Arsenic(V) Incorporation in Vivianite during Microbial Reduction of

Feb 1, 2016 - The dissolution of arsenic-bearing iron(III) (oxyhydr)oxides during combined microbial iron(III) and arsenate(V) reduction is thought to...
2 downloads 0 Views 3MB Size
Subscriber access provided by Chicago State University

Article

Arsenic(V) incorporation in vivianite during microbial reduction of arsenic(V)-bearing biogenic Fe(III) (oxyhydr)oxides E. Marie Muehe, Guillaume Morin, Lukas Scheer, Pierre Le Pape, Imène Esteve, Birgit Daus, and Andreas Kappler Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.5b04625 • Publication Date (Web): 01 Feb 2016 Downloaded from http://pubs.acs.org on February 2, 2016

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.

Environmental Science & Technology 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 38

Environmental Science & Technology

1

Arsenic(V) incorporation in vivianite during microbial reduction

2

of arsenic(V)-bearing biogenic Fe(III) (oxyhydr)oxides

3 4

E. Marie Muehe1,2*, Guillaume Morin3, Lukas Scheer1, Pierre Le Pape3,

5

Imène Esteve3, Birgit Daus4, Andreas Kappler1

6 7

1

Geomicrobiology, Center for Applied Geosciences, University of Tuebingen, Germany

8

2

Now: Environmental Soil Biogeochemistry, Earth System Science, Stanford University, USA

9

3

Environmental Mineralogy, Institut de Minéralogie, de Physique des Matériaux et de

10

Cosmochimie (IMPMC), UMR7590 - CNRS - UPMC, France

11

4

12

Germany

UFZ – Helmholtz Centre for Environmental Research, Department Analyt. Chem., Leipzig,

13 14

For re-submission to Environmental Science and Technology

15 16

*To whom correspondence should be sent:

17

E. Marie Muehe, Environmental Soil Biogeochemistry, Earth System Science, Stanford

18

University, 473 Via Ortega, Stanford, CA 94305, USA

19

Phone: +1-650-291-9715, email: [email protected]

20 21

Running title: As-incorporation in microbially produced vivianite

22

Keywords: Arsenate, arsenite, biomineralization, biogenic iron minerals, Fe(III)-reducing

23

bacteria

24 25 26

ACS Paragon Plus Environment

Environmental Science & Technology

27

ABSTRACT

28

The dissolution of arsenic-bearing iron(III) (oxyhydr)oxides during combined microbial

29

iron(III) and arsenate(V) reduction is thought to be the main mechanism responsible for arsenic

30

mobilization in reducing environments. Besides its mobilization during bio-reduction, arsenic

31

is often re-sequestered by newly forming secondary iron(II)-bearing mineral phases. In

32

phosphate-bearing environments, iron(II) inputs generally lead to vivianite precipitation. In

33

fact, in a previous study we observed that during bio-reduction of arsenate(V)-bearing biogenic

34

iron(III) (oxyhydr)oxides in phosphate-containing growth media, arsenate(V) was immobilized

35

by the newly-forming secondary iron(II) and iron(II)/iron(III)mineral phases, including

36

vivianite. In the present study, changes in arsenic redox state and binding environment in these

37

experiments were analyzed. We found that arsenate(V) partly replaced phosphate in vivianite,

38

thus forming a vivianite-symplesite solid solution identified as Fe3(PO4)1.7(AsO4)0.3•8H2O. Our

39

data suggests that in order to predict the fate of arsenic during the bio-reduction of abiogenic

40

and biogenic iron(III) (oxyhydr)oxides in arsenic-contaminated environments, the formation of

41

symplesite-vivianite minerals needs to be considered. Indeed, such mineral phases could

42

contribute to a delayed and slow release of arsenic in phosphate-bearing surface and

43

groundwater environments.

