Arctic and Subarctic Natural Soils Emit Chloroform ... - ACS Publications

May 9, 2017 - In situ emissions of chloroform from soil in nine Arctic and subarctic ecosystems were linked to soil trichloroacetyl turnover. The resi...
0 downloads 0 Views 507KB Size
Subscriber access provided by CORNELL UNIVERSITY LIBRARY

Article

Arctic and subarctic natural soils emit chloroform and brominated analogues by alkaline hydrolysis of trihaloacetyl compounds Christian Nyrop Albers, Ole Stig Jacobsen, Erico Marlon Moraes Flores, and Anders Risbjerg Johnsen Environ. Sci. Technol., Just Accepted Manuscript • Publication Date (Web): 09 May 2017 Downloaded from http://pubs.acs.org on May 15, 2017

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 23

Environmental Science & Technology

1

Arctic and subarctic natural soils emit chloroform and brominated analogues

2

by alkaline hydrolysis of trihaloacetyl compounds

3 4

Christian N. Albers1,2*, Ole S. Jacobsen1, Erico M. M. Flores3, Anders R. Johnsen1

5 6 7

1

8

1350 Copenhagen K, Denmark

9

2

Geological Survey of Denmark and Greenland (GEUS), Department of Geochemistry, Øster Voldgade 10, DK-

Center for Permafrost (CENPERM), Department of Geosciences and Natural Resource Management, University

10

of Copenhagen, Denmark

11

3

Departamento de Química, Universidade Federal de Santa Maria, 97105-900, Santa Maria, RS, Brazil

12 13

* Email: [email protected], phone +45 91333557, address: Øster Voldgade 10, DK-1350 Copenhagen K

14

1 ACS Paragon Plus Environment

Environmental Science & Technology

Page 2 of 23

15

Abstract

16

There has been increasing recognition of the occurrence of natural, halogenated organic compounds in marine

17

and terrestrial environments. Chloroform is an example of a halogenated organic compound with natural

18

formation as its primary source. Chloroform emission from soil has been reported from diverse Arctic,

19

temperate and (sub)tropical ecosystems. The terrestrial environment is a significant source to the atmosphere,

20

but little is known about the formation pathway of chloroform in soil. Here, we present evidence that

21

chloroform is formed through the hydrolysis of trichloroacetyl compounds in natural, organic-rich soils. In-situ

22

emissions of chloroform from soil in nine Arctic and subarctic ecosystems were linked to soil trichloroacetyl

23

turnover. The residence time from formation of the trichloroacetyl compounds in soil to the release of

24

chloroform to the atmosphere varied between 1 and 116 active months in unfrozen topsoil, depending on soil

25

pH. Non-specific halogenation that leads to trihaloacetyl formation does not discriminate between chloride and

26

bromide, and brominated analogues were formed alongside chloroform. Soil may therefore be a previously

27

unrecognised, natural source of brominated haloforms. The formation pathway of haloforms through

28

trihaloacetyl compounds can most likely be extended to other ecosystems with organic topsoils.

29 30

Introduction

31

In this article, we report on the formation mechanism of chloroform and its brominated analogues in natural

32

Arctic-subarctic soil. Chloroform has received considerable attention as a frequently detected pollutant in

33

groundwater1. Increasing attention has also been focused on the effects in the troposphere of short-lived

34

organohalogens, such as chloroform and its brominated analogues2-4. In the last 20 years, it has been

35

recognized that natural formation is the primary source of chloroform5 and that substantial amounts of

36

chloroform may be emitted from soils of temperate, coniferous plantations6-9 as well as natural forest

37

floors10,11. Indeed, based on atmospheric measurements in Mace Head, Ireland, the main sources of chloroform

38

in Europe are the less populated areas of Scandinavia, Ireland and Scotland12. This is in contrast to other

39

volatile organohalogens that have their primary European sources in industrialized areas12.

40

Although most previous studies have been conducted in forest plantations and other non-natural areas, it

41

seems that the formation of chloroform is a common process in many natural ecosystems. However, there is

42

very limited understanding about the mechanism of chloroform formation in soil.

43

2 ACS Paragon Plus Environment

Page 3 of 23

Environmental Science & Technology

44

Soil organic matter from chloroform-emitting forest plantations has recently been found to contain chemical

45

structures that can release chloroform at high pH13. The only known organochlorine structure that shows high

46

stability at low pH and hydrolyses to release chloroform at high pH is the trichloroacetyl group14,15.

