Effects of Simultaneous Application of Ferrous Iron and Nitrate on

Subscriber access provided by UNIV OF DURHAM

Article

Effects of simultaneous application of ferrous iron and nitrate on arsenic accumulation in rice grown in contaminated paddy soil Xiangqin Wang, Tongxu Liu, Fangbai Li, Bin Li, and Chuanping Liu ACS Earth Space Chem., Just Accepted Manuscript • DOI: 10.1021/ acsearthspacechem.7b00115 • Publication Date (Web): 29 Dec 2017 Downloaded from http://pubs.acs.org on January 2, 2018

Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a free service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are accessible to all readers and citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.

ACS Earth and Space Chemistry is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.

Page 1 of 30 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

ACS Earth and Space Chemistry

1

Effects of simultaneous application of ferrous iron and nitrate on arsenic accumulation in rice

2

grown in contaminated paddy soil

3 4

Xiangqin Wang1, Tongxu Liu1, Fangbai Li*, Bin Li, Chuanping Liu

5

Guangdong Key Laboratory of Integrated Agro-environmental Pollution Control and Management, Guangdong

6

Institute of Eco-Environmental Science ＆ Technology, Guangzhou 510650, P. R. China

7 8 9

*

Corresponding author. Tel.: +86 20 37021396

10

E-mail address: [email protected] (F.B. Li)

11

1

Xiangqin Wang and Tongxu Liu contributed equally to this work.

12 13


14 15

(Submitted on December 2017)

16 17 18 19 20 21 22 23 24 25

1

ACS Paragon Plus Environment

ACS Earth and Space Chemistry 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Page 2 of 30

26

ABSTRACT:

27

The objective of this study was to investigate the effects of simultaneous application of ferrous

28

iron (Fe(II)) and nitrate (NO3–) on arsenic (As) accumulation in rice plants during the entire

29

growth period. To this end, Fe(II) and NO3– were simultaneously applied to As-contaminated soil

30

in a pot experiment conducted under climate-controlled greenhouse conditions. Compared with the

31

control and the sole treatments with Fe(II), NO3–, or amorphous iron (Fe) oxides, the simultaneous

32

application of Fe(II) and NO3– significantly reduced As bioavailability by enhancing As(V)

33

immobilization in the soil and also significantly inhibited As accumulation in rice plants,

34

especially that of iAs in the grain. The presence of Fe(II) and nitrate can decrease As releasing via

35

inhibiting reductive dissolution of iron minerals, and the Fe(II) oxidation coupled with nitrate

36

reduction can immobilize As via incorporating As into iron secondary minerals. Therefore, the

37

simultaneous application of Fe(II) and NO3– effectively decreased As accumulation in rice plants

38

by enhancing As oxidation/immobilization mediated by abiotic/biotic Fe redox transformation and

39

mineralization. These findings provided new insights into the Fe/N/As biogeochemical cycles and

40

are also important from the view of agronomic management of As toxicity and mitigation in

41

As-contaminated paddy fields.

42 43

KEYWORDS: Arsenic; Ferrous iron; Nitrate; Paddy soil; Rice

44

2


Page 3 of 30 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


45

INTRODUCTION

46

Arsenic (As) exhibits four different valences (-III, 0, III, and V) with several chemical forms, in

47

which III and V are the most encountered species in terrestrial and aqueous environments, with

48

As(III) being more toxic than As(V) and their inorganic forms being much more toxic than organic

49

forms.1 As is released into the environment during mining activities, resulting in the contamination

50

of soil and water,2 and may threaten the human health through the food chain.3 Paddy fields

51

downstream of mines are severely contaminated with As, which leads to high levels of As

52

accumulation in rice plants.1, 4 Inorganic As (iAs), which is more toxic than organic As, is highly

53

accumulated in the rice grain,5 and thus, human health can be seriously affected by the consumption

54

of As-contaminated rice grown near mine areas. Therefore, new agronomic practices that will

55

reduce As concentrations in rice plants grown near mine or other type of As-contaminated areas are

56

urgently needed.

57

A previous study reported that the application of Fe materials, such as Fe(II), Fe powder,

58

amorphous Fe(III) (hydr)oxides, converter furnace slag containing 20% Fe, and Fe oxide materials

59

containing 56% Fe, reduce As uptake by rice plants,6 since an increase of Fe(III) (hydr)oxides in the

60

soil regulates As mobility and bioavailability via reductive dissolution or mineralization processes.3,

61

7, 8

62

(hydr)oxides in paddy soil efficiently reduces As bioavailability.9 Under natural oxic conditions, As

63

is strongly absorbed by Fe(III) (hydr)oxides, in which As(V) has a higher affinity than As(III).10 In

64

flooded paddy soil, Fe(III) (hydr)oxides are reduced to Fe(II), a process that, combined with As(V)

65

reductive release,3, 11, 12 is impacted by a series of factors such as soil characteristics (pH, Eh, and

66

NO3–) and microbial species.13, 14 The simultaneous presence of Fe(III) (hydr)oxides and Fe(II), as

67

commonly observed in environments inhabited by Fe-reducing microorganisms, induces the

68

oxidation of As(III) to As(V) and consequently, reduces the mobility of As.15 The application of

69

amorphous ferrihydrite Fe(II)7 or (Am-FeOH)8 to paddy soil increases the amount of Fe(III)

Moreover, previous field studies have suggested that the increase of amorphous Fe(III)

3



Page 4 of 30

70

(hydr)oxides in the Fe-plaque and significantly reduces the concentration of As(III) in the

71

rhizosphere. In addition, the rice radial oxygen loss (ROL) plays an important role in As

72

detoxification.16 O2 released from the root surfaces directly oxidizes Fe(II) to Fe(III) (hydr)oxides in

73

the rhizosphere,17 and simultaneously, As(III) is oxidized to As(V) by reactive oxygen species via

74

Fenton-like reactions18 and incorporated in Fe(III) (hydr)oxides. Microbial Fe oxidation by

75

Fe-oxidizing bacteria (FeOB) in the rhizosphere of wetland plants substantially contributes to the

76

precipitation of the Fe-plaque,19 which adsorbs As and co-precipitates it on the root surfaces.

77

Therefore, the presence of Fe(II) oxidation process promotes As immobilization processes in the

78

rhizosphere.

79

The amount and form of Fe in the soil substantially affect As mobility and bioavailability, and

80

thus, the soil characteristics (pH, Eh, and NO3–) may affect As bioavailability via regulating Fe

81

redox processes.2, 13, 14 In O2-depleted paddy soil, NO3– oxidizes Fe(II) through biological processes

82

and inhibits Fe release.20, 21 The processes of Fe oxidation coupled with NO3– reduction have been

83

studied in mixed cultures from natural environments as well as in pure isolate cultures, in which the

84

dominant genera were collected from freshwater sediments, submarine hydrothermal systems,

85

hypersaline sediments,22 and paddy soils.13 It has been reported that some bacteria directly mediate

86

As(III) oxidation by NO3– under anoxic conditions or at the oxic-anoxic interfaces.23, 24 Therefore,

87

the presence of NO3– may facilitate Fe(II) oxidation, enhancing As immobilization,25, 26 whereas the

88

simultaneous presence of Fe(II) and NO3– may influence As immobilization in paddy soil via biotic

89

or abiotic processes. A field study has shown that the application of NO3– to Bangladesh sediments

90

reduces the mobility of As due to the biological oxidation of Fe(II) to Fe(III) (hydr)oxides.27 The

91

simultaneous application of NO3– and Fe(II) to a continuous flow sand-filled column has been used

92

to induce As immobilization by forming Fe(III) (hydr)oxides with adsorbed As(V) in a natural

93

anaerobic sediment.28 NO3–-dependent Fe(II) oxidation has been demonstrated in paddy soil, and

94

the production of various Fe(III) oxide minerals potentially immobilizes soluble As.29 Due to As 4


Page 5 of 30 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


95

immobilization, the uptake of As by rice plants may be decreased, alleviating As accumulation.

96

However, the interactive mechanisms of Fe/N/As involved in the soil-plant system remain unclear

97

and thus, further research is needed.

