total organic carbon (TOC) and BDE-52, the major debromination product of BDE-153, were the three main factors explaining the variations in microbial community compositions in BDE-treated sediments; whereas salinity, TOC and pH were the main contributing factors in control sediments without BDE-153. The daughter congeners generated during anaerobic debromination process need more attention, especially their effect on the microbial communities in aquatic sediments. © 2017 Elsevier B.V. All rights reserved.
1. Introduction ⁎ Corresponding author at: Department of Chemistry, City University of Hong Kong, Tat Chee Avenue, Kowloon, Hong Kong, China. E-mail address:
[email protected] (N.F.Y. Tam).
http://dx.doi.org/10.1016/j.scitotenv.2017.09.130 0048-9697/© 2017 Elsevier B.V. All rights reserved.
Polybrominated diphenyl ethers (PBDEs) are commonly used brominated flame retardants, which have been extensively applied as
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the coating material on plastics, textiles, and building materials over the past few decades. Due to their highly lipophilic and hydrophobic properties, PBDEs are likely to accumulate in the organic portion of sediments, resulting in very high sediment concentrations, especially in aquatic areas, which can be their final sink in the environment (Voorspoels et al., 2004; Cui et al., 2013). However, this sink could become the source of secondary pollution and affected aquatic organisms such as fish and shellfish, which then transferred PBDEs to the organisms at higher trophic levels through food intake, leading to the bioaccumulation and biomagnification of PBDEs in a food web (Sun et al., 2015). Mangrove, mudflat, open sea, and freshwater pond are typical ecosystems in aquatic environments, and each has unique physico-chemical properties and microbial community structure in its sediment. Mangrove and mudflat are two important habitats in intertidal zones and receive regular tidal flushing, leading to periodic alternations of anaerobic and aerobic conditions and fluctuating salinities in sediments (Tam, 1998). Unique groups of plants colonize in a mangrove ecosystem, whereas mudflat in front of the seaward fringe of a mangrove ecosystem does not have any vegetation. The freshwater pond sediment and the marine sediment from an open sea are always under water, forming a permanent anaerobic condition. Some hydrophytes are found in the freshwater pond but relatively fewer plants grow in the bottom of an open sea (Gee et al., 1997). These four sediments have different salinities, pH, and other physico-chemical properties, which not only affect the adsorption and desorption processes of organic contaminants in sediments, but also control the natural attenuation and the fate of contaminants in the environment (You et al., 2010). The microbial community structures in the four types of sediments also differ from each other. Wang et al. (2012) found that freshwater sediment had the highest microbial diversity, whereas intertidal and marine sediments had moderate and lowest values, respectively. The bacterial community in freshwater sediment was dominated by Actinobacteria, Verrucomicrobia, and Cytophaga-FlavobacteriumBacteroides groups (Hahn, 2006). Syntrophic bacteria and fermenters dominated mudflat sediment and correlated well with the types and amounts of carbon sources in the environment (Wilms et al., 2006). Thatoi et al. (2013) reported that mangrove sediment had a unique microbial diversity, and the common groups were sulfate-reducing, nitrogen-fixing, phosphate-solubilizing, anoxygenic photosynthetic, and methanogenetic microorganisms. Compared with the other three types of sediments, marine sediment comprised more anaerobic chemoautotrophs and heterotrophs, and had a higher proportion of sulfate reducers (Zinger et al., 2011). The sediment harboring diverse groups of microorganisms has a potential to remove PBDEs, and changes in microbial community during the removal could reflect the impact of PBDEs on the sediment (Zinger et al., 2011; Zanaroli et al., 2015). The potential of individual sediment to remove PBDEs has been demonstrated, but it is difficult to make direct comparisons among different studies because of different experimental setups or relate the removal potentials to their microbial community compositions (Liu et al., 2011; Wang et al., 2014; Chen et al., 2015; Song et al., 2015). Some of these studies reported the changes in the microbial community structure under PBDE pollution, but they mainly focused on soil or river sediment. Less attention has been paid to other types of aquatic sediments with different properties, such as salinities, pH, total organic carbon (TOC) content, etc. The present study compared the microbial response to BDE-153 amendments on four types of aquatic sediments, aiming to understand the important factors affecting the microbial community compositions in PBDE-treated sediments. The study also attempts to identify the potential functional microbial groups involved in the removal of BDE-153. BDE-153 was chosen as the model PBDE congener because it was commonly and frequently detected in aquatic sediments, especially in mangrove wetlands, human bodies, and breast milk (Zhang et al., 2013; Zhu et al., 2014). This congener was also less studied when compared to the other PBDE congeners such as BDE-47, -99, and -209 (Wang et al., 2014; Chen et al., 2015; Pan et al., 2016).