47

Trihaloacetyl compounds are known intermediates in the nonspecific halogenation reactions that lead to

48

haloform formation during chemical water chlorination and paper pulp bleaching14. We therefore hypothesized

49

that the natural formation of chloroform and brominated analogs occurs through nonspecific halogenation of

50

soil organic matter leading to the formation of trihaloacetyl compounds in soil. These compounds will

51

eventually undergo nucleophilic attack by hydroxide ions (alkaline hydrolysis) and release haloforms (equation

52

1). The rate of hydrolysis will depend on the concentration of the hydroxide ion16, which is determined by the

53

soil pH.

SOM-R 54

HOX

O SOM-C-CX3

OH- hydrolysis

O CHX3 + SOM-C-O-

Trihaloacetyl compounds

(1)

55

where SOM-R is soil organic matter with a reactive group, such as a phenol, quinone, ketone etc. X is a halogen

56

atom, such as chlorine, bromine and possibly iodine.

57 58

At present, known halogenation mechanisms in the terrestrial environment include enzymatic reactions with

59

flavin-dependent halogenases, α-ketoglutarate dependent halogenases, methyl halide transferases or heme-

60

and non-heme haloperoxidases17,18 and non-enzymatic Fenton-like reactions19,20. Of these, only extra-cellular

61

chloro- or bromoperoxidases and Fenton-like reactions have the capacity to form free reactive chlorine or

62

bromine species such as HOCl and HOBr, and hence in theory lead to the formation of trihaloacetyl-groups in

63

soil organic matter. Using carbon and chlorine stable isotopes analysis, it was recently demonstrated in a lab-

64

experiment, that soil humic acid can be chlorinated by both hypochlorite and a commercial chloroperoxidase,

65

which led to pH dependent formation of chloroform, most likely through hydrolysis of trichloroacetyl

66

intermediates15,21. Indeed, most previous research on this subject has been conducted in the laboratory using

67

chemical chlorination with hypochlorite, which is extremely artificial compared to natural processes.

68

Trichloroacetyl compounds were detected in a limited study of three temperate, coniferous plantations13, but

69

data on the general occurrence of trichloroacetyl compounds in natural environments as well as the natural

70

occurrence of brominated analogs has not been reported previously. Empirical support of the trihaloacetyl

71

hypothesis based on analyses of environmental samples is therefore strongly needed.

3 ACS Paragon Plus Environment

Environmental Science & Technology

Page 4 of 23

72 73

The trihaloacetyl hypothesis has two testable predictions:

74

1. Trihaloacetyl compounds will be formed in haloform-producing soils, so that there will be a quasi-steady

75

state between trihaloacetyl formation and hydrolysis to haloforms. Trihaloacetyl compounds will hydrolyze

76

faster at higher pH, and these compounds will therefore show a shorter residence time in soils of higher pH.

77

2. The trihaloacetyl formation mechanism will be nonspecific and will not discriminate between chloride and

78

bromide. Brominated analogues of chloroform will therefore be formed if bromide is present in the soil.

79 80

We carried out a study to test these predictions for nine Arctic and subarctic ecosystems, in which chloroform

81

emissions have recently been reported11 (Fig. S1).

82 83

Experimental

84

Study sites

85

Four Arctic and five subarctic sites with different vegetation and soil properties were chosen for the study (Fig.

86

S1, Table 1). At each site, a 12-m permanent transect was established, with a distance of three metres between

87

the individual 0.06 m2 flux chamber bases. A detailed description of the transects and the study sites has

88

previously been published11.

89 90

Haloform analyses

91

Emissions of chloroform and brominated analogues were determined as described previously11. Briefly, 20-L

92

flux chambers were fitted onto the chamber bases for 65 minutes. Haloforms in the chamber headspace air

93

were trapped and stored in custom-made thermal desorption tubes (89×6.35 mm, containing Carbotrap B (22

94

mm), Carboxen 1003 (16 mm) and Carboxen 1000 (16 mm), Supelco, USA) for subsequent GC-ECD/MS analysis.

95

Before entering the thermal desorption tubes, the air was dried by passage through a Nafion™ desiccant

96

membrane dryer (DM-110-24, Perma Pure, NJ, USA). Each haloform emission was calculated based on four 1-L

97

samples. The chloroform emissions in Table 1 are the mean of two (Kan and Nar sites) or four (Abi and Dis

98

sites) sampling campaigns during the active season from late May to early September.

