Environ. Sci. Technol.

2009 43, 93549360

A Novel Combination of Anaerobic

Bioleaching and Electrokinetics for
Arsenic Removal from Mine Tailing
Soil
KEUN-YOUNG LEE, IN-HO YOON,
B Y U N G - T A E L E E , S O O N - O H K I M , * , A N D
K Y O U N G - W O O N G K I M * ,
Department of Environmental Science and Engineering,
Gwangju Institute of Science and Technology (GIST),
Gwangju 500-712, Republic of Korea, Department of
Chemistry and Geochemistry, Colorado School of Mines,
1500 Illinois Street, Golden, Colorado 80401, and Department
of Earth and Environmental Sciences and Research Institute
of Natural Science, Gyeongsang National University,
Jinju 660-701, Republic of Korea

Received June 7, 2009. Revised manuscript received

October 23, 2009. Accepted October 24, 2009.

This study provides evidence that a hybrid method integrating

anaerobic bioleaching and electrokinetics is superior to
individual methods for arsenic (As) removal from mine tailing
soil. Bioleaching was performed using static reactors in batch
tests and flow conditions in column test, and each test was
sequentially combined with electrokinetics. In the bioleaching,
indigenous bacteria were stimulated by the injection of
carbon sources into soil, leading to the mobilization of As with
the concurrent release of Fe and Mn. Compared with the batchtype bioleaching process, the combined process showed
enhanced removal efficiency in the equivalent time. Although
the transport fluid bioleaching conditions were inadequate for As
removal, despite long treatment duration, when followed by
electrokinetics the combined process achieved 66.5% removal
of As from the soil. The improvement of As removal after
the combined process was not remarkable, compared with
single electrokinetics, whereas a cost reduction of 26.4% was
achieved by the reduced duration of electrokinetics. The As
removal performance of electrokinetics was significantly
dependent on the chemical species of As converted via microbial
metal reduction in the anaerobic bioleaching. The synergistic
effect of the combined process holds the promise of significant
time and cost savings in As remediation.

Introduction
The introduction of arsenic (As) into the environment has
significantly adverse effects and the major sources are mining
and smelting operations, As-containing pesticides and
herbicides, and various industrial activities that use As (1).
Concern has been raised, particularly in some South Asian
countries, over the danger represented by As-contaminated
* Address correspondence to either author. Phone: +82-55-7516275 (S.O.K.); +82-62-970-2442 (K.W.K.). Fax: +82-55-757-2015
(S.O.K.); +82-62-970-2434 (K.W.K.). E-mail: sokim@gnu.ac.kr (S.O.K.);
kwkim@gist.ac.kr (K.W.K.).

Gwangju Institute of Science and Technology (GIST).

Colorado School of Mines.

Gyeongsang National University.