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2. Materials and methods 2.1. Collection and analysis of physico-chemical properties of sediments Freshwater, mangrove, and mudflat sediments were sampled from Mai Po Nature Reserve, Hong Kong, which usually receives various pollutants from human activities. Marine sediment was collected from an open sea, which is farther away from coastlines and anthropogenic contamination. The temperature, pH, redox potential (Eh), and salinity of the sediment were measured in situ, using a thermometer, a pH meter (E.W. System Soil tester, Japan), an Eh meter (TPS WP-81, Australia), and a refractometer (Atago S-10, Japan), respectively. Particle size distribution (from 0.02 to 2800 μm) of the sediment was determined using the Microtrac S3500 particle size analyzer (Microtrac, USA). Water content was measured by the weight loss of the sediment after drying at 105 °C. Total organic carbon (TOC) was determined after oxidation by potassium dichromate (K2Cr2O7) according to the standard procedure described by Chen et al. (2016). Ammonium (NH+ 4 ) and nitrate (NO− 3 ) were extracted into 2 M potassium chloride (KCl) and determined by the Flow Injection Analyzer (FIA) (Lachat QuikChem Method 8000, USA). Sulfate (SO24 −) was extracted with deionized water and measured by ion chromatography (IC) (Dionex Ion Chromatograph Model LC20, Dionex Corp.). The background physicochemical properties of sediments are summarized in Table S1. 2.2. Anaerobic removal potential of BDE-153 A microcosm experiment under an anaerobic condition was conducted using 250 mL quick-fit conical flasks, each containing 100 g fresh sediment and 100 mL sterilized mineral salt medium (MSM). The medium consisted of the following chemicals (in g L−1): K2HPO4, 0.27; KH2PO4 0.35; NH4Cl, 2.7; MgCl2·6H2O, 0.1; CaCl2·2H2O, 0.1; FeCl2·4H2O, 0.009; MnCl2·4H2O, 0.004; ZnCl2, 0.0014; CoCl4·6H2O, 0.001, and (NH4)6 Mo7O24·4H2O, 0.001 (Zhu et al., 2014). MSM was used in the present study to provide the essential inorganic nutrients for the growth of microorganisms during the entire experiment. This common medium is widely used in many microcosm experiments related to the removal of PCBs, PAHs, BDE-47, -209 and other organic pollutants (Li et al., 2009; Zhu et al., 2014; Pan et al., 2016). The relatively low levels of N and P were unlikely to alter the cell numbers of microorganisms in sediments (Swindoll et al., 1988). The pH of MSM for each type of sediment was adjusted to 7.2 while the salinity was adjusted to the same value as in its respective natural environment. For each type of sediment, nine flasks were divided into three treatments, each in triplicate. The treatments were (i) BDE-treatment: 50 μg BDE-153 was spiked into the sediment slurry; (ii) Sterilized control: the sediment was autoclaved at 121 °C for 1 h on three consecutive days, the same amount of BDE-153 as (i) was then spiked into the sediment and sodium azide was added to the slurry to a concentration of 200 mg L−1 to inhibit microbial activity, and (iii) Acetone control: the sediment slurry was spiked with the same volume of acetone as (i) but without BDE-153. This spiking concentration (50 μg BDE-153 to 100 g fresh sediment) was selected to simulate the contamination level in one watershed in Shenzhen, adjacent to Hong Kong (Sun et al., 2013), where the concentration of BDE-153 reached 1.647 μg g− 1 dry sediment. For each flask, headspace was repeatedly vacuumed and refilled with high purity nitrogen gas (N2) for three times in a Bactron anaerobic chamber (Sheldon Manufacturing, USA) before sealed with silicone suba-seal septa (Sigma-Aldrich). All flasks were shaken at 150 rounds per minute (rpm) at 25 °C in the dark for 150 days. Five milliliter sediment slurries from the BDE-treatment and the sterilized control were collected on days 0, 15, 60, 90, 120, and 150, and freeze-dried for PBDE analysis. The nominal concentrations of BDE-153 in freshwater, mangrove, mudflat, and marine sediments at the beginning of the experiment were 1038.1, 1182.3, 1017.7, and 941.8 ng g−1, respectively, while the respective measured values were 1127.6 ± 24.2, 1380.7 ± 34.9, 1125.9 ± 9.2,
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and 885.3 ± 7.8 ng g−1 (mean and standard deviation of three replicates), due to their differences in water contents. In spite of the difference, the same weight of fresh sediment, MSM medium and same amount of BDE-153 were used to simulate the situation that the four types of sediments encountered the same contamination input. On days 0, 60, and 150, additional 5 mL sediment slurries were collected from the BDE-treatment and the acetone control for DNA extrac− 2− tion and the measurement of pH, TOC, NH+ 4 , NO3 and SO4 as described above. Since the microbial community and physico-chemical properties of BDE-treated and control sediments were the same on day 0, only BDE-treated sediments were measured, while both BDE-treated and control sediments were measured on days 60 and 150. A total of 60 samples were collected based on this sampling design. 2.3. PBDE analysis Extraction, purification and analysis of PBDEs were carried out according to Zhu et al. (2014). In brief, 0.3 g freeze-dried sediments were extracted by n-hexane using an accelerated solvent extractor (ASE-200, Dionex, USA). Before the extraction, decachlorobiphenyl (PCB-209) purchased from AccuStandard (USA) was added as a surrogate internal standard. The extract was purified by a silica-gel column and concentrated to accurate 1 mL under a gentle stream of nitrogen. The analysis of PBDEs was performed on an Agilent 6890 gas chromatography-negative chemical ionization mass spectrometry (5975, Agilent Technologies) equipped with a 30-m HP-5 fused silica capillary column (0.25 mm i.d. × 0.25 μm), using the selected ionmonitoring (SIM) mode. A mixture standard containing 39 PBDE congeners and standards of individual congener, BDE-101 and -52 (all purchased from AccuStandard, USA), were used to identify and quantify BDE-153 and its major debromination products with available standards, including BDE-101, -99, -52, -49, and -47. BDE-28 and -15 were not detected during the entire experiment. The recoveries