Dimethylamine biodegradation by mixed culture enriched from drinking water biofilter

Chemosphere 119 (2015) 935–940

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Dimethylamine biodegradation by mixed culture enriched from drinking water biofilter Xiaobin Liao a,1, Chao Chen a,1, Jingxu Zhang b, Yu Dai b, Xiaojian Zhang a, Shuguang Xie b,⇑ a b

School of Environment, Tsinghua University, Beijing 100084, China State Key Joint Laboratory of Environmental Simulation and Pollution Control, College of Environmental Sciences and Engineering, Peking University, Beijing 100871, China

h i g h l i g h t s  Carbon and nitrogen sources have different impacts on DMA removal.  Carbon and nitrogen sources impact DMA-degrading bacterial community.  Proteobacteria predominates in DMA-degrading bacterial community.

a r t i c l e

i n f o

Article history: Received 28 February 2014 Received in revised form 26 August 2014 Accepted 5 September 2014

Handling Editor: I. Cousins Keywords: Biofiltration Dimethylamine Microbial community N-nitrosodimethylamine Proteobacteria

a b s t r a c t Dimethylamine (DMA) is one of the important precursors of drinking water disinfection by-product N-nitrosodimethylamine (NDMA). Reduction of DMA to minimize the formation of carcinogenic NDMA in drinking water is of practical importance. Biodegradation plays a major role in elimination of DMA pollution in the environment, yet information on DMA removal by drinking water biofilter is still lacking. In this study, microcosms with different treatments were constructed to investigate the potential of DMA removal by a mixed culture enriched from a drinking water biofilter and the effects of carbon and nitrogen sources. DMA could be quickly mineralized by the enrichment culture. Amendment of a carbon source, instead of a nitrogen source, had a profound impact on DMA removal. A shift in bacterial community structure was observed with DMA biodegradation, affected by carbon and nitrogen sources. Proteobacteria was the predominant phylum group in DMA-degrading microcosms. Microorganisms from a variety of bacterial genera might be responsible for the rapid DMA mineralization. Ó 2014 Elsevier Ltd. All rights reserved.

1. Introduction Dimethylamine (DMA) and other aliphatic amines are important raw materials or intermediates that are widely used in chemical and pharmaceutical industries (Rappert and Muller, 2005; Zhang et al., 2012a). The presence of these aliphatic amines in the environment has aroused increasing concerns, due to their potential toxicity to human health and odorous smell (Zhang et al., 2012a). DMA was found to be one of the major aliphatic amines in source waters of major cities in China (Zhang et al., 2012a). DMA has been known as one of important precursors of carcinogenic N-nitrosodimethylamine (NDMA) when it reacts with chloramines or chlorine in water (Sharma, 2012). ⇑ Corresponding author at: College of Environmental Sciences and Engineering, Peking University, Yiheyuan Street 5, Haidian District, Beijing 100871, China. Tel./ fax: +86 10 62751923. E-mail address: [email protected] (S. Xie). 1 These authors contributed equally to this study. http://dx.doi.org/10.1016/j.chemosphere.2014.09.020 0045-6535/Ó 2014 Elsevier Ltd. All rights reserved.

Microbial degradation is usually the major mechanism of dissipation of xenobiotic contaminants in the environment (Rappert and Muller, 2005; Zhang et al., 2012b; Zhou et al., 2013). DMA can be biologically oxidized to methylamine (MA) and then ammonia nitrogen under aerobic conditions (Rappert and Muller, 2005; Ho et al., 2008). For the purpose of biological removal or bioremediation practices, DMA-degrading microorganisms from diverse bacterial genera have been isolated and characterized (Rappert and Muller, 2005). Ho et al. (2008) found that biofilter inoculated with degraders could effectively purify waste gas containing trimethylamine (TMA), DMA, and MA. However, traditional culture-dependent approaches can underestimate the diversity of DMA-degrading populations. In addition, the function of pollutant removal in the natural environment or man-made bioreactor can be performed by a whole microbial community, instead of one or few isolated degraders alone (Liao et al., 2013; Yang et al., 2014). Therefore, molecular biology tools can aid in our better understanding of the structure of DMA-degrading microbial community. Unfortunately,