44

TOC art:

45 46 47

ACS Paragon Plus Environment

Page 2 of 38

Page 3 of 38

Environmental Science & Technology

48

INTRODUCTION

49

Arsenic (As) is one of the most widely studied metalloids since it has been recognized as a

50

major threat to human health, especially when present at concentrations above the

51

recommended WHO levels (10 µg L-1) in groundwater aquifers.1,

52

concentrations as found in the aquifers of Bengal and Mekong deltas are caused by a

53

combination of various geochemical and microbial processes.1-3 The transformation of As-

54

bearing minerals during their riverine transport from Himalaya leads to the binding of As to

55

Fe(III) (oxyhydr)oxide minerals within the deltaic sediments.4-6 Arsenic may then be released

56

from the surface of these Fe(III) minerals by sorption competitors, such as phosphate,7

57

bicarbonate,8 silicic acid,9 natural organic matter (NOM, e.g. humic substances)10, 11 as well as

58

by the formation of mobile humic-Fe-As complexes and colloidal aggregates.12, 13 Additionally,

59

microbial reduction of the mineral-bound As(V) to the more mobile As(III) form was suggested

60

to lead to As mobilization.14-17 The most important factor responsible for the high As

61

concentrations in the groundwater, however, is thought to be related to reductive dissolution of

62

the As-bearing Fe(III) (oxyhydr)oxide minerals by Fe(III)-reducing bacteria in anoxic As-

63

contaminated aquifers.16, 18 By using allochthonous and autochthonous organic matter these

64

bacteria reductively dissolve Fe(III) (oxyhydr)oxides, leading to the release of the bound As.2-

65

4, 18, 19

66

which As release was accompanied by the progressive export of aqueous Fe(II) from the

67

columns.20, 21

68

Fe(III) (oxyhydr)oxides in the environment are formed either via chemical or microbial

69

oxidation of Fe(II).22,

70

environments24-30 and were typically associated with cell-derived organic matter.31-35 Organic

71

carbon and ion impurities hinder homogenous crystal growth,22 leading to smaller and less

72

crystalline biogenic minerals compared to abiogenic Fe(III) (oxyhydr)oxides.36-39 Phosphate is

73

one such ion impurity and is thus frequently encountered as a major constituent of Fe(III)

2

Elevated aqueous As

The feasibility of this process was also simulated with long-time column experiments, in

23

Biogenic Fe(III) (oxyhydr)oxides have been found in various

ACS Paragon Plus Environment

Environmental Science & Technology

74

(oxyhydr)oxides found in many different environmental systems.40-45 Bacteriogenic Fe(III)

75

(oxyhydr)oxides were shown to be highly susceptible to microbial reduction compared to

76

synthetic, poorly crystalline Fe phase analogues, though the rate of bio-reduction varied

77

according to the mineralogy of the biogenic Fe(III) (oxyhydr)oxide.46, 47 The resulting biogenic

78

Fe(II) mineral products able to capture As include siderite (FeCO3),48 magnetite (FeIIFeIII2O4),20,

79

48-50

80

column experiments. Especially vivianite is of interest as secondarily formed Fe(II) mineral

81

phase in culture media,47,48 aquifers,52 and in fertilized and non-fertilized paddy soils.53, 54 More

82

specifically, Islam et al.48 showed that vivianite sorbs As(V) after bio-reduction of soluble

83

Fe(III) but did not observe direct evidence for As(V) incorporation in the vivianite structure.

84

More recently, Muehe et al.46 found that microbial reduction of As(V)-bearing biogenic Fe(III)

85

(oxyhydr)oxides in freshwater medium containing 1 mM phosphate resulted mainly in the

86

formation of vivianite. They discussed that As(V) is very likely to be associated with vivianite

87

but so far, the mechanism of As(V) immobilization during this process is unknown.

88

The goal of the present study was to investigate the fate of As after microbial reduction of

89

As(V)-bearing biogenic Fe(III) (oxyhydr)oxides. More specifically, the objectives were (I) to

90

identify the localization and binding mode of As(V) and As(III) in the newly formed Fe mineral

91

phases using electron microscopy and synchrotron-based X-ray absorption spectroscopy and

92

(II) to identify arsenic speciation changes in the solid and liquid phase to better understand the

93

mobility of As in the system. The presentation of the data will conclude to the discussion of the

94

mechanisms of As scavenging and release processes under the reducing conditions investigated.

