Environ. Sci. Technol. 2010, 44, 3772–3778
Evaluating Environmental Influences
on AsIII Oxidation Kinetics by a
Poorly Crystalline Mn-Oxide
S A N J A I J . P A R I K H , * ,†
BRANDON J. LAFFERTY,‡
TERRY G. MEADE,‡ AND
DONALD L. SPARKS‡
Department of Land, Air and Water Resources, The University
of California, One Shields Avenue, Davis, California 95616,
and Department of Plant and Soil Sciences, Delaware
Environmental Institute, The University of Delaware,
152 Townsend Hall, Newark, Delaware 19716
Received November 9, 2009. Revised manuscript received
March 17, 2010. Accepted April 1, 2010.
The oxidation of arsenite (AsIII) via Mn-oxides is an important
process for natural arsenic (As) cycling and for developing in situ
strategies for remediation of As-contaminated waters. In this
study, the influence of goethite (R-FeOOH), phosphate, and
bacteria/biopolymer coatings on the initial AsIII oxidation kinetics
by a hydrous Mn-oxide (δ-MnO2) is examined via both batch
experiments and rapid scan ATR-spectroscopy. Under natural
conditions the presence of various mineral surfaces, bacteria,
organic matter, and ions in solution can block Mn-oxide
reaction sites, alter reaction rates, and thus inhibit AsIII oxidation.
Previous studies of As-Mn systems demonstrate rapid
oxidation of AsIII, catalyzed by Mn-oxides, producing less toxic
and mobile arsenate (AsV). Subsequent to oxidation, reaction
products from reductive dissolution of δ-MnO2 by AsIII, bind to
and passivate the mineral surface. This study demonstrates
enhanced passivation through interaction with phosphate and
bacteria. Increased As oxidation with high concentrations of
goethite is observed, attributed to AsV sorption to R-FeOOH and
diminished surface passivation of δ-MnO2. Specific competition
between phosphate and AsV for δ-MnO2 was confirmed
through diminished As sorption and decreased AsV production
when oxidation occurred in the presence of phosphate.
Kinetic experiments reveal that the extent of initial AsIII oxidation
in the presence of low phosphate and R-FeOOH concentration
is reduced; however, initial reaction rates are generally not
affected. Reaction rates are reduced when bacterial adhesion
and high phosphate concentrations strongly passivate
δ-MnO2 and reduce AsIII interactions with the mineral surface.
The data presented in this study highlight the importance of
considering natural heterogeneity when investigating reaction
mechanisms and initial reaction kinetics.
Introduction
Inorganic arsenic (As) contamination in soils, sediments, and
water from natural and anthropogenic sources pose environmental and human health risks. The predominate species
of As in soil and aquatic environments are arsenite (AsIII) and
* Corresponding author e-mail: sjparikh@ucdavis.edu.
†
The University of California.
‡
The University of Delaware.
3772
9
ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 44, NO. 10, 2010
arsenate (AsV) (1), with AsV being both less toxic and less
mobile than AsIII (2). Oxidation of AsIII in soil and aquatic
systems can be carried out via both abiotic (3) and biotic
pathways (4). Manganese oxides are widespread in the natural
environment and readily serve as electron acceptors in the
abiotic oxidation of AsIII (5, 6). Biotic oxidation and reduction
of As have been observed in a wide range of bacteria isolated
from soil and natural waters (4).
Kinetic investigations of AsIII oxidation by Mn-oxides have
revealed rapid AsIII depletion rates (5-9), with equilibrium
reached on a scale of minutes to hours. During this rapid
reaction, sorption of AsIII to the Mn-oxide surface is believed
to be a necessary step for oxidation (5, 6). Subsequent to AsIII
oxidation, the retention of AsV on Mn-oxides surfaces has
been documented experimentally (5, 8-10) and via density
functional theory calculations (11). Binding of AsV on Mnoxide surfaces passivates the mineral surface, as AsIII binding
sites are blocked and oxidation is inhibited. It is expected
that similar passivation will occur in heterogeneous environments where bacteria, biopolymers, and ions in solution
interact with Mn-oxide binding sites, thus influencing the
rate and amount of AsIII oxidized. This has been observed for
AsIII oxidation by manganite in the presence of phosphate
where the extent and rate of oxidation was reduced (12).
Bacterially catalyzed oxidation of AsIII is typically slower
than oxidation via Mn-oxides. For example, AsIII half-lives
(t1/2) during logarithmic growth have been measured at 12
(Variovorax paradoxus), 7.2 (Agrobacterium tumefaciens), and
4.8 h (Pseudomonas fluorescens) (13). Upon reaction with
Mn-oxides, t1/2 for AsIII can be as rapid as less than 1 min
(7, 8) to 0.15 h (6); however, longer values for t1/2 (37 h) have
also been reported (14), with differences attributed to Mnoxide crystallinity, Mn:As ratio, and sorption processes.
