Cadmium and mercury removal from non-point source wastewater by a hybrid bioreactor

Bioresource Technology 102 (2011) 9927–9932

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Cadmium and mercury removal from non-point source wastewater by a hybrid bioreactor Rong Yan a,b, Fan Yang b, Yonghong Wu b,⇑, Zhengyi Hu b, Bibhash Nath c, Linzhang Yang b, Yanming Fang a,⇑ a

College of Forest Resource and Environment Science, Nanjing Forestry University, Nanjing 210037, Jiangsu, People’s Republic of China State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Sciences, Chinese Academy of Sciences, 71 East Beijing Road, Nanjing 210008, Jiangsu, People’s Republic of China c School of Geosciences, University of Sydney, Sydney, NSW 2006, Australia b

a r t i c l e

i n f o

Article history: Received 28 April 2011 Received in revised form 11 August 2011 Accepted 12 August 2011 Available online 19 August 2011 Keywords: Bioreactor Bacterial diversity Wastewater Organic matter Metals

a b s t r a c t The purpose of this study was to remove cadmium (Cd) and mercury (Hg) from non-point source wastewater by a hybrid bioreactor consisting of two different processes (anaerobic–anoxic–aerobic and photoautotrophic). The results showed that the bioreactor could concurrently culture heterotrophic and autotrophic microorganisms, and removed Cd and Hg from the wastewater successfully. The average removal efficiencies were 79% and 66%, respectively for Cd and Hg. The relationship between Cd removal rate and biofilm mass was observed to be significant (p < 0.05) during different seasons. The Hg removal was mainly due to the bioaccumulation in macrophytes via a photoautotrophic process. Due to the increase of the bacterial diversity under the rejuvenated conditions modulated by the hybrid bioreactor, the growth conditions of the native bacterial habitat were improved. The results demonstrate that the environmentally benign, easily-deployed, sludge free and cost-effective hybrid bioreactor can efficiently remove Cd and Hg from non-point source wastewater. Ó 2011 Elsevier Ltd. All rights reserved.

1. Introduction Heavy metal pollution (especially in wastewater) is of concern due to its non-biodegradable nature (Quintelas et al., 2009a,b). The heavy metals generally cause long-term exposure (bioaccumulation as well as biomagnifications) to some flora and fauna (Gönen and Aksu, 2009). Therefore, removal of those heavy metals from the wastewater was now become an issue of major concern (Yang et al., 2009). Cadmium (Cd) and mercury (Hg) are the most commonly observed heavy metals in both domestic and industrial wastewater. To date, several methods have been developed to remove Cd and Hg from the aqueous solution, such as precipitation and electrochemistry (Pascal et al., 2007), ion exchange (Chen et al., 2008), electrodialysis and solvent extraction (Wan Ngah and Hanafiah, 2008). Adsorption has been regarded as the important process to remove heavy metals (e.g., Cd and Hg) from the aqueous solution. Among the common adsorbents, activated carbon has been widely used. However it is relatively expensive (Demirbas, 2008). Research interests are now focused to replace those adsorbents by generating low-cost alternatives (Wan Ngah and Hanafiah, 2008). For example, untreated Pinus halepensis sawdust and Aspergillus versicolor biomass have been applied to remove Cd and Hg from aqueous ⇑ Corresponding authors. Tel.: +86 25 8688 1330; fax: +86 25 8688 1000. E-mail addresses: [email protected] (Y. Wu), [email protected] (Y. Fang). 0960-8524/$ - see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.biortech.2011.08.049

