Delineating the Convergence of Biogeochemical Factors Responsible for Arsenic Release to Groundwater in South and Southeast Asia

CHAPTER TWO

Delineating the Convergence of Biogeochemical Factors Responsible for Arsenic Release to Groundwater in South and Southeast Asia J.W. Stuckey*,1, D.L. Sparks*, S. Fendorf** *

Delaware Environmental Institute, Interdisciplinary Science and Engineering Laboratory, Newark, DE, United States Department of Earth System Science, Stanford University, Stanford, CA, United States

**

1

Corresponding author. E-mail address: [email protected]

Contents 1. Introduction 2. Spatial Distribution of Factors Controlling Arsenic Release 2.1 Suboxic/Anoxic Conditions and Sulfur Supply 2.2 As(V)/Fe(III)-Reducing Microorganisms 2.3 Reactive As-Fe Complex 2.4 Reactive Organic C 3. Arsenic Release in Near-surface Permanently Saturated Soils/sediments 4. Implications for Arsenic Mitigation in South/southeast Asian Groundwater Acknowledgments References

44 46 46 46 50 53 59 62 64 64

Abstract Arsenic (As), a toxic metalloid common throughout the Earth’s crust, accounts for the most widespread poisoning of a human population in history. Within the major deltas of South and Southeast (S/SE) Asia, rivers annually deposit As-bearing iron oxides, oxyhydroxides, and hydroxides (collectively referred to as Fe oxides hereafter) derived from the Himalaya. The high primary productivity and monsoonal flooding in the tropical deltas promote microbially driven As release to groundwater through dissimilatory As(V)/Fe(III) reduction. Groundwater is a primary source of drinking and irrigation water in the region, especially within rural areas. Prolonged consumption of

Advances in Agronomy, Volume 140 ISSN 0065-2113 http://dx.doi.org/10.1016/bs.agron.2016.06.002

© 2016 Elsevier Inc. All rights reserved.

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As-contaminated groundwater can lead to a multitude of serious health complications, including cancer and cardiovascular disease. Here we define the parameters controlling the locations of active microbially driven As release to groundwater, including suboxic/anoxic conditions, microbial communities capable of mediating As(V)/Fe(III) reduction, the reactivity of As-bearing Fe oxides, and the sources and reactivity of organic carbon (C). Conditions for microbially driven As release are optimized where the reactivity of both As-bearing Fe oxides and organic C is greatest. Optimal conditions for As release are found in near-surface sediments of the Red River, under permanent wetlands of the Mekong River, and at depth (∼20 m) in the Yangtze River Basin, whereas findings are variable within the Bengal Basin. Land and water management changes resulting in increased flood duration in deltaic environments may result in new locations of active microbial As release to groundwater.

1. INTRODUCTION Arsenic is a toxic element occurring naturally in the Earth’s crust at an average concentration of 5 mg kg
1, and may be enriched by geothermal activity, mining, and pesticide use (Garelick et al., 2008). Arsenic in soils and sediments presents increased risk to human health when partitioning from the solid to aqueous phase occurs, as drinking contaminated water is the most direct means of exposure. Oxyanions of pentavalent As (AsO43
, known as arsenate) and trivalent arsenite (AsO33
) are the most common species of As in groundwater. Arsenate, mimicking inorganic phosphate, interferes with cellular metabolism (Dixon, 1997). However, within the human body, arsenate is reduced to the more toxic arsenite, which possesses a high affinity for sulfhydryl groups commonly found in cellular enzymes (Hughes, 2006). Arsenite is methylated to monomethylarsenite and finally to dimethylarsenite before excretion (Hayakawa et al., 2005; Marapakala et al., 2012; Vahter and Concha, 2001). Chronic exposure to As through drinking water can lead to a myriad of cancers, chronic respiratory symptoms and renal disease, cardiovascular disease, skin lesions, diabetes, and neurological impairments (Argos et al., 2010; Bra¨uner et al., 2014; Chen and Ahsan, 2004; Chen et al., 2011; Dauphine et al., 2011; Karagas et al., 2015; Ramos-Cha´vez et al., 2015; Smith et al., 1992, 2012, 2013; von Ehrenstein et al., 2005). Large-scale human exposure to As results from geogenic sources in the major rivers basins of S/SE Asia (Berg et al., 2007; Buschmann et al., 2008; Chakraborti et al., 2013; Currell et al., 2011; Fatmi et al., 2013; He and Charlet, 2013; Phan et al., 2010; Wang et al., 2012; Zhang et al., 2012).

Delineating the Convergence of Biogeochemical Factors

45

In the Bengal Basin alone, 100 million people are currently at risk to chronic As exposure through drinking contaminated groundwater (Rahman et al., 2015). Weathering of Himalayan As-bearing rock in basin headwaters followed by riverine transport and monsoonal flooding leads to widespread deposition of As-bearing sediment in deltaic regions (Saunders et al., 2005). The high primary productivity and annual monsoonal flooding in tropical deltas promote factors leading to As release to groundwater, namely the codeposition of organic C and As-bearing sediment under reducing conditions (Meharg et al., 2006). Here, microbially driven oxidation of organic C coupled to the dissimilatory reductive dissolution of As-bearing Fe oxides causes the transfer of As from sediment solids to groundwater (Akai et al., 2004; Islam et al., 2004; McArthur et al., 2001; Nickson et al., 1998, 2000; Van Geen et al., 2004): CH2 O þ 4FeOOH
ðH2 AsO4 Þx þ ð7 þ 3xÞHþ ⇔ 4Fe2þ þHCO
3 þ ð6 þ xÞH2 O þ xH3 AsO3

