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Heavy metal removal from aqueous solution by wasted biomassfrom a combined AS-biofilm process

W.C. Chang a,*, G.S. Hsu a, S.M. Chiang b, M.C. Su c

a Department of Environmental & Safety Engineering, National Yunlin University of Science and Technology, Touliu, 640 Yunlin, Taiwanb Science Park Administration, Hsinchu 300, Taiwan

c Graduate Institute of Environmental Policy, National Dong Hwa University, Hualien 974, Taiwan

Received 10 February 2005; received in revised form 14 June 2005; accepted 15 June 2005Available online 19 August 2005

Abstract

This study evaluated the capability of metal biosorption by wasted biomass from a combined anaerobic–anoxic–oxic (A2O)-bio-film process with simultaneous nitrogen and phosphorus removal. Zinc, cadmium and nickel were rapidly adsorbed in 20 min by theharvested sludge from a continuous-flow pilot-plant. Biosorption equilibrium was then reached in 6 h. The biosorption isothermshowed that metal biosorption behavior had fitted well to the Freundlich isotherm, but not Langmuir isotherm. The capacity con-stants k of Freundlich model for nickel, zinc and cadmium were 0.471, 0.298 and 0.726, respectively; the affinity constants 1/n were0.444, 0.722 and 0.718, respectively. The order of metal affinity for the wasted biomass was Zn > Cd > Ni, which was in conformityto the other biosorption results with different biological sludge.Ó 2005 Elsevier Ltd. All rights reserved.

Keywords: Wasted sludge; Extracelluler polymer; Metal removal; Biosorption; Wasteweater treatment

1. Introduction

The presence of heavy metals in excess amount inter-feres with many beneficial uses of the water because of their toxicity and biomagnification effect on ecology;therefore, controlling the concentrations of these sub-stances is frequently desirable. Chemical precipitation,ion exchange, electrolysis and reverse osmosis are thecommon conventional treatment processes to removal

heavy metals from dilute aqueous solution. However,these processes usually require high capital and opera-tion costs. Biosorption of heavy metals by wasted sludgefrom a biological wastewater treatment process there-fore exhibited a potential alternative to the existingmethods (Volesky, 1990; Su et al., 1995). In general,

the capacities of heavy metal uptake by the sludges var-ied significantly for different types of biological treat-ment processes.

The anaerobic–anoxic–oxic (A2O) activated sludgeprocess has been currently modified from the conven-tional activated sludge process to simultaneouslyremove nutrients, i.e., nitrogen and phosphorus, inwastewater, which will otherwise be the critical nutrientfor eutrophication of closed water body. The anaerobic

and anoxic zones of this biological nutrient removal(BNR) process selectively favor the floc-forming micro-organisms, i.e., phosphate accumulating organisms(PAOs), denitrifying organisms (DNOs), and discouragethe possible filamentous microorganisms; therefore, theanaerobic and anoxic zones are usually termed as anaer-obic and anoxic selectors, respectively (Wanner, 1994).

Floc-forming microorganisms in activated sludgeflocs carried a substantial amount of negatively chargedextracellular polymers (ECPs) that can adsorb a variety

0960-8524/$ - see front matter Ó 2005 Elsevier Ltd. All rights reserved.doi:10.1016/j.biortech.2005.06.011

* Corresponding author. Tel.: +886 5 5342601; fax: +886 5 5312069.E-mail address: [email protected] (W.C. Chang).

Bioresource Technology 97 (2006) 1503–1508

mailto:[email protected]

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of metal ions (Lawson et al., 1984; Norberg and Pers-son, 1984; Geesey and Jang, 1989). Potential interactingmechanisms of metals with ECP has been intensively re-viewed and the removal of metal ions from solution bythis biological material is frequently termed biosorption(Gadd, 1992). With the selection function of enriching

ECP-producing bacteria by anaerobic and anoxic selec-tors, a BNR process would provide high capacity of adsorbing heavy metals.