solutions, respectively (Semerjian, 2010; Das et al., 2007). Although, many low-cost adsorbents have already been used, such as rice hull and sawdust (Asadi et al., 2008), chitosan, zeolites, slurry waste (Babel and Kurniawan, 2003), brewery waste (Chen and Wang, 2008), fly ash (Cho et al., 2005), amine-functionalized mesoporus silica (Aguado et al., 2009), and nano-alumina modified with 2,4-dinitrophenylhydrazine (Afkhami et al., 2010). However, application of such low-cost adsorbents should require further testing in practical environments. Heavy metal pollution is mainly associated with the areas of intensive industry. However, non-point source wastewater, such as from industrial parks, community areas, and stormwater runoff has been considered as the largest sources of heavy metals (especially Cd and Hg) in the environment (Xiao and Ji, 2007). However, it is difficult to remove Cd and Hg from the wastewater due to large variations in the hydraulic loading and concentration of the metals (Wu et al., 2010). Moreover, the suspended particles carried by the non-point source wastewater may fill the cavities of the adsorbent, thereby reducing the removal efficiency. In addition, Cd and Hg are generally bound to the surfaces of the road dust or other particulates (Brunner et al., 2008; Covelo et al., 2007). This also poses difficulties to the removal processes because the removal efficiency is mainly governed by the chemical nature of the metals, soil and sediment particles, as well as the pH of the surrounding environment (Brunner et al., 2008; Covelo et al., 2007). Therefore, to remove Cd and Hg simultaneously from non-point source

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wastewater, a pre-treatment system of the wastewater should be designed together with suitable remedial options. The bioreactor is a treatment technology with multiple functions (i.e., collection and storage of the wastewater, deposition of the suspended particles/materials and removal of the pollutants) based on the living microbial communities, and which has vast potential to remove heavy metals from wastewater (Wilkie et al., 2004). However, most of the bioreactors, to date, contained a single dominant species of microorganism such as Arthrobacter viscosus (Quintelas et al., 2009a,b). The single dominant species of microorganism is generally vulnerable if there is any change in hydrological loading and/or pollutant concentrations. Therefore, a hybrid bioreactor containing different microbial communities should be considered prior to removal of heavy metals (e.g., Cd and Hg) from the non-point source wastewater. Some researchers (Kaushik et al., 2010) have investigated a three stage bioreactor adopting Emericella nidulans var. lata, Neurospora intermedia and Bacillus sp. to remove color and chemical oxygen demand (COD) in microcosm experiments. However, performance of removing heavy metals from wastewater requires further testing. In this study, a hybrid bioreactor comprising collection, storage and depositional tanks was proposed to culture heterotrophic and autotrophic microorganisms to remove Cd and Hg simultaneously from non-point source wastewater. In addition, environmental benefits and industrial applications were also addressed: (1) that the removal process does not produce any potentially hazardous compounds or materials; and (2) that the cultured microorganisms should be native, thus shortening the acclimation and adaptation periods. We anticipate that the findings of this study will provide a promising bio-measure to remove Cd and Hg from the non-point source wastewater, and provide a new insight into the concurrent culturing of heterogeneous microbial aggregates composed of heterotrophic and autotrophic microorganisms.

2. Methods 2.1. Description of the hybrid bioreactor The hybrid bioreactor consisted of two treatment systems, (i) anaerobic–anoxic–aerobic (A2/O), and (ii) photoautotrophic processes (Fig. 1). Eight compartments were linked together in the bioreactor: (i) the depositional tank, 30 m3 in volume was planted with macrophytes (Canna indica, Juncus minimus and Cyperus alternifolius species) with a planting density of 0.5  0.5 m; (ii) the anaerobic tank, 96 m3 in volume was filled with coarse

