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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

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ACS Earth and Space Chemistry

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

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grown in contaminated paddy soil

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

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

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

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*

Corresponding author. Tel.: +86 20 37021396

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

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1

Xiangqin Wang and Tongxu Liu contributed equally to this work.

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(Submitted on December 2017)

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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

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ABSTRACT:

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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As-contaminated paddy fields.

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

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INTRODUCTION

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

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

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

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

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

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

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

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

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

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

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urgently needed.

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

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

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

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

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7, 8

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

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

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

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

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

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

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

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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)

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

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

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

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

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

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

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

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

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rhizosphere.

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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


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

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

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and thus, further research is needed.

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

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

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

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

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

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

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

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MATERIALS AND METHODS

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

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

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

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

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

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

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

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

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

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following pot experiments.

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

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

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



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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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RESULTS

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

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


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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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



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

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

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

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

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

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

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

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

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

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the soil.

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< Fig. 1>

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

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

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

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

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

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

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

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

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

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

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

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

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


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

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

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

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

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

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

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

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< Fig. 2, Fig. 3>

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

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

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

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

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

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

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

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

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

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

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

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

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

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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

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

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

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



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

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

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

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

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

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

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< Fig. 4>

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

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

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

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

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

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

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

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

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

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

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

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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

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

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

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

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


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

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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

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reduces As accumulation in rice plants via As immobilization.

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< Fig. 5>

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

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

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

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

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

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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).

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

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

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

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DISCUSSION

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

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

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

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

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

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

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

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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



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

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

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≡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

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(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

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(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.

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

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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

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1234-1242.

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(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,

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

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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.

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

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

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

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

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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 ... - ACS Publications

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