98

In this study, we conducted a pot experiment using severely contaminated paddy soil with As30

99

that collected downstream of the Xikuangshan mining area in Hunan Province, China, to investigate

100

As accumulation in rice plants and As speciation in the soil in relation to the application of Fe(II)

101

and NO3– during the entire growth period. The objectives were to: (i) investigate the effects of Fe(II)

102

and NO3– simultaneous application on the soil and rice plant As status throughout the entire growth

103

period and (ii) reveal the underlying mechanisms responsible for Fe(II)-NO3–-induced As

104

immobilization in the soil and the alleviation of As accumulation in rice plants.

105 106

MATERIALS AND METHODS

107

Soil Description. The paddy soil (0-20 cm) was collected 1 km downstream from the

108

Xikuangshan antimony mine (UTM 27°42′53.46″N; 111°27′06.12″) in Hunan Province of China in

109

October, 2012. A comprehensive description of the mineralogy of the mine was provided in He et

110

al.31 High As concentrations in the soil were caused by occasional flooding and irrigation with

111

As-contaminated water from a nearby river draining from the mine.12 The soil was sandy loam with

112

a pH of 6.8 ± 0.1 and contained 86.3 ± 6.13 mg kg-1 of total As (T-As). A comparison experiment

113

was also conducted using another paddy soil from Lianhuashan tungsten mine, which is located in

114

the (sub)-tropical areas in Guangdong Province of China. The soil characteristics were shown in

115

Table S1 in supporting information (SI). All the soils were air-dried, sieved to < 2 mm for the

116

following pot experiments.

117

Pot Experiments. The pot cultivation experiments were conducted in a climate-controlled

118

greenhouse. FeCl2 (0.54 mmol kgsoil-1) and NaNO3 (7.5 mmol kgsoil-1) (Fe(II) + NO3–) were applied

119

to the soil surface simultaneously and mixed thoroughly. Then the soil was immediately transferred 5



Page 6 of 30

120

into 8 L pots (6 kg soil per pot) and sufficiently flooded with tap water. A nylon mesh bag (height of

121

20 cm, diameter of 80 mm, containing 600 g soil) was placed in the center of each pot to create the

122

rhizosphere soil as adopted by Ultra et al.8 and the remaining 5.4 kg soil out of the bag was taken as

123

the bulk soil. The mesh of the bag was 25 µm, which allowed the transport of water and dissolved

124

nutrients but not the roots. Four treatments using no additives (Control), Am-FeOH (0.1%w/w

125

amorphous ferrihydrite),32 FeCl2 (0.54 mmol kgsoil-1, Fe(II)) and NaNO3 (7.5 mmol kgsoil-1, (NO3–)),

126

respectively were conducted for comparison with Fe(II) + NO3–. The Am-FeOH was synthesized

127

according to a method developed by Okazaki et al.32 and Kang et al.,33 the oxalate-extractable Fe,

128

specific surface area, zero point of charge and pH for Am-FeOH were 460.5 g kg-1, 273.6 m2 g-1 and

129

7.4, respectively. Four sample times were set during the entire rice growth stage, including the

130

seedling stage, maximum tiller number stage (tillering stage), heading stage and maturing stage;

131

therefore, the treatments were prepared in 4 groups with three triplicates for each group. In addition,

132

chemical fertilizers including P and K (P2O5: K2O =1: 1.5) were applied at a rate of 0.0625 g kg-1

133

dry weight soil. Urea was used as the nitrogen fertilizer, and the application rate was 8.33 mmol

134

kg-1 dry weight soil. The rice seedlings, preparation of which was described in SI (SI-1), were

135

transplanted on 10-April-2013. Tap water was added on a daily basis to maintain flooding of the

136

soils during the entire growth stage, and all the pots were rearranged randomly every week until two

137

weeks before harvest. The details of all the sampling methods for plants and soil, measurements of

138

As in rice plants and Fe/As species in soil, and statistical analysis of experimental data were

139

described in the SI (SI-2, SI-3, SI-4 and SI-5). All the measured parameters, the recovery and

140

precision of the As speciation were listed in Tables S2, S3, and S4, respectively.

141 142

RESULTS

143

As in Rice Plants during the Growth Period. As in the root and straw in all treatments during the

144

entire growth period is shown in Fig. 1A & B (statistical differences were showed in Table S5). 6


Page 7 of 30 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


145

T-As and iAs in the brown rice in all treatments at the maturity stage are shown in Fig. 1C. In the

146

control at the maturity stage, As in the root was approximately 20 times higher than that of the straw

147

and 400 times higher than that of the brown rice. Compared with the control, As in the root and

148

straw in the Am-FeOH, Fe(II), and Fe(II)+NO3– treatments decreased significantly with growth,

149

whereas that of the straw in the NO3– treatment was higher at the tillering stage. During the entire

150

growth period, As in the root in all treatments as well as that of the straw in the control increased

151

from the seedling stage to the maturity stage. However, As in the straw in the Fe(II) and NO3–

152

treatments did not show any significant changes. In the control, As in the straw reached a peak at

153

the filling stage, but significantly reduced at the maturity stage. The results were consistent with

154

those reported by Zheng et al.,34 in which As in the straw increased 2–3 folds after flowering,

155

reached a peak at the filling stage, and then decreased by 50–85% at the maturity stage. These

156

changes could be attributed to As translocation from the straw to the grain from the filling stage to

157

maturity stage. Carey et al.35 estimated that phloem transport accounted for 90% and 55% of As(III)

158

and dimethylarsinic acid (DMA) in the caryopsis, respectively.

159

T-As and iAs, particularly As(III) in the brown rice were significantly lower in all treatments

160

compared with those in the control; the lowest values were observed in the Fe(II)+NO3– treatment,

161

followed by those in the Fe(II), NO3–, and Am-FeOH treatments. The iAs/T-As ratio in the brown

162

rice was also significantly lower in all treatments compared with that in the control (74.1%),; the

163

lowest value was observed in the Fe(II)+NO3– treatment (35.3%), followed by that in the NO3–

164

(51.5%), Fe(II) (60.2%), and Am-FeOH (68.4%), treatments. As shown in Fig. S1(A), T-As in the

165

hull was higher than that of the brown rice in all treatments. Compared with the control, the

166

Fe(II)+NO3– treatment significantly decreased As in the hull.

167

The results showed that the dry weight of the root and straw increased with growth (Table S6). At

168

the seedling and filling stages, the soil amendments had no significant effects on the dry weight of

169

the root and straw. Variability in the dry weight of the root was mainly observed at the tillering stage, 7



Page 8 of 30

170

but of all other plant parts at the maturity stage and Fe(II) and NO3- significantly reduced brown

171

rice yield, respectively. However, the dry weight of all plant parts in the Fe(II)+NO3- treatment did

172

not differ significantly from that in the control. To illustrate the differences in As in the brown rice

173

due to dilution effects of grain yields or the decrease in As bioavailability, T-As in the brown rice

174

was normalized by the dry weight (g pot-1) of the brown rice at the maturity stage. As shown in Fig.

175

S1(B), the normalized As in the brown rice showed a similar trend with T-As and was significantly

176

lower in the Fe(II) and Fe(II)+NO3- treatments, suggesting that the differences in As in the brown

177

rice were not caused by the dilution effects of brown rice yields, but by the decrease in As

178

bioavailability. Therefore, As in different plant parts was associated with the As and Fe species in

179

the soil.

180

< Fig. 1>

181 182

Fe/As Speciation in Soil during the Growth Period. As and Fe in the rhizosphere during the

183

growth period were extracted with H2O, HCl, ammonium oxalate (Ox), and phosphate (PO4). As

184

shown in Fig. 2A & B (statistical differences were showed in Table S5), H2O-As and HCl-As in the

185

Fe(II) and NO3– treatments were lower than those in the control. H2O-As in all treatments was very

186

low at the seedling and tillering stages, markedly increased at the filling stage, and then, decreased

187

at the maturity stage. HCl-As maintained stable from the seedling stage to the filling stage, but

188

increased substantially at the maturity stage. As shown in Fig. 2C & D, Ox-As and Plaque-As in the

189

Fe(II) and NO3– treatments were higher than those in the control. Ox-As slightly decreased

190

throughout the entire growth period. Plaque-As maintained stable from the seedling stage to the

191

filling stage, but markedly increased from the filling stage to the maturity stage. T-H2O-As,

192

T-HCl-As, and T-PO4-As at the maturity stage were the lowest in the Fe(II)+NO3– treatment,

193

followed by those in the Am-FeOH, Fe(II), and NO3– treatments, and finally, in the control (Fig. 3).