of these PBDE congeners in sediments ranged from 85.6 to 95.3%. The reported concentrations were not corrected by the recovery rate. 2.4. DNA extraction, DNA sequencing and data processing Total DNA from 60 sediment samples (each had 0.5 g fresh weight) was extracted using the FastDNA SPIN kit for Soil (MP Biomedicals, USA) according to the manufacturer's protocol. The extracted DNA was sent to Groken Bioscience Limited (Hong Kong, China) for 16S rRNA gene amplification, library construction, and sequencing. The 515f/806r primer pair was used to amplify the V4 hypervariable region of the 16S rRNA gene and triplicate amplifications were pooled for each sample as described previously (Jia et al., 2016). Illumina adapters were attached to amplicons to construct sequencing library before purification and applied for sequencing on Illumina HiSeq2500 platform to generate paired-end 250 bp sequences. The sequences have been deposited at the Sequence Read Archive of the National Center for Biotechnology Information under the project PRJNA390696. The sequences were processed and analyzed using the Quantitative Insights into Microbial Ecology (QIIME) 1.9.1 pipeline. In brief, sequences were quality trimmed (N25 quality score and 200 bp in length) and assigned to each sample based on unique 5-bp barcodes. The resulting high quality sequences were de-noised and then binned into Operational Taxonomic units (OTUs) using a 97% identity threshold. Representative sequences of OTUs were aligned using PyNAST and the taxonomy was assigned to bacterial/archaeal OTUs against the Greengenes database. All the OTUs were used to characterize the microbial community of each sample. For alpha- and beta-diversity analyses, samples were normalized at a depth of 29,311, the minimum number of sequences across all samples. Four alpha-diversity indices, observed species, Simpson, Shannon, and Chao1, were calculated based on the average of 10 repeated measurements.
2.5. Statistical analyses The differences in physico-chemical properties, PBDE concentrations, removal rates of BDE-153, relative abundances of dominant lineages and alpha-diversity indices (observed species, Simpson, Shannon, and Chao1) among the four types of sediments were evaluated by a parametric one-way analysis of variance (ANOVA). An independent sample t-test was used to compare differences in physico-chemical properties and alpha-diversity indices (observed species, Simpson, Shannon, and Chao1) between BDE-treated sediments and their corresponding controls without PBDEs. The correlations between BDE-153 removal rates and relative abundances of dominant lineages in fresh sediments (background values) collected from different sites were determined by Pearson's correlation analysis. These statistical analyses were done using SPSS Version 11.5 (USA). Analyses related to microbial communities were performed in Primer 6 (Primer-E, Plymouth, United Kingdom) with the PERMANOVA+ add-on package. Principal coordinate analysis (PCoA) based on Bray-Curtis similarity matrix of all 60 samples was plotted to show the changes in microbial community compositions during the experiment. Permutational multivariate analyses of variance (PERMANOVA) were carried out to test the differences in community compositions among the four types of sediments. PERMANOVA was also used to explore the difference in the microbial community compositions between BDE-treatment and its corresponding control in each type of sediment. Statistical significance (P value) was obtained based on 999 possible permutations. The correlations between environmental variables and microbial community compositions were assessed by Mantel test. The distance-based multivariate multiple regression analysis (DISTLM) was performed to explore the influence of nine sediment physico-chemical parameters (including salinity, TOC, pH, NH+ 4 , 2− NO− 3 , SO4 , % sand, % silt, and % clay) and six PBDE congeners (including BDE-153, 101, -99, -52, -49, and -47) on the microbial communities in the four types of BDE-treated sediments. For control sediments, only nine sediment physico-chemical parameters were used since no PBDE was added. The factors most closely related to the community data were identified through DISTLM analysis using the stepwise variable selection procedure and corrected akaike information criterion (AICc). Distance-based redundancy analysis (dbRDA) was used to visualize the results of the stepwise DISTLM. 3. Results 3.1. Intrinsic anaerobic removal potential of BDE-153 There were no significant changes in BDE-153 concentrations in sterilized controls of the four types of sediments, but significant decreases were found in sediments with live microorganisms (Fig. 1). The extent and rate of BDE-153 removal varied among sediment types. At the end of the 150 days' experiment, mangrove and mudflat sediments showed higher potentials to remove BDE-153 than marine and freshwater sediments, and their respective removal percentages were 77.1, 76.2, 66.2, and 62.3% (Fig. 1, Table S2). The removal kinetics of BDE-153 in the four types of sediments were all best fitted by the first-order rate model, with regression coefficients (R2) larger than 0.92 (Table S2). Mangrove and mudflat sediments had comparable removal rates (0.013 day−1) and were significantly higher than that of marine and freshwater sediments. Similarly, the half-lives of the former two sediments were also shorter (Table S2). BDE-153 spiked into sediments was gradually debrominated to less brominated congeners, with a significant accumulation of penta-BDE congeners (BDE-101 and -99) and tetra-BDE congeners (BDE-52, -49, and -47), and the penta-ones were more dominant after 60 days of the experiment (Table 1). However, more tetra-BDEs than penta-BDEs were accumulated on day 150, indicating that penta-BDEs could be further debrominated as the experiment proceeded. The concentrations of debromination products were different among the four types of
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Fig. 1. Removal curves of BDE-153 in four types of sediments during the 150 days' experiment (% = concentration of BDE-153/initial concentration × 100%; mean and standard deviation of triplicates are shown).
