Beruflich Dokumente
Kultur Dokumente
Department of Hydraulic and Environmental Engineering, Ponticia Universidad Catlica de Chile, Santiago, Chile
Department of Civil and Environmental Engineering, The Pennsylvania State University, University Park, PA, USA
H I G H L I G H T S
a r t i c l e
i n f o
Article history:
Received 15 January 2013
Received in revised form 29 June 2013
Accepted 2 July 2013
Available online xxxx
Editor: F.M. Tack
Keywords:
Fluvial arsenic
Biological arsenic oxidation
AroA-like
Chemical arsenic speciation
Altiplano
a b s t r a c t
Rivers in northern Chile have arsenic (As) concentrations at levels that are toxic for humans and other organisms. Microorganism-mediated redox reactions have a crucial role in the As cycle; the microbial oxidation of
As (As(III) to As(V)) is a critical transformation because it favors the immobilization of As in the solid phase.
We studied the role of microbial As oxidation for controlling the mobility of As in the extreme environment found
in the Chilean Altiplano (i.e., N4000 meters above sea level (masl) and b 310 mm annual rainfall), which are conditions that have rarely been studied. Our model system was the upper Azufre River sub-basin, where the natural
attenuation of As from hydrothermal discharge (pH 46) was observed. As(III) was actively oxidized by a microbial consortium, leading to a signicant decrease in the dissolved As concentrations and a corresponding increase
in the sediment's As concentration downstream of the hydrothermal source. In-situ oxidation experiments demonstrated that the As oxidation required biological activity, and microbiological molecular analysis conrmed the
presence of As(III)-oxidizing groups (aroA-like genes) in the system. In addition, the pH measurements and solid
phase analysis strongly suggested that the As removal mechanism involved adsorption or coprecipitation with
Fe-oxyhydroxides. Taken together, these results indicate that the microorganism-mediated As oxidation contributed to the attenuation of As concentrations and the stabilization of As in the solid phase, therefore controlling the
amount of As transported downstream. This study is the rst to demonstrate the microbial oxidation of As in
Altiplano basins and its relevance in the immobilization of As.
2013 Elsevier B.V. All rights reserved.
1. Introduction
Arsenic (As) is a toxic element widely distributed in natural environments (Cullen and Reimer, 1989; Smedley and Kinniburgh, 2002).
The contamination of surface and groundwater by As is a serious
environmental concern because such contamination limits the use
of the water and has adverse effects on human health (Berg et al.,
Corresponding author at: Departamento de Ingeniera Hidrulica y Ambiental, Escuela
de Ingeniera, Ponticia Universidad Catlica de Chile, Vicua Mackenna 4860, Macul,
Santiago, Chile. Tel.: +56 2 2354 4872; fax: +56 2 2354 5876.
E-mail address: ppasten@ing.puc.cl (P.A. Pasten).
0048-9697/$ see front matter 2013 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.scitotenv.2013.07.009
E.D. Leiva et al. / Science of the Total Environment 466467 (2014) 490502
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E.D. Leiva et al. / Science of the Total Environment 466467 (2014) 490502
Fig. 1. (a) Map of Chile highlighting the location of the upper section of the Azufre River sub-basin in the Lluta River watershed of northern Chile; (b) transects selected for the
study. Each transect drains into the Azufre River.*Distance after the origin of the Azufre River (panel a).