194

The opposite trend was observed for T-Ox-As and T-Plaque-As at the maturity stage that were the 8


Page 9 of 30 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


195

highest in the Fe(II)+NO3– treatment, followed by those in the Am-FeOH, Fe(II), and NO3–

196

treatments and finally, in the control. Except for Ox-As, H2O-As, PO4-As, and HCl-As followed the

197

same trend as that of T-As. Compared with the control, Ox-As(V) was higher, whereas Ox-As(III)

198

was lower in all treatments, especially in the Fe(II)+NO3– and Am-FeOH treatments. The

199

underlying chemical and microbial processes may induce the As(III) oxidation and immobilization

200

in the soil, resulting in PO4-As(III) oxidation to As(V) and its incorporation into immobilized As

201

(e.g., Ox-As).36

202

< Fig. 2, Fig. 3>

203

Fe speciation in the rhizosphere during the entire growth period is shown in Fig. 2. Similar to As

204

in the soil, H2O-Fe(II) and HCl-Fe(II) in the Fe(II) and NO3– treatments were lower than those in

205

the control, whereas Ox-Fe and Plaque-Fe were higher than those in the control. In all treatments,

206

H2O-Fe(II) was very low at the seedling and tillering stages, but markedly increased at the filling

207

stage and then decreased at the maturity stage (Fig. 2E); HCl-Fe(II) gradually increased during the

208

entire growth period (Fig. 2F); Ox-Fe maintained stable from the seedling stage to the filling stage,

209

but markedly increased at the maturity stage (Fig. 2G); Whereas Plaque-Fe remained stable at the

210

seedling, filling, and maturity stages, but markedly increased at the tillering stage (Fig. 2H). Nanzyo

211

et al.37 reported that Plaque-Fe in the root reached a peak at the tillering stage and then, gradually

212

decreased. Rice plants release more O2 from roots at the tillering stage than at the other stages,

213

resulting in a higher degree of oxidation of Fe(II) and then forming Fe plaque on root surfaces.38

214

However, the effects of the rhizosphere on As uptake by rice plants are complicated, and the

215

Fe-plaque may serve as an As sink or source at different growth stages.39, 40 Wang et al.38 reported

216

that Plaque-Fe was 10.9 ± 0.6 g kgroot-1 at the seedling stage and 35.2 ± 1.51 g kgroot-1 at the

217

emergence stage, whereas As showed no significant differences in the rice root and shoot at the two

218

stages. At the maturity stage, H2O-Fe(II) and HCl-Fe(II) were the highest in the control, followed

219

by those in the NO3–, Fe(II), Am-FeOH, and Fe(II)+NO3– treatments, whereas Ox-Fe was the lowest 9



220

Page 10 of 30

in the control, followed by that in the NO3–, Fe(II), Am-FeOH, and Fe(II)+NO3– treatments.

221

The pH and Eh of the soil were also examined during the entire growth period. The pH in the

222

Am-FeOH and NO3– treatments was similar to that in the control, whereas the pH in the

223

Fe(II)+NO3– and Fe(II) treatments was markedly lower than that in the control. The Eh was the

224

highest in the NO3– treatment, followed by that in the Am-FeOH, Fe(II)+NO3–, and Fe(II)

225

treatments and finally, in the control (Fig. 4).

226

< Fig. 4>

227

To validate our key findings, the same experiments with Fe(II) and NO3– were conducted using

228

soil from the Lianhuashan mine area. The results showed that the Fe(II)+NO3– treatment

229

significantly reduced As accumulation in rice plants, especially in the brown rice, in which As was

230

42.4% lower than that in the control (Fig. S2). T-H2O-As, T-HCl-As, and T-PO4-As in the

231

Fe(II)+NO3– treatment at the maturity stage were significantly lower than those in the control.

232

However, Ox-As and Plaque-As in the Fe(II)+NO3– treatment were markedly higher than those in

233

the control. From April 10 to July 16, 2015, we also conducted a field experiment downstream of

234

the Lianhuashan tungsten mine (Fig. S3) that included two treatments, control and Fe(II)+NO3–,

235

with three replications each, applied in 4 × 4-m plots. The plots 1–3 represented the control, and the

236

plots 4–6 represented the Fe(II)+NO3– treatment. The results showed that T-As in the brown rice

237

was significantly lower by 33.4% in the Fe(II)+NO3– treatment (0.23 ± 0.03 mg kg-1) compared with

238

that in the control (0.35 ± 0.04 mg kg-1).

239 240

Correlations among Rice Plant As, Soil As, and Soil Fe. Correlation analysis between Fe in

241

different soil fractions (H2O-Fe(II), HCl-Fe(II), Ox-Fe, and Plaque-Fe) and the bioavailable As

242

species (PO4-As) was conducted to investigate whether Fe affects As speciation (Fig. 5). H2O-Fe(II)

243

and HCl-Fe(II) represent the mobile Fe in the soil, Ox-Fe represents the amorphous Fe(III)

244

(hydr)oxides that efficiently immobilize As in the soil, and Plaque-Fe is a sink of immobilized As, 10


Page 11 of 30 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


245

which is accumulated outside the root surface. The bioavailable As, PO4-As and H2O-As, were

246

significantly positively correlated with H2O-Fe(II) and HCl-Fe(II), but significantly negatively

247

correlated with Ox-Fe and Plaque-Fe (Fig. S4), suggesting that Fe in the solid phase of the soil

248

reduces As accumulation in rice plants via As immobilization.

249

< Fig. 5>

250

Fe in the soil not only immobilizes As via adsorption/incorporation, but also causes the redox

251

transformation of As via biotic/abiotic Fe cycling processes, affecting As accumulation in rice

252

plants. Correlation analysis between Fe (H2O-Fe(II), HCl-Fe(II), Ox-Fe, and Plaque-Fe) and

253

H2O-As, Ox-As, and PO4-As in different soil fractions was conducted to investigate the impact of

254

Fe speciation on As transformation in the soil. Correlations between As and Fe species (Fig. 5) were

255

different for Ox-As(III) and Ox-As(V), indicating that H2O-Fe(II) and HCl-Fe(II) promoted the

256

immobilization of As(III), whereas Ox-Fe and Plaque-Fe promoted the immobilization of As(V).

257

These results were supported by those obtained for H2O- As and PO4-As (Fig. S5), indicating that

258

Fe cycling in the soil might play a key role in the redox transformation of As, which is followed by

259

As release or immobilization, consequently affecting As accumulation in rice plants.

260

DISCUSSION

261

Possible Mechanisms of Alleviating As Accumulation in Rice by Fe(II) and NO3–. The

262

transformation processes of As in the soil and its transportation from the soil to rice plants could be

263

divided into three steps: (i) As in the soil is mobilized or immobilized via biogeochemical processes;

264

(ii) the bioavailable As in the soil is transported to the near-root environment and partially

265

transformed into organic forms, which are taken up by the roots or incorporated into the Fe-plaque;

266

and (iii) As in the roots is finally transported to the rice straw, hull, and brown rice.