9354

ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 43, NO. 24, 2009

groundwater due to its potential for immediate human

exposure (2, 3). Biotic and abiotic processes can easily
transform immobile or insoluble As into a soluble form under
environmental conditions (4, 5), thereby allowing As in the
soil to enter the groundwater and eventually the food chain.
Therefore, active remediation of As-contaminated soils is of
great importance and such strategies fall into two main
categories: chemical solidification/stabilization (6) and separation processes by washing/flushing, electrokinetics, and
phytoremediation (7, 8).
Anaerobic As bioleaching, which has been represented
by microbial metal reduction, is ubiquitous in subsurface
environments (1, 9-12), including mining-impacted areas
(5, 13-16). In our recent works, the dissolution of As, along
with Fe and Mn, under anaerobic conditions was significantly
enhanced by activating the indigenous bacteria in several
tailing soils collected from different sites, although the extent
of mobilization varied depending on the forms of As, the
original biomass, and the utilized carbon sources (15, 16).
Though such a phenomenon could be interpreted as an
extension of As contamination, from a different viewpoint,
it could be applied as an active remediation technique for
the microbial extraction of As from soils, such as the
previously reported examples of microbial Fe and Mn
reductions for other heavy metals (17, 18). Because As
associated with such Fe and Mn (hydro)oxides forms a high
proportion in tailing soils, as well as other As-contaminated
soils, anaerobic bioleaching is favorable to mobilize As from
soils.
Although electrokinetic remediation technology has been
shown in laboratory and field studies to be a promising
method for simultaneously recovering multiple metal contaminants, the mobility and removal efficiency of As can be
low relative to other heavy metals (19, 20). In common
environments, the major As species are oxyanions; As(V) as
H2AsO4- and HAsO42-, As(III) as H2AsO3-, and a neutral
hydroxy complex, As(III) as H3AsO30. Due to the specific
characteristics of these species, their mobility is affected by
pH and the valence states, more so than with other heavy
metals, which introduces some difficulties in As removal using
electrokinetics and other techniques. Thus, the development
of remediation technology specifically focused on As removal
in soils is a priority. As(III) is more mobile than As(V) in
nature, and the redox chemistry of As needs to be considered
in any attempt to elevate the applicability of electrokinetics.
Generally, anionic and neutral forms of As migrate toward
the anode and cathode, respectively, in electrokinetics. To
achieve the desired process efficiency and system performance, several studies have reported enhancement schemes
via electrolyte conditioning (7, 21, 22). Based on the results
of these studies, alkaline conditions appear the most favorable
for As electromigration, with the drawback that As migration
is very slow and time-consuming (19).
Currently, most combinations of electrokinetics and
bioremediation, termed bioelectrokinetics, have been used
to introduce microorganisms, water, and nutrients into lowpermeability soil by applying an electric field to enhance the
biodegradation of organic pollutants (23). While this approach
has been actively studied, little research has focused on
combination approaches for heavy metal contaminants,
probably due to the nondegradable nature of heavy metals.
Maini et al. (24) first reported microbially enhanced electrokinetic remediation for the removal of a heavy metal, in
which soils artificially contaminated by Cu were treated by
the sequential application of aerobic bioleaching and electrokinetics. Although their study demonstrated the ap10.1021/es901544x CCC: $40.75

2009 American Chemical Society

Published on Web 11/05/2009

FIGURE 1. Experimental scheme of the individual and combined processes.

TABLE 1. Experimental Conditions, Removal Efficiency, and Mass Balance of the As Removal Processes
bioleaching
experiment

comment

type

electrokinetics

duration current
(days) (mA)

voltage (V)

duration power consumption total As

(days)
(kWh/ton)
removal (%) recovery (%)c

until 2 days after 2 days

control
1
2
3a
control
4
5
6b

no carbon
batch BL only
batch BL only
batch BL and EK
no carbon
column BL only
EK only
column BL and EK

batch
batch
batch
batch
column
column
column

14
8
20
8
20
28
28

10

43.2 ( 21.5

3.9 ( 2.3

12

74.3

10
10

45.4 ( 16.9
62.9 ( 32.7

3.9 ( 2.4
4.4 ( 2.9

44
16

150.9
111.1

3.88
31.1 ( 4.7
35.0 ( 2.7
68.2 ( 6.3
0.38
17.3 ( 15.6
63.6 ( 2.3
66.5 ( 3.7

98.3
105.7
97.6
97.0

The soil pretreated by batch-type bioleaching was transferred into the electrokinetic soil cell. b The soil cell used in the
column-type bioleaching experiment was directly connected with electrode compartments in the electrokinetic apparatus.
c
Recovery ) (amount of As in both electrolytes/amount of As removed from soil) 100.

plicability of the electrokinetic process for the removal of

heavy metals through the amendment of the soil using
inexpensive sulfur addition, the decreased soil pH induced
by bacterial sulfur oxidation, while suitable for normal heavy
metals, is not suitable for As, as mentioned above.
In the present study, therefore, the combination of
anaerobic bioleaching and electrokinetic remediation was
applied to highly As-contaminated mine tailing soils. Bioleaching was performed using static reactors in batch tests
and flow conditions in column tests, and each test was
sequentially combined with electrokinetic treatment. The
main study objectives were to evaluate the process efficiency
of both the combined process and its individual components
in terms of As removal and cost expenditure, and to
investigate the effects of the accompanying geochemical and
microbial transformations of As on the process efficiency.