sediments. For instance, the concentrations of BDE-52 in mangrove and mudflat sediments were significantly higher than those in other sediments on days 60 and 150 (Table 1). No debromination products were detected in sterilized controls of all sediments during the 150 days' experiment, indicating that debromination was only carried out by indigenous live microorganisms in sediments. 3.2. Microbial community compositions and their relationships with BDE153 removal rates A total of 5,755,450 sequences of V4 region were generated from the 60 sediment samples, ranging from 31,194 to 190,178 sequences per sample (Table 2). After quality filtering, de-noising and removal of chimeric sequences, the remained 5,365,254 high quality sequences were clustered into 60,081 OTUs based on 97% identity cutoff, with 6897–18,599 OTUs for each sample. All the OTUs were affiliated to 79 phyla, 202 classes, and 598 genera of known bacteria and archaea across all samples. Proteobacteria, Firmicutes, Chloroflexi, and Actinobacteria were the top four dominant phyla in all samples, accounting for over 80% of all sequences, while Euryarchea, an archaeal phylum, was the fifth dominant one, accounting for 4.82% (Fig. 2). This archaeal phylum, when compared
with its proportion in initial fresh sediments (background values), was enriched in both BDE-treatment and control under an anaerobic condition during the 150 days' experiment. At the beginning of the experiment, the relative abundances of phyla Euryarchaeota, Acidobacteria, Planctomycetes, and TM7 were comparable among the four types of aquatic sediments (Fig. 2). By contrast, the more saline sediments, including marine, mudflat and mangrove sediments, harbored more Proteobacteria than the freshwater sediment. The removal rates of BDE-153 positively correlated with the relative abundances of phylum Proteobacteria in the four types of sediments at the beginning of the experiment according to Pearson's correlation analysis (R = 0.55, P b 0.05). At the genus level, the top 20 genera made up over 80% of all the known genera detected in the four types of fresh sediments. Bacteria from genus Acinetobacter were predominant in microbial communities of mangrove and mudflat sediments, whereas the most dominant genera in freshwater and marine sediments were Desulfosporosinus and Marinobacter, respectively (Fig. S1). The removal rates of BDE-153 positively correlated with the relative abundances of five genera among the top 20 genera, that is, Acinetobacter, Sulfurimonas, Pseudomonas, Psychromonas, and Pelobacter, with R values of 0.59, 0.87, 0.52, 0.70, and 0.70, respectively (all P b 0.05).
Table 1 Concentrations of residual BDE-153 and debromination products (BDE-101, -99, -52, -49, and -47) in ng g−1 dw, in four types of sediments amended with BDE-153 on days 60 and 150 (mean and standard deviation of triplicates are shown; at the same sampling time, values of each PBDE congener with different letters indicate significant differences among sediment types at P ≤ 0.05 according to one-way ANOVA; ND: not detected). Time
Sediments
BDE-47
BDE-52
BDE-49
BDE-99
BDE-101
BDE-153
Day60
Freshwater Mudflat Marine Mangrove Freshwater Mudflat Marine Mangrove
12.6 ± 0.8a 10.8 ± 1.8a 9.6 ± 1.5a 14.9 ± 4.1a 13.4 ± 0.7c 9.7 ± 0.4b 6.7 ± 0.3a 8.7 ± 0.3b
18.6 ± 3.8a 76.5 ± 3.5c 48.1 ± 5.7b 71.9 ± 5.1c 14.4 ± 1.2a 376.2 ± 21.2c 202.6 ± 18.8b 380.7 ± 6.9c
1.8 ± 0.8a 1.1 ± 0.3a ND 0.9 ± 0.3a 5.9 ± 0.6a 6.6 ± 0.3a 15.4 ± 1.2c 12.3 ± 1.4b
12.9 ± 0.9b 10.3 ± 1.2ab 8.9 ± 0.7a 12.2 ± 1.7ab 8.8 ± 0.3c 4.6 ± 0.1a 6.1 ± 0.4b 5.2 ± 0.3a
98.7 ± 7.9a 247.9 ± 11.7c 190.5 ± 20.3b 251.4 ± 10.4c 104.4 ± 3.9a 145.3 ± 5.2b 194.2 ± 13.5c 203.3 ± 13.2c
568.6 ± 48.6b 474.4 ± 16.2b 359.5 ± 35.8a 535.4 ± 21.2b 424.9 ± 14.7c 267.6 ± 4.8a 298.9 ± 13.1ab 315.5 ± 23.5b
Day150
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Table 2 Summary of 16S rRNA Illumina HiSeq sequences, operational taxonomic units (OTUs) and microbial α-diversity indices in four types of sediments. Microbial α-diversity indices (observed species, Simpson, Shannon, and Chao1) were estimated based on 97% OTU clusters according to a subset of 29,311 randomly selected sequences per sample with 10 iterations (BDE: sediment with BDE-153 amendment, CK: control sediment without BDE-153 amendment; mean and standard deviation of triplicates are shown). Time
Treatment
Day0
Day60
CK
Day60
BDE
Day150
CK
Day150
BDE
Sediments
Sequences
OTUs
Observed species
Simpson
Shannon
Chao1
Freshwater Marine Mudflat Mangrove Freshwater Marine Mudflat Mangrove Freshwater Marine Mudflat Mangrove Freshwater Marine Mudflat Mangrove Freshwater Marine Mudflat Mangrove
106,260 ± 16,440 170,221 ± 15,272 154,543 ± 25,209 83,941 ± 15,205 119,675 ± 3797 101,538 ± 28,042 134,031 ± 25,787 49,903 ± 11,535 68,859 ± 7473 107,314 ± 7485 85,790 ± 14,099 71,703 ± 13,862 70,986 ± 18,043 101,676 ± 7833 97,559 ± 13,855 39,496 ± 6273 42,634 ± 9398 76,556 ± 9070 43,049 ± 4796 62,685 ± 4806
13,926 ± 1774 17,885 ± 714 16,270 ± 1343 12,330 ± 831 13,895 ± 462 13,378 ± 1863 15,000 ± 1815 8438 ± 1068 10,155 ± 469 13,969 ± 729 12,264 ± 927 10,867 ± 1405 10,548 ± 973 11,597 ± 663 11,631 ± 1186 7627 ± 549 7777 ± 880 9152 ± 674 7838 ± 644 10,069 ± 537