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phylogenetic information on DMA-degrading microbial community is still lacking. Reduction of precursors to minimize the formation of disinfection by-product NDMA in waters is a preferred preventive management strategy, because the removal of NDMA has been found to be very difficult once it is formed (Kristiana et al., 2013). To date, investigations on the reduction of NDMA precursors have been extensively carried out (Bond et al., 2012). Drinking water biofilters can usually perform well in reduction of natural organic matter (NOM), pharmaceuticals and personal care products, precursors of disinfection by-products (DBPs), ozonation by-products, and odor and taste compounds (Farre et al., 2011; Feng et al., 2013; Liao et al., 2012, 2013). Kristiana et al. (2013) suggested that biofiltration might be applied for the removal of low to medium molecular weight NOM to minimize the formation of NDMA in drinking water. NDMA formation potential in wastewater could be dramatically reduced by biological activated carbon (BAC) filter (Farre et al., 2011). However, direct information on DMA removal by drinking water biofilter is still lacking. Moreover, organic matter and nitrogen compounds are two major pollutants in drinking water, yet their impacts on DMA removal remain unclear. Therefore, the aim of the present study was to assess the potential of DMA removal by a mixed culture enriched from drinking water biofilter and the effects of carbon and nitrogen sources. In addition, the structures of DMA-degrading microbial communities were characterized using bacterial clone library analysis. 2. Materials and methods 2.1. Inocula preparation Granular activated carbon (GAC) particles (5 g) were collected from a pilot-scale BAC filter system used for drinking water treatment. The schematic diagram of the BAC filtration system and its operation conditions were described in our previous study (Liao et al., 2013). GAC particles were placed into a 250-mL erlenmeyer flask containing deionised water (100 mL), and were under ultrasonication (10 min; frequency 30 kHz) and then vortexing (5 min). The supernatant was collected and cultured using R2A nutrient medium. Bacterial growth was monitored by measuring the optical density (OD) at 600 nm (OD600 nm). Viability was determined by counting colony-forming units (CFUs) on R2A agar plates. Cells grown until OD600 nm = 1.0 (5.6  108 CFU mL1), were harvested by centrifugation (6000 rpm for 10 min at 4 °C) and washed three times with NaCl (8.5 g L1).

using a Shimadzu 5000A TOC analyzer. Ammonia nitrogen levels were measured according to the standard methods described by China Environmental Protection Agency (2002). DMA was determined according to the literature (Sacher et al., 1997). The membrane filters were cut into quarters with a sterile scalpel and were used for further molecular analysis. DNA was extracted using the E.Z.N.A.Ò Water DNA kit (Omega, USA) according to the manufacturer’s protocol. Bacterial clone libraries of selected samples were constructed, as previously described (Zhang et al., 2012b,c). Bacterial 16S rRNA genes were amplified using primers 27F (50 -GAGTTTGATCMTGGCTCAG-30 ) and 1492R (50 -GGTTACCTTGTTACGACTT-30 ). Sequences with P 98% identity were assigned as operational taxonomic units (OTUs). OTUs, rarefaction curves and Shannon community diversity indices were determined using the MOTHUR program (Schloss et al., 2009). The Ribosomal Database Project analysis tool ‘‘classifier’’ was used to classify the taxonomic identities of the bacterial sequences (Wang et al., 2007). The sequences obtained in this study were submitted to GenBank, under accession numbers KF756610– KF756929.