ð1Þ

where CH2O generically represents organic C and may include other fermentation products such as H2(aq), As (as arsenate) is bound to sedimentary Fe oxide (goethite as written) and x is the stoichiometric coefficient of As content associated with the Fe oxides [∼ 0.0002 in S/SE Asian sediments (Kocar and Fendorf, 2009; Stuckey et al., 2016)]. Dissimilatory As(V)/Fe(III) reduction (Reaction 1) requires (1) anaerobic conditions with low sulfate supply, (2) reactive As-Fe complexes, (3) reactive organic C, and (4) a microbial community equipped for executing the process. In principle, locations of As release across the landscape and/or within a sediment profile could be delineated based on the coincidence of these four factors. The source(s) of reactive organic C driving As release to groundwater remains the least resolved factor (Fendorf et al., 2010). This review evaluates surface-derived, near-surface, and subsurface organic C as potential drivers of As release, and adopts current paradigms regarding organic C persistence in soils/sediments to help explain observed As release patterns. Switching to As-safe wells is the most common As mitigation option exercised in the rural areas of Bangladesh, where the largest impacted population resides (Ahmed et al., 2006; George et al., 2012). Moreover, installation of domestic wells continues to increase across S/SE Asia. Thus, maintaining groundwater as a drinking water source requires that we develop the ability to identify areas of active As release to pore-water, areas with low capacity to release As, and to predict changes in release patterns

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over time. In other words, we need to identify the conditions that promote As release, and where these conditions occur across the landscape and within a sediment profile. The governing reaction rates and rate controlling processes/steps of As release need to be defined. Further, the biogeochemical parameterization of As release must be coupled to hydrologic measurements defining groundwater flow, forming the basis for a reactive transport model capable of predicting As concentrations in space and time (Kocar et al., 2014).

2. SPATIAL DISTRIBUTION OF FACTORS CONTROLLING ARSENIC RELEASE 2.1 Suboxic/Anoxic Conditions and Sulfur Supply Rates of oxygen consumption generally exceed the diffusion rate of atmospheric oxygen into groundwater recharge in the low-lying river deltas and sedimentary basins of S/SE Asia, resulting in pervasive suboxic/anoxic conditions throughout sediment profiles (Table 1) (Hasan et al., 2007; Kocar et al., 2008; Mukherjee et al., 2008; Nath et al., 2008; Ni et al., 2016; Pi et al., 2016; Swartz et al., 2004; Zheng et al., 2005). Elevated As levels are often found in groundwater within an Eh range of
200 to +200 mV at circumneutral pH (Berg et al., 2007; Mukherjee and Fryar, 2008; Nguyen and Itoi, 2009; Phuong et al., 2012). More important than Eh values are the actual set of microbial metabolic processes occurring within an environment. High As levels are found in areas devoid of present or past sulfate reduction, indicated by low sulfate and sulfide levels (Buschmann and Berg, 2009; Jessen et al., 2008). Colocalized sulfate reduction and Fe(III) reduction can sequester As through Fe sulfide precipitation (Lowers et al., 2007; Stuckey et al., 2015b).

2.2 As(V)/Fe(III)-Reducing Microorganisms Several studies have probed the spatial distribution of As(V)/Fe(III)-reducers in the basins of S/SE Asia. In general, these studies report that anaerobic bacterial communities are more prominent in Holocene sediments than in the underlying Pleistocene sediments in river basins of Asia (Liu et al., 2014; Sultana et al., 2011; Sutton et al., 2009). In the Munshiganj and Jessore districts of Bangladesh, As concentrations ranged from ∼ 0.1–0.2 μM As in the Holocene aquifer (approx. < 150 m), and

Bangladesh (Araihazar Upazila) Bangladesh (Brahmanbaria District) Bangladesh (Munshiganj District) Bangladesh (Rajshahi District) Bangladesh (Satkhira District) Datong Basin, China Hetao Basin, Inner Mongolia Mekong Delta, Cambodia Mekong Delta, Cambodia Mekong Delta, Cambodia Mekong Delta, Vietnam Mekong Delta, Vietnam Red River Delta (Chan Ly Commune) Red River Delta (Hop Ly Commune) Red River Delta (Xuan Khe Commune) West Bengal West Bengal West Bengal

4–89 18–235 5–165 15–79 24–63
0–50 4–23 Not Available 8–12 20–60 Not Available 15–440 Not Available Not Available Not Available
20–400 8–305 5–279


180, +40 +184, +299 +20, +100 +41, +288
40, +210
222,
32 +54, +190
410, +190
86, +350
190, +290
303, +625
260, +124
157, +11
153,
101
154,
102
40, +310
151,
37
160, +206


100 +206 +62 Median = +195 Median =
8
140 +99
65 +110 +70 +14
62
68
135
134 +81
68 +106.5

Zheng et al. (2005) Mukherjee et al. (2008) Swartz et al. (2004) Hasan et al. (2007) Hasan et al. (2007) Pi et al. (2016) Ni et al. (2016) Berg et al. (2007) Kocar et al. (2008) Kocar et al. (2008) Berg et al. (2007) Nguyen and Itoi (2009) Phuong et al. (2012) Phuong et al. (2012) Phuong et al. (2012) Mukherjee and Fryar (2008) Nath et al. (2008) Mukherjee et al. (2008)

Delineating the Convergence of Biogeochemical Factors

Table 1 Ranges and average values of oxidation-reduction potential (Eh) as a function of depth in Asian river basins. Well depth Eh range Eh average Region range (m) (Low, High) (mV) (mV) References

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J.W. Stuckey et al.