gravels (diameter 3–10 cm); (iii) the overflow pool, 4 m3 in volume was used to reduce suspended particles/materials from the wastewater; (iv) the settling tank, 24 m3 in volume was used to further reduce suspended materials; (v) the anoxic fluidized bed, 72 m3 in volume contained biofilm substrates (Industrial Soft Carriers, Wuxi Guozhen Environmental Protection Co. Ltd.) with density of 0.3 m3 per m3 water; (vi) the aerobic fluidized bed, 72 m3 in volume contained suspended biofilm substrates ‘Artificial Aquatic Mats’ (Wuhan Zhongke Environmental Engineering Co. Ltd.) with density of 0.3 m3 per m3 water; (vii) The clarification tank, 24 m3 in volume was also used to reduce suspended materials, and (viii) The photoautotrophic system was built in an ecological ditch with a total length of 230 m and width of 2.5 m (soil wall gradient 45°). A series of nylon tanks (0.04 m3), containing ceramsite adsorbent (Kunming Yuxi Materials Co. Ltd.), was placed on the bottom of the ecological trunk channel at 2.0 m intervals for the adsorption of pollutants from the wastewater. Macrophytes, including Scirpus tabernaemontani, Canna indica, Zizania latifolia, Juncus minimus, Cyperus alternifolius, Zantedeschia aethiopica, and Acorus calamus, were planted along the walls of the ecological ditches at 0.5 m intervals. Sampling sites are designated as B1 to B6. Sampling sites B1 was located at the inlet of the depositional tank, B2 was located at the outlet of the anaerobic tank, B3 was located at the inlet of the anoxic fluidized bed, B4 was located at the outlet of the aerobic fluidized bed, while B5 and B6 were located at the inlet and outlet of the photoautotrophic system, respectively. 2.2. Characterization of the wastewater The non-point source wastewaters were collected from the industrial park (containing nine processing factories) and the communities of Liangjia Village, Kunming City, Western China. The quantity of domestic wastewater was 120 m3 day1, while the quantity of industrial wastewater was 80 m3 day1. The physicochemical characteristics of the wastewater have been tabulated in Table 1. 2.3. Experimental design Prior to achieving the steady state condition, microorganisms were cultured in the bioreactor to improve removal efficiency of the pollutants. Mixed microbial communities (0.6 m3 active sludge) from the domestic wastewater treatment plant were placed in both anoxic and aerobic fluidized beds. This has been done to immobilize

B4

B3

Pump

B5

B6

Influent B1

B2

(3)

(1)

(4)

(5)

(6)

(7)

(8)

Outlet

(2)

Anaerobic-anoxic-aerobic (A2/O) phase

Photoautotrophic phase

Fig. 1. The schematic diagram showing multi-level hybrid bioreactor. The numbered components are: (1) depositional tank, (2) anaerobic tank filled with gravels, (3) overflow pool, (4) settling tank, (5) anoxic fluidized bed, (6) aerobic fluidized bed, (7) clarification tank, and (8) photoautotrophic system. The arrows indicate the direction of wastewater flow. Sampling sites are designated as B1 to B6.

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R. Yan et al. / Bioresource Technology 102 (2011) 9927–9932 Table 1 The physicochemical characteristics of the non-point source wastewater (n = 23). pH

DO (mg L1)

UV absorbance (254 nm)

COD (mg L1)

BOD (mg L1)