Attenuated total reflectance (ATR) Fourier transform
infrared (FTIR) spectroscopy is an established technique for
studying sorption (15, 16) and redox processes (17, 18),
providing bonding mechanisms and, under certain reaction
conditions, kinetic data (8, 17). Rapid-scan ATR-FTIR was
previously used to collect rapid in situ kinetic data, providing
molecular scale data, to examine the initial oxidation of
arsenite (AsIII) via hydrous Mn-oxide (δ-MnO2) (8). Through
observation and analysis of IR bands corresponding to
arsenate (AsV), rapid AsIII oxidation was observed (initial pH
6-9) with 50% of the reaction occurring within the first
minute.
The primary objective of this paper is to examine the
initial oxidation kinetics of AsIII via poorly crystalline Mnoxides in the presence of competing ions, mineral surfaces,
and bacteria/biopolymer coatings. It has been previously
shown that ion competition influences AsV sorption processes
to a range of soil minerals (19-21), and only one study has
examined the effect of ion competition on Mn-oxide catalyzed
As oxidation kinetics (12). In that study, reactions with a
crystalline MnIII-oxide (manganite) are slower than what has
been observed for AsIII oxidation via poorly crystalline MnIVoxides (7, 8). Additionally, research on the initial oxidation
kinetics of As via Mn-oxides in the presence of competing
mineral surfaces and bacterial films has not been presented.
This current study focuses on the initial moments of reaction
and probes the effects of competition on the first minutes
of As oxidation by δ-MnO2, whose poorly crystalline structure
approaches that of Mn-oxides found in soil and sediment
(22). While studies that investigate pure two-reactant systems
are helpful for elucidating reaction mechanisms (10, 23, 24)
and studies using soils and sediments (25-27) are useful to
evaluate reaction rates and concentrations under natural
10.1021/es903408g
 2010 American Chemical Society
Published on Web 04/19/2010
conditions, this study serves as a bridge by examining the
initial oxidation kinetics of a relatively simple system and
increasing its complexity under controlled conditions. The
research presented here focuses on how additional environmentally relevant reactants influence the initial AsIII
oxidation reaction via δ-MnO2 through use of rapid-scan
ATR-FTIR spectroscopy.
Experimental Procedures
An abbreviated description of experimental procedures is
given here; for details regarding methods please see the
Supporting Information.
Materials. Synthesis of δ-MnO2 was performed using
methods described in previous publications (8, 28) to give
a mineral phase representative of natural Mn-oxides. δ-MnO2
was stored at 4 °C for less than 2 weeks prior to use in
experiments. Goethite was synthesized using KOH and
Fe(NO3)3 following the methods of Cornell and Schwertmann
(29). Sodium arsenite (Fisher Scientific, >99%), sodium
hydrogen arsenate heptahydrate (Alfa Aesar, 98-102%), and
sodium phosphate (Fisher Scientific, 100.2%) were used as
sources of AsIII, AsV, and phosphate, respectively. AsIII
oxidizing bacteria were isolated and used in previous studies
(13, 30, 31). As-oxidizing bacteria were grown on R2A agar
plates, followed by inoculation into growth media (13) until
the late exponential phase.
Batch Sorption Isotherms and As Oxidation Kinetic
Experiments. δ-MnO2 was reacted for 0 to 1440 min with
AsIII (5 mmol kg-1 NaAsO2) and AsIII-phosphate (5 mmol kg-1
NaAsO2 and 5 mmol kg-1 NaH2PO4) at pH 6 and 9 in 5 mmol
kg-1 NaCl. Samples (including blanks) were mixed via a
reciprocal shaker (100 rpm, 25 °C). To promote flocculation
of δ-MnO2, 1 mL of 1.0 mol kg-1 NaCl was added to each
sample before being centrifuged at 5500 rpm for 10 min.
After centrifugation, supernatants were filtered (0.2 µm) prior
to analysis. For sorption isotherm experiments, δ-MnO2 (∼40
g kg-1) was reacted with 1, 2.5, 5, 10, and 15 mmol kg-1
NaH2PO4, Na2AsO2, and Na2HAsO4 at pH 6 and 9 in 5 mmol
kg-1 NaCl. Samples were placed on a reciprocal shaker (100
rpm, 25 °C) for 24 h. Samples were centrifuged at 5500 rpm
for 10 min and supernatants filtered (0.2 µm) prior to analysis.
Bacterially-Catalyzed As Oxidation Kinetics. Bacteria
were grown in 25 mL of growth media with 75 µmol L-1 AsIII
until the late exponential phase. Cells were centrifuged at
5500 rpm (10 min, 4 °C) and resuspended in growth media
with no AsIII. Washed bacteria were spiked with AsIII (pH 6)
at 0, 1, 5, 15, and 25 mmol kg-1 AsIII and placed on an oribital
shaker (100 rpm, 23 ( 2 °C). Aliquots (0.1 mL) were taken
from each of the flasks at specific time intervals and analyzed
via LC-ICP/MS analysis. Following reaction with AsIII concentrations up to 25 mmol kg-1 P. fluorescens and A. faecalis
were plated on R2A agar after 24 and 48 h; growth of bacteria
colonies demonstrates the As levels used as nonlethal.