3. Results 3.1. DMA biodegradation In this study, microbial community originally from drinking water biofilter was enriched using R2A nutrient medium and used for inocula. Fig. 1 illustrates the pattern of residual DMA in the microcosms with four different treatments during the 7-day incubation time. During the incubation, the decline of DMA was negligible in the non-inoculated microcosm (control). However, a rapid reduction of DMA was found in each microcosm with inoculation of microorganisms. These results confirmed biological removal of DMA. On day 3, more than half of DMA in the inoculated microcosms was removed. Moreover, in 5 d inoculation, a nearly complete removal was observed in the microcosm amended with glucose (with treatment I), while the DMA level in the other two inoculated microcosms was still above 1.5 mg L1. Therefore, glucose supplement could enhance DMA removal by the inoculated enrichment culture enriched from drinking water biofilter. In addition, at each sampling date, DMA levels in the microcosms with treatments II and III were similar, suggesting that ammonia nitrogen amendment did not have a marked impact on DMA biodegradation. 14

Treatment I Treatment II Treatment III Treatment IV

2.2. Microcosm experiments 12

2.3. Chemical and molecular analyses Liquid samples were collected at days 0, 1, 3, 5 and 7, and filtered with 0.22 lm pore-size membranes (diameter 50 mm; Millipore). The filtrate was ready for analyses of total organic carbon (TOC), ammonia nitrogen and DMA. TOC levels were determined

10

DMA (mg/L)

Microcosms were prepared in 1000-mL brown glass bottles with 500 mL basic salt medium solution (pH 7.0) and incubated on a horizontal shaker (about 120 rpm) at 22 °C. The composition of basic salt medium solution was as follows (mg L1): MgSO47H2O 4, CaCl2 0.1, NaCl 0.2, KCl 4, FeSO4 0.01, KH2PO4 0.5, and K2HPO4 0.5. Four sets of treatments in triplicate were performed as follows: (I) 10 mg L1 DMA + 18 mg L1 glucose + 11.2  108 CFU bacteria L1; (II) 10 mg L1 DMA + 1.15 mg L1 NH+4–N + 11.2  108 CFU bacteria L1; (III) 10 mg L1 DMA + 11.2  108 CFU bacteria L1; and (IV) 10 mg L1 DMA (as control).

8 6 4 2 0

0

1

3

5

7

Incubation time (days) Fig. 1. Biodegradation of DMA in the microcosms with various treatments during the 7-day incubation period. Treatment I: 10 mg L1 DMA + 18 mg L1 glucose + 11.2  108 CFU bacteria L1; Treatment II: 10 mg L1 DMA + 1.15 mg L1 NH+4–N + 11.2  108 CFU bacteria L1; Treatment III: 10 mg L1 DMA + 11.2  108 CFU bacteria L1; and Treatment IV: 10 mg L1 DMA (as control).

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3.2. Bacterial growth Bacterial growth in each microcosm was estimated using OD600 nm. Fig. 2 shows the pattern of bacterial growth in the microcosms with four different treatments during the 7-day incubation time. Marked bacterial growth was found in each inoculated microcosm during the incubation. At days 1, 3, 5 or 7, the value of OD600 nm in the microcosm with treatment I was much higher than that in the other inoculated microcosms. Moreover, at each sampling date, the value of OD600 nm in the microcosms with treatment II were slightly higher than that in the microcosms with treatment III. 3.3. TOC reduction Change of TOC level in each microcosm with time is shown in Fig. 3. TOC level remained unchanged in the non-inoculated microcosm during the 7-day incubation. However, a rapid reduction of TOC was observed in each inoculated microcosm, indicating the occurrence of mineralization of DMA by inoculated microorganisms. Although the initial TOC level in the microcosm with treatment I was much higher than that in the microcosms with

Optical density at 600 nm (cm-1)

0.40

0.30

3.4. Change of ammonia nitrogen level Change of ammonia nitrogen level in each microcosm with time is shown in Fig. 4. During the incubation, no marked accumulation of ammonia nitrogen was found in the non-inoculated microcosm. In contrast, a continuous rise in ammonia nitrogen level was found in each inoculated microcosm. At each sampling date, the microcosm with treatment II had the highest ammonia nitrogen level. In addition, at days 1, 3, 5 or 7, ammonia nitrogen in the microcosm with treatment I was much higher than that in the microcosm with treatment III. 3.5. Clone library analysis In this study, 16S rRNA clone library analysis was used to depict the bacterial community composition of the enrichment culture and its changes with DMA removal. The composite sample from the microcosms with treatments I–III on day 0 was referred to Sample A. The samples from the microcosms with treatments I, II and III on day 7 were referred to Samples B, C, and D, respectively. Sequences in the bacterial clone libraries with Samples A–D were grouped into 7, 6, 9 and 9 OTUs, respectively (Table 1). The rarefaction curves for the four samples nearly approached a plateau (Fig. S1), suggesting that the bacterial communities were well sampled. OTU-based Shannon index values showed the highest bacte-