Experimental Section
Soil. As-contaminated mine tailing soil was taken from the
abandoned Songcheon gold mine located in the mideastern
region of the Korean Peninsula. Collected at a depth of 0-30
cm from the surface of the tailing-dumping area, a composite,
representative sample was prepared by mixing five samples
taken within a 10 m2 area and the sample was stored without

drying to ensure survival of the indigenous bacteria. The

tailing soil was predominantly sandy loam (soil texture
according to the U.S. Department of Agriculture) with a 0.89%
mass loss on ignition (400 C for 24 h) and pH 5.7-6.2 (5 g
soil in 50 mL water). The Fe/As minerals in this soil were
arsenopyrite (FeAsS) as the primary mineral and scorodite
(FeAsO4 2H2O) as the secondary mineral (see Supporting
Information (SI) Figures S1 and S2), with a total As concentration of 4,023 ( 71 mg kg-1.
Bioleaching Batch Experiments. A diagram of the individual and combined processes is shown in Figure 1 and all
As removal and control experiments are summarized in Table
1. Three hundred grams of the soil sample were mixed with
300 mL of leaching solution, containing 100 mM of glucose
and lactate, at a ratio of 2:1 (v/v) as carbon sources, and the
pH of the solution was adjusted to 7 using 0.1 M NaOH.
This mixture was placed in two rectangular, polypropylene,
1.2 L, bioleaching reactors, agitated in a rotating shaker (180
rpm) at 30 C under anaerobic conditions for 8 days
(experiments 1 and 3) and 20 days (experiment 2), with
distilled water but without carbon sources as a control. All
experiments repeated in triplicate. Following these experiments, soil samples were taken directly from the soil bed for
further analysis.
VOL. 43, NO. 24, 2009 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

9355

Bioleaching Column Experiments. Arsenic was removed

under transport conditions in duplicate using a cylindrical
column (20 cm length, 4 cm diameter) packed with soil for
a total mass of 370 ( 5 g (bulk density ) 1.47 ( 0.05 g cm-3),
with the same 10 mM carbon source used in the batch
experiments, and deoxygenated by constant N2 purging. The
influent at the bottom of the column had a continuous flow
of 18.2 mL h-1 (4.1 pore volume/day, pore water velocity )
1.45 cm h-1) for 28 days (experiments 4 and 6), and the control
had distilled water as the influent. The process performance
was monitored periodically by collecting the effluent and
measuring the pH, Eh, and concentrations of free As, Fe, and
Mn. After treatment, the soil cell was divided into four sections
for sample collection (Figure 1B).
Electrokinetic Experiments. Two experiments combining
the bioleaching and electrokinetic processes (experiments 3
and 6) and one using only electrokinetics (experiment 5)
were performed for the specified durations. A soil sample of
batch-type bioleaching that had been pretreated for 8 days
was transferred into the electrokinetic soil cell in experiment
3 (Figure 1A and C), by discarding the leaching solution. The
column bioleaching apparatus was initially designed to be
connected to the electrode compartments (Figure 1B and
C). Experiment 5 was conducted using electrokinetics without
any bioleaching pretreatment. Apart from these variations,
the experimental conditions of the three electrokinetic
applications were the same.
For electrical applications, the cathodes were stainless
steel and anodes titanium-coated stainless steel. Mesh-type
electrodes lined with filter paper to allow the passage of ions
and water were located between the soil cell and electrode
compartments. Each electrode compartment was connected
to an electrolyte reservoir, and the solutions were circulated
by peristaltic pumps (Figure 1C). In all experiments, 0.1 M
Na2CO3 and 0.1 M NaOH were used as the anolyte and the
catholyte solutions, respectively. Such a combination of
electrolytes has been shown to promote the As removal
efficiency in contaminated field soils from our previous
research (7) and by others (21). The electrolyte solutions were
refreshed regularly to maintain consistent pH conditions. A
current density on the electrode surface area of 0.79 mA
cm-2 was applied with monitoring of the voltage changes of
the soil cell. Both electrolyte solutions were periodically
collected to analyze the amount of accumulated As in both
electrode compartments. After electrokinetic processing, soil
samples were obtained from the four soil bed sections to
determine the residual concentrations of As and the final
soil pH. The pore water samples were also collected from
each section and passed through a silica-based, anionexchange resin (LC-SAX SPE Tube, Supelco) to separate the
anionic and neutral forms of As (25). The As passing through
the resin was regarded as neutral As, and anionic As
concentrations were calculated by subtracting the neutral
As from the total As.
Analytical Methods. The residual concentrations of As in
the soil after each experiment were investigated by digesting
the collected soil samples with aqua regia, composed of
concentrated HNO3 and HCl (1:3, v/v), and heated to 70 C
on a shaker for 1 h (26).
The chemical form of each As fraction in the tailing soils
was examined using a sequential extraction technique, as
suggested by Wenzel et al. (27). The sequential extraction of
Fe and Mn was originally suggested by Tessier et al. (28).
Although each corresponding fraction cannot be exactly
defined by each step in the sequential extraction, its results
can be used to speculate on the binding strength of As, Fe,
and Mn. As concentrations were determined using graphite
furnace-atomic absorption spectroscopy while flame-AAS
was used for Fe and Mn (see SI for the quality control of the
analysis).
9356

ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 43, NO. 24, 2009

FIGURE 2. Results of experiment 3. (A) Variation of soil pH

within 6 days at each section during electrokinetics, (B) final
soil pH after bioleaching process (BL) and combined bioleaching and electrokinetics (BL and EK) in the four sections of
the cell, (C) transported water volume in the cathode compartment by electroosmotic flow, and (D) accumulated As in
each electrolyte.
XANES Analysis. The speciation of As in the tailing soil
was investigated using X-ray absorption near edge structure
(XANES) spectroscopy (see SI for the detailed analytic
method).

Results
Batch Bioleaching and Electrokinetics. The final removal
efficiencies in terms of residual As concentrations in the
tailing soils from each experiment are presented in Table 1.
Compared to the abiotic control, a significant amount of As
leaching was observed with the batch-type bioleaching
simulating biotic processing stimulated by a carbon source
injection. Arsenic was moved to the leaching solution at 31.1
and 35.0% efficiency within 8 and 20 days, respectively.
Previous investigations have shown that the tailing soil used
here contained a relatively high fraction of bioavailable As
(16). The main As species in the leaching solution was As(III)
(up to 80%), which was attributed to the microbial reduction
of As(V) originally present in the soil. Twenty-day bioleaching
(experiment 2) did not show a significant improvement in
removal efficiency compared to 8 days (experiment 1),
suggesting that batch-type bioleaching reached a stationary
phase within 8 days (see SI Figure S3).
Compared with the single batch-type bioleaching, the
combined processes of bioleaching and electrokinetics
(experiment 3) showed significantly enhanced removal
efficiency (68.2%) in the same time (Table 1). The soils slightly
decreased pH of 5.2 after bioleaching pretreatment gradually
increased during the electrokinetic process, to exceed pH 12
by the end of the experiment. These highly alkaline conditions

FIGURE 3. Results of experiment 4 on column-type bioleaching

(BL) and control column (Cont). Variation in (A) pH and Eh of
effluent solution, (B) released amount of Fe and Mn, and (C)
removed amount of As from soil column.
resulted from the cathode production of hydroxide ions
reinforced by the added NaOH solution while the anodeproduced hydrogen ions were counteracted by the Na2CO3
solution. Migration of hydroxide ions gradually increased
the soil pH over time, progressing from sections 1 to 4 (Figure
2A and B). However, a buffering effect in the early stages
(within 4 days) degraded the As removal and the pH increase.
The anionic As electromigration was initiated after 4 days
(Figure 2D), at which time most of the As was rapidly removed
toward the anode while a small amount of neutral As was
transported toward the cathode by electroosmosis.
Column Bioleaching and Electrokinetics. Similar to the
batch bioleaching results, there was a significant difference
in As removal between the column-type bioleaching (experiment 4) and the control (Table 1). Furthermore, the pH and
Eh variations of the effluent solution were insignificant in
the control, which lacked a carbon source, while those of the
bioleaching experiments significantly decreased with time
(Figure 3). Although continuous N2 gas purging promoted
anaerobic conditions inside the soil column, no dissolution
of Fe, Mn, or As occurred for nearly 4 days, indicating a lag
phase for the initiation of anaerobic bioleaching in columntype processing. After 4 days, As removal progressed with
the release of both Fe and Mn. Up to 90% of the dissolved
Fe, Mn, and As was in a reduced form, Fe(II), Mn(II), and
As(III) (See SI Table S1), which corresponded with the
decreased Eh value.
Despite the significant dissolution of As in the columntype bioleaching process, the removal efficiency of As after
28 days remained inadequate (at 17.3%), whereas the
combined process (experiment 6) showed enhanced As
removal efficiency of 66.5% after continuous electrokinetic
treatment for 16 days (Figure 1B and C). In single electrokinetics for 44 days (experiment 5), the increase of soil pH
was efficiently driven, and the pH was increased from neutral
to 10-12 within 2 days (Figure 4A), which enabled the As