had higher bacterial diversity than the Pleistocene aquifer, but no As(V) or Fe(III) reducers were detected; merely bacteria with documented As tolerance/resistance were observed (Sutton et al., 2009). The Pleistocene aquifer had no detectable dissolved As and had a less diverse bacterial community indicative of oxic conditions (Sutton et al., 2009). In the Titas subdistrict of Bangladesh, the shallow aquifer sediments (9–21 m) similarly exhibited greater bacterial diversity including aerobic, facultative, and anaerobic bacteria, while the more oxidized, deeper (85 m) aquifer sediments exhibited predominantly aerobic bacteria (Sultana et al., 2011). Likewise, bacterial diversity reportedly decreased from the Holocene aquifer sediments relative to the underlying Pleistocene aquifer sediments in the Pearl River Delta (Liu et al., 2014). Arsenic-resistant bacteria, which may reduce As(V) through the Ars operon system at high As(V) concentrations (Ji and Silver, 1992), are detected in surface water and groundwater within the Bengal Basin (Chowdhury et al., 2009; Goswami et al., 2015; Paul et al., 2015b). Clostridia, some of which are known Fe(III) reducers and/or contain the As-resistance operon arsD, were identified in 3–10 m deep sediment in Bangladesh using 16S rDNA analysis (Akai et al., 2008). However, the Ars operon system is a detoxification pathway, which upregulates only upon cell stress (Li et al., 2010), and possession of a gene does not equate to expression. The extent to which an upregulated Ars operon within a microbial community influences As(V) reduction in natural sediments remains unclear. Bacterial communities extracted from As-contaminated groundwater from depths of 27–53 m in West Bengal were dominated by genera Pseuodomonas, Flavobacterium, Brevundimonas, Polaromonas. Rhodococcus, Methyloversatilis, and Methylotenera (Paul et al., 2015b). Select strains of Pseudomonas, Brevundimonas, and Rhodococcus contained the arrA gene (Paul et al., 2015b), and isolated strains of Acinetobacter, Arthobacter, Brevundimonas, Pseudomonas, Phyllobacterium, Rhizobium, and Rhodococcus were able to drive As release in microcosm studies apparently by As(V) reduction as a means of detoxification, energy generation, or both (Paul et al., 2015a). The addition of labile organic C to sediments in microcosm incubation studies repeatedly demonstrates microbially driven As release (Freikowski et al., 2013; Postma et al., 2010; Stuckey et al., 2016) (Fig. 1). However, arrA phylotypes and microbial communities in general are often distinct in C-enriched sediments relative to those in the native sediments (He´ry et al., 2015; Islam et al., 2004). Addition of 13C-labeled acetate and As(V)

49

Delineating the Convergence of Biogeochemical Factors

(B)

(A)

1.0

600 Glucose, total Fe

500

0.6

Fe (μM)

As (μM)

0.8

Glucose, total As

0.4

Glucose, As(III)

0.2

Sterile control, total As, As(III) Live control, total As, As(III)

0.0

400

Glucose, Fe(II)

300 200 Sterile control, total Fe, Fe(II) Live control, total Fe, Fe(II)

100 0

0

10

20 Time (d)

30

40

0

10

20 Time (d)

30

40

Figure 1 Induction of dissimilatory As(V) (A) and Fe(III) (B) reduction by 1 mM glucose addition to near-surface (0.1-m deep) sediment of a seasonal wetland of the Mekong Delta in groundwater medium. The glucose-amended, unaltered control, and sterile control (achieved by antibiotic addition) data are presented as circles, squares, and diamonds, respectively. Filled symbols indicate total elemental concentration and empty symbols indicate reduced species concentration. Total elemental concentration data for glucose-amended and unaltered control treatments are from Stuckey et al., 2016.

to 9-m deep sediment in the upper Mekong Delta produced clones with 100% identity with Sulfurospirillum strain NP4 according to 16S rRNA analysis, whereas addition of 13C-labeled acetate without As(V) enriched for gene sequences similar to the known As(V) respiring bacteria Desulfotomaculum and Desulfosporosinus spp. (He´ry et al., 2008; Lear et al., 2007). A bacterium of the As(V)/Fe(III)-respiring Desulfuromonas genus was isolated by enrichment with acetate and As(V) from sediment at the Holocene-Pleistocene boundary at a depth of 35 m in West Bengal, India (Osborne et al., 2015). Geobacter spp. are one of the most commonly found dissimilatory As(V)/ Fe(III) reducing bacteria in river basin sediments of S/SE Asia (He´ry et al., 2015; Ying et al., 2015). In the Nadia District of West Bengal, India, Geobacter spp. were identified throughout the profile down to 30 m (Rowland et al., 2009) following up on an earlier study in which no known As(V)-reducers were located and dissimilatory Fe(III) reduction activity was detected at a depth of 24 m (Gault et al., 2005). At 22 m, Sulfurospirillum- and Geobacter-related bacteria were dominant (44.5% and 25% of 16S rRNA sequences, respectively), and the Sulfurospirillum-related gene sequences had a 99% similarity to those of a known As(V)-respiring Sulfurospirillum (strain NP4) species (He´ry et al., 2008; MacRae et al., 2007; Rowland

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J.W. Stuckey et al.

et al., 2006, 2009). A more recent study at the Nadia District site identified the As(V)-reducing arrA gene related to Geobacter at a depth of 15 m (Hery et al., 2010), and a similar cluster of arrA gene sequences were found in Holocene sediments (11–11.5 m) of the upper Mekong Delta of Cambodia (He´ry et al., 2015). In the same Cambodian field area, a phylogenetically distinct clade of bacteria with highest sequence similarity to As(V)-reducing Geobacter was detected within near-surface clay/silt layers (top 4 m) in four different sites (Ying et al., 2015). No Geobacter sequences were found at 9 m (still in near-surface clay layer), but clone libraries contained ∼ 17% Geobacter sequences in the underlying sandy aquifer (28 m) (Pederick et al., 2007; Rowland et al., 2007). In Holocene and deeper Pleistocene aquifer sediments in the Red River Delta of Vietnam, microbial clone libraries were dominated by α-, β-, and γ- Proteobacteria not known to be able to reduce As(V) or Fe(III) (Al Lawati et al., 2012). Geobacter were detected at low abundance by PCR of 16S rRNA genes (Al Lawati et al., 2012). No correlations between groundwater As concentrations and microbial community inclusive of arrA phylotype have been detected (Al Lawati et al., 2012; Ying et al., 2015), likely complicated by As transport from the site of As(V) reduction through groundwater flow. Though Geobacter spp. are the most conspicuous potential culprits driving dissimilatory As(V)/Fe(III) release in S/SE Asian deltaic sediments, a definitive link between Geobacter (or other identified Fe(III)/As(V) reducers) and As release to groundwater remains to be demonstrated (He´ry et al., 2015; Ying et al., 2015). At the very least, microbial communities poised for dissimilatory As(V)/Fe(III) reduction appear more prominently within shallower Holocene sediments than in deeper Pleistocene strata—a finding consistent with As release to groundwater.