Treatment I Treatment II Treatment III Treatment IV

0.35

treatments II or III, TOC levels in all the three microcosms were similar in 3 d of incubation. This indicated the added glucose could also be rapidly consumed by the inoculated enrichment culture. Moreover, at each sampling date, TOC levels in the microcosms with treatments II and III were similar, indicating that ammonia nitrogen amendment did not have a marked impact on TOC removal.

0.25 0.20 0.15 0.10 0.05

2.5

0.00

0

1

3

5

7

Treatment I Treatment II Treatment III Treatment IV

2.0

NH4+-N (mg/L)

Incubation time (days) Fig. 2. Bacterial growth in the microcosms with various treatments during the 7-day incubation period. Treatment I: 10 mg L1 DMA + 18 mg L1 glucose + 11.2  108 CFU bacteria L1; Treatment II: 10 mg L1 DMA + 1.15 mg L1 NH+4–N + 11.2  108 CFU bacteria L1; Treatment III:10 mg L1 DMA + 11.2  108 CFU bacteria L1; and Treatment IV: 10 mg L1 DMA (as control).

1.5

1.0

0.5

14

Treatment I Treatment II Treatment III Treatment IV

12

TOC (mg/L)

10

0.0

0

1

3

5

7

Incubation time (days) Fig. 4. Change of ammonia levels in the microcosms with various treatments during the 7-day incubation period. Treatment I: 10 mg L1 DMA + 18 mg L1 glucose + 11.2  108 CFU bacteria L1; Treatment II: 10 mg L1 DMA + 1.15 mg L1 NH+4–N + 11.2  108 CFU bacteria L1; Treatment III:10 mg L1 DMA + 11.2  108 CFU bacteria L1; and Treatment IV: 10 mg L1 DMA (as control).

8 6 4 2 0

0

1

3

5

7

Incubation time (days) Fig. 3. Change of TOC levels in the microcosms with various treatments during the 7-day incubation period. Treatment I: 10 mg L1 DMA + 18 mg L1 glucose + 11.2  108 CFU bacteria L1; Treatment II: 10 mg L1 DMA + 1.15 mg L1 NH+4–N + 11.2  108 CFU bacteria L1; Treatment III:10 mg L1 DMA + 11.2  108 CFU bacteria L1; and Treatment IV: 10 mg L1 DMA (as control).

Table 1 OTU-based community richness and diversity indices for Samples A–D. Sample A represents the composite sample from the microcosms with treatments I–III on day 0. Samples B, C, and D represent the samples from the microcosms with treatment I, II and III on day 7, respectively. Sample

No. of sequences

OTUs

Shannon index

A B C D

82 75 86 77

7 6 9 9

1.34 1.06 1.56 1.76

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rial community diversity for Sample D, followed by Samples C, A, and then B. This indicated different treatments could have various impacts on bacterial community diversity of the enrichment culture. Bacterial community diversity could be increased by addition of DMA, but it could be lowered by further amendment of carbon or nitrogen sources. Fig. 5 shows the bacterial phylum compositions of the four samples. The identified phyla included Proteobacteria, Bacteroidetes and Firmicutes. Phylum Proteobacteria predominated in each sample, with a relative abundance of 75.3–92.7%. The relative abundance of Alphaproteobacteria was 76.8% in Sample A, while became much less in Sample C (66.3%) and Sample D (51.9%). The proportion of Betaproteobacteria in Sample C (11.6%) or Sample D (11.7%) gained a slight increase, compared with that in Sample A. However, both Alphaproteobacteria and Betaproteobacteria were not detected in Sample B. Gammaproteobacteria was the predominant group in Sample B, but was much less abundant in the other three samples (2.3–11.7%). The proportion of Bacteroidetes in Sample C (10.5%) was much higher than that in the other samples (0–2.6%). In addition, the proportion of Firmicutes in Sample D (22.1%) was higher