coupled with the oxidation of inorganic As(III) under aerobic, nitratereducing, or denitrifying conditions (Oremland et al., 2002; Rhine
et al., 2006; Santini et al., 2002). Microbial oxidation of As is mediated
by enzymes called arsenite oxidases, such as AroA/B, AsoA/B, and
AoxA/B (Inskeep et al., 2007; Kashyap et al., 2006; Lebrun et al., 2003;
Santini and vanden Hoven, 2004). In hydrothermal systems, the As(III)
oxidation activity correlates to the presence of arsenite-oxidizing microorganisms (Hamamura et al., 2009; Inskeep et al., 2007; Macur et al.,
2004). However, there is no information available concerning the impact of arsenite-oxidizing microorganisms on hydrothermal systems at
E.D. Leiva et al. / Science of the Total Environment 466467 (2014) 490502
mixes downstream with more alkaline waters (pH increase), consequently forming Al hydroxides and Fe oxyhydroxides (Guerra et al.,
2012). These solid phases are well-known sorbents of As and occur as
suspended solids or coatings on other particles, which are transported
downstream or deposited depending on the ow velocity. Intense
storms during the wet season trigger events that mobilize As-enriched
sediments deposited along the river bed. The imminent construction
of a dam to increase water availability throughout the year for agricultural purposes causes additional concern because the new structure
will most likely become an As repository. The microbial reactions that
control the inux of As at the head waters play a signicant role in the
overall As budget and the ux of As into the Lluta River Valley water
resources. Specically, this research was performed to investigate the
inuence of the As oxidation processes mediated by arsenite oxidizers
on the changes in As speciation and attenuation within a hydrothermal
spring; these ndings will aid the development of future remediation
strategies. Furthermore, we also expect that this case will serve as a
model for other high-altitude hydrothermal systems containing elevated AsD concentrations of reduced As in the CVZ.
3. Methods
3.1. Experimental design in the study site, sampling and on site
measurements
The hydrothermal site chosen for detailed study in this work is
located on the west ank of the Tacora volcano (Fig. 1b). Two hot surface runoff channels that drain from the same hot spring were chosen
for a transect sampling, each containing four sampling points for
hydrogeochemical and microbiological analyses. The average ow
velocities were 25.4 cm s1 in transect 1 and 12.9 cm s1 in transect
2, based on suspended particle travel times within a distance of 2 m
in the surface water ow (procedure modied from Langner et al.,
2001). The transects were selected based on preliminary data analyses from July, 2010 that indicated a decrease in the AsD concentrations downstream from the discharge of the hydrothermal spring
source. In addition, the sampling points were chosen based on their
proximity to high concentrations of Fe-oxyhydroxides, allowing
the simultaneous evaluation of the effects caused by the changes
in As speciation and the natural attenuation of AsD concentrations
(adsorption onto Fe-oxyhydroxides).
As-rich waters, sediments, and microbial samples were collected
from ve eld campaigns, occurring in October 2010, February 2011,
July 2011, November 2011, and May 2012. Water samples from the
Azufre River were collected in 300 ml High Density Polyethylene
(HDPE) bottles and were immediately ltered in the eld with 0.22-m
nylon lters. Filtered subsamples were acidied with HNO3 (1:100 v/v,
Merck) for the analysis of the AsD concentration (McCleskey et al.,
2004). Unltered subsamples were also acidied to a pH of approximately 2 in the eld with HNO3 immediately after sampling (1:100 v/v,
Merck) for total As (AsT) (includes particulate As) concentration analysis
along the river.
Water samples from the hydrothermal transects were collected
in 300 ml HDPE bottles and immediately ltered in the eld with
0.22-m nylon lters. Filtered subsamples were acidied to pH 2
with HNO3 for later laboratory measurements of AsD, total dissolved
Fe (FeD) concentrations, and major dissolved cation analysis (sodium,
potassium, calcium). For the As speciation analysis (As(III) and
As(V)), the ltered subsamples were acidied in the eld to a pH of
approximately 3 with HCl (1:100 v/v, Merck) (McCleskey et al.,
2004).
Additional ltered and non-acidied water samples were collected along the Azufre River and in sampling points of the hydrothermal transects for the later determination of dissolved anions (sulfate,
nitrate, and chloride) analysis. All water samples (ltered/acidied,
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unltered/acidied, and ltered/non-acidied) were stored in darkness at 4 C until processing and analysis occurred within 1 week of
sampling.
The on-site water analyses included temperature (PHC301, HACH),
pH (PHC301, HACH), dissolved oxygen (DO) (LDO101, HACH), and
electrical conductivity (CDC401, HACH) (Hq40d Multi, HACH, Loveland,
CO, USA). Undisturbed surface sediment samples (depth 6 cm) at each
sampling point of the hydrothermal transects were collected with
50 ml polypropylene tubes (BD Biosciences, Mountain View, CA) and
150 ml HDPE bottles, and were kept in darkness at 4 C until processing
and analysis.