ATR-FTIR Spectroscopy and Analysis. FTIR spectra were
collected with a Thermo Nicolet Nexus spectrometer (Thermo; MCT/A) using a diamond single bounce ATR accessory
(Smart Orbit, Thermo) and on a multibounce ZnSe horizontal
ATR (HATR, Pike Technologies) using standard spectral
collection techniques. FTIR spectra for experiments with
R-FeOOH were collected on a Thermo Nicolet 6700 spectrometer (Thermo; MCT/A) using a diamond single bounce
accessory (GladiATR, Pike Technologies).
As Oxidation: Rapid-Scan FTIR Experiments. In situ
FTIR experiments were carried out via single-bounce ATR.
All experiments were conducted using 25 mmol kg-1 AsIII in
5 mmol kg-1 NaCl at pH 6. The accuracy/validity of this
method has been previously addressed (8). The rapid-scan
FTIR experiments conducted (pH 6, 25 mmol kg-1 AsIII)
include the following: (i) varying δ-MnO2 concentrations at
7.5, 11, 15, and 22 g kg-1; (ii) with 15 g kg-1 δ-MnO2 and
varying phosphate at 4, 8, 12, and 25 mmol kg-1; (iii) with P.
fluorescens and A. faecalis at steady state concentration (105
cells mL-1); (iv) with 8 g kg-1 R-FeOOH and mixtures of δ-MnO2
and R-FeOOH (8 g kg-1 R-FeOOH and 15 g kg-1 δ-MnO2, 15 g
kg-1 R-FeOOH and 15 g kg-1 δ-MnO2; and (v) with bacteria
after 24 h reaction with 15 g kg-1 δ-MnO2, 15 g kg-1 R-FeOOH,
and 15 g kg-1 R-FeOOH and 15 g kg-1 δ-MnO2. Experiments
with goethite were conducted on a different FTIR and with
different batches of minerals, resulting in slightly different peak
areas and corresponding AsV concentrations.
A conservative approach has been used to compare rapidscan kinetic data. The amount of AsV produced (AsVmax) is
estimated by calculating the average AsV peak area from 4
to 15 min. Linear regression analysis of the first 30 s of reaction
was carried out to determine the initial slope of the reaction
(m30s) to compare initial reaction rates. The amount of time
required for half of AsVmax has been defined as t1/2 and was
determined by using an exponential fit for the data (0 to 15
min) and calculated t for half of AsVmax. This approach is only
required for reactions where t1/2 exceeds 30 s. For t1/2 less
than 30 s calculation for t1/2 could also be made using the
linear regression equation for the first 30 s of reaction.
Examining Binding Mechanisms during Passivation of
δ-MnO2. To explore As binding mechanisms during passivation of δ-MnO2 subsequent to reaction with AsIII, a series
of ATR-FTIR spectra were acquired (ZnSe HATR). Spectra
collected include 12 mmol kg-1 AsV, 15 g kg-1 δ-MnO2, 12
mmol kg-1 AsV plus 12 mmol MnII (MnCl2), 12 mmol kg-1 AsV
plus 15 g kg-1 δ-MnO2, and 12 mmol kg-1 AsIII reacted with
15 g kg-1 δ-MnO2 at 20 and 60 min.
Results and Discussion
Batch AsIII-δ-MnO2 Experiments. Arsenic sorption by
δ-MnO2 increased during AsIII oxidization compared to AsV
sorption (Figure 1a), which is in agreement with the
observations of previous studies using a synthetic birnessite
(10). It is possible that reductive dissolution of δ-MnO2 by
AsIII liberates MnII and may lead to increased binding sites
for AsV and greater As retention. Although AsIII is more
mobile than AsV (2), it is clear that chemical reactions influence
transport in soil and subsurface environments. Since oxidation/
sorption can increase As retention, AsIII entering a system
dominated by Mn-oxides may exhibit increased retention as
compared to AsV entering the same system.
The presence of phosphate during AsIII oxidation leads to
decreased total As sorption to δ-MnO2 (Figure 1a). These
data demonstrate competition between AsV and phosphate,
resulting from similarity in chemical structure and reactivity
(20, 32), and decreased retention of both anions (Figure 1).
The reduced As sorption in the presence of phosphate is
especially important for agricultural settings where animal
waste containing As (and P) is land applied (33). A competitive
ion effect has been demonstrated through addition of
phosphate fertilizer to AsV contaminated soils, resulting in
an increase of AsV leaching (34).