267

Based on these steps, the bioavailable As in step (i) is a pool for As uptake by rice plants, and

268

thus, As bioavailability in the soil determines its accumulation in rice plants. As speciation in the

269

simulated system with As(V)/As(III) and ferrihydrite in the pH range of 5.0–7.0 was calculated with 11



Page 12 of 30

270

Visual Minteq 3.1, assuming the solid phase as ferrihydrite. The dominant H2O-As species were

271

H3AsO3, HAsO42–, and H2AsO4–; the dominant PO4-As species were ≡FeHAsO3–, ≡FeH2AsO3,

272

≡FeOHAsO43–, and ≡FeAsO42–; and the Ox-As species included ferrihydrite-associated As and all

273

PO4-As species. With the application of Fe(II)+NO3– to the soil, As bioavailability was significantly

274

inhibited via the following three possible mechanisms:

275

1) The application of Fe(II) and/or NO3– decreased As release by inhibiting the reductive dissolution

276

of Fe minerals containing As. With the application of Fe(II) and Fe(II)+NO3–, the soil pH at the

277

maturity stage decreased to 5.3 and 5.9, respectively (Fig. 4), which increased the positive surface

278

charge of minerals, such as Fe(III) (hydr)oxides, in the soil and consequently, increased the sorption

279

capacity for anions (e.g., ≡FeHAsO3–, ≡FeH2AsO3, ≡FeOHAsO43–, and ≡FeAsO42–).12 Therefore,

280

the application of Fe(II) to paddy soil retards Fe(III) (hydr)oxides reductive dissolution and As

281

release from crystalline minerals. A very low level of H2O-As was observed at pH less than 6.2–6.3,

282

accompanied by a low level of dissolved Fe(II) in the paddy soil solution.41 The increase in soil Eh

283

due to the application of NO3– also decreased As release to the soil solution from Fe(III)

284

(hydr)oxides, results that were consistent with those reported in a previous study, which

285

demonstrated that the application of NO3– inhibits the reductive dissolution of Fe(III) (hydr)oxides

286

in O2-depleted paddy soil.42

287

2) Direct As(III) oxidation by reactive Fe(III) at the Fe(II)-Fe oxide interface increased As(V)

288

immobilization in the soil, which was supported by the increase of Ox-As(V) in the Fe(II) treatment

289

(Fig. 3). Amstaetter et al.15 reported that As(III) oxidation is observed immediately after the

290

application of Fe(II)-Goethite. It has been suggested that reactive Fe(III) species, such as Fe(III)

291

oxide-Fe(II)-As(III) or Fe(III) oxide-As(III)-Fe(II) surface ternary complexes, are responsible for

292

As(III) oxidation to As(V), followed by As(V) incorporation into newly formed Fe minerals.

293

Specifically, the elementary reactions are described as Rxn. 1, in which free Fe2+ is adsorbed onto

294

the surface via surface complexation; Rxn. 2, in which an electron transfer occurs between Fe(II) 12


Page 13 of 30 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


295

and Fe(III); Rxn. 3, in which free Fe2+ is released, and a new surface Fe(III) is formed; and Rxn. 4,

296

in which the new surface directly oxidizes As(III) to As(V). 15, 43, 44

297

≡ Fe(III)OH+Fe 2+ →≡ Fe(III)OFe(II) + +H +

(Rxn. 1)

298

≡ Fe(III)OFe(II) + →≡ Fe(II)OFe(III) +

(Rxn. 2)

299

≡ Fe(II)OFe(III) + +H + →≡ Fe(III) new OH+Fe 2+

(Rxn. 3)

300

≡ Fe(III) new OH+As(III) →≡ Fe(II)OH - +As(V) (Rxn. 4)

301

3) Microbial NO3– reduction coupled with Fe(II) and As(III) oxidation caused substantial As

302

immobilization in newly formed Fe(III) (hydr)oxides. In flooded paddy soil, the main oxidant (O2)

303

is absent, and thus, other oxidants, such as nitrate and MnO2, play key roles in Fe(II) oxidation

304

under such anoxic conditions.45 Particularly, the NO3–-dependent Fe(II) oxidation has been

305

recognized as a very important subsurface process.46 Several strains of denitrifying microorganisms

306

have been reported to couple As(III) oxidation with NO3– reduction under anoxic conditions,23, 24, 47

307

as in Rxn. 5. Moreover, anaerobic NO3–-reducing Fe(II)-oxidizing bacteria have the ability to

308

oxidize Fe(II) using NO3– as an electron acceptor to produce various biogenic Fe(III) (hydr)oxides,

309

as in Rxn. 6.48 For single electron transfer reactions, the free energy (∆Gr0) has been estimated to be

310

-132.2 kJ mol-1 and -28.8 kJ mol-1 for Rxns. 5 and 6, respectively, indicating that As(III) oxidation

311

may be more favorable than Fe(II) oxidation coupled with NO3– reduction. The simultaneous

312

oxidation of As(III) and Fe(II) may result in the incorporation of As(V) into biogenic Fe(III)

313

(hydr)oxides, which promote As immobilization, and not into abiogenic Fe(III) (hydr)oxides.27, 48

314

Therefore, Ox-Fe probably increased due to the action of functional microorganisms such as

315

denitrifying microorganisms and NO3–-reducing Fe(II)-oxidizing bacteria (Fig. 2G).

316

1 1 1 1 4 1 NO 3− + H 3 AsO 3 → HAsO 42− + N 2 ( g ) + H + + H 2 O 5 2 2 10 5 10

∆Gr0 = -132.2 kJ mol-1

(Rxn. 5)

1 7 1 9 NO3− + Fe 2+ + H 2 O → am-FeOOH + N 2 ( g ) + H + 5 5 10 5

∆Gr0 = -28.8 kJ mol-1

(Rxn. 6)

In step (ii), bioavailable As is partially transformed into organic forms, and both iAs and organic 13



Page 14 of 30

317

As are incorporated into the Fe-plaque on the root surfaces or taken up by the roots. In step (iii), iAs

318

and organic As are transported to the root, straw, hull, and brown rice. The translocation factors,

319

indicated by the ratio of As in the shoot to As in the root (TF = Cshoot Croot-1),12 were calculated, and

320

the results showed a significant decrease in the Am-FeOH (0.051 ± 0.003), Fe(II) (0.043 ± 0.008),

321

NO3– (0.072 ± 0.01) and Fe(II)+NO3– (0.031 ± 0.004) treatments compared with that in the control

322

(0.142 ± 0.010). As accumulation in rice plants per pot decreased from 1.00 ± 0.06 mg pot-1 in the

323

control to 0.84 ± 0.03 mg pot-1 in the Am-FeOH treatment, 0.50 ± 0.05 mg pot-1 in the Fe(II)

324

treatment, 0.63 ± 0.08 mg pot-1 in the NO3– treatment, and 0.50 ± 0.07 mg pot-1 in the Fe(II)+NO3–

325

treatment. Previous studies reported that many micro-organisms are able to transform iAs to DMA49

326

in the rhizosphere and that DMA translocates more efficiently than iAs in rice plants.35 In the brown

327

rice, iAs was accounted for 68.4%, 60.2%, 51.5%, and 35.3% of T-As in the Am-FeOH, Fe(II),

328

NO3–, and Fe(II)+NO3– treatments, respectively, percentages that were markedly lower than that in

329

the control (74.1%) (Fig. 1C). The iAs was lower in all treatments compared with that in the control,

330

probably due to the lower iAs uptake than that of DMA by rice plants.

331

A previous study showed that iAs decreases linearly with the increasing T-As in the brown

332

rice.6, 11 In addition, Khan et al.11 revealed that iAs decreased slower than DMA with the decreasing

333

T-As in the brown rice. Hence, a possible explanation for the increase of iAs is that the translocation

334

of iAs from the root/shoot to the rice grain is more difficult than that of DMA.6, 11, 50 In the present

335

study, iAs, particularly As(III) decreased with the decreasing T-As, which could be attributed to

336

changes in soil properties after the application of external materials. As speciation in the soil and

337

rice was directly influenced by the environmental conditions (i.e., soil type and greenhouse vs.