2.3 Reactive As-Fe Complex 2.3.1 Arsenic Bangladesh sediments generally have total As concentrations less than 3 mg As kg
1 (Dowling et al., 2002; Swartz et al., 2004). In the Red River Delta and Cambodian Mekong Delta, total As concentrations are highest in nearsurface (< 15 m) clay layers (∼ 10–20 mg As kg
1) before levels in underlying sands generally decrease to comparable values found in sediments of Bangladesh (Berg et al., 2007; Kocar et al., 2008; Polizzotto et al., 2008; Postma et al., 2007). Mean total As concentrations found in the Datong,

Delineating the Convergence of Biogeochemical Factors

51

Hetao, Huhhot, and Yinchuan basins of China range from ∼ 7 to 23 mg As kg
1 (Guo et al., 2014; Han et al., 2013; Xie et al., 2008, 2013, 2014), and increase to 36 mg As kg
1 in the Jianghan Plain with an observation range of 11 to 108 mg As kg
1 (Gan et al., 2014). Phosphate-extractable (Zheng et al., 2005) and reducible As pools generally decrease with depth in Bangladesh, though are fairly constant with depth when normalized by total solid-phase concentration (Swartz et al., 2004). Similarly, in the Datong Basin of China, phosphate-extractable and reducible As pools are relatively constant with depth when expressed as a percentage of total solid-phase concentration (Xie et al., 2008). Solid-phase As speciation indicates the degree to which microbially driven As release to groundwater may occur by dissimilatory As(V) reduction. In clay(< 0.2 μm)-rich Holocene sediments, As(V) may persist in the vadose zone, but is generally depleted in favor of As(III) below the lowest extent of the water table (Stuckey et al., 2015a) (Fig. 2A). The predominance of reduced solid-phase As species suggests that As(V) reduction occurred in the past within the near-surface sediments, but that dissimilatory As(V) reduction is not a major release mechanism presently on a mass basis relative to Fe(III) reduction (Kocar et al., 2014). However, As(V) may reemerge on the solid-phase in more oxidized Pleistocene aquifer environments (Stollenwerk et al., 2007), making dissimilatory As(V) reduction a potential As release mechanism in deeper sediments in the future. Total dissolved As concentrations are typically elevated above the 10 μg As L
1 World Health Organization limit within 10 m of the surface in Holocene aquifers of S/SE Asian river basins and peak around 30 m in the case of Bangladesh (Fig. 2B–D). Arsenite, the more toxic and mobile form, predominates within the 10–20 m depth range (and deeper in the case of Bangladesh), though a fraction of the dissolved pool persists as As(V) (Fig. 2B–D). 2.3.2 Iron Oxides As in the case of As, solid-phase Fe speciation constrains the extent to which dissimilatory Fe(III) reduction may contribute to As release. Solidphase Fe(II)/Fe(III) ratios increase with depth in Holocene sediments of Bangladesh (Horneman et al., 2004; Polizzotto et al., 2006). Likewise, acid-extractable Fe(II)/Fetotal levels are high in shallow sediments (< 50 m)

52

J.W. Stuckey et al.

(A)

Seasonal wetland

0

–5

HxAsO4x–3

–5

As sulfides

–10

Permanent wetland H3AsO3

Depth (m)

Depth (m)

0

HxAsO4x–3

H3AsO3

–10 As sulfides –15

–15

–20

Aquifer sands (30 m): 59% H3AsO3, 41% HxAsO4x–3 0 20 40 60 80 100 Proportion of arsenic species (%) As total (μM)

10

(C) 0.1 0

0

Astotal (μg/L) 1 10 100 1000

(D) % As (III) 0 0 20 40 60 80 100 0

–10 As(V) (μM)

10

Depth (m)

60 0

80 100 120 140

0

Dissolved As (μg L–1) 50 100 150 a

200

Total As As(III)

40

As(III) (μM)

10 Elevation (m)

0 20 40 60 80 100 Proportion of arsenic species (%)

20

–10

Elevation (m)

Aquifer sands (27 m): 36% H3AsO3, 64% HxAsO4x–3

Unfiltered 200 nm 50 nm

Depth below ground (m)

Elevation (m)

(B)

–20

5

10

15

20

160

–10 10

20

30

40

50 60 70 Distance (m)

80

90

100

180

25

Figure 2 (A) Arsenic speciation as a function of depth in seasonal and permanent wetlands of the Mekong Delta. Panels to the left of each profile show the basic stratigraphy of a ∼ 15-m deep clay/silt layer (solid or mottled colors) overlying aquifer sands (checks). The dashed lines approximate the average seasonal variation in the water table. Both sites have an elevation of ∼ 6 MASL (Benner et al., 2008; Kocar et al., 2008). Depth profiles of aqueous total As and As(III) concentrations are shown for the (B) Red River Delta (Postma et al., 2007), (C) Ganges-Brahmaputra-Megna River Delta (Swartz et al., 2004), and (D) Datong Basin (Pi et al., 2015). The horizontal dashed lines in part (B) represent the groundwater level. Part (A): Data are from Stuckey et al., 2015a.

in Bangladesh, probably resulting from reductive dissolution of Fe oxides (Swartz et al., 2004; Zheng et al., 2005). Reducible As-bearing Fe oxide content generally decreases with sediment depth (Kocar et al., 2014; Stuckey et al., 2015a) and age (Postma et al., 2012) within Holocene sediments. Thus, reactive Fe oxide pools generally are enriched in nearsurface Holocene sediments, especially those that are clay(< 0.2 um)-rich

Delineating the Convergence of Biogeochemical Factors

53

(Postma et al., 2010) (Fig. 3). Up to 50% of the total Fe is in the form of As-bearing, reducible Fe oxides in clay-rich near-surface sediments (< 6 m) of the Mekong Delta (Stuckey et al., 2015a). Likewise, reducible As-bearing Fe oxides persist in shallow (< 25 m), reduced sediments of Bangladesh (Hasan et al., 2009). The partial depletion of Fe oxides in Holocene sediments suggests that Fe(III) reduction occurred in the past, but alone, does not indicate whether or not active dissimilatory Fe(III) reduction is occurring at present. In contrast to the Holocene sediments, the underlying Pleistocene sediments have low acid-extractable Fe(II)/Fetotal levels (Swartz et al., 2004; Zheng et al., 2005), indicating that little to no Fe(III) reduction has occurred. Pleistocene sediments generally have an orange to brown hue and diffuse spectral reflectance measurements indicative of Fe oxides (Horneman et al., 2004). Sediment facies of Late Pleistocene age distributed heterogeneously throughout the subsurface of the Bengal Basin are upland paleosols of prolonged subaerial exposure during the last sea-level lowstand, resulting in highly weathered sediments dominated by Fe oxidecoated quartz sands, and depleted in micas and organic C (< 0.1%) (Goodbred and Kuehl, 2000; McArthur et al., 2004; Stollenwerk et al., 2007; Swartz et al., 2004). Iron oxides within Pleistocene sediments are (chemically) reactive, and contain As, predominantly as As(V) (Stollenwerk et al., 2007). The persistence, albeit in low total concentration, of a reactive As-bearing Fe oxide complex, suggests that dissimilatory As(V)/ Fe(III) reduction is not occurring in the deep Pleistocene aquifers, and would not occur without the influx of a sufficiently reactive reductant (e.g., DOC).