Recently, a novel hybrid process combining the A2Oactivated sludge process and RBC (rotating biologicalcontactor) biofilm, i.e., the combined AS-biofilm pro-cess, was designed to solve the conflict of requirementson sludge retention time (SRT) for PAOs and nitrifiersin conventional A2O process (Su and Ouyang, 1996;Chuang et al., 1998a). That is, in such an A2O processnitrifying organisms need a longer SRT for preventingwashout of the system while PAOs require shorterSRT to improve removal efficiency by wasting more

sludge. The performance and advantages of the AS-bio-film process, which is also called TNCU (Taiwan Na-tional Central University) process, were extensivelydiscussed (Su and Ouyang, 1997; Chuang et al., 1998b;You et al., 2000). Since microorganisms grown on thebiofilm attached the substratum by their ECP, thesloughing biomass from the biofilm may be capable of adsorbing a variety of heavy metals. Therefore, theA2O and RBC combined process potentially enrichedECP-producing organisms and the wasted biomass fromthe process could be an efficient adsorbent for heavymetals.

Although a variety of specific microbial biomass (Sagand Kutsal, 1995; Boyer et al., 1998; Ucun et al., 2002)and waste sludge from conventional biological process(Arican et al., 2002; Bux et al., 1999; Cheng et al.,

1975) have demonstrated substantial biosorption of sol-uble metals in aqueous solution, little information isavailable on biosorption capability of wasted biomassfrom the combined AS-biofilm process. Cheng et al.(1975) reported that in a complex system such as thatof the activated sludge process, direct application of the-

oretical solubility products may not be appropriate. Nel-son et al. (1981) demonstrated that calculated solubilitygenerally differed even two or more orders of magnitudefrom experimental determinations. The objective of thiswork was, therefore, to evaluate the biosorption capa-bility of biomass from a continuous-flow AS-biofilmpilot-plant on cadmium, zinc and nickel via conductinga series of biosorption batch tests. Since sludge mixedliquor contains several constituents, special emphasiswas placed on the isolation of precipitation effect of metal ions in solution during batch tests. The metalsorption data were also fitted to the Freundlich isothermmodel so as to compare the affinity of these three metals

on BNR sludge by using the Freundlich constants.

2. Methods

2.1. Description of the combined AC-biofilm system

Waste biomass used for biosorption tests washarvested from a continuous-flow AS-biofilm combinedpilot-plant (Fig. 1), installed in a 20 °C constant-temper-ature laboratory. Synthetic wastewater at a constantflow rate of 220 ml/min was continuously fed with a

pump to the reactor in which the anaerobic:anoxic:oxicvolume ratio was 1:2:3. All the basins were constructedfrom an amber acrylic polymer and all zones of reactorswere completely stirred with agitators or diffusers to

sludge recycle pump

blower oxic zone

anaerobiczone

DO pH

DO

AC

pH

pH

AIR

DO

AIR

caustic solution

effluent

clarifier

wasted sludge

Timer

Influent

anoxiczone

AIT AIT

AS

waste sludgepump

M M M

mixed liquor recycle pump

Fig. 1. Schematic diagram of the combined AS-biofilm pilot-plant.

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facilitate reaction and suspension of mixed liquor. Flowfrom anaerobic zone through anoxic, oxic zones to sec-ondary clarifier was by gravity. Total volume of reactorswas 130 l and total hydraulic retention time was 10 h.Ten RBC sets (each with 32 cm in diameter) were in-stalled in the aeration tank. Total surface area of RBC

was 1.6 m2

, with 40% submerged beneath the water.The recycle ratios of return sludge and mixed liquorwere 0.5 and 2.5, respectively, and the F/M ratio wassteadily maintained at 0.332 g COD/g MLSS/day. Ex-cess sludge was removed by discharging mixed liquorfrom the oxic zone of reactor to maintain a sludge reten-tion time of 10 days. pH in the oxic zone was automat-ically maintained at 7.0 ± 0.2 by NaOH–NaHCO3

solution. The DO concentration in the oxic zone waskept at 2 mg/l.

Table 1 shows the composition of the synthetic waste-water. It had total COD (TCOD) 300 ± 10 mg/l, totalBOD (TBOD) 210 ± 20 mg/l, total nitrogen (TN)

40 ± 6.0 mg/l, ammonium nitrogen 20 ± 2.0 mg/l, totalphosphorus (TP) 5 ± 0.5 mg/l and pH 7.0 ± 0.2.