Relative abundance (%)

100 90 80 70 60

Firmicutes

50

Bacteroidetes

40

Gammaproteobacteria

30

Betaproteobacteria

20

Alphaproteobacteria

10 0 A

B

C

D

Sample Fig. 5. Comparison of the quantitative contribution of the sequences affiliated with different phyla and subphyla to the total number of sequences from Samples A–D. Sample A represents the composite sample from the microcosms with treatments I–III on day 0. Samples B, C, and D represent the samples from the microcosms with treatment I, II and III on day 7, respectively.

Table 2 Distribution of the sequences affiliated with the identified genera in Samples A–D. Sample A represents the composite sample from the microcosms with treatments I–III on day 0. Samples B, C, and D represent the samples from the microcosms with treatment I, II and III on day 7, respectively.

a

Phylogenetic affiliation

Sample A

Sample B

Sample C

Sample D

Alphaproteobacteria Brevundimonas

45

–a

44

20

Betaproteobacteria Pandoraea Achromobacter Methyloversatilis Simplicispira

6 – – –

– – – –

1 3 6 –

5 – 3 1

Gammaproteobacteria Stenotrophomonas Pseudomonas Acinetobacter Alkanindiges

5 2 – –

– – 15 1

2 – – –

9 – – –

Bacteroidetes Sphingobacterium Terrimonas

1 –

– –

– 9

1 1

Firmicutes Bacillus

5

10

8

17

Total

64

26

73

57

–, not detected.

than that in the other samples (6.1–14.7%). Therefore, the compositions of the major bacterial groups and their proportions were much different. These results indicated that bacterial community structure varied with DMA biodegradation, which was also affected by co-substrate. Most of sequences retrieved from Samples A, C, and D could be affiliated with the known genera. However, less than half of sequences retrieved from Sample B could be classified at genus level. Table 2 shows the detected 12 known genera in the four samples. The differences among the four samples became much more obvious at the genus level. For example, only Bacillus was detected among all the four samples. Brevundimonas was the largest genus group in Samples A, C, or D, but was not detected in Sample B. Acinetobacter was the largest genus group in Sample B, but was absent in the other three samples. Moreover, Terrimonas was abundant in Sample C, but were absent or were the minor components in the other samples.

4. Discussion Biodegradation of NDMA by isolated degraders or mixed cultures has been reported (Fournier et al., 2009; Sharp et al., 2010; Tezel et al., 2011; Weidhaas et al., 2012). A few previous studies revealed that biofilters could be a viable treatment option for NDMA in waters (Hatzinger et al., 2011; Ho et al., 2011; Webster et al., 2013). Moreover, DMA is one of the intermediates of TMA biodegradation (Rappert and Muller, 2005; Ho et al., 2008). Biodegradation of DMA, TMA and other aliphatic amines by isolated degraders has been well-documented (Rappert and Muller, 2005). Several previous studies indicated that biofilters inoculated with isolated degraders or enriched mixed cultures could effectively purify TMA- or DMA-containing waste gas (Chang et al., 2004; Ding et al., 2007; Ho et al., 2008; Wan et al., 2011; Yin and Xu, 2012). However, there has been no report on biodegradation of DMA or other aliphatic amines by water treatment biofilter. To the authors’ knowledge, this was the first report on DMA removal by the mixed culture enriched from water treatment biofilter. In this study, a rapid depletion of DMA was found by the enrichment culture. This result suggested drinking water BAC biofilter could have a strong potential for DMA removal. In this study, the basic salt medium solution used for biodegradation tests contained no carbon and nitrogen sources. Therefore, DMA biodegradation and bacterial growth in the microcosm without addition of glucose or ammonia nitrogen indicated that DMA was utilized by the added enrichment culture as both carbon and nitrogen sources. Supplement of carbon and nitrogen sources can have different impacts on biodegradation of xenobiotic contaminants by isolated degraders or mixed cultures, dependent on many factors (e.g. culture conditions and properties of contaminants) (Xie et al., 2013; Zhou et al., 2013; Zhang et al., 2013a). To the authors’ knowledge, this was the first report on the impacts of carbon and nitrogen sources on biodegradation of aliphatic amines by inoculated microorganisms in biofilter. Glucose and ammonia nitrogen are the carbon and nitrogen sources easily utilized by microorganisms. In this study, ammonia nitrogen amendment showed no marked impact on DMA biodegradation by the inoculated enrichment culture, while glucose amendment could even significantly increase DMA removal. This suggested the potential for DMA removal by drinking water BAC biofilter would not be negatively affected by carbon and nitrogen compounds in water. TMA can be initially oxidized to DMA and further to MA. MA can be completely oxidized to ammonia nitrogen under aerobic conditions (Rappert and Muller, 2005; Ho et al., 2008). In this study, a rise in ammonia nitrogen level was found in the inoculated microcosm during the incubation, confirming that DMA could be