338

field). The soil characteristics, such as Eh, pH, Fe fractions, and As species, changed in the

339

Am-FeOH, Fe(II), NO3–, and Fe(II)+NO3– treatments, resulting in different As translocation in the

340

brown rice, and also different iAs. TF revealed a significant decrease in As translocation from the

341

root to the shoot, which might indicate a significant decrease in iAs translocation, since iAs is less 14


Page 15 of 30 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

342


efficient to translocate from the soil to the brown rice compared with its organic forms.11

343

The Fe-plaque is a side pathway of As transportation/incorporation that induces competition

344

between As uptake by rice plants and As incorporation into the Fe-plaque. An increase in As

345

immobilization in the Fe-plaque results in a decrease in As uptake by rice plants. The formation of

346

the Fe-plaque on the root surfaces increased in the Am-FeOH, Fe(II), NO3–, and Fe(II)+NO3–

347

treatments, decreasing As accumulation in rice plants (Fig. 3). These results were consistent with

348

those reported in previous studies and showed that the application of Am-FeOH and Fe(II) to paddy

349

soil increases the Fe-plaque around the rice roots.7, 8 O2 secretion from ROL stimulates both the

350

chemical and microbial Fe(II) oxidation, resulting in As immobilization in the rhizosphere.

351

Based on the analysis of As immobilization in the soil, the mechanisms for reducing As

352

accumulation in rice plants by the application of Fe(II)+NO3– could be summarized as follows: (i)

353

the application of Fe(II) and/or NO3– decreases As release by inhibiting the reductive dissolution of

354

Fe minerals containing As; (ii) direct As(III) oxidation by reactive Fe(III) at the Fe(II)-Fe oxide

355

interface increases As(V) immobilization in the soil; (iii) microbial NO3– reduction coupled with

356

Fe(II) and As(III) oxidation causes substantial As immobilization in the newly formed Fe(III)

357

(hydr)oxides; (iv) As uptake by rice plants decreases due to the lower amount of bioavailable As in

358

the soil and its incorporation into the Fe-plaque around the roots; and (v) the iAs/T-As ratio

359

decreases due to the lower iAs uptake by rice plants.

360 361

Environmental Implications. Our results showed that the application of Fe(II)+NO3– significantly

362

inhibited As accumulation in rice plants. Fe is a highly abundant element in the red soil zones of

363

southern China and plays an important role in rice production.51 When switching from oxic to

364

anoxic conditions after flooding, anaerobic microorganisms use electron acceptors (e.g., Fe(III) and

365

NO3–) for the oxidation of organic matter.52, 53 Fe and NO3– redox transformation may have a

366

significant contribution to the Fe/N cycles in paddy soil and also strongly influence the fate of 15



54

Page 16 of 30

367

contaminants.43,

368

Fe(II)-oxidizing bacteria in anoxic environments.21,

369

NO3–-dependent Fe(II) oxidizers has been estimated to be 4.5 × 104–4.2 × 106 cells g-1 sediment dry

370

weight in different freshwater sediments and 1.6 × 106 cells g-1 dry soil in flooded paddy soil.28, 55

371

Therefore, further research on the synergetic effects of Fe(II) and NO3– on As bioavailability might

372

help to evaluate and better understand the contribution of coupled Fe(II)-NO3– redox processes to

373

As immobilization in flooded paddy soil.

Fe(II) oxidation processes at neutral pH are mediated by neutrophilic 52

In Europe, the number of mixotrophic

374

The relative iAs varies widely among rice grains collected from different regions of the world.56

375

In China, iAs is the predominant species in rice plants,47 whereas the iAs/T-As ratio reaches 95% in

376

mining-impacted rice grains.57 In the present study, iAs in the brown rice in the control was twice

377

the Chinese standards for iAs (maximum contaminant level, 0.15 mg kg-1), indicating the high risk

378

for human health caused by As ingestion. However, iAs decreased significantly to 0.061 mg kg-1 in

379

the Fe(II) and NO3– treatments. Therefore, the application of Fe and N biogeochemical processes for

380

alleviating As stress in rice plants could not only provide a new insight into the fundamental aspects

381

of Fe/N/As biogeochemical cycles, but also be helpful for improving the current agronomic strategy

382

in As-contaminated paddy soils.

383

This study aimed to decrease As uptake by rice plants via the simultaneous application of Fe(II)

384

and NO3– to severely contaminated paddy soil with As collected from mine areas. Consequently, As

385

mobility and bioavailability decreased, followed by a markedly lower As accumulation in rice

386

plants. Additionally, the NO3– application rate (7.5 mmol kg-1 soil) was lower than the annual N

387

fertilizer rates in major Chinese cereal systems (approximately 14 mmol N kg-1 soil).58 In the

388

presence of both NH3 and NO3–, rice plants take up the former faster than the latter.59 We applied

389

urea as N fertilizer at a rate of 8.33 mg kgsoil-1. Since the concentration of urea was the same across

390

different treatments, no significant differences were expected in grain yield. In the Fe(II)+NO3–

391

treatment, urea was applied as an N fertilizer, whereas NO3– was applied to induce Fe(II) oxidation 16


Page 17 of 30 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


392

and enhance As immobilization in severely contaminated paddy soil. The effect of nitrate addition

393

on enhancing As immobilization in rice plants60 and paddy soils61 are reported, and the underlying

394

processes of N and Fe cycles are fairly well established in sediments.62 However, their combined

395

interactions on As translocation from anaerobic paddy soil to rice plants are far less understood and

396

not systematically. Furthermore, practical application of the agronomic practices in anaerobic paddy

397

soils is urgently needed. Hence, the simultaneous application of Fe(II) and NO3– in flooded paddy

398

soil might be a feasible remediation strategy for growing rice in As-contaminated areas. Despite the

399

recent progress, we still face major challenges in unraveling and understanding the unknown

400

coupled environmental processes that control contaminant fate and transport; thus, more

401

bioremediation and biogeochemical studies need to be conducted under greenhouse and field

402

conditions to establish an efficient strategy for alleviating As accumulation in rice plants.

403 404

Acknowledgements

405

This work was financially supported by the National Natural Science Foundation of China

406

(41330857, 41201504, and 41522105), the National Key Research and Development Program

407

(2017YFD0801002), the Natural Science Foundation of Guangdong Province (2015A030313752),

408

Science and Technology Planning Project of Guangdong Province, China (2015B020237008,

409

2015B020207001), NSFC-Guangdong Joint Fund (U1401234), and the SPICC Program of GDAS.

410

We acknowledge the four anonymous reviewers for constructive comments.

411

Supporting Information

412

Additional data can be found in the Supporting Information including detailed descriptions of

413

experiment method SI-1 - SI-5, Figures S1-S5 and Table S1-S6 with illustrations. This material may

414

be found in the online version of this article.

415

References

416

(1) Williams, P. N.; Lei, M.; Sun, G.; Huang, Q.; Lu, Y.; Deacon, C.; Meharg, A. A.; Zhu, Y. Occurrence and Partitioning

417

of Cadmium, Arsenic and Lead in Mine Impacted Paddy Rice: Hunan, China. Environ. Sci. Technol. 2009, 43(3), 17



Page 18 of 30

418

637-642.

419

(2) Wilson, S. C.; Lockwood, P. V.; Ashley, P. M.; Tighe, M. The Chemistry and Behaviour of Antimony in the Soil

420

Environment with Comparisons to Arsenic: A critical review. Environ. Pollut. 2010, 158 (5), 1169-1181.

421

(3) Mitsunobu, S.; Harada, T.; Takahashi, Y. Comparison of Antimony Behavior with that of Arsenic under Various Soil

422

Redox Conditions. Environ. Sci. Technol. 2006, 40 (23), 7270-7276.

423

(4) Cai, L. M.; Xu, Z. C.; Qi, J. Y.; Feng, Z. Z.; Xiang, T. S. Assessment of Exposure to Heavy Metals and Health Risks

424

among Residents near Tonglushan Mine in Hubei, China. Chemosphere 2015, 127 (0), 127-135.

425

(5) Tomohito, A.; Akira, K.; Koji, B.; Shinsuke, M.; Shingo, M. Effects of Water Management on Cadmium and Arsenic

426

Accumulation and Dimethylarsinic Acid Concentrations in Japanese Rice. Environ. Sci. Technol. 2009, 43 (24),

427

9361-9367.