FIGURE 4. Results of experiment 5. (A) Variation of soil pH

within 6 days at each section during electrokinetics, (B) final
soil pH after single electrokinetics (EK) in the four sections of
the cell, (C) transported water volume in the cathode
compartment by electroosmotic flow, and (D) accumulated As
in each electrolyte.
removal to begin almost immediately and reach a final As
removal efficiency of 63.6% (Figure 4D). In both combined
and single treatments, the normal electroosmosis occurred
throughout the process, leading to the accumulation of small
amounts of neutral As in the catholyte solution (Figures 2C
and 4C).
Chemical Forms of Fe, Mn, and As. The results of the
sequential extraction of Fe and Mn showed that their oxide
fractions were significantly reduced after both anaerobic
bioleaching processes (Figure 5), which strongly indicates
that the indigenous bacteria, stimulated by the added carbon
sources, mainly utilized the oxide fractions of Fe and Mn as
electron acceptors. The results (see SI Figure S5) confirmed
that the As relative to such oxide fractions was removed from
the soil. Although the As fraction of the poorly crystalline
hydrous oxides remained in the soil after bioleaching, this
fraction was transformed into weakly bound forms which
were quickly removed in the electrokinetic steps. Such results
were reflected to the reduction of the treatment duration of
combined process, despite the total As removal efficiencies
of combined process and single electrokinetics were not
significantly different from each other.
As Speciation in Soil and Pore Water. The As species was
predominantly As(V) in initial tailing soil (Figure 6A). The
significant amount of As(III) transformed from As(V) in the
anaerobic bioleaching was reflected in the XANES peak as
a shoulder in front of the As(V) peak, and the As(III) in the
soil was sequentially removed in the electrokinetic step, as
indicated by the shrunken As(III) peaks. In examining the
distribution of residual As in the pore water collected from
each section, the results indicated that anionic and neutral
VOL. 43, NO. 24, 2009 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

9357

FIGURE 5. Accumulative concentrations (mg/kg) of Fe and Mn

by sequential extraction before and after bioleaching experiments. Each step of the sequential extraction was in terms
of the exchangeable fraction (step 1), carbonate and specifically adsorbed fraction (step 2), Fe-Mn (hydro)oxides (step
3), organic matter and sulfides (step 4), and the residual
fraction (step 5). Results of batch-type bioleaching (Batch BL)
for 8 days (8 d) and 20 days (20 d), and column-type bioleaching
(Column BL) at all sections (1, 2, 3, and 4).

FIGURE 7. Biogeochemical reaction model in (A) anaerobic

bioleaching and (B) electrokinetics.

FIGURE 6. As speciation in soil and pore water after

experiment 3. (A) Derivative As K-edge XANES spectra of the
As standard materials (As powder for As(0), sodium (meta)
arsenite (NaAsO2) for As(III) and sodium arsenate (Na2HAsO4
7H2O) for As(V)) and of the tailing soil before (Initial) and after
(BL) batch-type bioleaching, and all sections (1, 2, 3, and 4)
after batch-type bioleaching with electrokinetics, and (B)
distribution of anionic and neutral As concentrations in pore
water collected at all sections (1, 2, 3, and 4).
As were transported in electric fields toward the anode by
electromigration and toward the cathode by electroosmosis,
respectively (Figure 6B). In an alkaline environment (pH >
9), As(III) as well as As(V) predominantly exist as anionic
forms, and it was confirmed here that the dominant species
of As was anionic, migrating toward the anode.

Discussion
Reaction in Anaerobic Bioleaching. Direct evidence of
microbial reduction in anaerobic bioleaching was clearly
9358

ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 43, NO. 24, 2009

presented. The biogeochemical model in this step is presented here by extracting a reasonable reaction path from
previous suggestions (29, 30) (Figure 7A). The model consisted
of the tailing soil initially containing As, mainly As(V),
associated with Mn and Fe (hydro)oxides such as pyrolusite,
ferrihydrite, goethite, hematite, and magnetite. This initial
state was visually detected by spectroscopic analysis in a
previous investigation (see SI Figures S1 and S2). The injected
organic carbon was oxidized at the expense of such (hydro)oxides as electron acceptors, thus leaching Mn(II), Fe(II),
and As(III) into solution, as confirmed by the speciation
analysis conducted in this study and a previous investigation
(16). Some of the dissolved As(III) was separated by discarding
the solution from the soil, and a considerable portion of
residual As(III) was readsorbed onto the soil particle, as
detected in the XANES peak (Figure 6).
Reaction in Electrokinetics. The critical process in
electrokinetics for As removal from soil is the ligand exchange
reaction of hydroxide ions with anionic As. Moreover, the
mobilization of anionic As is enhanced by the increased
negative charge on the soil surface when the pore water pH
is above the point of zero charge (PZC) (31, 32). Anionic As
released from the soil migrates toward the anode in the
electric field. The dominant reaction in electrokinetics is
modeled in Figure 7B. This series of processes explains the
effect of the anaerobic bioleaching pretreatment in accelerating the As removal rate in the electrokinetic step. As
aforementioned, both As(III) (H2AsO3-) and As(V) (HAsO42-)
exist as oxyanions at pH > 9 and previous investigations have
reported the diffusion coefficient of H2AsO3- to be up to
three times higher than that of HAsO42- (diffusion coefficients
based on molar mobility, 1.03 10-9 m2s-1 and 0.32 10-9
m2s-1, respectively) (33). In other words, the transformation
of As(V) to As(III) by anaerobic bioleaching is preferable to
alkaline electrokinetic process. Even though the buffering
effect initiated by the bioleaching pretreatment was a side
effect that obstructed the increase of soil pH, the As
conversion through microbial metal reduction was clearly
sufficient to reduce the duration of electrokinetics owing to
the enhanced electromigration. The present study results
have demonstrated that the As removal performance of

electrokinetics is significantly dependent on the species and

chemical forms of As in the soil.
Beneficial Effects of the Combined Process. Table 1
shows the average voltages until 2 days and after 2 days, as
well as the power consumption in each electrokinetic
experiment. The electrical resistance and voltage across the
soil bed were high due to the initially dominant dissociation
and desorption mechanisms and, with the increasing dominance of the migration of hydroxyl ions and dissolved and/
or desorbed As species, the voltage gradually decreased. The
electrical energy per unit volume (E, kWh/m3) for electrokinetics was calculated by
E)

I(V)TR
vs

(1)

where I is the applied current, V the voltage, TR the

duration, and vs the soil volume. The power consumption
(kWh/ton) in Table 1 is based on a specific gravity of tailing
soil of 1.6 ton/cm3. At a power cost of $0.06/kWh, the
expenditures for electricity of experiments 5 and 6 are
$9.1 and $6.7 per ton, respectively. The 26.4% cost
reduction is achieved by the combination of electrokinetics
with column-type bioleaching. The extra cost for each
process does not markedly affect the cost effectiveness,
because both processes require the operation of two pumps
(for injection and extraction of leaching solution in columntype bioleaching, and for circulation of the two electrolytes
in electrokinetics) and only a small amount of chemicals
and water (for glucose/lactate in bioleaching, and NaOH/
Na2CO3 in electrokinetics).
On the other hand, a cost reduction of 50.5% was achieved
by using the combined process of electrokinetics and batchtype bioleaching. It is improper to compare this ex situ type
combination with single electrokinetics because of the
difference of extra cost. However, the significant reduction
of total process duration (20 days) achieved by using this
combination, as well as the slightly improved removal
efficiency (68.2%), proves its technical advantage.
In the bioleaching processes performed here, the use
of inexpensive carbon sources, with their less hazardous
effects compared with chemical washing, was a desirable
feature. The promotion of anaerobic bioleaching and the
significant enhancement of As mobility were clearly
demonstrated. However, the process drawbacks included
the ex situ nature of the batch-type bioleaching, despite
its rapidly achieved high efficiency, which decreased the
cost effectiveness in terms of the excavation and transportation of contaminated field soils. Moreover, single
processing by column-type bioleaching, used to simulate
in situ fluid conditions, exhibited low efficiency despite
the long treatment duration and mostly only increased
the mobility of solid phase As. We consequently concluded
that this technique was not appropriate for single flushing
treatments for As. On the other hand, the sequential
application of electrokinetic remediation incorporated with
in situ bioleaching demonstrated a capability to solve this
problem, with enhanced removal efficiency. Furthermore,
the synergistic effects of this combination promise reduced
treatment duration and cost. This novel combination is
therefore considered a more efficient technology than the
individually applied processes.