6445 ± 325 6147 ± 193 5868 ± 112 6584 ± 388 5931 ± 170 6291 ± 302 5883 ± 37 6090 ± 75 6035 ± 356 6286 ± 386 6360 ± 218 6306 ± 83 6336 ± 538 5304 ± 221 5557 ± 111 6385 ± 432 6244 ± 232 4979 ± 140 6174 ± 225 6348 ± 54
0.98 ± 0.01 0.99 ± 0 0.98 ± 0 0.99 ± 0 0.90 ± 0 0.98 ± 0.01 0.97 ± 0 0.97 ± 0 0.96 ± 0.01 0.99 ± 0.01 0.99 ± 0 0.98 ± 0.01 0.98 ± 0.01 0.97 ± 0.01 0.97 ± 0 0.98 ± 0 0.97 ± 0.01 0.96 ± 0.02 0.98 ± 0 0.99 ± 0
9.83 ± 0.34 9.64 ± 0.21 9.12 ± 0.11 9.75 ± 0.42 9.15 ± 0.15 9.50 ± 0.27 9.01 ± 0.12 9.24 ± 0.14 9.10 ± 0.44 9.77 ± 0.54 9.70 ± 0.14 9.50 ± 0.22 9.74 ± 0.54 8.56 ± 0.2 8.80 ± 0.26 9.71 ± 0.41 9.46 ± 0.31 8.26 ± 0.32 9.62 ± 0.26 10.06 ± 0.07
15,641 ± 850 15,511 ± 608 15,234 ± 255 15,874 ± 831 14,515 ± 250 15,987 ± 718 15,090 ± 424 14,544 ± 234 14,778 ± 953 15,736 ± 741 15,642 ± 420 15,255 ± 435 14,950 ± 1148 13,748 ± 751 13,939 ± 257 15,389 ± 1191 15,133 ± 721 12,888 ± 237 15,086 ± 570 15,106 ± 153
3.3. Changes in microbial diversity and community composition during removal of BDE-153 Rarefaction curves did not reach a plateau at a normalized sequencing depth of 29,311 sequences (Fig. S2), suggesting the high diversity of microorganisms in all sediments, even after the anaerobic incubation with BDE-153 for 150 days. Based on the 29,311 sequences randomly selected from each sample, there were no significant differences in the four alpha (α)-diversity indices, namely observed species, Simpson, Shannon, and Chao1, between the BDE-treatment and its corresponding control in each type of sediment according to t-test at P N 0.05 (Table 2). These suggested that BDE-153 amendment did not change the microbial α-diversity during the 150 days' experiment. Principal coordinate analysis (PCoA) plot based on the calculated Bray-Curtis similarity matrix of all 60 samples revealed strong clustering of sediment samples collected from the same site, whereas the separations between BDEtreated and control sediments or among three sampling times were not so obvious (Fig. 3). Freshwater sediment samples clearly separated from marine sediment samples, while mudflat and mangrove sediment samples were closer to each other and distributed in the data space between freshwater and marine sediment samples. This indicated that mudflat and mangrove sediments had similar microbial community compositions. Significant differences were also found among the four
types of sediments over the 150 days' experiment according to PERMANOVA (Table S3), confirming that the sediment microbial community compositions were significantly affected by sediment type. Within the same sediment type, significant differences were found among sampling times (Table S4). The effect of BDE-153 amendment on microbial community compositions was only significant in three saline sediments, marine, mudflat, and mangrove, on day 150, whereas no significant differences were detected between BDE-treated and control in freshwater sediment at all sampling times (Table S5). These results indicated that the effect of BDE-153 on sediment microbial community compositions was not only sediment type specific, but also depended on sampling time. 3.4. Relationships between microbial community compositions and environmental variables The sampling time or BDE-153 amendment did not significantly change sediment physico-chemical properties, including salinity, TOC, − 2− in each type of sediment (Table S6). By conpH, NH+ 4 , NO3 and SO4 trast, significant differences of these variables were detected among the four types of sediments on days 60 and 150, irrespective of BDE153 amendment. The microbial community compositions in BDEtreated sediments were significantly correlated with the combined
Fig. 2. Phylum-level taxonomic distribution in different sediment samples spiked with BDE-153 (BDE) and control without BDE-153 (CK) on days 0, 60, and 150. The top nine phyla across all sediment samples are indicated. Y-axis indicates proportion of 16S rRNA gene sequences for each phylum in each sediment sample (Fw, Mr, Mf, and Mg are sediments collected from freshwater pond, open sea, mudflat, and mangrove, respectively).
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12.9% (P = 0.001), and 11.6% (P = 0.003) of the variation in microbial compositions, respectively (Fig. 4A). The formation of BDE-52, a debromination product of BDE-153, in BDE-treated sediments was an important factor affecting the microbial community compositions. In control sediments without BDE-153 amendment, the nine sedi− 2− ment properties, including salinity, TOC, pH, NH+ 4 , NO3 , SO4 , % sand, silt, and clay, could explain 68.2% of the variance of the microbial community compositions in the four types of aquatic sediments (Table 3) with spearman Rho equal to 0.514 (P = 0.001). Salinity, pH, and TOC were the most important factors in determining the microbial community compositions in these control sediments according to DISTLM stepwise analysis, which explained 24.9% (P = 0.001), 24.3% (P = 0.001), and 23.1% (P = 0.001) of the variation in microbial community compositions, respectively (Fig. 4B). These results confirmed the importance of salinity and TOC in shaping the microbial community compositions in aquatic sediments, irrespective of BDE-153 amendment. Interestingly, the step-wise analysis showed that sulfate and nitrate, compared to other physico-chemical properties (salinity, pH, and TOC) in sediment, were not important factors in affecting the variations of microbial community structures among the four types of sediments with and without BDE-153 amendment (Fig. 4B). 4. Discussion 4.1. Influence of sediment indigenous microbial linkages on intrinsic removal potential of BDE-153