428

(6) Matsumoto, S.; Kasuga, J.; Makino, T.; Arao, T. Evaluation of the Effects of Application of Iron Materials on the

429

Accumulation and Speciation of Arsenic in Rice Grain Grown on Uncontaminated Soil with Relatively High Levels of

430

Arsenic. Environ. Exp. Bot. 2016, 125, 42-51.

431

(7) Rahman, M. A.; Hasegawa, H.; Rahman, M. M.; Maki, T.; Lim, R. P. Effect of Iron (Fe2+) Concentration in Soil on

432

Arsenic Uptake in Rice Plant (Oryza sativa L.) when Grown with Arsenate [As(V)] and Dimethylarsinate (DMA).

433

Water Air Soil Poll. 2013, 224 (7), 1-11.

434

(8) Ultra, V. U.; Nakayama, A.; Tanaka, S.; Kang, Y.; Sakurai, K.; Iwasaki, K. Potential for the Alleviation of Arsenic

435

Toxicity in Paddy Rice Using Amorphous Iron-(hydr)oxide Amendments. Soil Sci. Plant Nutr. 2009, 55(1), 160-169.

436

(9) Liu, C.; Yu, H.; Liu, C.; Li, F.; Xu, X.; Wang, Q. Arsenic Availability in Rice from A Mining Area: Is Amorphous

437

Iron Oxide-bound Arsenic A Source or Sink? Environ. Pollut. 2015, 199, 95-101.

438

(10) Leuz, A. K.; Mönch, H.; Johnson, C. A. Sorption of Sb(III) and Sb(V) to Goethite: Influence on Sb(III) Oxidation

439

and Mobilization. Environ. Sci. Technol. 2006, 40 (23), 7277-7282.

440

(11) Khan, M. A.; Stroud, J. L.; Zhu, Y.; McGrath, S. P.; Zhao, F. Arsenic Bioavailability to Rice is Elevated in

441

Bangladeshi Paddy Soils. Environ. Sci. Technol. 2010, 44 (22), 8515-8521.

442

(12) Okkenhaug, G.; Zhu, Y.; He, J.; Li, X.; Luo, L.; Mulder, J. Antimony (Sb) and Arsenic (As) in Sb Mining Impacted

443

Paddy Soil from Xikuangshan, China: Differences in Mechanisms Controlling Soil Sequestration and Uptake in Rice.

444

Environ. Sci. Technol. 2012, 46 (6), 3155–3162.

445

(13) Li, X.; Zhang, W.; Liu, T.; Chen, L.; Chen, P.; Li, F. Changes in the Composition and Diversity of Microbial

446

Communities During Anaerobic Nitrate Reduction and Fe(II) Oxidation at Circumneutral pH in Paddy Soil. Soil Biol.

447

Biochem. 2016, 94, 70-79. 18


Page 19 of 30 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


448

(14) Senn, D. B.; Hemond, H. F. Nitrate Controls on Iron and Arsenic in An Urban Lake. Science 2002, 296 (5577),

449

2373-2376.

450

(15) Amstaetter, K.; Borch, T.; Larese-Casanova, P.; Kappler, A. Redox Transformation of Arsenic by Fe(II)-activated

451

Goethite (α-FeOOH). Environ. Sci. Technol. 2009, 44 (1), 102-108.

452

(16) Liu, W.; Zhu, Y.; Hu, Y.; Williams, P.; Gault, A.; Meharg, A.; Charnock, J.; Smith, F. Arsenic Sequestration in

453

Iron Plaque, Its Accumulation and Speciation in Mature Rice Plants (oryza sativa L.). Environ. Sci. Technol. 2006, 40

454

(18), 5730-5736.

455

(17) Colmer, T. D. Long-distance Transport of Gases in Plants: A Perspective on Internal Aeration and Radial Oxygen

456

Loss from Roots. Plant Cell Environ. 2003, 26 (1), 17-36.

457

(18) Wang, X.; Liu, C.; Yuan, Y.; Li, F. Arsenite Oxidation and Removal Driven by a Bio-Electro-Fenton Process under

458

Neutral pH Conditions. J. Hazard. Mater. 2014, 275 (2), 200-209.

459

(19) Emerson, D.; Moyer, C. Isolation and Characterization of Novel Iron-oxidizing Bacteria that Grow at

460

Circumneutral pH. Appl. Environ. Microb. 1998, 63 (12), 4784-4792.

461

(20) Achtnich, C.; Bak, F.; Conrad, R. Competition for Electron Donors among Nitrate Reducers, Ferric Iron Reducers,

462

Sulfate Reducers, and Methanogens in Anoxic Paddy Soil. Biol. Fert. Soils 1995, 19 (1), 65-72.

463

(21) Straub, K. L.; Benz, M.; Schink, B.; Widdel, F. Anaerobic, Nitrate-dependent Microbial Oxidation of Ferrous Iron.

464

Appl. Environ. Microb. 1996, 62 (4), 1458-1460.

465

(22) Coby, A. J.; Picardal, F.; Shelobolina, E.; Xu, H.; Roden, E. E. Repeated Anaerobic Microbial Redox Cycling of

466

Iron. Appl. Environ. Microbiol. 2011, 77 (17), 6036–6042.

467

(23) Oremland, R. S.; Hoeft, S. E.; Santini, J. M.; Nasreen, B.; Hollibaugh, R. A.; Hollibaugh, J. T. Anaerobic Oxidation

468

of Arsenite in Mono Lake Water and by A Facultative, Arsenite-oxidizing Chemoautotroph, Strain MLHE-1. Appl.

469

Environ. Microb. 2002, 68 (10), 4795-4802.

470

(24) Terry, L. R.; Kulp, T. R.; Wiatrowski, H.; Miller, L. G.; Oremland, R. S. Microbiological Oxidation of Antimony(III)

471

with Oxygen or Nitrate by Bacteria Isolated from Contaminated Mine Sediments. Appl. Environ. Microb. 2015, 81 (24),

472

8478-8488.

473

(25) Sun, W.; Sierra-Alvarez, R.; Milner, L.; Oremland, R.; Field, J. A. Arsenite and Ferrous Iron Oxidation Linked to

474

Chemolithotrophic Denitrification for the Immobilization of Arsenic in Anoxic Environments. Environ. Sci. Technol.

475

2009, 43 (17), 6585-6591.

476

(26) Sun, J.; Chillrud, S. N.; Mailloux, B. J.; Bostick, B. C. In Situ Magnetite Formation and Long-term Arsenic

477

Immobilization under Advective Flow Conditions. Environ. Sci. Technol. 2016, 50 (18), 10162−10171. 19



Page 20 of 30

478

(27) Harvey, C. F.; Swartz, C. H.; Badruzzaman, A. B. M.; Nicole, K. B.; Winston, Y.; M Ashraf, A.; Jenny, J.; Roger, B.;

479

Volker, N.; Daniel, B. Arsenic Mobility and Groundwater Extraction in Bangladesh. Science 2002, 298 (5598),

480

1602-1606.

481

(28) Ratering, S.; Schnell, S. Nitrate-dependent Iron(II) Oxidation in Paddy Soil. Environ. Microbiol. 2001, 3 (2),

482

100-109.

483

(29) Yu, H.; Xiao L.; Li, F.; Liu C.; Huang, W.; Yu, W. Iron Redox Cycling Coupling Transformation and

484

Immobilization of Heavy Metals: Implication for Paddy Rice Safety in Red Soil of South China. Adv. Agron. 2016, 137,

485

279-317.

486

(30) Wang, X.; He, M.; Xi, J.; Lu, X. Antimony Distribution and Mobility in Rivers around the World's Largest

487

Antimony Mine of Xikuangshan, Hunan Province, China. Microchem. J. 2011, 97 (1), 4-11.

488

(31) He, M. Distribution and Phytoavailability of Antimony at An Antimony Mining and Smelting Area, Hunan, China.

489

Environ. Geochem. Hlth. 2007, 29 (3), 209-219.

490

(32) Okazaki, M.; Sakaidani, K.; Saigusa, T.; Sakaida, N. Ligand Exchange of Oxyanions on Synthetic Hydrated Oxides

491

of Iron and Aluminum. Soil Sci. Plant Nutr. 1989, 35 (3), 337-346.