3.2. Hydrogeochemical and solid-phase analyses
AsT (unltered, acid-soluble), AsD (ltered, acid-soluble), and FeD
(ltered, acid-soluble) analyses in water samples were carried out
by Total X-ray Reection Fluorescence (TXRF) (S2 Picofox, Total
X-ray reection uorescence spectrometer, Bruker AXS, Billerica,
MA, USA) (Borgese et al., 2009). The AsT, AsD, and FeD concentrations
in the water samples were conrmed by Inductively Coupled Plasma
Optical Emission Spectrometry (ICP-OES) (PerkinElmer Optima 7300
DV ICP-OES, Shelton, CT, USA) (data not shown). The dissolved inorganic As species [As(III) and As(V)] were measured in the laboratory
using ltered/HCl-acidied subsamples. The dissolved As(III) concentrations were determined by hydride generation with cysteine and
sodium borohydride reductants, as well as Inductively Coupled Plasma Mass Spectrometry (ICP-MS) detection (PerkinElmer ELAN 6100,
Shelton, CT, USA) (detection limit b 0.002 mg l1) (Garbarino et al.,
2002). The As(V) concentration was determined by subtracting the
As(III) content from the AsD concentration measured with TXRF.
The contents of the dissolved inorganic Fe species [Fe(II) and Fe(III)]
were determined by spectrophotometry. The ferrous (Fe(II)) iron concentration was determined in the eld immediately after sampling in
ltered/non-acidied subsamples with a HACH spectrophotometer
DR/2010 (110 Phenanthroline method 8146, adapted from Standard
Methods for the examination of water and wastewater 15th ed 201
(1980)) (HATCH, Loveland, CO, USA). Ferric (Fe(III)) iron concentration
was determined by subtracting the Fe(II) content from the FeD concentration measured with TXRF. Sodium, potassium, and calcium were
analyzed via ICP-OES from the ltered/acidied subsamples. Sulfate,
nitrate, and chloride were analyzed using Ion Chromatography (IC)
(882 compact IC plus, Metrohm, Herisau, Switzerland) with ltered/
non-acidied subsamples.
The sediment samples were dried at 40 C and the analysis of the
total As in the solid phase was performed with the prior microwave
digestion (Microwave Accelerated Reaction Systems, model MARS
(CEM corporation, Mattheus; North Carolina 28106)) of ~ 100 mg of
dry sample (b2 mm) in 9 ml of concentrated HNO3 and 3 ml of concentrated HCl (EPA method 3051A). The As content of the digests was
determined by TXRF. The results of the As analyses in the solid phase
were conrmed by ICP-OES (PerkinElmer Optima 7300 DV ICP-OES,
Shelton, CT, USA) (data not shown).
3.3. Analytical quality control
Continuous quality assurance/quality control (QA/QC) procedures
were performed for both the eld measurements and laboratory
analyses by TXRF, ICP-OES and IC. All eld and laboratory instruments
were calibrated using certied reference standards or analytical grade
synthetic standards. The acceptable standard deviation for results of
metals, cations, and anions was always b10%, and all analyses were
interspersed with and checked against standard reference materials.
The AsT, AsD and FeD measurements of the water samples and the
As content of acid digest samples were measured by TXRF in triplicate. The QC of the measurement was performed by inserting a synthetic standard with a known concentration of As and Fe into the
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4. Results
greater reduction (from 3.4 to less than 1.0 mg l1) along this same
length of the river that cannot be explained solely by this phenomenon
(the stream ow increases only 2.1 times). Based on these data, we studied the attenuation of As in hydrothermal transects in this area of the
wetland.
The AsT and AsD concentrations along the Azufre River were
observed between 3.4 and 1.0 mg l1 (Fig. 2a), widely exceeding the
maximum level for drinking water (10 g l1) (WHO, 1993). The AsT
and AsD were very high at the origin of the Azufre River (distance
0 m) (3.4 0.3 mg l1 and 3.1 0.3 mg l1, respectively), possibly
due to hydrothermal discharges with high As concentrations. There
were no signicant differences between the AsT and AsD concentrations because the pH along the river was very low b2.5, preventing
the sequestration of As by particulate solids.