2.2. Batch sorption test

Mixed liquor samples from the oxic zone of the hy-brid process were harvested for the sorption experimentsof cadmium, zinc, and nickel. A series of batch experi-ments with initial metal concentrations 10, 5, 3, 1, and0.3 mg/l were conducted at 20 °C to determine the sorp-tion isotherms. Metal uptake experiments were per-formed by batch reactors (250 ml flasks) in a shaker

bath. MLSS concentration of the harvested sludge wasaround 2000 mg/l with pH 7.0. Precipitation effect of metals in the batch reactors was assessed by monitoringthe metal concentration in control batch reactors con-taining only the filtrate from the wasted sludge. The fil-trate of the sludge was obtained by filtering theharvested activated sludge with a 0.45 lm membrane fil-ter. Soluble metal concentrations were determined by aLEEMAN PS1000 ICP. Standard Method (APHA,1989) techniques were used for all other wastewateranalyses.

3. Results and discussion

3.1. Process performance of the combined AS-biofilm

system

Steady-state performance of the AS-biofilm BNR pi-

lot-plant was achieved after more than three months of continuous operation. Operating parameters of the benchscale pilot-plant are summarized in Table 2. Fig. 2 de-picted the COD, TN, TP variation in the pilot-plant.Anaerobic phosphate release and its oxic uptake behaviorindicated that PAOs were successfully enhanced in thesystem and decline of TN from anaerobic zone to anoxiczone implied cultivation of DNOs. Since denitrificationoccurred in the anoxic zone with phosphate uptake, den-itrifying PAOs (DNPAOs) also existed in the BNR sys-tem. This showed that ECP-producing floc-formers, i.e.,PAOs and DNOs, were successfully cultivated in theAS-biofilm pilot-plant. Sludge mixed liquor from the oxic

zone of steady-state AS-biofilm system was then obtainedfor the biosorption batch tests.

Table 1

The constituents of synthetic wastewater

Constituentsa Dosage (mg)

Full-fat dry milk powderb 163.2Sucrose 16.2Acetate 37.6KH2PO4 15NH4Cl 40Urea 30FeCl3 0.1NaOH For neutralizing

a The constituents were dissolved in 1 l distilled water.b Average components are protein 26.5%, lactose 36.8%, fat 28%,

mineral 5.7% and water 3%.

Table 2Operating parameters and average values for the bench scaleAS-biofilm system

Parameter Value

Influent flow rate (ml/min) 220Ratio of return sludge (r) 0.5Ratio of supernatant (R) 2.5SRT (day) 10Mean HRT of anaerobic basin 1.67

Mean HRT of anoxic basin 3.33Mean HRT of aerobic basin 5Anaerobic basin ORP (mv) À300 to À350Anoxic basin ORP (mv) À270 to À250Aerobic basin pH 6.8–7.2MLSS (mg/l) 2200MLVSS/MLSS 0.85–0.88

F/M (g COD/g MLSS day) 0.332

0

50

100

150

200

250300

350

400

I An Anox Ox

C O D

( m g / L )

0

5

10

15

20

25

30

35

40

45

P O 4 3

- P , T

N

( m g / L

)

COD

PO43- -P

TN

-

Fig. 2. COD, TN and P variation in the pilot-plant (I: influent, An:anaerobic zone, Anox: anoxic zone, Ox: oxic zone).

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3.2. Time course of metal uptake

Removal kinetics of heavy metals by wasted sludgewas firstly studied in batch reactors with initial metalconcentration of 10 mg/l. Fig. 3 depicted the time courseof the metal mass adsorbed per unit mass of wasted bio-

mass. All the three metals exhibited two stages of adsorption mechanism proposed by Lawson et al.(1984) and Brown and Leaster (1982), i.e., the rapid up-take within the first stage corresponded to the passiveuptake and slow uptake of the second stage correlatedto be metabolism-dependent intracellular uptake. Morethan 80% of cadmium and nickel biosorption was com-pleted within the first 20 min, i.e., the first stage; how-ever, zinc apparently was uptaken less (36%) in thefirst stage. Further, 90% of zinc uptake was not accom-plished until 90 min; still, biosorption equilibrium of thethree metals was slowly achieved in 6 h. All batch bio-sorption tests were, therefore, performed with 6 h of

contact time between heavy metals and BNR sludge.