2.4 Reactive Organic C 2.4.1 Subsurface Particulate and/or Dissolved Organic Carbon (POC/DOC) The apparent ubiquity within S/SE Asian deltaic sediments of the oxidants—Fe oxides, and to a lesser extent, As(V)—in the dissimilatory As(V)/Fe(III) reduction reaction merits an investigation into the spatial distribution of the reductant (e.g., organic C). In fact, the source (or sources) of organic C is the most contentious issue and important factor limiting our ability to spatially constrain microbially driven As release and to predict future groundwater As distributions (Fendorf et al., 2010). The mobility of the reactants and products of dissimilatory As(V)/Fe(III) reduction

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J.W. Stuckey et al.

mt µmol/g River mud 80 60 40 m0 76 μmol/g 20

k′

4.1×10–4s–1

γ

0.99

0 0

100,000

200,000

300,000

400,000

River sand

25 20 15 10

m0 24 μmol/g

5

k′

2.1×10–5s–1

γ

1.45

0 0 25

100,000

200,000

300,000

400,000

500,000

Aquifer OX

20 15 10 m0 24 μmol/g 5

k′

2.1×10–5s–1

γ

1.45

0 0

50,000 100,000 150,000 200,000 250,000 300,000 Time (s)

Figure 3 The reactivity of Fe(III) in river (surface) and oxidized aquifer (6.6–7.5 m depth) sediments. Data points are obtained as the difference between ascorbate and HClextractable Fe. The lines are data fits to the equation: mt = m0[1 – (1 – k’(1 – γ)t)1/

Delineating the Convergence of Biogeochemical Factors

55

including As, DOC, dissolved inorganic C (DIC), and Fe(II) presents a great challenge in determining the where reaction is actively taking place in situ. Arsenic, DOC, DIC, and Fe(II) may both repartition to differential degrees and move with groundwater flow at differential rates from the point of release (Herbel and Fendorf, 2006; Jakobsen and Postma, 1999; Kocar et al., 2010; Rawson et al., 2016; Tufano and Fendorf, 2008; Tufano et al., 2008; van Geen et al., 2013). Therefore, co-localization of dissolved As, DOC, DIC, and/or Fe(II) at a particular location does not demonstrate the active occurrence of dissimilatory As(V)/Fe(III) reduction. The potential sources of sedimentary (autochthonous) organic C largely depend on the depositional environment and include vascular C3 plants, C4 plants, freshwater derived POC, and microbial cellular components (Eiche et al., 2016; Ghosh et al., 2015a,b; Huang et al., 2015). Plantderived organic C is co-deposited and co-buried with As-bearing sediment within the river basins of S/SE Asia (Meharg et al., 2006), and the fermentation products of organic C degradation may serve as the electron donor for dissimilatory As(V)/Fe(III) reduction (Postma et al., 2007). Therefore, both subsurface and near-surface autochthonous organic C (POC and/or DOC) should be evaluated as potential reductants fueling As release to groundwater, in addition to surface water-derived DOC. Total C levels, which represent total organic C (TOC) levels with a minor contribution from calcite, range from 0.1–7.8 g C kg
1 in the Bengal Basin and 1.7–13.4 g C kg
1 in the Cambodian Mekong Delta with the exception of discontinuous peat layers pervasive throughout S/SE Asian deltas, in which total C levels reach up to 387–406 g C kg
1 (McArthur et al., 2004, 2008; Stuckey et al., 2015a; Swartz et al., 2004; Tamura et al., 2009; Zheng et al., 2005). However, a high TOC content in sediments does not imply a high supply of organic C that is reactive toward dissimilatory As(V)/Fe(III) reduction; in fact, the opposite is shown in a peat layer in the Mekong Delta that does not promote microbial As/Fe release, and actually concentrates As as arsenian pyrite, which is stable under anoxic conditions (Stuckey et al., 2015b).

◂ (1 – γ)], where m0 is the initial sum of reactive Fe oxides, mt is the dissolved Fe attributed

to reductive dissolution of Fe oxides at a given point in time, and k’ and γ are fitted rate parameters. The plot shows a decrease in Fe oxide reactivity with increasing depth and increasing Fe oxide reactivity in clay(<0.2 μm)-rich sediments versus sands. The difference between ascorbate and HCl-extractable Fe is zero for reduced aquifer (9.5–10 m depth) sediments (not shown), indicating Fe oxide reactivity is below detection. Data are from Postma et al., 2010.