Figure 2 shows the percent of initial As (AsIII and AsV) and
phosphate in solution after reaction with δ-MnO2 as a
function of time at pH 6 and 9. Increased AsIII oxidation rates
via manganite have been previously observed with decreased
pH (6.3 to 4.0); however, the current data, and our previous
paper (8), reveal no significant effect of pH on the initial AsIII
oxidation rate via δ-MnO2 (Figure 2). The figure reveals that
the concentration of AsIII in solution rapidly drops to near
zero, with full removal from solution occurring between 5
and 30 min. At 24 h, both phosphate and As concentrations
are stable, and solution AsV concentrations are higher when
phosphate is present. Increasing AsV concentrations from 5
to 960 min indicate that reactions are still occurring at the
solid-liquid interface. High phosphate concentrations continue to exist in solution, indicating that As release is not due
VOL. 44, NO. 10, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
9
3773
FIGURE 1. Sorption isotherms from batch experiments at pH 6 (solid symbols) and 9 (open symbols) in 5 mmol kg-1 NaCl for a) As
sorption to δ-MnO2 when added as AsV and AsIII (including oxidation) in the presence and absence of phosphate (P) and b)
phosphate sorption to δ-MnO2 in the presence and absence of AsIII.
to phosphate exchange reactions. Due to the similarity in
chemical structure between phosphate and AsV, it follows
that AsV sorption will not occur on these sites. It is our
interpretation that AsIII is binding to δ-MnO2, oxidized, and
AsV is subsequently released to solution with either the
oxidation or desorption step occurring relatively slowly. It is
well documented that during AsIII oxidation via Mn-oxides,
MnIV can go through a MnIII intermediate before reducing to
MnII (35). AsIII reaction with MnIII δ-MnO2 may lead to much
slower AsIII oxidation rates and contribute to the release of
AsV to solution between 30 and 960 min. Batch experiments
alone cannot be used to determine reaction mechanisms;
however, at high AsIII concentrations our previous FTIR study
suggested AsIII binding to δ-MnO2 without the expected rapid
oxidation (8). Although likely minimal in amount, density
3774
9
ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 44, NO. 10, 2010
functional theory calculations also suggest possible MnIII and
AsIII accumulation on Mn-oxides (11).
In Situ ATR-FTIR Investigations of AsV Binding Mechanisms. It is believed that AsIII initially binds to MnIV sites
and is rapidly oxidized to AsV, while reductive dissolution of
the mineral leads to MnII release (through an MnIII intermediate). MnIII on δ-MnO2 may permit limited AsIII binding
without immediate oxidation. Assuming no sorption of
reaction products, AsIII oxidation would continue until one
of the reactants was no longer present. However, surface
passivation of δ-MnO2 binding sites by AsV and/or MnII
sorption inhibits complete oxidation (8, 11). It has previously
been proposed that AsV binds directly to MnIV within Mnoxides (10) or through MnII bridging (5, 8, 9). FTIR data from
this current study support both of these theories (Figure 3),
FIGURE 3. ATR-FTIR spectra (diamond IRE) of a) 12 mM AsV
standard, b) 15 g L-1 δ-MnO2 standard, c) AsV reacted with MnII
(MnCl2), d) AsV reacted with δ -MnO2, and 12 mM AsIII reacted
with δ-MnO2 for e) 20 and f) 60 min.
FIGURE 2. Kinetic plots of batch experiments showing percent
of initial As (5 mmol L-1 AsIII), as solution AsIII and AsV, and
phosphate in solution during the course of reaction with
δ-MnO2 at a) pH 9 and b) pH 6 in 5 mmol kg-1 NaCl. Insets are
included to allow viewing of data within the first 60 min of
reaction. Solid symbols correspond to experiments where
δ-MnO2 was reacted with AsIII, and open symbols correspond to
experiments where AsIII and phosphate were simultaneously
reacted with δ-MnO2.
as spectra of AsIII reacted with δ-MnO2 contain IR bands
consistent with both AsV reacted with MnII and AsV reacted
with δ-MnO2 (see the Supporting Information for specific
peak assignments). It is not possible to examine AsIII binding
with this approach as concentrations used are below the
AsIII FTIR detection limit at pH 6 (8).
Using the spectra of As standards, and working near the
FTIR detection limits for AsV, interpretation of AsV binding
to δ-MnO2 can be achieved. IR spectra of AsIII reacted with
δ-MnO2 closely resemble the spectrum of AsV- δ-MnO2, and
indicate that AsV is bound to MnIV. However, the peak at
∼790 cm-1 falls between standard peaks for AsV-MnII (767
cm-1) and AsV-MnIV (798 cm-1) and may represent a
combination of both peaks. Although these data suggest that
two different binding mechanisms are possible, our interpretation of the IR spectra is that most binding to δ-MnO2
is occurring between AsV and MnIV.
As Oxidation Kinetics via Rapid-Scan ATR-FTIR: Abiotic
Experiments. The presence of phosphate, R-FeOOH, and
bacteria influence the amount of initial As oxidation and in
some cases the initial reaction rates. For all reactions, the
initial AsIII oxidation is carried out via reaction with δ-MnO.