Downstream of the Azufre River, in the wetland area (4001500 m)
the AsT and AsD concentrations decreased. This decrease was explained
by a dilution effect caused by owing water with lower As concentrations
and by the active natural As attenuation processes in this area. The ow in
the Azufre River is ~14 l s1 upstream of the wetland and ~30 l s1
downstream of the wetland. The dilution effect is made evident by
changes in chloride concentrations (Fig. 2b), which decreased by approximately 60% (from 536 to 205 mg l1). The AsD concentrations exhibit a
ratios
(data not shown). The AsD/SO2
4 , AsD/Na , and AsD/Cl
exhibited a marked reduction in both transects, which was likely
inuenced by the AsD attenuation along the two transects.
restriction enzyme (HhaI and MspI), and these datasets were crossed
to rene the assignment of candidate species at the sampling point.
Fig. 2. Decreases in the AsT and AsD concentrations (a); and dissolved chloride
(b) along the Azufre River in the wetland area. The graphs are presented relative to the
distance from the origin point of the Azufre River (P1). Altitude (masl) is shown for reference. The wetland area extends between 400 and 1500 m after the origin of the Azufre
River. The data are presented as the mean SEM (error bars).
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Fig. 3. As concentrations in the sampling points of transect 1 (a) and transect 2 (b). The AsD concentrations are expressed as the relative concentration (Ci/C0) down gradient of the
discharge from the hydrothermal source (Ci = concentration at distance i, C0 = concentration at source). C0 in aqueous phase was 0.8 0.2 mg l1. The data are presented as the
mean SEM (error bars).
was active in this area. In particular, the reduction in the As concentrations in the surface runoff of hydrothermal waters reveals the
presence of active As stabilization processes. Additionally, there
were no signicant changes in the ionic matrix of this runoff to suggest any local dilution processes were occurring.
The stability of the conductivity (approximately 4 mS cm1) along
both transects suggests that there is no mixture of waters to explain
the results of As attenuation; although the evidence is compelling, it is
not conclusive. However, the conservative behavior of the anions and
cations observed in both transects precludes the possibility of dilution.
+
ratios
The obvious reduction in the AsD/SO2
4 , AsD/Na , and AsD/Cl
supports the hypothesis that the As attenuation has a different geo+
5. Discussion
5.2. Arsenic stabilization occurs onto Fe minerals
5.1. Arsenic natural attenuation occurs in the transects
The difference between the reduction of chloride concentrations
(~ 60%) and the reduction in the As concentrations (~ 71%) along the
Azufre River indicates than an active natural As attenuation process
Fig. 4. Solid phase As concentrations in the sampling points of transect 1 (a) and transect 2 (b). The As concentrations in the solid phase are expressed as the relative concentrations
(Ci/C0) down gradient of the discharge from the hydrothermal source (Ci = concentration at distance i, C0= concentration at source). C0 in solid phase was 6.4 1.7 mg kg1 soil.
The data are presented as the mean SEM (error bars).
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497
Fig. 5. Geochemical parameters in the water samples from the sampling points of transect 1 (a) and transect 2 (b). DO () and temperature () reveal the expected behavior for
hydrothermal waters in contact with the atmosphere. The decrease in pH () is important for the adsorption processes of As, and stability of the conductivity () suggests that
there is no dilution. The data are presented as the mean SEM (error bars).
formation of ferric arsenate precipitates are the main natural attenuation processes for the removal of As (Drahota et al., 2012; Haffert
and Craw, 2008; Leblanc et al., 1996), supporting the hypothesis of
the relevance of these minerals in the attenuation of As in the studied
transects (Fig. 3). Incidentally, amorphous Fe-oxyhydroxides have a
high adsorption capacity for As because they have a large surface
area and therefore provide more active sorption sites (Wang and
Mulligan, 2006). Consequently, the presence of unidentied amorphous Fe-oxyhydroxides lends credence to the idea that these minerals are crucial for the attenuation of As observed in both transects.