99 100

On 29 August 2014, 35 additional emission measurements were performed at site Kan-C, to better establish

101

the observed correlation between chloroform and bromodichloromethane emissions. Mobile chamber bases

4 ACS Paragon Plus Environment

Page 5 of 23

Environmental Science & Technology

102

instead of permanently installed bases were used for these samples, to allow the high number of

103

measurements to be performed. Concentrations of CFC11, which is neither consumed nor produced in the soil

104

and therefore should decrease in the chamber after each sampling, were used as a check that the system was

105

not leaking11. In addition, only analyses showing emissions of more than 15 ng m-2 h-1 chloroform or 0.2 ng m-2 h-

106

1

107

uncertain. Out of 35 samples, 18 fulfilled these criteria.

bromodichloromethane were used for further data analysis, as emissions lower than these values were highly

108 109

To sample soil air, a custom made probe comprising a 17-mm brass filter (Propartner, Denmark) connected to a

110

4-mm inner diameter polyamide tube (MB-LONGLIFE™ PA-12, Propartner, Denmark) was pushed to a depth of

111

20 cm. Soil air was then drawn using a membrane pump at 100 mL min-1 (210-1003MTX Twin Port Pocket

112

Pump, SKC, UK). The first 200 mL air was discarded to clean the probe and the following 400 mL was sampled in

113

thermal desorption tubes. A 0.45 µm PTFE filter (Midisart 2000, Sartorius, Germany) and a Nafion™ desiccant

114

membrane dryer were placed between the probe and the pump to remove dust particles and water vapour.

115

The system for collecting soil air was tested in the laboratory and found to neither emit nor adsorb measurable

116

levels of haloforms.

117 118

Soil samples

119

Soil was sampled from the transects by removing living mosses and lichens and then hammering a steel core (Ø

120

= 6 cm) to a depth of 10 cm. Two sets of soil samples were used in this study. The first set was sampled at the

121

nine sites during 2012 before the emission measurements. The 2012 samples were sampled 0.8 m from the

122

center of the chamber bases and used to determine total organic halogen. The second set, used for all other

123

measurements, was sampled in 2014 at the center of each flux chamber after the emission measurements

124

were terminated. The soil for analysis of total halogen and trichloroacetyl compounds was frozen on the day of

125

sampling and stored frozen at -18 °C. Before analysis, the soil was freeze dried and ground to fine powder. In

126

2014 an additional soil core was taken within each chamber base and stored at 5 °C until homogenization and

127

shaking with water (1:2.5, soil:water) to determine pH and perform the analysis of chloride and bromide by ion

128

chromatography (LC50-CD50, Dionex, CA, USA). Soil organic matter was determined as loss on ignition (550 °C,

129

2 hours).

130 131

Analysis of trichloroacetyl compounds

5 ACS Paragon Plus Environment

Environmental Science & Technology

Page 6 of 23

132

The concentration of trichloroacetyl compounds in soil from the nine sites was quantified after alkaline

133

hydrolysis followed by gas chromatographic detection of the formed chloroform as previously described13.

134

Briefly, 0.5 g freeze-dried and homogenized soil was put into a 120-mL serum bottle and then 2.5 mL 0.6M

135

NaOH was added and the bottle closed with crimp-caps containing an alumina-coated septum (Mikrolab

136

Aarhus, Denmark). After overnight shaking, a 9-mL headspace sample was taken with an airtight syringe and

137

injected into thermal desorption tubes for subsequent GC-ECD/MS analysis11. The chloroform in the headspace

138

(>80% of total chloroform) was corrected for sorption to organic matter and dissolution into water based on

139

partitioning experiments with different amounts of water and soil organic matter (supplementary methods).

140 141

The concentration of trichloroacetyl compounds was calculated as chloroform equivalents. The weight-based

142

trichloroacetyl concentrations were recalculated to area-based trichloroacetyl concentrations at each sampling

143

point based on the weight of the 10 cm soil core. The area-based trichloroacetyl concentration was then

144

divided by the mean chloroform emission at the same sampling point to obtain the mean residence time of

145

trichloroacetyl compounds in units of “months with non-frozen topsoil” (active months) for that specific

146

sampling point. Trichloroacetyl mean residence times at site Nar-B could not be reasonably calculated due to

147

chloroform emissions being too low and hence uncertain.