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The reactivity of the organic C and that of the As-bearing Fe oxides must be considered jointly when determining whether in situ dissimilatory As(V)/ Fe(III) reduction is thermodynamically favorable (Kocar and Fendorf, 2009) and kinetically viable. As long as dissimilatory As(V)/Fe(III) reduction is thermodynamically favorable, reaction kinetics will control the release of As to groundwater (Postma et al., 2007). Whether due to a thermodynamic restriction or slow kinetics, dissimilatory As(V)/Fe(III) reduction utilizing endogenous POC/DOC and native As-bearing Fe oxides has not been shown to occur definitively for subsurface (≥ 9 m) sediments of the Cambodian Mekong Delta (Stuckey et al., 2016). Dissimilatory As(V)/Fe (III) reduction driven by endogenous POC/DOC has been observed (where Fe(III) reduction preceded As(V) reduction) in batch incubations of Bengal Basin sediments containing a ferrihydrite-like phase (Islam et al., 2004). However, ferrihydrite has been identified definitively only in near-surface (< 0.1 m) sediments (Kocar et al., 2014); poorly crystalline ferrihydrite-like phases have been identified in subsurface sediments only after exposure to oxygen (Hasan et al., 2009; Uddin et al., 2011). In fact, a ∼ 7 month in-well incubation of ferrihydrite-coated sand showed that endogenous DOC from 2 to 40 m deep was sufficiently reactive to drive dissimilatory Fe(III) reduction of the ferrihydrite (Stuckey et al., 2016). Thus, ferrihydrite is expected to be too reactive to persist in subsurface sediment environments where reductants are present. Rather, goethite and hematite are the dominant Fe oxides identified in anaerobic subsurface sediments within S/SE Asian river basins (Postma et al., 2010; Stuckey et al., 2015a). However, endogenous POC/DOC does not appear sufficiently reactive to drive As release through dissimilatory Fe(III) reduction of goethite or hematite in subsurface Holocene sediments of the Cambodian Mekong Delta (Stuckey et al., 2016). In the case of subsurface (30 m) gray Holocene sands in Bangladesh, dissimilatory As (V)/Fe(III) reduction is not operative where Fe oxides are depleted below limits of detection (Polizzotto et al., 2005, 2006). In contrast, endogenous POC/DOC and native Fe oxides are reactive within strata 20 m deep in sediments of the Yangtze River Basin (Schaefer et al., 2016). Indeed, observed stimulation of dissimilatory As(V)/Fe(III) reduction of subsurface sediments has largely required the introduction of exogenous, reactive forms of organic C in batch incubations (Akai et al., 2004; Stuckey et al., 2016; Van Geen et al., 2004), as well as in the field (Harvey et al., 2002; Neidhardt et al., 2014). In contrast, a few studies have shown dissimilatory As (V)/Fe(III) reduction in unamended subsurface sediments (8–30 m) deep in West Bengal (Hery et al., 2010; Rowland et al., 2009), in the Cambodian

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Mekong Delta (Rowland et al., 2007), and subsurface sediments (20 m) from the Jianghan Plain of the Yangtze River (Schaefer et al., 2016). Many of the past studies have relied upon local drilling techniques where sample integrity can be compromised, and, in particular, vertical mixing is unavoidable. Continued improvement in sampling should allow for greater depth resolution of organic C and Fe oxide reactivity. Natural and anthropogenic changes in hydrologic gradient may introduce biogeochemical conditions supportive of dissimilatory As(V)/Fe(III) reduction driven by endogenous organic C in the subsurface (Schaefer et al., 2016; van Geen et al., 2013). In one case, seasonal changes in groundwater flow direction induce transient oxidizing conditions followed by a period of reducing conditions in which As release is driven by endogenous organic C within an isolated depth range of ∼ 20–23 m in the Jianghan Plain of the Yangtze River Basin, potentially due to the presence of Fe oxides of increased reactivity in response to the seasonal oxidation (Schaefer et al., 2016). In another case, groundwater pumping has drawn DOC-rich Holocene groundwater laterally into As-bearing Fe oxide-rich Pleistocene sediments at 25–30 m deep in the Vietnamese Mekong Delta, resulting in Fe(III) reduction and As contamination in the Pleistocene aquifer (van Geen et al., 2013). Yet, the relative contributions of autochthonous Pleistocene organic C and the Holocene aquifer-derived DOC to the observed As contamination of the Pleistocene aquifer remain unresolved (van Geen et al., 2013). 2.4.2 Surface-Derived DOC Advecting to Subsurface Surface-derived DOC may serve as a natural exogenous source of organic C that that could stimulate dissimilatory As(V)/Fe(III) reduction in the subsurface (Harvey et al., 2002, 2005, 2006; Lawson et al., 2013, 2016; Mailloux et al., 2013; Majumder et al., 2016; Neumann et al., 2010), though this is a matter of controversy (McArthur et al., 2011a; Sengupta et al., 2008; Stute et al., 2007). Studies in Bangladesh show that pond water of ∼50-year-old 3 H-3He age recharges the groundwater at the depth range (30–40 m) of maximum aqueous As concentration and where irrigation wells are screened (Harvey et al., 2002; Klump et al., 2006; Neumann et al., 2010). Dissolved inorganic C (DIC) and methane are significantly younger than the DOC at the 30–40 m depth range, and the DIC may be explained as a composite of modern pond DIC, modern oxidized biologically degradable organic C (BDOC), and DIC produced from carbonate mineral weathering (Neumann et al., 2010). Alternative to, or perhaps in conjunction with, being a function

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of surface-derived DOC driving subsurface As release, the “bell-shaped” groundwater As profile peaking near ∼30 m may be a product of the proximity of a well nest hydrologically linked by both vertical and lateral flow components to a zone of near-surface As release (Kocar et al., 2014). Proxies of organic C reactivity, such as DOC age, BDOC, optical properties, and spectroscopic signatures have been used to evaluate surface-derived DOC and autochthonous subsurface organic C as potential drivers of As release (Lawson et al., 2016; Mladenov et al., 2010, 2015; Neumann et al., 2010; Pi et al., 2015), though identifying the organic C that microorganisms are using to drive dissimilatory As(V)/Fe(III) reduction remains a challenge. A study defining the organic C source that microorganisms are using at a particular depth through radiocarbon dating shows that microbial DNA extracted from groundwater at depths ranging from 11–57 m in Bangladesh is older than advected surface-derived DOC, but younger than autochthonous POC (Mailloux et al., 2013). Although the age of microbial DNA from a groundwater sample does not alone indicate whether or not the microbial community is actively (or even capable of) engaging in the specific metabolic reaction of dissimilatory As(V)/Fe(III) reduction, this nevertheless suggests that the microbial community as a whole within this depth range are utilizing a combination of surface-derived DOC and autochthonous organic C. Retardation of DOC may result in a fraction of the surface-derived DOC sorbing onto the solidphase, contributing to a lumped pool of solid-phase organic C (Kocar et al., 2014; Mailloux et al., 2013), though further sorption may be limited by the DOC already present in the groundwater. The stoichiometry of the dissimilatory As-bearing Fe(III) reduction reaction prevents surface-derived DOC oxidation alone from fully accounting for the groundwater As levels observed in the Cambodian Mekong Delta (Kocar et al., 2014). Thus, more work is needed to elucidate the roles and capacities of surface-derived DOC and subsurface autochthonous POC/DOC in driving As release to groundwater within the subsurface. 2.4.3 Near-Surface POC/DOC Whereas the role of surface-derived DOC in driving As release within the subsurface warrants further refinement, surficial DOC is shown in column experiments to contribute to near-surface As release in West Bengal. Pond water used for jute processing releases As within the top 2.6 m of the sediment profile, likely through a combination of reductive dissolution of As-bearing Fe oxides and competitive desorption (Farooq and Chandrasekharam, 2015;