Mean ± SD

7.6 ± 0.40

Mean ± SD

Cu (lg L1) 605 ± 8.3

1.4 ± 0.30

0.7 ± 0.04

147 ± 46

71 ± 25

Zn (lg L1) 378 ± 18

Fe (lg L1) 384 ± 12

Hg (lg L1) 1.3 ± 0.06

Cd (lg L1) 405 ± 6.9

robust native microorganisms and to form native biofilms in the substrates, and facilitates large-scale industrial application. The biofilms from the bioreactor were cultured and incubated under natural conditions (temperature ranges from 15 to 28 °C). The combined hydraulic load of the bioreactor was 200 m3 day1. The mode of the wastewater throughputs to the bioreactor was for 12 h daily (i.e., 12 h on and off period, so that the average inflow to the hybrid bioreactor was approximately 16.7 m3 h1). The air temperature ranged from 8 to 31 °C and the UV-B radiation strength ranged from 0.15 to 0.68 W m2 during the experimental period. To support the growth of native microbes in the photoautotrophic system, the sludge from the bottom of the anoxic and aerobic fluidized beds was pumped directly into the photoautotrophic system using a strong-pressure sludge-pump during the no throughput periods. 2.4. Sampling and analyses The wastewater samples were collected in triplicate and measured for dissolved oxygen (DO) and pH in situ by a multimeter (YSI 52 dissolved oxygen and pH meters). Chemical oxygen demand (COD) was measured by the potassium dichromate method (APHA-AWWA-WEF, 1998). Biological oxygen demand (BOD) was calculated as the difference between DO level at the time of sample collection and the DO level at the end of each day for five days (APHA-AWWA-WEF, 1998). Samples for measuring UV254 absorbance were filtered (pore size 0.45 lm) before being measured in order to eliminate the variations in UV absorption caused by the particulate matter (Wu et al., 2005). After filtration (pore size 0.22 lm) of the water samples, the filtrate residues were observed using optical microscopy. Common microorganisms such as the species of bacteria, diatoms and cyanobacteria, were identified using the national standard guide of microorganisms or common phytoplankton in freshwater (ChinaEPA, 2002). The cadmium (Cd) and copper (Cu) concentrations were measured using graphite furnace atomic absorption spectrometry (AA-7001, Beijing). The zinc (Zn) and iron (Fe) concentrations were determined using the flame atomic absorption spectrometry (AA-7001, Beijing). The mercury (Hg) concentrations were determined using cold vapor atomic fluorescence spectrometry (QM201D, Jiangsu). These procedures are described in the national standard methods of water and wastewater analyses, China (ChinaEPA, 2002). Macrophyte samples (leaf and roots) from two sampling sites (B5 and B6) were collected quarterly in triplicate between June 2007 and May 2008. The samples were mixed together and dried at 103 °C for 12 h before being digested with HNO3/HClO4 (5:1 v/v) at 60–70 °C. The digested samples were analyzed for Hg concentration using cold vapor atomic fluorescence spectrometry. Biofilm samples (n = 10, in triplicate) were also collected from different locations of the substrates and later kept at 25–30 °C until their moisture contents were reduced to 85%. The biofilms were then weighed and total biofilm mass was estimated based on the biofilm weight and specific surface area of the substrates. The Shannon diversity index (Eichner et al., 1999) was also calculated to evaluate the bacterial community diversity in the biofilms. The use of Shannon diversity index to quantify bacterial diversity was referred to previously (Miura et al., 2007).

The DNA was also isolated from the biofilm following the procedure previously reported (Hill et al., 2002). The biofilm aliquots (1 mL) were thawed in an ice-bath, and the cells were harvested by centrifugation for 5 min. DNA was then purified by sequential extraction with Tris-equilibrated phenol, phenol–chloroform–isoamyl alcohol (25:24:1), and chloroform isoamyl alcohol (24:1) followed by precipitation with two volumes of ethanol. The detailed procedures were described previously (Wei et al., 2004). The community fingerprints were obtained for bacteria in the biofilms using total bacterial DNA as templates for ERIC-PCR. The sequence of the ERIC primers and the detailed procedures were described previously (Li et al., 2006), E1 (ERIC-PCR): 50 -ATGTAAGCTCCTGGGGATTCAC-30 , E2 (ERIC-PCR): 50 -AAGTAAGTGACTGGGGTGAGCG-30 . Data analysis was performed using SPSS statistical software (version 15.0), with the level of statistical significance set at p < 0.05. Statistically significant differences were evaluated on the basis of standard deviation determinations and the analysis of variance (one way ANOVA). Non-parametric correlation between total biofilm mass and removal efficiency of Cd was analyzed by Kendall’s tau-b. 3. Results and discussion 3.1. Microorganisms in the hybrid bioreactor The microscopic studies showed the presence of bacteria (including methanosarcina, diplobacillus, bacilli, brevibacterium and cocci), chladophora, diatoms (including Cyclostephanos dubius, Aulacoseira granulate, and Stephanodiscus minutulus) and cyanobacteria (including Microsystis aeruginosa and Aphanizomenon flosaquae) within the hybrid bioreactor. These observations indicate that the hybrid bioreactor simultaneously supports both heterotrophic and autotrophic microorganisms. 3.2. Removal of Cd and Hg from the wastewater The results showed the presence of high concentrations of heavy metals (especially Cd and Hg) in the wastewater with annual average of 420 and 2.0 lg L1, respectively (Fig. 2). The average removal efficiencies were 79% for Cd and 62% for Hg during the experimental period (June 2007–May 2008). However, the Cd removal efficiency decreased slightly during June to October 2007 (79–74%), while it increased in January 2008 and again decreased in May 2008. At the same time, however, the Hg removal efficiency behaved differently, increasing from 50% to 68% during June–October 2007, slightly decreasing in January followed by a slight increase in May 2008 (Fig. 2). The metal concentrations during different stages of the treatment process (sampling sites B1 to B6) were also determined. Fig. 3a shows that the Cd concentrations predominantly decreased during the first stage of the treatment phase (i.e., during A2/O process), while the concentrations did not markedly decrease during latter stages of the treatment phase (i.e., during the photoautotrophic process). This indicates that the majority of Cd (81–96%) was removed by the A2/O process. However, Hg concentrations were only reduced to 16–18% during the A2/O process, while removal efficiency increased rapidly (39–63%) during the photoautotrophic process (Fig. 3b).