3.3. Metal speciation in batch reactors

Heavy metals could be removed in batch reactorsthrough both biosorption and precipitation. In an at-tempt to isolate the biosorption effect from metal precip-itation, the speciation of metals in the batch reactorsshould be considered. In batch reactors, total metalmass can be differentiated to its species as the following:

MT ¼ MS1 þ MB þ MP ð1Þ

where MT is total mass of metals, MS1 is mass of metalsin solution, MB is mass of biosorbed metals, and MP ismass of precipitated metals. Since simply MS1 could beexperimentally analyzed in the above Eq. (1), controlbatch reactors containing only the filtrate from thewasted sludge were conducted. The mass balance on

the control reactors where only precipitation occurredwas

MT ¼ MS2 þ MP ð2Þ

where MS2 is mass of metals in solution in control reac-tors. Combining Eqs. (1) and (2) yield the following

equation in which the biosorbed fraction of metals couldbe obtained:

MB ¼ MS2 À MS1 ð3Þ

Fig. 4 showed the distribution of metals in the BNRsludge for the total metal concentration of 5 mg/l. Pre-cipitation effects contributed significantly to total metalremoval due to the complexity of the sludge mixedliquor. Among the three tested metals, precipitation inthe cadmium batch reactor exhibited the most signifi-cant effect, i.e., 24% of the total cadmium. Besides, batchtests with higher initial metal concentration demon-strated higher precipitation amount. Nevertheless, as is

shown in Fig. 5, higher precipitation fractions of totalmetal were observed in batch tests with lower initial me-tal concentration (e.g., 0.3 and 1 mg/l). That is, precipi-tation effect impact was more on tests of lower initialmetal concentration than higher ones. The substratefed to the biological wastewater treatment process

0

0.5

1

1.5

2

2.5

0 100 200 300 400

Time (min)

m g m e t a l b i o s o r p t i o n

p e r g M L S S

Ni

Zn

Cd

Fig. 3. Time course of metal biosorption.

Precipitated14%

Dissolved48%

Sorbed38%

(a)

Dissolved63%

Precipitated13%

Sorbed24%

(b)

Precipitated24%

Sorbed52%

Dissolved24%

(c)

Fig. 4. Metal distribution in the AS-biofilm sludge (total concentra-tion for each metal = 5 mg/l): (a) nickel, (b) zinc and (c) cadmium.


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should include substantial organic and inorganic nutri-ents for cell synthesis. The mixed liquor from the aera-tion tank could contain cytoplasmic material fromcells lysis also because the whole system should operateunder long sludge retention time. In the tested AS-bio-film process with nitrogen and phosphorus removal, an-

oxic denitrification required sufficient nitrification in theoxic zone. Since nitrification process consumed alkalin-ity, caustic solution supplemented to aeration tankmight further formed metal hydroxide and enhancedprecipitation effect. These confounding phenomena ac-counted for higher precipitation behavior in batch reac-tors with sludge mixed liquor as biosorption matrix.These findings implied that performing biosorption testby using activated sludge from wastewater treatmentsystems should carefully examine the precipitation effectso as not to overestimate the biosorption behavior.

3.4. Freundlich isotherm of metal biosorption

Precipitated portions were isolated by the prior meth-od to obtain the actual adsorbed quantity of metal bythe waste biomass. Fig. 6 compares the biosorption iso-therms of nickel, zinc and cadmium for AS-biofilm bio-mass. The AS-biofilm biomass demonstratedsignificantly higher biosorption amount on cadmiumthan on zinc and nickel; whereas there was not much dif-ference for biosorption of nickel and zinc.

Two models, Freundlich and Langmuir equations,are frequently applied for evaluating the biosorptionbehavior of heavy metals on activated sludge. The Fre-

undlich isotherm, commonly used to describe theadsorption of solutes from dilute solution on adsorbent,can be expressed as

MB=X ¼ kC 1=n ð4Þ

where MB/X is mg metal biosorbed per g of MLSS, C isequilibrium concentration of metals in solution (mg/l), k

is constant related to capacity, and 1/n is constant re-lated to affinity. This non-linear equilibrium equationcan be linearized to determine the Freundlich constantsfrom the slope (1/n) and intercept (log k ) by plottingMB/X vs. C on double logarithmic paper.