The obvious As(III) oxidation to As(V) in both transects could
enhance the adsorption of As onto Fe-oxyhydroxides under varying pH
conditions. As(V) interacts with Fe-oxyhydroxides more strongly than
As(III) (Oremland and Stolz, 2003) because the adsorption mechanism
is strongly inuenced by pH changes. Therefore, the As(III) oxidation
to As(V) and the subsequent As(V) adsorption onto Fe-oxyhydroxides
might explain the As attenuation observed downstream from the
hydrothermal streams.
The presence of similar Fe concentrations in the solid phase of
both transects downstream of the hydrothermal source suggests
that changes in the concentrations of As in the aqueous phase were
due to an active process at the solidliquid interface and not by increasing As sorbent concentrations (Fe-oxyhydroxides). pH decrease
along the transects supports this because at low pH it does not
favor the formation of these minerals. However, the circumneutral
pH in the hydrothermal source and the presence of Fe(III) in the
aqueous phase may favor the formation of Fe-oxyhydroxides in this
location and therefore increase the availability of sediments with
free surface sites for As(III) adsorption. This phenomenon would explain the higher As concentrations in solid phase at this location
(source) (Fig. 4). Additionally, the co-precipitation of As and Fe can
also occur during the formation of Fe-oxyhydroxides (e.g., Ferrihydrite),
which may help to mitigate the As concentration in aqueous phase
(Fuller et al., 1993). Additionally, the co-precipitation of As(V) and
Fe(III) may be favored by the As(III) oxidation (Jia and Demopoulos,
2008; Richmond et al., 2004; Twidwell et al., 2005). However, the low
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Fig. 6. Sulfate, sodium, and chloride concentrations in the sampling points of study transect 1 (a) and transect 2 (b). AsD/SO2
4 , AsD/Na , and AsD/Cl ratios in study transect 1 (c) and
transect 2 (b). Both transects reveal the stability of ion concentrations between the different sampling points. The AsD/ion ratios indicate a marked reduction in both transects. The ratios
were calculated from the As and ion concentrations (mg l1) and were plotted by multiplying the values by 104. The data are presented as the mean SEM (error bars).
Fig. 7. Arsenite oxidation in the water samples from transect 1 (a) and transect 2 (b). Concentrations of As(III) and As(V) are presented relative to the concentration of the total AsD.
There is an obvious oxidation of As in both transects from the hydrothermal source (0 m).
E.D. Leiva et al. / Science of the Total Environment 466467 (2014) 490502
499
Fig. 8. Fe speciation (Fe(II) and Fe(III)) in the water samples from transect 1 (a) and transect 2 (b). Concentrations of Fe(II) and Fe(III) are presented relative to the concentration of
the total dissolved Fe. In both transects, Fe(III) predominates over Fe(II) and is stable along the transects.
at low pH) (Chiu and Hering, 2000; Oscarson et al., 1983). Although Mn
oxides may form on the surface of Fe-oxyhydroxides and As(III) can be
oxidized more rapidly at high temperatures (N48 C) through a photocatalytic process (Schwenzer et al., 2001), the low concentrations of Mn
in solid phase (b 0.5 g kg1) and the results of in-situ experiments
discount this mechanism. Additionally, the formation of Mn oxides is
favored at a higher pH than those observed in this system (pH 46)
(Morgan, 1967).
The photochemical oxidation of As(III) was also studied by Hug
et al. (2001), who observed a 90% removal of As(III) within 2 to 3 h
in solutions containing Fe(II, III) and citrate. At 25 C under natural
sunlight, the half-life of As(III) is 0.7 h at pH 5 in a solution of
18 M Fe(III) and 100 mg l1 DOC (Kocar and Inskeep, 2003).
Accordingly the photocatalytic As oxidation has faster kinetics
(hours) than a strictly oxygen-dependent abiotic As oxidation. However, the lack of signicant differences between the in situ oxidation
Fig. 9. In-situ As(III) oxidation assays with sediments from transect 1 (a) and transect 2 (b). As oxidation is evident when the biological activity is not inhibited by formaldehyde.