The primary factor influencing the amount of AsIII oxidized
is limitation of MnIV binding sites. Increasing δ-MnO2
concentration leads to increased AsV production (Figure 4).
The AsVmax, t1/2, and m30s for all reactions are given in Tables
S1, S2, S3, and S4. The initial reaction rate is similar (m30s)
FIGURE 4. Rapid-scan ATR-FTIR plots of AsV IR peak area as a
function of reaction time for 25 mmol kg-1 AsIII reacted with
varying concentrations of δ-MnO2 suspensions at pH 6 in 5
mmol kg-1 NaCl.
for the three highest δ-MnO2 concentrations but decreases
when δ-MnO2 becomes limiting (7.5 g kg-1). Reactions rapidly
approach completion with t1/2 ranging from 0.21 to 0.28 s.
These initial reaction rates are not dependent on AsIII
concentration, as nearly identical rates were observed for
δ-MnO2 oxidation of 5 mmol kg-1 AsIII via batch and quickscanning X-ray absorption (Q-XAS) spectroscopy (7).
In all cases the addition of phosphate reduces the total
extent AsIII oxidation (Figure 5a, Table S2). The initial slope
(m30s) and t1/2 are similar for all reactions, except for addition
of 25 mmol kg-1 phosphate (m30s decreases and t1/2 increases).
Although phosphate (and low R-FeOOH concentrations)
reduces the amount of AsV produced, the initial oxidation
rate is not affected. Since initial reaction rates are not strongly
influenced by concentration of reactants, including other
ions and surfaces, the reaction is not transport limited, and
this implies primarily chemically controlled kinetics. The
exception is observed at the high phosphate concentration
VOL. 44, NO. 10, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
9
3775
FIGURE 5. Rapid-scan ATR-FTIR plots of AsV IR peak area as a
function of reaction time for 25 mmol kg-1 AsIII (pH 6, 5 mmol
kg-1 NaCl) reacted with varying concentrations of a) phosphate
(P) and b) r-FeOOH (experiments conducted on a different FTIR
and with different batches of δ-MnO2 and r-FeOOH).
where the reaction is slower. In this case we hypothesize that
exchange/desorption of phosphate from δ-MnO2 permits
prolonged reaction. This is in agreement with a previous
study which reports a decrease in rate and extent of AsIII
oxidation by manganite when phosphate concentrations were
high, relative to AsIII (12). Reduced AsIII oxidation when reacted
with phosphate is also observed in batch experiments (Figure
2); however, the rate of reaction does not seem to be affected.
Under these conditions we propose that phosphate binding
to δ-MnO2 blocks AsIII reaction sites, thus hindering oxidation.
AsV forms inner-sphere complexes with Mn-oxides (10, 36)
and sorption of AsV is favored over phosphate to numerous
mineral surfaces, including Mn-oxides (19). Since phosphate
and AsV have very similar structures and chemical reactivities
(20), inner-sphere sorption of phosphate to δ-MnO2 is
believed to be the reason for competition.
Under certain conditions AsIII can be oxidized by Fe-oxides
(37); however, no oxidation via R-FeOOH is observed within
15 min of reaction (Figure 5b). All experiments examining
AsIII oxidation via δ-MnO2 in the presence of R-FeOOH were
conducted at the University of California, Davis using a
different spectrometer and batches of both δ-MnO2 and
R-FeOOH (other experiments performed at the University of
Delaware), and small differences in the amount of AsIII
oxidized by δ-MnO2 are reflected in Figure 5 and Table S3.
When δ-MnO2 is reacted with AsIII and 4 g kg-1 R-FeOOH the
amount of AsV detected decreases. However, with increasing
R-FeOOH concentration increased production of AsV is
observed. At the highest R-FeOOH concentration the amount
3776
9
ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 44, NO. 10, 2010
FIGURE 6. Rapid-scan ATR-FTIR plots of AsV IR peak area as a
function of reaction time for 25 mmol kg-1 AsIII (pH 6, 5 mmol
kg-1 NaCl) reacted with a) P. fluorescens and b) A. faecalis
suspensions (10 times steady state) with and without δ-MnO2
and r-FeOOH.
of AsV produced exceeds what is observed for δ-MnO2 alone
(Figure 5b). It is important to note that ATR-FTIR detects AsV
both in solution and bound to mineral surfaces, thus an
approximation of total AsV can be made. While binding of
R-FeOOH to δ-MnO2 may be possible, we believe that the
observed result arises from interactions between AsIII and
AsV with the mineral surfaces and not from interaction
between the two minerals.