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Farooq et al., 2012). Arsenic released through reductive dissolution is subsequently retained on the solids within in the near-surface (2.6–6.1 m) sediments, preventing As transport to greater depths during the timescale of the column experiments (42 days) (Farooq et al., 2012). However, continuous DOC supply under reducing conditions over prolonged timescales in the field may facilitate As transport to the underlying aquifer (Farooq et al., 2012). Within the Cambodian Mekong Delta, near-surface (< 2 m), permanently saturated soils/sediments are the unique depositional environment where microbially driven As release occurs (Fig. 4) (Kocar et al., 2008; Polizzotto et al., 2008; Stuckey et al., 2016). The introduction of continuous flooding and natural organic C inputs (a site-harvest grass Cynododdactylon) to a seasonally saturated wetland stimulates As and Fe release (probably from Asbearing goethite and hematite reduction), whereas flooding alone and no treatment do not, suggesting that organic C degradation under continuously anaerobic conditions is required to drive As release (Stuckey et al., 2016). Deeper sediments (9–30 m) below the seasonal water table require addition of a reactive organic C source (e.g., glucose) to drive dissimilatory As(V)/Fe (III) reduction of As-bearing goethite and hematite as well (Fig. 4). However, endogenous DOC is able to induce dissimilatory Fe(III) reduction of ferrihydrite at a depth range of 2–40 m (Fig. 4), suggesting the lack of observed microbially-mediated As release in the subsurface may be due to a thermodynamic restriction of the electron acceptor. Thus, the reactivity of the organic C and that of the As-bearing Fe oxides jointly control whether or not dissimilatory As(V)/Fe(III) reduction may occur in a given location within a sediment profile. The reactivity of organic C and that of As-bearing Fe oxides toward dissimilatory As(V)/Fe(III) reduction appear to be optimized in near-surface depositional environments of the Red River and Mekong River Deltas (Postma et al., 2010; Stuckey et al., 2016). For instance, in surface floodplain muds of the Red River Delta, the reactivity of organic C approaches that of acetate, and the reactivity of Fe oxides approaches that of ferrihydrite (Postma et al., 2010).

3. ARSENIC RELEASE IN NEAR-SURFACE PERMANENTLY SATURATED SOILS/SEDIMENTS So far we have outlined the factors that will dictate the locations of microbially driven As release within sediment profiles of S/SE Asian river basins. In the absence of saltwater intrusion or other significant sources of

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Figure 4 Evaluation of limitations to dissimilatory Fe(III) reduction as a function of depth in a permanently saturated wetland. Bars indicate citrate-bicarbonate-dithionite-extractable Fe for pre-incubated (Initial) Al-substituted ferrihydrite-coated sand (Al-fhy), as well as for the Al-fhy with and without glucose amendment (Glucose and Control, respectively) that remained after ∼ 7 months of incubation in wells of 2, 16, and 40 m depth. Wells of ≤ 16 m depth had 2 m screening, and the 40 m wells had 1 m screening. Scatterplots show total Fe release in batch incubations of sediments from depths of 1.7, 12, and 27 m with 2 mM glucose amendment (glucose) and without amendment (control). The Fe oxides in the sediments at all three depths were goethite and hematite. The Control Al-fhy treatment indicates that the native DOC was able to fuel dissimilatory Fe(III) reduction at all groundwater depths to 40 m, whereas native sedimentary POC/DOC (control) was able to stimulate dissimilatory Fe(III) reduction of goethite and hematite only in the near-surface (1.7 m) sediments. Data are from Stuckey et al., 2016.

sulfate, the convergence of sustained suboxic/anoxic conditions, microbial communities poised for dissimilatory As(V)/Fe(III) reduction, reactive As-Fe complexes, and reactive organic C constrains active As release to Holocene sediments rather than underlying Pleistocene sediments (Fig. 5).

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Figure 5 Factors controlling the potential for microbially driven As release are optimized in the permanently saturated, near-surface Holocene sediments where fresh organic C and As-bearing Fe oxides are supplied annually. Arsenic-bearing Fe oxide reactivity generally decreases with depth within Holocene sediments. Plantderived organic C may serve as the electron donor for the dissimilatory reductive dissolution of As-bearing Fe oxides, releasing As, Fe(II), and organic C into solution. The released DOC from the Fe oxide-organic C complex may be available to drive further As(V)/Fe(III) reduction. Root exudates, in particular, may directly or indirectly promote dissimilatory As(V)/Fe(III) reduction by serving as electron donors or by acting as ligands that liberate organic C from mineral-organic complexes, respectively. These potential rhizosphere impacts on organic C accessibility may contribute to the observed higher organic C reactivity toward microbial driven As/Fe release relative to deeper sediments, and warrant further study. Pleistocene sediments in general have low organic C and Asbearing Fe oxide concentrations, as well as lower anaerobic microbial diversity inclusive of detected dissimilatory As(V)/Fe(III) reducers. Redox potential is generally conducive to anaerobic metabolic processes below the water table.