The same data depicted in Fig. 6 showed straight lineon double logarithmic paper (figure not shown), hencethe biosorption behavior of the three metals could beconcluded to closely follow the Freundlich isothermmodel. Statistical tests (ANOVA F -test) revealed that

these simple linear regressions were significant(a = 0.05) for all the three metals. Table 3 summarizedthe Freundlich isotherm constants and the related statis-tical test results for metal biosorption on wasted AS-bio-film biomass. The capacity constants k of the Freundlichmodel for nickel, zinc and cadmium were 0.471, 0.298and 0.726 and the affinity constants 1/n were 0.444,0.722 and 0.718, respectively. Furthermore, the sameexperimental data failed to fit well to the Langmuirmodel after plotting 1/(MB/X) vs. 1/C to determinethe Langmuir constants from the slope and intercept.

The removal of heavy metals by sludge from waste-

water is influenced by several factors such as initial

0% 20% 40% 60% 80% 100%

10

5

3

1

0.3

I n i t i a l Z n c o n c e n t r a

t i o n ( m g / L )

Distribution of Zn

Dissolved

Precipitated

Sorbed

Fig. 5. Distribution of zinc at different initial concentrations.

-1.5

-1.2

-0.9

-0.6

-0.3

0

0.3

0.6

0 2 4 6 8

Equilibrium metal concentration (mg/L)

L o g ( M B / X )

( m g m e t a l b i o s o r p t i o n / g M L S S )

Ni

Cd

Zn

Fig. 6. Comparison of biosorption of metals by the AS-biofilmbiomass.

Table 3Freundlich isotherm constants for metal biosorption

Freundlich constants R2a p-Valueb

1/n k

Cd 0.718 0.726 0.91 0.01143Zn 0.722 0.298 0.91 0.01148Ni 0.444 0.471 0.85 0.02653

a Coefficient of determination.b p-Value for testing significance of regression.

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metal concentration (Cheng et al., 1975), pH (Nelsonet al., 1981), temperature (Sag and Kutsal, 1995), sludgetypes (Bux et al., 1999), precipitation effects (Aricanet al., 2002; Su et al., 1995), etc. The adsorption of heavymetals between different sludges should be compared onthe same evaluation basis. Previous studies focused

more on comparing the adsorption affinity of some spe-cific sludge on different metals, rather than comparingthe metal adsorption from different biomass.

According to the result of Freundlich model, cad-mium showed better affinity to BNR sludge than nickel.The sequence of biosorption affinities for metals Cd andNi found in this study was consistent with the sequencereported by Brown and Leaster (1979) where activatedsludge was utilized as an absorbent. Metal affinities bycells of K. aerogenes found by Brown and Leaster(1982) also demonstrated similar results, Cd > Co > Ni.Su et al. (1995) compared the ability of metal sorptionbetween aerobic selector activated sludge system and a

conventional completely stirred tank reactor (CSTR)system. The affinity of the two sludges from the experi-mental results of Su et al. (1995) exhibited the same re-sults with this study, i.e., Zn > Cd > Ni.

The biosorption affinity of CSTR sludge on Cd, Niand Zn were 0.56, 0.72 and 0.77, respectively as wasreported by Su et al. (1995). AS-biofilm sludge had ahigher biosorption affinity on Cd than CSTR sludge;nevertheless, less Ni biosorption was obtained by AS-biofilm sludge than by CSTR sludge. That is, differentsludge could have different biosorption affinity on met-als, although AS-biofilm sludge was supposed to pro-

vide higher metal biosorption.

4. Conclusion

Zinc, cadmium and nickel were rapidly adsorbed in20 min, i.e., passive uptake by the harvested sludge froma continuous-flow AS-biofilm BNR pilot-plant, fol-lowed by a slow active uptake. The sorption isothermshowed that metal biosorption behavior fitted well tothe Freundlich isotherm. The order of metal affinityfor AS-biofilm sludge was Zn > Cd > Ni. Precipitation

effects of metals obviously should be carefully examinedand isolated during biosorption batch tests with sludgemixed liquor so as to prevent overestimating the bio-sorption behavior.

Acknowledgements

The authors would like to thank the National ScienceCouncil of Taiwan (ROC) for financially supporting thisresearch under contract no. NSC-88-2211-E-182-002.

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