Fig. 3. Principal coordinated analysis (PCoA) plot of microbial community composition based on the Bray-Curtis similarity matrix, showing similarities of microbial community compositions among freshwater, mangrove, marine, and mudflat sediments (BDE: sediment with BDE-153 amendment; CK: control sediment without BDE-153 amendment).
environmental variables, including nine physico-chemical properties − 2− (salinity, TOC, pH, NH+ 4 , NO3 , SO4 , % sand, % silt, and % clay) and six PBDE congeners (BDE-153, -101, -99, -52, -49, and -47) according to Mantel test (spearman Rho = 0.294, P = 0.001), indicating the strong effect of environmental variables on sediment microbial communities. These variables together explained 77.4% of the total variation in microbial community compositions (Table 3). If only the nine sediment physico-chemical properties were considered, 56.2% of the variation could be explained, while 53.7% of the variation could be explained by just taking the six PBDE congeners in consideration. The remaining unexplained proportion of variance (~23%) might relate to other sediment properties, such as other forms of carbon and nitrogen, phosphorous, heavy metals and so on, which were not measured in the present study. According to DISTLM step-wise analysis, the most important factors determining the microbial compositions in BDE-treated sediments were salinity, BDE-52, and TOC, which explained 21.6% (P = 0.001),
Table 3 Distance-based multivariate multiple regression analysis (DISTLM) of the relationships between environmental variables (including 9 physico-chemical properties and/or 6 PBDE congeners) and microbial community compositions in four types of sediments on days 60 and 150. Treatment
Environmental variables
BDE-treated 9 physico-chemical properties 6 PBDE congeners All of the above Control 9 physico-chemical properties
% explained by the first axis
% explained by all axes
43.8
56.2
46.8 35.8 40.4
53.7 77.4 68.2
Microorganisms are the key players in the self-remediation activity of sediments, and their compositions that are largely controlled by the specific functional microbial linkages determine the performance of sediments in the decomposition of external pollutants (Fukami et al., 2010). Bier et al. (2015) proposed microbial process/function was likely to correlate with the relative or absolute memberships of responsible microorganisms in the community. The removal rate of BDE-153 in each sediment was calculated based on the data collected from six time points, thus reflected the overall removal potential of each sediment. Similar correlation analysis was also adopted in previous studies investigating the potential of sediment/soil in removing BDE-47 and PCBs (Kjellerup et al., 2012; Liang et al., 2014; Pan et al., 2016).The phylum of Proteobacteria and its five genera in the four types of sediments investigated in the present study were related to the removal of BDE153, as reflected by significant positive correlations between removal rates of BDE-153 and relative abundances of these microbial linkages in fresh sediments. Proteobacteria consisting of myriad of well-known degraders was recorded as the phylum that dominated the zones with high concentrations of toxic pollutants such as perfluorooctanoic acid (PFOA), creosote and so on (Sun et al., 2016). Bacteria from this phylum were also reported to be robust degraders of organic pollutants in hot spots of pollution, such as e-waste recycling sites, industrial wastewaters, pharmaceutical waste, petroleum refinery, and sewage (Mukherjee et al., 2014; Ma et al., 2015). A metagenomic analysis found that most of the genes for the biodegradation of persistent organic pollutants (POPs) belonged to the Proteobacteria phylum, confirming its potential to remove POPs (Fang et al., 2014). Not only the phylum of Proteobacteria itself, the five genera, Acinetobacter, Sulfurimonas, Pseudomonas, Psychromonas, and Pelobacter, affiliated to this phylum were also positively related to the removal rates of BDE-153 in the four types of aquatic sediments. These five genera are well-known degraders for organic pollutants, indicating the importance of this phylum in removal of BDE-153. Acinetobacter, one important soil microbial genus, was proved to be the functional bacterial group for the bioremediation of aromatic compounds (Hanson et al., 1997). Sulfurimonas, which usually correlated with sulfur-oxidizing or nitrate-reducing process, had been suggested to coexist with the removal of chlorinated compounds (Sievert et al., 2008; Matturro et al., 2016). Sun et al. (2016) also reported that Sulfurimonas positively