492

(33) Kang, Y.; Inoue, N.; Rashid, M. M.; Sakurai, K. Fixation of Soluble Selenium in Contaminated Soil by Amorphous

493

Iron (hydr)oxide. Environ. Sci. 2002, 15, 173-182.

494

(34) Zheng, M.; Cai, C.; Hu, Y.; Sun, G.; Williams, P.; Cui, H.; Li, G.; Zhao, F.; Zhu, Y. Spatial Distribution of Arsenic

495

and Temporal Variation of Its Concentration in Rice. New Phytol. 2011, 189 (1), 200-209.

496

(35) Carey, A. M.; Meharg, A. A. Grain Unloading of Arsenic Species in Rice. Plant Physiol. 2009, 152 (1), 309-319.

497

(36) Alam, M. G. M.; Tokunaga, S.; Maekawa, T. Extraction of Arsenic in A Synthetic Arsenic-contaminated Soil Using

498

Phosphate. Chemosphere 2001, 43 (8), 1035-1341.

499

(37) Nanzyo, M.; Yaginuma, H.; Sasaki, K.; Ito, K.; Aikawa, Y.; Kanno, H.; Takahashi, T. Identification of Vivianite

500

Formed on the Roots of Paddy Rice Grown in Pots. Soil Sci. Plant Nutr. 2010, 56 (3), 376-381.

501

(38) Wang, X.; Yao, H.; Ming, H. W.; Ye, Z. Dynamic Changes in Radial Oxygen Loss and Iron Plaque Formation and

502

Their Effects on Cd and As Accumulation in Rice (Oryza sativa L.). Environ. Geochem. Hlth. 2013, 35 (6), 779-788.

503

(39) Tripathi, R. D.; Tripathi, P.; Dwivedi, S.; Kumar, A.; Mishra, A.; Chauhan, P. S. Roles for Root Iron Plaque in

504

Sequestration and Uptake of Heavy Metals and Metalloids in Aquatic and Wetland Plants. Metallomics 2014, 6 (10),

505

1789-1800.

506

(40) Zhao, F. J.; Mcgrath, S. P.; Meharg, A. A. Arsenic as A Food Chain Contaminant: Mechanisms of Plant Uptake and

507

Metabolism and Mitigation Strategies. Ann. Rev. Plant Biol. 2010, 61 (4), 535-559. 20


Page 21 of 30 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


508

(41) Honma, T.; Ohba, H.; Kaneko-Kadokura, A.; Makino, T.; Nakamura, K.; Katou, H. Optimal Soil Eh, pH, and Water

509

Management for Simultaneously Minimizing Arsenic and Cadmium Concentrations in Rice Grains. Environ. Sci.

510

Technol. 2016, 50 (8), 4178–4185.

511

(42) Liu, T.; Zhang, W.; Li, X.; Li, F.; Shen, W. Kinetics of Competitive Reduction of Nitrate and Iron Oxides by

512

Aeromonas Hydrophila HS01. Soil Sci. Soc. Am. J. 2014, 78 (6), 1903-1912.

513

(43) Hiemstra, T.; Riemsdijk, W. H. V. Adsorption and Surface Oxidation of Fe(II) on Metal (Hydr)oxides. Geochim.

514

Cosmochim. Acta 2007, 71 (24), 5913-5933.

515

(44) Dixit, S.; Hering, J. G. Sorption of Fe(II) and As(III) on Goethite in Single- and Dual-sorbate Systems. Chem. Geol.

516

2006, 228 (1–3), 6-15.

517

(45) Borch, T.; Kretzschmar, R.; Kappler, A.; Cappellen, P. V.; Ginder-Vogel, M.; Voegelin, A.; Campbell, K.

518

Biogeochemical Redox Processes and Their Impact on Contaminant Dynamics. Environ. Sci. Technol. 2010, 44 (1),

519

15-23.

520

(46) Melton, E. D.; Swanner E. D.; Behrens S.; Schmidt C.; Kappler A. The Interplay of Microbially Mediated and

521

Abiotic Reactions in the Biogeochemical Fe Cycle. Nat. Rev. Microbiol. 2014, 12 (12), 797-808.

522

(47) Hoeft, S. E.; Jodi Switzer, B.; Stolz, J. F.; Robert, T.; Brian, W.; King, G. M.; Santini, J. M.; Oremland, R. S.

523

Alkalilimnicola ehrlichii sp. nov., A Novel, Arsenite-oxidizing Haloalkaliphilic Gammaproteobacterium Capable of

524

Chemoautotrophic or Heterotrophic Growth with Nitrate or Oxygen as the Electron Acceptor. Int. J. Syst. Evol Micr.

525

2007, 57 (3), 504-512.

526

(48) Xiu, W.; Guo, H.; Shen, J.; Liu, S.; Ding, S.; Hou, W.; Ma, J.; Dong, H. Stimulation of Fe(II) Oxidation, Biogenic

527

Lepidocrocite Formation, and Arsenic Immobilization by Pseudogulbenkiania sp. Strain 2002. Environ. Sci. Technol.

528

2016, 50 (12), 6449–6458

529

(49) Jia, Y.; Huang, H.; Zhong, M.; Wang, F.; Zhang, L.; Zhu, Y. Microbial Arsenic Methylation in Soil and Rice

530

Rhizosphere. Environ. Sci. Technol. 2013, 47 (7), 3141-3148.

531

(50) Arao, T.; Kawasaki, A.; Baba, K.; Mori, S.; Matsumoto, S. Effects of Water management on Cadmium and Arsenic

532

Accumulation and Dimethylarsinic Acid Concentrations in Japanese Rice. Environ. Sci. Technol. 2009, 43 (24),

533

9361-9367.

534

(51) Xu, L. N.; Li, Z. P.;

535

Anaerobic Condition. Environ. Sci. 2009, 30 (1), 221-226.

536

(52) Li, H.; Peng, J.; Weber, K. A.; Zhu, Y. Phylogenetic Diversity of Fe(III)-reducing Microorganisms in Rice Paddy

537

Soil: Enrichment Cultures with Different Short-chain Fatty Acids as Electron Donors. J Soil Sediment 2011,11 (7),

Che, Y. P. Influences of Humic Acids on the Dissimilatory Iron Reduction of Red Soil in

21



Page 22 of 30

538

1234-1242.

539

(53) Yin, S. X.; Chen, D.; Chen, L. M.; Edis, R. Dissimilatory Nitrate Reduction to Ammonium and Responsible

540

Microorganisms in Two Chinese and Australian Paddy Soils. Soil Biol. Biochem. 2002, 34 (8), 1131-1137.

541

(54) Ishii, S.; Ikeda, S.; Minamisawa, K.; Senoo, K. Nitrogen Cycling in Rice Paddy Environments: Past Achievements

542

and Future Challenges. Microbes Environ. 2011, 26 (4), 282-292.

543

(55) Straub, K. L.; Buchholzcleven, B. E. Enumeration and Detection of Anaerobic Ferrous Iron-oxidizing,

544

Nitrate-reducing Bacteria from Diverse European Sediments. Appl. Environ. Microb. 1998, 64 (12), 4846-4856.

545

(56) Meharg, A. A.; Williams, P. N.; Adomako, E.; Lawgali, Y. Y.; Deacon, C.; Villada, A.; Cambell, R. C.; Sun, G.; Zhu,

546

Y.; Feldmann, J. Geographical Variation in Total and Inorganic Arsenic Content of Polished (white) Rice. Environ. Sci.

547

Technol. 2009, 43 (5), 1612-1617.

548

(57) Zhu, Y.; Sun, G.; Lei, M.; Teng, M.; Liu, Y.; Chen, N.; Wang, L.; Carey, A. M.; Deacon, C.; Raab, A. High

549

Percentage Inorganic Arsenic Content of Mining Impacted and Nonimpacted Chinese Rice. Environ. Sci. Technol. 2008,

550

42 (13), 5008-5013.

551

(58) Guo, J.; Liu, X.; Zhang, Y.; Shen, J.; Han, W.; Zhang, W.; Christie, P.; Goulding, K.; Vitousek, P.; Zhang, F.