, green rust (FeII4FeIII2(OH)12CO3),51 and vivianite (Fe3(PO4)2)48, 49 in batch and short-time

95 96

MATERIAL AND METHODS

97

Source of microorganism, microbial growth conditions, and biogenic Fe(III)

98

(oxyhydr)oxide synthesis. We used the Fe(III)-reducing γ-Proteobacterium Shewanella

99

oneidensis strain MR-1, which utilizes a wide range of organic substrates and uses Fe(III) as an ACS Paragon Plus Environment

Page 4 of 38

Page 5 of 38

Environmental Science & Technology

100

electron acceptor in the absence of O2.55 Iron-free pre-cultures (20 mM lactate, 40 mM

101

fumarate) and experimental cultures (20 mM lactate, 5-7 mM Fe(III) biogenic minerals) of

102

strain MR-1 were grown in freshwater medium (0.14 g L-1 KH2PO4, 0.2 g L-1 NaCl, 0.3 g L-1

103

NH4Cl, 0.5 g L-1 MgSO4·7H2O, 0.1 g L-1 CaCl2·2H2O, 22 mM bicarbonate buffer, pH 7, 1 mL

104

L-1 vitamin solution, 1 mL L-1 trace element solution, 1 mL L-1 selenate-tungstate solution) and

105

prepared under an N2/CO2 (80/20 v/v) atmosphere according to Muehe et al.46 The biogenic

106

material used in the experiments here was produced independently of the Muehe et al.46 study,

107

as large quantities of minerals were needed for analysis. However, these experiments were run

108

at the same time when the Muehe et al.46 study was performed, using the same chemicals,

109

apparatuses, and incubators, ensuring maximum compliance between both studies. As the

110

geochemical, XRD, and microscopic data of this study and Muehe et al.46 are in accordance,

111

we assume that the mineralogy of the here-used biogenic material is the same as in Muehe et

112

al.46.

113

The As(V)-bearing biogenic Fe(III) (oxyhydr)oxides were synthesized using Acidovorax sp.

114

strain BoFeN1 according to Hohmann et al.56 and Muehe et al.46, and harvested and processed

115

according to Muehe et al.46. Biogenic Fe(III) minerals with two initial Fe(III) to As(V) ratios

116

of 250 to 1 and of 50 to 1 [w/w] were investigated, which approximates to 335 to 1 and 67 to 1

117

[Fe mol/ As mol] or 0.003 to 1 and 0.015 to 1 [As mol/ Fe mol], respectively.

118

For Fe(III) reduction experiments with strain MR-1, 50 mL of freshwater medium were set-up

119

in 100 mL bottles and amended with 5 to 7 mM of As-bearing biogenic Fe(III) minerals, 20 mM

120

of Na-lactate, and 100 µM of 9,10-anthraquinone-2,6-disulfonate (AQDS). 2×105 cells mL-1 of

121

strain MR-1 were added to the set-ups from an iron-free pre-culture grown on 20 mM lactate

122

as electron donor and 40 mM fumarate as electron acceptor. The synthesis of the biogenic

123

Fe(III) (oxyhydr)oxide and their reduction with MR-1 were performed in the dark at 28°C.

124

Aqueous and solid-phase samples were taken at the end of the microbial exponential growth

ACS Paragon Plus Environment

Environmental Science & Technology

125

phase after 5 days of reduction to ensure the analysis of freshly formed and non-aged secondary

126

Fe(II) minerals according to Muehe et al.46.

127 128

Sampling of batch experiments. All experiments were conducted in triplicate. Samples were

129

taken anoxically in a N2-filled glove box before and after inoculation with strain MR-1 as well

130

as after 5 days. For each time point, three parallel individual bottles were sampled for

131

determining the solution chemistry followed by harvesting the minerals for mineralogical

132

analyses. Aqueous samples were taken with anoxic syringes and analyzed for total and

133

dissolved Fe(II) and Fe(III), total dissolved As and As speciation according to Muehe et al.46.

134

Samples for quantification of total dissolved As were frozen at -20°C until measurement. The

135

minerals were harvested in the glove box by decanting the supernatant followed by

136

centrifugation (13,200 g for 2 min) and vacuum drying of the mineral pellet. Once dry, the

137

minerals of three parallel bottles were pooled in equal amounts for mineral analysis.