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converted to ammonia nitrogen by the inoculated enrichment culture. The accumulation of metabolite ammonia nitrogen has also been reported in the others’ previous studies using activated sludge microorganisms to eliminate TMA (Chang et al., 2004; Ding et al., 2007). Biofiltration of aliphatic amines-containing waste gas by immobilized Paracoccus sp. CP2 could also result in the accumulation of ammonia nitrogen (Ho et al., 2008). In addition, glucose addition could increase the formation of ammonia nitrogen by the inoculated enrichment culture. This was in agreement with the positive effect of carbon source on DMA biodegradation. Rappert and Muller (2005) proposed the degradation pathway of TMA and DMA by microorganisms in the environment under aerobic conditions and they suggested that TMA and DMA could be mineralized. However, information about mineralization of TMA and DMA in biofilters is still very limited. Only Wan et al. (2011) reported that about 53.1% of TMA carbon was mineralized in biotrickling filter inoculated with B350 mixed microorganisms. In this study, a significant TOC reduction in the microcosm without amendment of glucose or ammonia nitrogen indicated that most of DMA was mineralized to inorganic carbon by the inoculated enrichment culture during the incubation time. Therefore, DMA could be converted to inorganic carbon and ammonia by the inoculated enrichment culture. The documented DMA-degrading isolates included members of genera Arthrobacter, Bacillus, Hyphomicrobium, Methylobacterium, Psuedomonas, Mycobacterium, Paracoccus, Methylophilus, and Micrococus (Rappert and Muller, 2005). Microorganisms from genera Arthrobacter, Psuedomonas and Paracoccus have been commonly used to remove DMA and TMA in waste gas and water (Chang et al., 2004; Ho et al., 2008). To date, information on phylogenetic composition of the TMA- or DMA-degrading microbial community is still scant. Wan et al. (2011) used denaturing gradient gel electrophoresis (DGGE) analysis to characterize the bacterial community in biotrickling filter treating waste gas containing high-concentration TMA. They found the stable state bacterial community in the biotrickling filter was dominated by six species. However, they did not provide the detailed phylogenetic information of TMA-degrading bacterial community. In this study, clone library analysis showed that the mixed culture enriched from drinking water BAC biofiltration system (Sample A) was composed of mainly Alphaproteobacteria, and some less abundant components (Betaproteobacteria, Gammaproteobacteria, Bacteroidetes, and Firmicutes). Our previous study also indicated that Alphaproteobacteria was the largest bacterial group in the BAC biofiltration system (Liao et al., 2013). To date, little is known about the impacts of aliphatic amines on microbial community (Wan et al., 2011). In this study, amendment of either carbon or nitrogen sources was found to have a great impact on DMA-degrading bacterial community. Except for Bacillus (Firmicutes) and Pseudomonas (Gammaproteobacteria), the genera indentified in this study were not related to any known DMA-degraders. Although Pseudomonas was present in Sample A, its absence in Samples B, C and D suggested that it was likely not involved in DMA degradation. Members of genus Bacillus are known for biodegradation of a variety of environmental organic chemicals, such as polyester polyurethane (Shah et al., 2013), Azo dye (Prasad and Rao, 2013), cypermethrin (Sundaram et al., 2013), amide (Sogani et al., 2012), and benzene, toluene and xylene (Mukherjee and Bordoloi, 2012). The enrichment of Bacillus species might have a specific role in DMA biodegradation. Acinetobacter (Gammaproteobacteria) can also degrade various organic pollutants, such as n-alkanes (Tanase et al., 2013), diesel oil (Luo et al., 2013), furazolidone (Zhang et al., 2013b), phenol (Kobayashi et al., 2012), and 4-fluoroaniline (Wang et al., 2013). Acinetobacter was the largest genus group in Sample B, but it was not found in the other samples. The significant enrichment of Acinetobacter species in Sample B suggested its unique role in DMA