The sorption of AsIII and AsV to Fe-oxides has previously
been demonstrated (38, 39), and it is proposed that reduced
AsIII oxidation results from competition between δ-MnO2
and R-FeOOH for AsIII. Increasing R-FeOOH increases
competition for AsV, and with high R-FeOOH concentrations
some AsV released from δ-MnO2 during oxidation binds to
R-FeOOH instead of δ-MnO2, thus passivation of δ-MnO2 is
reduced. In this case, the Fe-oxide is serving to promote and
hinder AsIII oxidation via δ-MnO2. This result was observed
when AsIII was oxidized by birnessite, todorokite, and
hausmannite in the presence of R-FeOOH (40). Analogous
to the current study, the produced AsV binds to goethite and
reduces passivation of the Mn-oxides. Another study observed
an increase in As attenuation through simultaneous oxidation
of AsIII and FeIII by Mn-oxides, whereby coprecipitation of
FeIII-oxides with AsV serves to sequester arsenic and prevent
Mn-oxide passivation (41). These results demonstrate a
possible remediation strategy to achieve increased As oxidation and attenuation through addition of Mn- and Fe-oxides
(or FeII) to As contaminated water.
Bacterially-Catalyzed As Oxidation. Analysis of solution
AsIII and AsV concentrations during the 48 h reaction period
reveal that the bacteria completely oxidize 1 mmol kg-1 AsIII
in approximately 24 h (Figure S1). Additionally, the results
show that these bacteria oxidize a maximum of ∼5 mmol
kg-1 AsIII within 48 h, with the highest oxidation rate after
24 h of reaction. Rapid-scan ATR-FTIR experiments do not
show detectable AsIII oxidation by either P. fluorescens or A.
faecalis alone during the 15 min reaction time (Figure 6) and
rapid AsIII oxidation is observed only when δ-MnO2 is present.
When bacteria are bound to only R-FeOOH no AsV is detected;
however, if δ-MnO2 is present with bacteria, a small IR peak
corresponding to AsV is observed. The AsVmax for P. fluorescens
with δ-MnO2 is 3.05 mmol kg-1 and 4.41 mmol kg-1 for A.
faecalis with δ-MnO2; with R-FeOOH also present these values
drop to 0.79 and 2.14, respectively (Table S4). The t1/2 values
are less than δ-MnO2 reacted with AsIII alone, with values
ranging from 0.64 to 0.88; however, m30s values are much
less with a value of 0.01.
Reaction of bacteria with minerals prior to reaction with
AsIII results in binding between bacterial surface proteins
and/or phosphate groups to both δ-MnO2 and R-FeOOH
(see the Supporting Information). Bacterial adhesion to
minerals blocks access to MnIV and reduces AsVmax. Bacteria
bound to δ-MnO2 hinder AsV production much more than
reaction with phosphate or R-FeOOH. Reaction rates are
significantly reduced, based on t1/2 (0.98-2.81) and m30s (0.01)
values (Table S4), and indicate that the reaction is transport
limited. Exchange of bacteria or biopolymers for AsIII at MnIV
sites is not likely; rather, it is believed that AsIII diffusion and
transport through bacteria extracellular material (biofilm)
retards AsIII oxidation. Water in the biopolymer matrix is
organized in structured channels allowing transport into the
biofilm (42). Oxidation of As by δ-MnO2 is reduced; however,
AsIII may still be transported within channels thus delaying
the oxidation reaction. In natural environments coatings of
organic materials exist on mineral surfaces, and similar effects
are expected. In a study where humic acid was preadsorbed
onto Fe-Mn nodules, a decrease in both oxidation and
sorption of As was observed due to reduced binding sites for
AsIII (43).
Examination of initial AsIII oxidation kinetics by Mn-oxides
in the presence of environmental factors improves our
understanding of their potential influence on reaction rates
and amounts. This study demonstrates that competing factors
generally reduce, or inhibit, the forward direction of the initial
reaction, and their presence should be considered when
trying to determine the fate of As in natural settings.
Additional work is needed to look at long-term reaction rates
for As-oxidizing bacteria bound to Mn-oxide surfaces, as
increased time may permit abiotic and biotic reactions to
work simultaneously and oxidize large amounts of As. Also,
the observation of Fe-oxides to bind reaction products and
enhance the extent of AsIII oxidation should be further
explored. Fe-oxides are ubiquitous in soils and subsurface
environments, and their presence at levels greater than Mnoxides may serve to reduce surface passivation and permit
greater As oxidation and subsequent sequestration.
Acknowledgments
We thank William P. Inskeep, Richard E. Macur, and Russ
Hille for generously providing the bacterial strains used in
this research. This project was supported by the National
Research Initiative of the USDA Cooperative State Research,
Education and Extension Service, grant number 2005-3510716105, and the National Science Foundation, grant number
EAR-0544246.
Supporting Information Available
Details regarding methodology and further discussion of
results. This material is available free of charge via the Internet
at http://pubs.acs.org.
Literature Cited
(1) Cullen, W. R.; Reimer, K. J. Arsenic speciation in the environment.
Chem. Rev. 1989, 89, 713–764.
(2) Ng, J. C. Environmental contamination of arsenic and its
toxicological impact on humans. Environ. Chem. 2005, 2, 146–
160.