138 139

Solution chemistry analysis. Total and dissolved Fe(II) and Fe(III) were quantified spectro-

140

photometrically using the ferrozine assay according to Stookey, 197057 and following the

141

protocol in Muehe et al.46. While Fe(II) was directly quantified with the ferrozine assay, Fe(III)

142

was first reduced by 10% hydroxylamine hydrochloride before determining total Fe by

143

complexation with ferrozine. Total dissolved As was quantified by diluting thawed samples in

144

2% HNO3 and measuring with an inductively-coupled-plasma mass-spectrometer (7700 series

145

ICP-MS, Agilent Technologies). Using a high-pressure-liquid chromatography-coupled ICP-

146

MS (7700 series ICP-MS, Agilent Technologies), the As redox speciation present before and

147

after incubation were quantified in a 10 mM phosphoric acid matrix, which preserves the redox

148

state of As.58

149

ACS Paragon Plus Environment

Page 6 of 38

Page 7 of 38

Environmental Science & Technology

150

Mineralogical and spectroscopic analyses. All samples for mineral and Fe-As bonding

151

environment analysis were prepared under anoxic conditions in glove boxes or bags, dried

152

under vacuum, and stored and transported anoxically in the dark. Samples were only exposed

153

to ambient air when taken out of the anoxic transporting container followed by direct insertion

154

into the analytical device. The mineralogy and the binding environment, location, and

155

speciation of Fe and As in the minerals present before (0 day) and during microbial Fe(III)

156

reduction (day 5) were investigated using powder X-ray diffraction (XRD), Scanning Electron

157

Microscopy (SEM) combined with Energy Dispersive X-ray Spectrometry (EDXS), as well as

158

with X-ray Absorption Near-Edge Structure (XANES) and Extended X-ray Absorption Fine

159

Structure (EXAFS) spectroscopy at the Fe and As K-edge.

160

XRD patterns were acquired using an X’Pert pro Panalytical Diffractometer equipped with an

161

X’celerator detector. Samples were deposited on a zero-background Si sample holder and

162

loaded into an anoxic sample chamber equipped with a curved Kapton window (constructed by

163

the IMPMC project group). Data were collected over the 5 to 80° two-theta range with a 0.017°

164

two-theta step, counting 4 hours per sample. Spectra were interpreted using the ICSD database

165

for goethite (# 15-9970), vivianite (# 20-0703), and siderite (# 68298).

166

SEM analyses of carbon-coated samples were performed with a Zeiss ultraTM 55 electron

167

microscope operating at 10 kV with a 60 µm diaphragm in high current mode. Secondary

168

electron images were obtained with an in-lens detector and EDXS analyses were collected using

169

a Bruker Si-drift detector. The As/Fe and P/Fe molar ratio for specific mineral phases were

170

determined by averaging 10 consecutive spot measurements per mineral phase. Semi-

171

quantitative analyses and elemental mapping was performed with the program Esprit 1.8(3)

172

using a spectra database for standard materials. Raw EDX elemental maps were built using the

173

integrated intensities of the Fe L, P K and As L emission lines. EDXS spectra were plotted

174

for selected areas by averaging the spectra recorded for the corresponding pixels. Background

175

subtracted EDX elemental maps were calculated via semi-quantitative elemental analysis using ACS Paragon Plus Environment

Environmental Science & Technology

176

the background subtracted intensities of the Fe L, P K and As K emission lines in individual

177

EDX spectra obtained by binning the mapping data over four pixels.

178

X-ray Absorption Spectroscopy (XAS) data at the Fe K-edge were collected in transmission

179

detection mode below 20K using a He cryostat on the SAMBA beamline at SOLEIL, Orsay,

180

France. Arsenic K-edge data were collected in fluorescence detection mode using a 30 element

181

Ge detector on the FAME-BM30B beamline at ESRF, Grenoble, France. Data for the

182

As:vivianite model compound were collected in fluorescence detection mode using a 38

183

element Ge array detector on the SAMBA beamline. In order to minimize the photo-reduction

184

of As under the X-ray beam, all As K-edge data were recorded below 20K using a He cryostat

185

and the focused beam (