Pleistocene aquifers may be vulnerable to active As release through DOC supply from Holocene aquifers (van Geen et al., 2013), inducing reductive dissolution of As-bearing Fe(III) oxides. Organic C in the form of sedimentderived POC/DOC and surface-derived DOC of variable chemical signature are pervasive throughout Holocene sediment profiles to varying degrees (Mailloux et al., 2013; Mladenov et al., 2010, 2015; Neumann et al., 2010; Postma et al., 2012). Dissimilatory As(V)/Fe(III) reduction fueled by endogenous organic C has been definitively demonstrated in permanently saturated near-surface (∼ < 12 m) sediments (Postma et al., 2010; Stuckey et al., 2016). Calculated rates of organic C oxidation, Fe oxide reduction, and As release applied to the near-surface (< 12 m) sediment pools, are sufficient to account for observed mass distributions of As within underlying aquifers (Kocar et al., 2014; Postma et al., 2010). However, active microbially driven

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As release may also occur in the subsurface (> 12 m) in response to shifting biogeochemical conditions induced by changing hydrologic gradients (Schaefer et al., 2016; van Geen et al., 2013). Near-surface sediments/soils within S/SE Asian delta floodplains annually receive fresh As-bearing sediment supply and fresh inputs of organic material from plant decomposition (Kocar et al., 2008; Meharg et al., 2006; Polizzotto et al., 2008). Hydrolytic enzyme activity can persist under anaerobiosis (Hall et al., 2014), and therefore may supply organic C substrates capable of driving dissimilatory As(V)/Fe(III) reduction (Postma et al., 2007). In some cases, plant litter decomposition rates may be comparable if not higher under permanent flooding than under periodic flooding in floodplain soils/sediments (Langhans and Tockner, 2006). A predominant mechanism inhibiting a microbial community’s ability to oxidize organic C within upland soils is protection from minerals (Baisden et al., 2002; Chorover and Amistadi, 2001; Conant et al., 2011; Eusterhues et al., 2003; Kaiser et al., 2002; Lehmann et al., 2007; Lehmann and Kleber, 2015; Mikutta et al., 2006, 2007, 2009; Torn et al., 1997). Within permanently saturated conditions of the surface and near-surface soils, freshly buried organic C can induce reductive release of Fe oxidebound organic C, likely diminishing the role of mineral protection as a kinetic limitation to the As release process (Fig. 5). Rather, anaerobic decomposition of organic C is the most probable rate limiting step in the As release process (Keiluweit et al., 2016; Postma et al., 2007). Permanently flooded, near-surface sediments/soils—with rapid supply rates of energy-rich oxidants and reductants—constitute an ecosystem ideally suited to facilitate dissimilatory As(V)/Fe(III) reduction (Fig. 5). Annual organic matter input, along with root exudates, supply fresh, energetically favorable DOC [relative to dissimilatory As(V)-Fe(III) oxide reduction], and additionally liberate organic C from mineral-organic assemblages through mineral dissolution under aerobic conditions (Keiluweit et al., 2015) (Fig. 5).

4. IMPLICATIONS FOR ARSENIC MITIGATION IN SOUTH/ SOUTHEAST ASIAN GROUNDWATER Demonstration of As release to groundwater in permanently saturated, near-surface sediments/soils implies that land and water management may dictate present and future locations of active dissimilatory As(V)/Fe(III)

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reduction. For instance, alteration of dam networks may change the duration and locations of flooding within deltaic environments. Highly vegetated zones with increased flooding duration are probable candidates for initiation of As release. Irrigated rice fields are a notable exception, as BDOC is consumed and As is sequestered within the top ∼ 2 m as soil desaturation occurs in between irrigation events and after the rice is harvested (Neumann et al., 2010, 2011). Wells that are downgradient from permanently saturated wetland environments are at highest risk for future As contamination. Surface parameters, such as net primary production, flood duration, and topographic position can be incorporated into models predicting As risk areas at the 103–104 m scale (Winkel et al., 2008), and reactive transport models coupling near-surface biogeochemical reaction and hydrologic transport can be used to predict groundwater As distribution at the 101–103 m scale (Kocar et al., 2014). Our synthesis of the factors controlling the locations of active microbially driven As release, which results from the confluence of microbially accessible organic C and reactive Fe oxides, shows that Holocene aquifers are especially susceptible to As contamination (Fig. 6). Pleistocene aquifers, particularly those that are hydrologically protected by confining clays, may provide at least a short-term (and potentially long-term) safe drinking water source provided they are not exploited for irrigation pumping (Burgess et al., 2010; McArthur et al., 2008, 2011b, 2016; Michael and Voss, 2008). Nevertheless, extensive groundwater pumping has already contaminated unprotected Pleistocene aquifers bordering incised paleochannels filled with Holocene sediments (McArthur et al., 2008; van Geen et al., 2013; Winkel et al., 2011). Furthermore, under extensive groundwater pumping scenarios, confining clays are susceptible to compaction and release of As to underlying aquifers (Erban et al., 2013), and therefore Pleistocene aquifers do not appear to be a viable long-term option for safe drinking water unless perhaps wells are screened with maximal vertical distance from overlying confining clays and maximal horizontal distance from Holocene age paleo-channels (Fig. 6). Arsenic-safe tubewells will likely contribute to clean water supplies in S/SE Asia into the foreseeable future (Hossain et al., 2015), but long-term safe drinking water solutions, which are beyond the scope of this review, may entail a suite of alternatives including rainwater harvesting, treated surface water, piped water, water vendor systems, and dug wells (with aeration) depending on watershed management, available resources, and consumer participation (Chamberlain and Sabatini, 2014; Rahman et al., 2015).

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Surface aquitard Holocene aquifer

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Figure 6 Generalized schematic of a S/SE Asian basin sediment profile. Drinking water wells placed in Holocene aquifer sediments and in Pleistocene aquifer sediments underlying paleo-channels are at risk for As contamination. Drinking water wells within paleo-interfluve Pleistocene sediments directly underlying aquitards may be vulnerable to As contamination from aquifer leakage due to intensive groundwater pumping. Low As wells screened within Pleistocene paleo-interfluve sediments with maximal lateral distance from paleo-channels and vertical distance from clayey aquitards will likely have the greatest longevity for drinking water.

ACKNOWLEDGMENTS We are grateful for the analytical contributions of Benjamin Kocar, Shawn Benner, Matt Polizzotto, Michael Schaefer, and Guangchao Li. Portions of this work were also supported by a US EPA STAR Fellowship awarded to J.W.S., the National Science Foundation (grant number EAR-0952019), the Stanford NSF Environmental Molecular Science Institute (NSF-CHE-0431425), the EVP programme of Stanford’s Woods Institute, and by the US Department of Energy, Office of Biological and Environmental Research, Terrestrial Ecosystem programme (award number DE-FG02-13ER65542).

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