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Fig. 4. Distance-based redundancy analysis (dbRDA) of microbial community compositions and environmental variables selected by DISTLM step-wise procedure, explaining variations in microbial community compositions of four types of sediments after amendment with (A) or without (B) BDE-153 on days 60 and 150.
correlated with the concentration of PFOA in fluorochemicalindustrialized areas. Notable species of Pseudomonas genus were identified as suitable candidates for the bioremediation and metabolism of chemical pollutants in water bodies (Wasi et al., 2013). Psychromonas contributed to the biodegradation of hydrocarbons, petroleum, and oleophilic fertilizers in both microcosm and field biodegradation experiments (Lozada et al., 2014). Pelobacter, commonly found in sediments, muds, and soils, played an important role in the syntrophic metabolism of unusual organic matters, and could be an ideal candidate for in situ bioremediation of complex organic substrates (Sun et al., 2010). The prevalence of the Proteobacteria phylum and its genera capable of degrading organic compounds well associated with the higher BDE153 removal rates in saline than freshwater sediments in the present study. 4.2. Influence of sediment physico-chemical properties and PBDEs on microbial communities in aquatic sediments In the present study, salinity, BDE-52, and TOC were the three major factors in structuring the microbial assemblages in BDEtreated sediments, whereas salinity and TOC were the main factors in control sediments without PBDE pollution. Previous studies also found that salinity was the major environmental determinant of microbial community composition along broad environmental gradients or across different habitat types (Lozupone and Knight, 2007; Canfora et al., 2014). A high concentration of salt, due to the formation of cation bridges at the mineral surfaces of soils, could generate an osmotic stress and reduced the solubility of organic molecules, thus changed the availability of water and nutrients to microorganisms (Bassin et al., 2012; Mavi et al., 2012). Quartaroli et al. (2017) showed the microbial taxa that possessed specific abilities to resist osmotic stress or other limiting factors associated with the presence of high salt concentrations could become dominant at high salinity, leading to the differences of microbial compositions in soil or sediment along a salinity gradient. Kuang et al. (2013) reported that salinity was the main factor in shaping microbial communities even in extreme natural environments or when exposed to stresses such as temperature or pH in laboratory. The salinity in sediment could affect the binding of organic pollutants to organic matters in waters and high salt concentration reduced the binding, thus increased the freely dissolved fraction (Kuivikko et al., 2010). In the present study, the high salinity of three saline sediments might also increase the concentration of dissolved PBDEs in water, which could pose more toxic effect on microbial communities in the sediment slurries with high salt concentrations than the freshwater
ones. Total organic carbon, a key source of carbon for microorganisms, was another important physico-chemical property affecting microbial compositions in sediments. Hu et al. (2014) revealed that organic carbon in soil was a key driving factor on the dynamics of microbial community in arid and semi-arid grasslands. The content of TOC was a key factor controlling the absorption of organic pollutants onto sediment particles (Ali et al., 2015), thus affected a series of processes, such as solubility, degradation, and bioavailability of organic pollutants (Akkanen et al., 2004). In this study, the high TOC content in freshwater sediment could help retain PBDEs in sediment particles, which might explain why the microbial community was not changed by BDE-153 amendment. The pollution of PBDEs could affect the microbial communities in aquatic sediments through various mechanisms. PBDEs could react with organic and inorganic components in the environment and produced reactive oxygen species (ROS), generating adverse effects on the growth and activity of microorganisms (Liu et al., 2015). PBDEs could also bind to DNA via quinone metabolites and generated a DNA-PBDE complex, causing a harmful impact on the structure of DNA (Tian et al., 2015). More, PBDEs could cross the cell membrane, accumulated in cells and induced an oxidative stress, thus reducing cell viability and increasing cell apoptosis (He et al., 2008). In this study, BDE-52 was the only congener affecting the microbial community compositions in polluted aquatic sediments based on DISTLM step-wise analysis. The present results showed that the concentration of BDE-52 continuously increased in sediments during the anaerobic debromination of BDE-153, especially in the three saline sediments, and its concentration even surmounted that of