552

Significant Acidification in Major Chinese Croplands. Science 2010, 327 (5968), 1008-1010.

553

(59) Sasakawa, H.; Yamamoto, Y. Comparison of the Uptake of Nitrate and Ammonium by Rice Seedlings. Plant

554

Physiol. 1978, 62 (4), 665-669.

555

(60) Chen, X.; Zhu, Y.; Hong, M.; Kappler, A.; Xu, Y. Effects of Different Forms of Nitrogen Fertilizers on Arsenic

556

Uptake by Rice Plants. Environ. Toxicol. Chem. 2008, 27 (4), 881–887.

557 558

22


Page 23 of 30 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


559

Figure Captions

560

Figure 1. Arsenic (As) concentrations (mg kg-1) in rice root (A) and straw (B) during the entire

561

growth stage; As speciation in brown rice at the maturing stage (C). DMA, dimethylarsinic acid;

562

MMA, monomethylarsonic acid. Multiple comparisons between different treatments were made by

563

the Turkey-Kramer test (p < 0.05). Different letters within a group indicate a significant difference,

564

while the same letters indicate the values are not significantly different.

565

Figure 2. Changes in As/Fe speciation of rhizosphere soil among different treatments during the

566

entire growth stage. H2O-As/Fe(II) (Figure 2(A)/(E)) represent dissolved As/Fe(II) extracted with

567

ultrapure deionized water; HCl-As/Fe(II) (Figure 2(B)/(F)) represent HCl-extractable As/Fe(II)

568

extracted with 0.5 M HCl; Ox-As/Fe (Figure 2(C)/(G)) represent oxalate-extractable As/Fe

569

extracted with 0.2 M ammonium oxalate; and Plaque-As/Fe (Figure 2(D)/(H)) represent total As/Fe

570

in iron plaque bound on rice roots extracted with DCB (0.03 M Na3C6H5O7·2H2O, 0.125 M

571

NaHCO3 and 0.5 g Na2S2O4).

572

Figure 3. As speciation in water-soluble (H2O-As(III)/As(V), dissolved As(III)/As(V) extracted

573

with ultrapure deionized water), phosphate-extractable (PO4-As(III)/As(V), phosphate-extractable

574

As(III)/As(V)

575

HCl-extractable As extracted with 0.5 M HCl), oxalate-extractable (Ox-As(III)/As(V),

576

oxalate-extractable As(III)/As(V) extracted with 0.2 M ammonium oxalate) soil fractions

577

determined by LC-AFS and Fe plaque bound on rice roots (Plaque-As extracted with DCB (0.03 M

578

Na3C6H5O7·2H2O, 0.125 M NaHCO3 and 0.5 g Na2S2O4)) at the maturing stage. The bar pattern

579

with dense represents As(III) and the other means As(V). Multiple comparisons between different

580

treatments were made by the Turkey-Kramer test (p < 0.05). Different letters within a group

581

indicate a significant difference, while the same letters indicate the values are not significantly

582

different.

583

Figure 4. Changes in soil pH (A) and Eh (B) among different treatments throughout the whole

extracted

with

0.05

M

NH4H2PO4),

HCl-extractable

(HCl-As(III)/As(V),

23



Page 24 of 30

584

growth period.

585

Figure 5. Correlations between the concentrations of PO4-As (total phosphate-extractable As

586

extracted with 0.05 M NH4H2PO4), Ox-As(III)/(V) (oxalate-extractable As(III)/(V) extracted with

587

0.2 M ammonium oxalate) and iron fractions (Dis-Fe(II), dissolved Fe(II) extracted with ultrapure

588

deionized water; HCl-Fe(II), HCl-extractable Fe(II) extracted with 0.5 M HCl; Ox-Fe,

589

oxalate-extractable Fe extracted with 0.2 M ammonium oxalate; and Plaque-Fe, Fe bound on rice

590

roots extracted with 0.03 M Na3C6H5O7·2H2O, 0.125 M NaHCO3 and 0.5 g Na2S2O4 (DCB)) in

591

rhizosphere soil at the maturing stage.

592 593

24


Page 25 of 30

Figure 1.

594

-1

-1

120

80

40 0

595

15

Fe(II)

Straw As (mg kg )

Control Am-FeOH NO3 Fe(II)+NO3

30

60

90

Time (d)

120

150

(B) Brown rice As (mg kg-1)

(A) 160

Root As (mg kg )

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


12 9 6 3 0

30

60

90

120

Time (d)

150

0.5

(C)

Unrecovered As MMA DMA As(V) As(III)

a

0.4

b

b c

0.3

d

0.2 0.1 0.0 Control

Am-FeOH

Fe(II)

−

NO3−

−

Fe(II)+NO3−

Treatments

25



Figure 2.

596

-1

As fractions (mg kg )

597

2.0

(B) HCl-As

50

(C) Ox-As

600

(D) Plaque-As

1.5 1.0

12

0.5

8

40

400

30

200

4 2.0

(E) H2O-Fe

0.015

20 6

(F) HCl-Fe

Fe(II) + NO3

0

500

(G) Ox-Fe

(H) Plaque-Fe

400

1.6

4 300

0.010

1.2

200

2

0.005

100

0.8 0.000

Control Am-FeOH Fe(II) NO3 -

0.0

-1

598

20

(A) H2O-As

16

0.020

Fe fractions (g kg )

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Page 26 of 30

0

30

60

90

Time (d)

120

150

0

30

60

90

Time (d)

120

150

0

0

30

60

90

Time (d)

120

150

0

0

30

60

90

120

150

Time (d)

26


Page 27 of 30

Figure 3.

599 50

800 -

-

40

a

20

10

0

600

As(III)

c

30

d

Plaque-As -1 (mg kgroot)

ab 600

ab a b abab

As(V)

b

1.2

0.8

Fe(II) + NO3

NO3

1.6

Fe(II)

Am-FeOH

Control

Soil As (mg kg-1)

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


ab b bc

d

400

c

0.4

a a

0.0

b cc

b cc

d

200

d

a dcbd H2O-As

0 PO4-As

HCl-As

Ox-As

Plaque-As

601 602 603

27



Figure 4.

604 7.5

(A)

Control NO3

7.0

Am-FeOH Fe(II) + NO3

0 (B)

Fe(II)

-20

Soil Eh (mV)

6.5

Soil pH

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Page 28 of 30

6.0

5.5

-40 -60 -80 -100

5.0 0

605 606

30

60

90

120

150

0

30

Time (d)

60

90

120

150

Time (d)

607 608 609

28


Page 29 of 30

Figure 5.

PO4-As (mg kg-1)

610

Ox-As(V) (mg kg-1) Ox-As(III) (mg kg-1)

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


r = 0.852, p < 0.0001

r = 0.885, p < 0.0001

r = - 0.843, p < 0.0001

r = - 0.828, p < 0.0001

r = 0.836, p = 0.0001

r = 0.857, p < 0.0001

r = - 0.806, p = 0.0003

r = - 0.884, p < 0.0001

12 10 8 18 16 14 12 24

r = 0.825, p = 0.0002

r = 0.764, p = 0.0009

18 15 12 3

611 612

r = - 0.798, p = 0.0004

r = - 0.701, p = 0.0036

21

6

9

12

H2O-Fe(II) (mg kg-1)

.9

1.2

1.5

HCl-Fe(II) (g kg-1)

1.8

4

5

Ox-Fe (g kg-1)

6

12

16

20

24

Plaque-Fe (g kgroot-1)

613

29



614

For TOC only

As↓ Biological reduction

≡Fe-As

Fe(II) NO3-

Fe(II) uptake

≡FeOH Biological oxidation

Bioavailable

As

Incorporation

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Page 30 of 30

NO3Biological

ROL

Plaque

As(III) O2 Fe(II)

615

Oxidation

As(V)

Chemical reactive Fe(III)

≡FeOH-Fe(II)

616 617 618

30


Effects of Simultaneous Application of Ferrous Iron and Nitrate on

Recommend Documents