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400

80

300

70

effuent

70 1.5 60

100

50

0.5

40

0.0

3-Jan

80

2.0

60

0

90

Hg

2.5

200

22-Jun 16-Oct

influent removal rate

3.0

90

Cd Hg (µg L-1)

Cd (µg L-1)

effuent

1.0 50 40 22-Jun

6-May

removal rate (%)

influent removal rate

500

removal rate (%)

9930

16-Oct

3-Jan

6-May

Fig. 2. The average influent and effluent Cd and Hg concentrations, including their removal efficiencies during June, and October of 2007 and January and May of 2008. The influent and effluent samples were collected from sampling sites B1 and B6 and shown as average values for respective sampling dates.

4.0 Cd

400

200

0 B1

B4 Jun-07

B6

B1

B4

Hg concentration (µg L-1)

Cd concentration (µg L-1)

600

Hg 3.0 2.0 1.0 0.0 B1

B6

B4

B6

Jun-07

May-08

B1

B4

B6

May-08

Fig. 3. The Cd and Hg concentrations during different stages of the treatment process in the hybrid bioreactor. Samples were collected from: (i) the influent of the bioreactor (sampling site B1), (ii) the effluent of aerobic fluidized bed (sampling site B4), and (iii) the outlet of the photoautotrophic system (sampling site B6).

The total biofilm masses (at 25–30 °C, moisture content 85%, estimated based on the weight and the specific surface area of the substrates) generated during the A2/O process were 157 ± 20 kg (in June 2007), 153 ± 7.6 kg (in October 2007), 193 ± 29 kg (in January 2008), and 184 ± 18 kg (in May 2008). The variation in the generation of biofilm masses and the Cd removal efficiency were very similar during different seasons, and the correlations were very significant (p < 0.05). The linear relationship between biofilm mass and Cd removal rate is as follows: [Biofilm mass] = 5.398  [100  Cd removal rate]  254.1 (n = 4, R2 = 0.982). This implies that the metal removal (i.e., Cd) was associated with the formation of biofilm during A2/O process. In most cases, such metals were removed from the wastewater due to adsorptions onto biofilms (Quintelas et al., 2008, 2009a). The Hg concentrations in the macrophyte samples (collected from the photoautotrophic system) were 0.6 ± 0.03 and 1.3 ± 0.15 lg kg1 of the biomass for June 2007 and May 2008, respectively. This suggests that the removal of Hg from the wastewater was attributable to the photoautotrophic phase. Similarly, Hg concentrations at sampling site B6 were low compared with the sampling sites B1 and B4 (Fig. 3b). The accumulation rate of Hg in the macrophytes was 0.7 lg kg1 of the biomass year1. These imply that the removal of Hg from the wastewater during the photoautotrophic phase was owed to the accumulation of Hg in the macrophytes. 3.4. Bacterial community structure Fig. 4 shows that the Shannon diversity indices increased from 1.3 to 1.8 (at sampling site B3), 1.5 to 2.1 (at sampling site B4), 1.7

to 2.7 (at sampling site B5) and 1.9 to 2.9 (at sampling site B6) during the experimental periods. By pair-wise comparisons, the Shannon diversity index at sampling sites B3, B4, B5 and B6 during May 2008 was significantly higher than June 2007 (p < 0.05). In addition, the Shannon diversity indices increased along the sampling sites (from B1 to B6) during both sampling periods, from 1.2 to 1.9 in June 2007 and from 1.1 to 2.9 in May 2008. It was well known that the bacterial community diversity changes with its habitat conditions (LaPara et al., 2002). For example, heavy organic contamination results in the dramatic decrease in community diversity (Li et al., 2007). In this study, the bacterial diversity increased with time (Fig. 4) following the decrease in the metal concentrations (Fig. 3). When compared with other studies,