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Fig. 10. Agarose gel displaying the amplication of an aroA-like gene (a) and aroA-like expression (b) in the microbial samples from the study transects. All samples were also
supplemented with 1 ppm As(III) to conrm the aroA-like gene's functional role (lower panel of (b)). The 16S rRNA gene was used as a control for DNA quality, and Agrobacterium
tumefaciens 5A was a positive control for arsenite oxidase activity.
Table 1
Closest matching species from the 16S rRNA gene T-RFs assignment in the 16S rRNA databases. The microbial characterization corresponds to the hydrothermal source (0 m).
Closest match species
AroA-like microorganisms
Hydrogenophaga sp. str. CL3
Thiobacillus sp. str. S1
Thermus thermophilus
Other microorganisms
Uncultured eubacterium env. OPS 6
Uncultured eubacterium clone BBACe10
Uncultured Chloroexi bacterium
Uncultured bacterium
Uncultured bacterium
a
b
16S rRNA
acc. no.
(GenBank)
AroA-like
acc. no.
(GenBank)
Phylogenetic afliation
Arsenic metabolism
AroA-like gene
DQ986320
DQ986319
X07998, NC_006461
EF015462
EF015459
BAD71923
-Proteobacteria
-Proteobacteria
DeinococcusThermus
CAOa
CAOa
HAOb
aroAB
aroAB
aroAB
AF018191
GU357466
HQ397171
HQ397189
HQ397194
DA067
GQ921453
GQ921460
GQ921465
Chloroexi
-Proteobacteria
E.D. Leiva et al. / Science of the Total Environment 466467 (2014) 490502
6. Conclusions
Our results indicate that there was a natural attenuation of As in the
model system. The AsD concentrations decreased along the transects,
while the conservative ion concentrations along the transects discount
the possible effects of dilution or mixing of waters. The rapid oxidation
of As(III), which occurred within a few meters of the hydrothermal
source (As(V)/AsD increases of +95% [transect 1] and + 100% [transect 2]), suggests the possible involvement of As oxidation in the natural
attenuation process. The increase in the As concentrations in the solid
phase after the source correlates with the As oxidation in transects 1
and 2, suggesting that the stabilization is mediated by the adsorption
of As onto Fe-oxyhydroxides and controlled by the environmental pH.
The results of the in-situ oxidation experiments reveal that live microorganisms were required to catalyze the As(III) oxidation at the studied
time scale. Complementary microbiological molecular analyses support
these ndings and suggest that both the oxidation of As(III) and the attenuation of AsD is mediated directly by microorganisms via enzymatic
activity (AroA-like). The results of the aroA-like gene expression suggests that changes in the expression of this gene can depend upon
As(III) concentration. The T-RFLP analysis supported the presence of
arsenite-oxidizing bacteria in the studied area and reveals the autotrophic and heterotrophic metabolisms that are most likely to be active in
the As oxidation.
Our ndings contribute to a better understanding of biogeochemical processes of As oxidation, as well as the biogeochemical controls
of As in uvial systems impacted by As-rich hydrothermal discharges;
these As-rich hydrothermal discharges occur in upper section of the
Azufre River sub-basin. The description of the microbial As oxidation
reactions involved in these processes is crucial for improving our understanding of the As cycle in extreme, arid environments. Together,
these results illustrate the complexity of the interactions involved in
the mobilization and stabilization of As due to the interplay between
redox and sorption reactions at the mineral-liquid interface involving
biotic and abiotic reactions at different scales.
Future research should include detailed spectroscopic analysis of the
solid-phases to determine the speciation of As and Fe on the surface of
the Fe minerals and to conrm the specic mechanisms involved in the
stabilization of As at the molecular level. Additional efforts are necessary to describe the environmental conditions that might inhibit or enhance this attenuation process. This knowledge is crucial for the design
of effective risk management and remediation efforts for uvial systems
enriched with As from hydrothermal discharges.
Acknowledgments
This research was supported by a FONDECYT 1100943/2010, a
FONDECYT 1130936/2013, and a CONICYT grant 24121233/2012, as
well as Fulbright Scholar Award 9561 for J.M.R. This study was also partially supported by a CORFO 09CN14-5709 grant and a CONICYT/FONDAP
15110020 grant. Thanks are extended to the reviewers for the corrections and suggestions, which signicantly improved the manuscript.
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