the parent BDE-153 at the end of the 150 days' experiment. Tetra-BDEs are generally more toxic than higher brominated PBDE congeners because of their differences in chemical structure (Luthe et al., 2008; Souza et al., 2016). Huang et al. (2010) found that the toxicity order of five common PBDE congeners on mouse cerebellar granule neurons was BDE-100 N BDE-47 N BDE-99 N BDE-153 ≫ BDE-209. In a toxicity assay using HepG2 cell line, a widely used model to test the toxicity of many xenobiotics, BDE-47 (tetra-BDE) was more toxic than BDE154 (hexa-BDE) and BDE-209 (deca-BDE) (Souza et al., 2016). In the present study, the three saline sediments (marine, mudflat, and mangrove sediments) accumulated more BDE-52 than freshwater sediment, explaining why significant differences in the microbial community compositions between BDE-treatment and controls were only detected in saline sediments towards the end of the experiment (on day 150), but not in the freshwater sediment which had a very low level of BDE-52. The changes in the microbial community structures and the higher BDE-153 biodegradation
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rates were also concurrently observed in the three saline sediments. Although differences in the initial BDE-153 concentration were detected between mangrove and marine sediments, the microbial community in these two types of sediments still had similar responses to BDE-153 amendment during the entire experiment, indicating the difference in initial BDE-153 level did not affect the microbial responses. In the present study, the microorganisms with the ability of resisting high salt concentrations were not identified, as our main objective was to understand the responses of microbial communities to PBDE amendment and analyze the underlying factors that shaped the microbial communities in aquatic sediments. In view of the importance of salinity as shown in the present results, the effect of salinity on the removal of PBDEs, the corresponding microbial community changes and the identification of the microorganisms with the ability of resisting high salt concentrations should be carried in further research. The total attenuation of BDE-153 instead of soluble BDE-153 was considered in this study, mainly because of its low solubility in water (0.00000087 ± 0.00000006 g L−1 as reported by Tittlemier et al., 2002), which is far less than the concentration we spiked into the system. The differences in the dissolved BDE-153 among four sediments should be small. It is also difficult to measure such low dissolved concentration. More, PBDEs were prone to adsorb onto the dissolved organic matter in the aqueous portion (Kuivikko et al., 2010), which make the measurement of the freely dissolved PBDEs very complex. Instead of using the dissolved PBDEs directly, many previous researches, similar to the present study, investigated the factors affecting their solubility such as total BDE-153, TOC, and salinity (Wang et al., 2014; Zhu et al., 2014; Chen et al., 2015, 2016). 5. Conclusion Our deep 16S rRNA sequencing provided a detailed examination on the composition and diversity of microbial communities in the four types of aquatic sediments, three saline (mudflat, marine, and mangrove) and one freshwater, with and without the amendment of BDE153, during the 150 days' experiment under an anaerobic condition. Results demonstrated the intrinsic potentials of aquatic sediments to remove BDE-153 but the removal rates varied among sediment types. The relative abundances of phylum Proteobacteria and the genera belonging to this phylum, including Acinetobacter, Sulfurimonas, Pseudomonas, Psychromonas, and Pelobacter, in fresh sediments at the beginning of the experiment significantly and positively correlated with the removal rates, and might be the microbial linkages in determining the removal of BDE-153 in aquatic sediments. In BDE-153 treated sediments, salinity, BDE-52 (the debrominated congener of BDE-153) and TOC were the key factors shaping their microbial community compositions. In three saline sediments, the microbial community compositions differed significantly between BDEtreatment and control (without BDE) at the end of 150 days, but such difference was not found in freshwater sediment. The three saline sediments also had significantly higher concentrations of BDE-52 than freshwater sediment, further suggesting that BDE-52 may exert a toxic effect on the indigenous microbial communities of saline sediments. More attention should be paid to the pathway and toxicity of the debromination products when adopting an in situ natural attenuation strategy for bioremediation purposes. Acknowledgements The work described in this paper was financially supported by the Research Fund from City University of Hong Kong (Project No. 7004709), the National Natural Science Foundation of China (41576086, 41306084), the National Key Research and Development Program of China (2017YFC0506100) and the Innovation of Science, Technology Commission of Shenzhen Municipality (JCYJ20150416163041307).
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