148 149

To test the pH-stability of trihaloacetyl compounds 0.2 g freeze dried and powdered Abi-A soil was weighed

150

into 120-mL serum bottles and pH was adjusted with 5 mL of a 1M citrate buffer (pH 4.7-5.8) or phosphate

151

buffer (pH 6.2-7.9) or just added 5 mL water (pH 4.3) and shaken gently for 24 hours at 23 °C.

152 153

Analysis of total organic halogen in soil

154

Total organic Cl and Br were determined using microwave-induced combustion and subsequent halogen-

155

specific detection, as previously described22,23. Briefly, inorganic halogen was removed from the powdered

156

samples by sequential washing (3 x 0.02M HNO3/0.2M KNO3 and 1 x water). The low pH during washing

157

ensured minimal loss of soil organic matter and ensured that trihaloacetyl compounds were not hydrolyzed.

158

The samples were then combusted in closed quartz vessels using 100 mg of sample in analytical triplicate. For

159

soil samples containing less than ~20% organic matter, a pyrohydrolysis method was applied according to the

160

conditions previously described24. Briefly, 100 mg of sample were mixed with 500 mg vanadium pentoxide in a

161

quartz boat and heated (10 min at 1000 °C; water flow-rate 1.0 mL min-1; humidified air flow-rate 200 mL min-

162

1

). In both methods, halogens were absorbed in 6 mL 50mM NH4OH that was diluted to 25 mL with water prior

6 ACS Paragon Plus Environment

Page 7 of 23

Environmental Science & Technology

163

to analysis by ion chromatography (chlorine) and inductively coupled plasma mass spectrometry (bromine)23.

164

Accuracy was evaluated using certified reference material of coal (NIST 1632c) and spiked samples were used

165

to evaluate the recovery of halogens.

166

Results and Discussion

167 168

Organic halogen in Arctic and subarctic soils

169

First, we determined the total organic and inorganic chlorine and bromine concentrations (Table 2) in soil from

170

nine transects where chloroform emission measurements were performed. Organic chlorine was present in all

171

chloroform emitting soils. These are the first such data reported for Arctic soils and interestingly, the total

172

organic chlorine concentrations of 63-341 mg kg-1 (175-1457 mg kg SOM-1) were very similar to what has been

173

reported for soils in warmer climates25,26. However, it is clear that chloroform emissions did not correlate with

174

total organic chlorine in soil (Table 1 and 2, Fig. S2), and that total organic chlorine in soil therefore cannot be

175

used as a proxy for chloroform emission. These results suggest that several chlorination mechanisms may occur

176

simultaneously in soil of which only some (those that produce free reactive chlorine species) contribute to

177

chloroform formation. An alternative explanation would be unspecific chlorination of different types of organic

178

matter leading to chlorinated compounds with different residence times at the different study sites. Organic

179

bromine was also present at all locations, ranging from 2-32 mg kg-1 (Table 2), corresponding to 6-90 mg kg

180

SOM-1. Organic bromine data are very scarce in the scientific literature, but our data from Arctic-subarctic

181

ecosystems are in the same range as those for temperate peatlands and coniferous plantations21,27. The organic

182

chorine/bromine ratio showed a substantial variation between study sites, ranging from only 4 at site Kan-C to

183

31 at site Abi-B (Table 2).

184 185

Trichloroacetyl compounds and their hydrolysis to chloroform

186

We then measured trichloroacetyl compounds in the soils of the transects and found that they were present in

187

all of the 44 soil samples analyzed, but at very different concentrations (Table 1, Fig. 1). Between sites, the

188

mean trichloroacetyl concentration varied 190-fold based on dry weight and 160-fold when expressed per soil

189

area (Table 1). There was also considerable within-site variation, often up to tenfold between soils in the five

190

haloform flux-chambers at each site. High trichloroacetyl concentrations were found only in soils with a pH

191

below 5.8 (Fig. 2a), which was in line with the first prediction that trichloroacetyl compounds become

192

increasingly unstable at higher soil pH. Furthermore, soils with higher pH (pH 6 to 7) showed up to 84 times

7 ACS Paragon Plus Environment

Environmental Science & Technology

193

higher chloroform emission:trichloroacetyl ratios compared to soils with lower pH (pH between 4 and 6). This

194

means that a low steady state concentration of trichloroacetyl compounds may be found even when

195

chloroform emissions are high. Our results are the first to demonstrate a general and natural occurrence of

196

trichloroacetyl compounds, and hence to support that chloroform is formed through trichloroacetyl

197

compounds in completely natural ecosystems. Furthermore, the correlation with pH has not previously been

198

demonstrated for environmental samples of any kind.