(3) Oscarson, D. W.; Huang, P. M.; Liaw, W. K. The oxidation of
arsenite by aquatic sediments. J. Environ. Qual. 1980, 9, 700–
703.
(4) Oremland, R. S.; Stolz, J. F. The ecology of arsenic. Science 2003,
300, 939–944.
(5) Tani, Y.; Miyata, N.; Ohashi, M.; Ohnuki, T.; Seyama, H.; Iwahori,
K.; Soma, M. Interaction of inorganic arsenic with biogenic
manganese oxide produced by a Mn-oxidizing fungus, strain
KR21-2. Environ. Sci. Technol. 2004, 38, 6618–6624.
(6) Scott, M. J.; Morgan, J. J. Reactions at oxide surfaces. 1. Oxidation
of As(III) by synthetic birnessite. Environ. Sci. Technol. 1995,
29, 1898–1905.
(7) Ginder-Vogel, M.; Landrot, G.; Fischel, J. S.; Sparks, D. L.
Quantification of rapid environmental redox processes with
quick-scanning x-ray absorption spectroscopy (Q-XAS). Proc.
Natl. Acad. Sci. U.S.A. 2009, 106, 16124–16128.
(8) Parikh, S. J.; Lafferty, B. J.; Sparks, D. L. An ATR-FTIR
spectroscopic approach for measuring rapid kinetics at the
mineral/water interface. J. Colloid Interface Sci. 2008, 320, 177–
185.
(9) Oscarson, D. W.; Huang, P. M.; Liaw, W. K.; Hammer, U. T.
Kinetics of oxidation of arsenite by various manganese dioxides.
Soil Sci. Soc. Am. J. 1983, 47, 644–648.
(10) Manning, B. A.; Fendorf, S. E.; Bostick, B.; Suarez, D. L.
Arsenic(III) oxidation and arsenic(V) adsorption reactions on
synthetic birnessite. Environ. Sci. Technol. 2002, 36, 976–981.
(11) Zhu, M.; Paul, K. W.; Kubicki, J. D.; Sparks, D. L. Quantum
chemical study of arsenic (III, V) adsorption of Mn-oxides:
Implications for As oxidation. Environ. Sci. Technol. 2009, 43,
6655–6661.
(12) Chiu, V. Q.; Hering, J. G. Arsenic adsorption and oxidation at
Manganite surfaces. 1. Method for simultaneous determination
of adsorbed and dissolved arsenic species. Environ. Sci. Technol.
2000, 34, 2029–2034.
(13) Macur, R. E.; Jackson, C. R.; Botero, L. M.; McDermott, T. R.;
Inskeep, W. P. Bacterial populations associated with the
oxidation and reduction of arsenic in an unsaturated soil.
Environ. Sci. Technol. 2004, 38, 104–111.
(14) Tournassat, C.; Charlet, L.; Bosbach, D.; Manceau, A. Arsenic(III)
oxidation by birnessite and precipitation of manganese(II)
arsenate. Environ. Sci. Technol. 2002, 36, 493–500.
(15) Tejedor-Tejedor, M. I.; Anderson, M. A. Protonation of phosphate
on the surface of goethite as a studied by CIR-FTIR and
electrophoretic mobility. Langmuir 1990, 6, 602–611.
(16) Parikh, S. J.; Chorover, J. ATR-FTIR spectroscopy reveals bond
formation during bacterial adhesion to iron oxide. Langmuir
2006, 22, 8492–8500.
(17) Voegelin, A.; Hug, S. J. Catalyzed oxidation of arsenic(III) by
hydrogen peroxide on the surface of ferrihydrite: An in situ
ATR-FTIR study. Environ. Sci. Technol. 2003, 37, 972–978.
(18) Chernyshova, I. V. An in situ FTIR study of galena and pyrite
oxidation in aqueous solution. J. Electroanal. Chem. 2003, 558,
83–98.
(19) Violante, A.; Pigna, M. Competitive sorption of arsenate and
phosphate on different clay minerals and soils. Soil Sci. Soc.
Am. J. 2002, 66, 1788–1796.
(20) Luengo, C.; Brigante, M.; Avena, M. Adsorption kinetics of
phosphate and arsenate on goethite. A comparative study. J.
Colloid Interface Sci. 2007, 311, 354–360.
(21) Roberts, L. C.; Hug, S. J.; Ruettimann, T.; Billah, M.; Khan, A. W.;
Rahman, M. T. Arsenic removal with iron(II) and iron(III) waters
with high silicate and phosphate concentrations. Environ. Sci.
Technol. 2004, 38, 307–315.
(22) Villalobos, M.; Toner, B.; Bargar, J.; Sposito, G. Characterization
of the manganese oxide produced by Pseudomonas putida strain
MnB1. Geochim. Cosmochim. Acta 2003, 67, 2649–2662.