Acknowledgments
This work was supported by Korea Ministry of Environment
as The GAIA Project. We gratefully acknowledge three
anonymous reviewers who provided constructive and invaluable comments for improving the quality of the
manuscript.

Note Added after ASAP Publication

There was an error in the fourth paragraph of the Results
section in the version of this paper published ASAP November
5, 2009; the corrected version published ASAP November 10,
2009.

Supporting Information Available

Additional information on the detailed analytical methods
and the experimental results cited in the text. This material
is available free of charge via the Internet at http://
pubs.acs.org.

Literature Cited
(1) Reisinger, H. J.; Burris, D. R.; Hering, J. G. Remediation subsurface
arsenic contamination with monitored natural attenuation.
Environ. Sci. Technol. 2005, 458464, November 15.
(2) Nickson, R. T.; McArthur, J.; Burgess, W.; Ahmed, K.; Ravenscroft,
P.; Rahmann, M. Arsenic poisoning of Bangladesh groundwater.
Nature 1998, 395, 338.
(3) Smedley, P. L.; Kinniburgh, D. G. A review of the source,
behaviour and distribution of arsenic in natural waters. Appl.
Geochem. 2002, 17, 517568.
(4) Jones, C. A.; Inskeep, W. P.; Neuman, D. R. Arsenic transport
in contaminated mine tailings following liming. J. Environ. Qual.
1997, 26, 433439.
(5) Macur, R. E.; Wheeler, J. T.; McDermott, T. R.; Inskeep, W. P.
Microbial populations associated with the reduction and
enhanced mobilization of arsenic in mine tailings. Environ. Sci.
Technol. 2001, 35, 36763682.
(6) Kim, J. Y.; Davis, A. P.; Kim, K. W. Stabilization of available
arsenic in highly contaminated mine tailings using iron. Environ.
Sci. Technol. 2003, 37, 189195.
(7) Kim, S. O.; Kim, W. S.; Kim, K. W. Evaluation of electrokinetic
remediation of arsenic-contaminated soils. Environ. Geochem.
Health. 2005, 27, 443453.
(8) Mulligan, C. N.; Yong, R. N.; Gibbs, B. F. Remediation technologies for metal-contaminated soils and ground water: An
evaluation. Eng. Geol. 2001, 60, 193207.
(9) Islam, F. S.; Gault, A. G.; Boothman, C.; Polya, D. A.; Charnock,
J. M.; Chatterjee, D.; Lloyd, J. R. Role of metal-reducing bacteria
in arsenic release from Bengal delta sediments. Nature 2004,
430, 6871.
(10) Ahmann, D.; Krumholz, L. R.; Hemond, H. F.; Lovley, D. R.;
Morel, F. M. M. Microbial mobilization of arsenic from sediments
of the Aberjona watershed. Environ. Sci. Technol. 1997, 31, 2923
2930.
(11) Cummings, D. E.; Caccavo, F.; Fendorf, S.; Rosenzweig, R. F.
Arsenic mobilization by the dissimilatory Fe(III)-reducing
bacterium Shewanella alga BrY. Environ. Sci. Technol. 1999, 33,
723729.
(12) Cooper, D. C.; Picardal, F. F.; Coby, A. J. Interactions between
microbial iron reduction and metal geochemistry: effect of redox
cycling on transition metal speciation in iron bearing sediments.
Environ. Sci. Technol. 2006, 40, 18841891.
(13) Cummings, D. E.; March, A. W.; Bostick, B.; Spring, S.; Caccavo,
F.; Fendorf, S.; Rosenzweig, R. F. Evidence for microbial Fe(III)
reduction in anoxic, mining-impacted lake sediments (Lake
Coeur dAlene, Idaho). Appl. Environ. Microbiol. 2000, 66, 154
162.
(14) Chatain, V.; Bayard, R.; Sanchez, F.; Moxzkowicz, P.; Gourdon,
R. Effect of indigenous bacterial activity on arsenic mobilization under anaerobic conditions. Environ. Int. 2005, 31, 221
226.
(15) Lee, J. U.; Lee, S. W.; Kim, K. W.; Yoon, C. H. The effects of
different carbon sources on microbial mediation of arsenic in
arsenic-contaminated sediment. Environ. Geochem. Health.
2005, 27, 159168.
(16) Lee, K. Y.; Kim, K. W.; Kim, S. O. Geochemical and microbial
effects on the mobilization of arsenic in mine tailing soils.
Environ. Geochem. Health. 2009, DOI: 10.1007/s10653-0099263-4.
(17) Lee, J. U.; Kim, S. M.; Kim, K. W.; Kim, I. S. Microbial removal
of uranium in uranium-bearing black shale. Chemosphere 2005,
59, 147154.
(18) Lee, E. Y.; Noh, S. R.; Cho, K. S.; Ryu, H. W. Leaching of Mn, Co,
and Ni from manganese nodules using an anaerobic bioleaching
method. J. Biosci. Bioeng. 2001, 92, 354359.
VOL. 43, NO. 24, 2009 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