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degradation and might account for the relatively rapid DMA degradation in the microcosm with glucose amendment. Brevundimonas (Alphaproteobacteria) has also been linked to biodegradation of a variety of environmental organic pollutants, such as crude oil (Mahjoubi et al., 2013), aliphatic and aromatic hydrocarbons (Vazquez et al., 2013), lactofen (Liang et al., 2010), and fenamiphos (Cabrera et al., 2010). The dominance of Brevundimonas species in Samples C and D suggested its potential roles in DMA degradation. However, the absence of Brevundimonas in Sample B indicated glucose amendment did not favor its growth. In addition, Pandoraea, Achromobacter and Methyloversatilis (Betaproteobacteria), Stenotrophomonas (Gammaproteobacteria), and Sphingobacterium (Bacteroidetes) are also known for their ability to biodegrade many kinds of organic pollutants (Takagi et al., 2012; Abraham and Silambarasan, 2013; Gao et al., 2013;Gunasundari and Muthukumar, 2013; Tanase et al., 2013; Zheng et al., 2013). Therefore, microorganisms from a variety of genera might contribute to DMA degradation and subsequent mineralization, which was responsible for rapid reduction of DMA and TOC by the inoculated enrichment culture. In addition, the composition of genera and their abundances in DMA-degrading system could be influenced by amendment of either carbon or nitrogen sources. Different bacterial consortia could be involved in DMA mineralization in the microcosms with various treatments. However, further efforts are necessary in order to elucidate the role of microbial community in DMA mineralization. 5. Conclusions A rapid mineralization of DMA occurred in the microcosms inoculated with the mixed culture enriched from drinking water BAC biofiltration system. DMA could be used as both carbon and nitrogen sources by the enrichment culture. Glucose amendment could enhance DMA removal, but ammonia nitrogen supplement showed no marked impact. The accumulation of metabolite ammonia nitrogen was observed with DMA biodegradation. DMA addition and its subsequent biodegradation induced a shift in bacterial community structure, which was greatly affected by further amendment of either carbon or nitrogen sources. Proteobacteria predominated in the DMA-degrading microcosms, while the composition of proteobacterial classes and their proportions were much different. Microorganisms from a variety of bacterial genera might contribute to the rapid DMA mineralization. Acknowledgment This project is supported by special fund of State Key Joint Laboratory of Environment Simulation and Pollution Control (No. 13K07ESPCT). Appendix A. Supplementary material Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.chemosphere. 2014.09.020. References Abraham, J., Silambarasan, S., 2013. Biodegradation of chlorpyrifos and its hydrolyzing metabolite 3,5,6-trichloro-2-pyridinol by Sphingobacterium sp. JAS3. Process Biochem. 48, 1559–1564. China Environmental Protection Agency, 2002. Methods for Water and Wastewater Determination. China Environmental Science Press, Beijing. Bond, T., Templeton, M.R., Graham, N., 2012. Precursors of nitrogenous disinfection by-products in drinking water-A critical review and analysis. J. Hazard. Mater. 235, 1–16. Cabrera, J.A., Kurtz, A., Sikora, R.A., Schouten, A., 2010. Isolation and characterization of fenamiphos degrading bacteria. Biodegradation 21, 1017–1027.

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