3.5 Shannon diversity index

3.3. Biomass characteristics

May-08

3

Jun-07

2.5 2 1.5 1 0.5 0 B1

B2

B3 B4 Sampling sites

B5

B6

Fig. 4. Changes in Shannon diversity indices of bacterial communities at different sampling sites (B1–B6) during June 2007 and May 2008.

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the bacterial communities in the bioreactor were very diverse. For example, the Shannon diversity index in the membrane bioreactor (MBR) and the combination of MBR and Hybrid MBR treating wastewater of similar loadings were on average 0.82 and 1.3–1.6 during 100-day operation (Miura et al., 2007; Stamper et al., 2003). This is less than half the community diversity observed in our study. 3.5. Benefits of no sludge discharge system Highly concentrated sludge (as slurry liquid) was discharged into the photoautotrophic system during July 2007 and March 2008, with the volumes estimated based on the pump flux and time to be approximately 22 and 43 m3, respectively. However, it was observed that the sludge disappeared within one week after being discharged into the photoautotrophic system of the hybrid ‘bioreactor’, thereby avoiding key environmental issues (such as toxic sludge pollution) associated with the current wastewater technology (i.e., mainly based on the A/O fluidized beds). In general, sludge treatment systems involve high costs, ranging from 20% to 60% of the total operating cost of the wastewater treatment plants (Uggetti et al., 2010). However, in the photoautotrophic system, aerobic conditions prompted the growth of aerobic microorganisms and ultimately improved the sludge mineralization (Nielsen, 2005). Moreover, the treatment of sludge by the photoautotrophic bioreactor might allow the wastes to be converted into a by-product such as organic fertilizer or soil conditioner suitable for the growth of native microbes and macrophytes (Uggetti et al., 2010). The discharge of the concentrated sludge into the photoautotrophic system further supplied the nutrients and provided a habitat for microbes, thereby enhancing the diversity and removal efficiency of the hybrid bioreactor. 4. Conclusion This study suggests that the proposed hybrid bioreactor affords a practical solution for simultaneously removing Cd and Hg from non-point source wastewater and concurrently culturing heterotrophic and autotrophic microorganisms. The diverse bacterial communities in the bioreactor strongly controlled the output water quality. The photoautotrophic system ‘ingests’ the sludge discharged from the A2/O process, which in turn could become one of the most suitable treatment technologies for not discharging contaminated sludge. The system was simple in terms of construction, operation and maintenance; therefore, this technology will be suitable in industrial parks to remove Cd and Hg from non-point source wastewater. Acknowledgements This work was supported by the Doctorate Fellowship Foundation of Nanjing Forestry University, the Innovative Project of Chinese Academy of Sciences (KZCX2-EW-QN401), the National Natural Science Foundation of China (41171363 and 41030640) and the Natural Science Foundation of Yunnan, China (2009CC006). References Afkhami, A., Saber-Tehrani, M., Bagheri, H., 2010. Simultaneous removal of heavymetal ions in wastewater samples using nano-alumina modified with 2,4dinitrophenylhydrazine. Journal of Hazardous Materials 181, 836–844. Aguado, J., Arsuaga, J.M., Arencibia, A., Lindo, M., Gascón, V., 2009. Aqueous heavy metals removal by adsorption on amine-functionalized mesoporous silica. Journal of Hazardous Materials 163, 213–221. APHA-AWWA-WEF, 1998. Standard Methods for Examination of Water and Wastewater, 20th ed. APHA, AWWA, and WEF, Washington DC.

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