9359

(19) Virkutyte, J.; Sillanpaa, M.; Latostenmaa, P. Electrokinetic soil

remediation - critical overview. Sci. Total Environ. 2002, 289,
97121.
(20) Wang, J. Y.; Zhang, D. S.; Stabnikova, O.; Tay, J. H. Evaluation
of electrokinetic removal of heavy metals from sewage sludge.
J. Hazard. Mater. 2005, B124, 139146.
(21) Le Hecho, I.; Tellier, S.; Astruc, M. Industrial site soils contaminated with arsenic or chromium: evaluation of the electrokinetic method. Environ. Technol. 1998, 19, 10951102.
(22) Yuan, C.; Chiang, T. S. Enhancement of electrokinetic remediation of arsenic spiked soil by chemical reagents. J. Hazard.
Mater. 2008, 152, 309315.
(23) Wick, L. Y.; Shi, L.; Harms, H. Electro-bioremediation of
hydrophobic organic soil-contaminants: A review of fundamental interactions. Electrochim. Acta 2007, 52, 3441,
3448.
(24) Maini, G.; Sharman, A. K.; Sunderland, G.; Knowles, C. J.;
Jackman, S. A. An integrated method incorporating sulfuroxidizing bacteria and electrokinetics to enhance removal of
copper from contaminated soil. Environ. Sci. Technol. 2000, 34,
10811087.
(25) Le, X. C.; Yalcin, S.; Ma, M. Speciation of submicrogram per liter
levels of arsenic in water: On site species separation integrated
with sample collection. Environ. Sci. Technol. 2000, 34, 2342
2347.
(26) Ure, A. M. Heavy Metals in Soils; Alloway, B. J., Ed.; Chapman
& Hall: Glasgow, 1995.

9360

ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 43, NO. 24, 2009

(27) Wenzel, W. W.; Kirchbaumer, N.; Prohaska, T.; Stingeder, G.;

Lombi, E.; Adriano, D. D. Arsenic fractionation in soils using an
improved sequential extraction procedure. Anal. Chim. Acta
2001, 436, 309323.
(28) Tessier, A.; Campbell, P. G. C.; Bisson, M. Sequential extraction
procedure for speciation of particulate trace metals. Anal. Chem.
1979, 51, 844851.
(29) Oday, P. A.; Vlassopoulos, D.; Root, R.; Rivera, N. The influence
of sulfur and iron on dissolved arsenic concentrations in the
shallow subsurface under changing redox conditions. Proc. Natl.
Acad. Sci. U.S.A. 2004, 101, 1370313708.
(30) Nealson, K. H.; Saffarini, D. Iron and manganese in anaerobic
respiration: Environmental significance, physiology, and regulation. Annu. Rev. Microbiol. 1994, 48, 31343.
(31) Jang, M.; Hwang, J. S.; Choi, S. I. Sequential soil washing
techniques using hydrochloric acid and sodium hydroxide for
remediating arsenic-contaminated soils in abandoned ironore mines. Chemosphere 2007, 66, 817.
(32) Jackson, B. P.; Miller, W. P. Effectiveness of phosphate and
hydroxide for desorption of arsenic and selenium species from
iron oxides. Soil Sci. Soc. Am. J. 2000, 64, 16161622.
(33) Urase, T.; Oh, J. I.; Yamamoto, K. Effect of pH on rejection of
different species of arsenic by nanofiltration. Desalination 1998,
117, 1118.

ES901544X