(23) Manning, B. A.; Fendorf, S. E.; Goldberg, S. Surface structures
and stability of arsenic(III) on goethite: Spectroscopic evidence
VOL. 44, NO. 10, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
9
3777
(24)
(25)
(26)
(27)
(28)
(29)
(30)
(31)
(32)
(33)
3778
for inner-sphere complexes. Environ. Sci. Technol. 1998, 32,
2383–2388.
Sun, X. H.; Doner, H. E. An investigation of arsenate and arsenite
bonding structures on goethite by FTIR. Soil Sci. 1996, 161,
865–872.
Amirbahman, A.; Kent, D. B.; Curtis, G. P.; Davis, J. A. Kinetics
of sorption and abiotic oxidation of arsenic(III) by aquifer
materials. Geochim. Cosmochim. Acta 2006, 70, 533–547.
Manning, B. A.; Suarez, D. L. Modeling arsenic(III) adsorption
and heterogeneous oxidation kinetics in soils. Soil Sci. Soc. Am. J.
2000, 64, 128–137.
Reynolds, J. G.; Naylor, D. V.; Fendorf, S. E. Arsenic sorption in
phosphate-amended soils during flooding and subsequent
aeration. Soil Sci. Soc. Am. J. 1999, 63, 1149–1156.
Gadde, R. R.; Laitlinen, H. A. Studies of heavy metal adsorption
by hydrous iron and manganese oxides. Anal. Chem. 1974, 46,
2022–2026.
Schwertmann, U.; Cornell, R. M. Iron oxides in the Laboratory:
Preparation and Characterization, 2nd ed.; Wiley-VCH: Weinheim, 1991.
Phillips, S. E.; Taylor, M. L. Oxidation of arsenite to arsenate by
Alcaligenes-faecalis. Appl. Environ. Microbiol. 1976, 32, 392–
399.
Anderson, G. L.; Williams, J.; Hille, R. The purification and
characterization of arsenite oxidase from Alcaligenes-faecalis,
a molybdenum-containing hydroxylase. J. Biol. Chem. 1992,
267, 23674–23682.
Mihaljevic, M.; Ettler, V.; Sisr, L.; Sebek, O.; Strnad, L.; Vonaskova,
V. Effect of low concentrations of phosphate ions on extraction
of arsenic from naturally contaminated soil. Bul. Environ.
Contam. Toxicol. 2009, 83, 422–427.
Jackson, B. P.; Bertsch, P. M.; Cabrera, M. L.; Camberato, J. J.;
Seaman, J. C.; Wood, C. W. Trace element speciation in poultry
litter. J. Environ. Qual. 2003, 32, 535–540.
9
ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 44, NO. 10, 2010
(34) Peryea, F. J.; Kammereck, R. Phosphate-enhanced movement
of arsenic out of lead arsenate-contaminated topsoil and through
uncontaminated subsoil. Water, Air, Soil Pollut. 1997, 93, 243–
254.
(35) Nesbitt, H. W.; Canning, G. W.; Bancroft, G. M. XPS study of
reductive dissolution of 7 angstrom-birnessite by H3AsO3, with
constraints on reaction mechanism. Geochim. Cosmochim. Acta
1998, 62, 2097–2110.
(36) Foster, A. L.; Brown, G. E.; Parks, G. A. X-ray absorption fine
structure study of As(V) and Se(IV) sorption complexes on
hydrous Mn oxides. Geochim. Cosmochim. Acta 2003, 67, 1937–
1953.
(37) Sun, X. H.; Doner, H. E. Adsorption and oxidation of arsenite
on goethite. Soil Sci. 1998, 163, 278–287.
(38) Peirce, M. L.; Moore, C. B. Adsorption of arsenite on amorphous
iron hydroxide from dilute aqueous solution. Environ. Sci.
Technol. 1980, 14, 214–216.
(39) Fendorf, S.; Eick, M. J.; Grossl, P.; Sparks, D. L. Arsenate and
chromate retention mechanisms on goethite. 1. Surface structure. Environ. Sci. Technol. 1997, 31, 315–320.
(40) Feng, X. H.; Tan, W. F.; Liu, F.; Ruan, H. D.; He, J. Z. Oxidation
of As-III by several manganese oxide minerals in absence and
presence of goethite. Acta Geol. Sin. 2006, 80, 249–256.
(41) He, Y. T.; Hering, J. G. Enhancement of Arsenic(III) Sequestration
by Manganese Oxides in the Presence of Iron(II). Water, Air,
Soil Pollut. 2009, xxx. in press.
(42) Schmitt, J.; Flemming, H. C. Water Binding in Biofilms. Water
Sci. Technol. 1999, 39, 77–82.
(43) Chen, Z.; Kim, K. W.; Zhu, Y. G.; McLaren, R.; Liu, F.; He, J. Z.
Adsorption(As-III, As-V) and oxidation (As-III) of arsenic by
pedogenic Fe-Mn nodules. Geoderma 2006, 136, 566–572.
ES903408G