Page 8 of 23

199 200

It can be speculated that transport processes in the soil column might modify the emission fluxes to an extent

201

that they become independent of the formation processes, this is however unlikely for our soils.

202

Physicochemical processes such as sorption/-desorption and varying porosity would not change haloform

203

fluxes in a quasi-steady-state system. Degradation processes, on the other hand, may weaken the link between

204

haloform production and emission. Haloform degradation via halorespiration, which may take place under

205

highly reduced conditions, was probably negligible for most of our study sites that were oxidized down to the

206

permafrost or at least to a depth of 70 cm. One notable exception was the Kan-C site where the soil was

207

saturated with water, which may have led to locally reduced conditions, though the water was not stagnant

208

and methane emissions were undetectable or negative. Alternatively, some trihalomethane may be degraded

209

via microbial oxidation in the topsoil9. We did not determine the aerobic degradation potential of our soils, but

210

this process may account for some of the unexplained variation in our dataset.

211 212

By combining the trichloroacetyl concentrations and chloroform emissions, we could estimate a mean

213

residence time in soil for the trichloroacetyl compounds. These estimates were based on the assumptions that:

214

1) most of the trichloroacetyl compounds that release chloroform are located in the topsoil and 2) emission to

215

the atmosphere is the main loss route of chloroform from Arctic soils. These assumptions are a simplification,

216

but they are supported by three facts: 1) almost all organic matter in the Arctic soils and in temperate

217

coniferous plantations is located in the topsoil, 2) previous studies conducted in temperate coniferous

218

plantations show that chloroform is primarily formed in the topsoil7,9, and 3) 90% of the net chloroform

219

formation is released to the atmosphere in temperate coniferous plantations9. In Arctic ecosystems, the topsoil

220

is frozen most of the year, and chloroform emissions are considered negligible during this period11. We

221

therefore estimated trichloroacetyl residence times based only on the active periods when the soils were not

222

frozen. The estimated mean residence times varied from three active months at site Kan-C to 59 active months

223

at site Abi-B (Fig. 2b) with a full range from 1 to 116 months for individual flux chambers (Fig. S3). The

8 ACS Paragon Plus Environment

Page 9 of 23

Environmental Science & Technology

224

residence time decreased with increasing soil pH (Fig. 2b). This pH-dependence strongly supports our

225

hypothesis that the soil chloroform emissions originated from alkaline hydrolysis of trichloroacetyl compounds.

226 227

The mean residence time often showed high within-site variation (Fig. 2b), which was partly caused by within-

228

site variation in soil pH (Fig. S3). At site Nar-C, the organic layer extended 10 cm that were used for determining

229

the trichloroacetyl concentrations. This means, that we may have underestimated the area-based

230

trichloroacetyl concentrations for this site if trichloroacetyl compounds were present in significant amounts

231

below 10 cm. In addition, the mean residence times may have been slightly overestimated if some of the

232

chloroform was oxidized in the topsoil or leached.

233 234

We further investigated the influence of pH on the stability of the natural trichloroacetyl compounds in

235

laboratory tests with soil from the site with the highest chloroform emissions (Abi-A). The chloroform-release,

236

i.e. the trichloroacetyl stability, showed strong pH dependence with increased hydrolysis at higher pH (Fig. 2c).

237

Such a strong pH response has not previously been shown for any environmental sample containing natural

238

trichloroacetyl compounds, but was similar to what has been reported for the hydrolysis of trichloroacetyl

239

compounds formed by non-natural, chemical chlorination14,15. It should be noted that the laboratory

240

experiment (Fig 2c) shows the pH dependence of trichloroacetyl hydrolysis under laboratory conditions, which

241

cannot be used for prediction of in situ residence time (Fig. 2b). This is exemplified by the fact that the pH of

242

the Abi-A soil on average was 4.2 (Table 1), which corresponds to 1% hydrolysis of the trichloroacetyl

243

compounds in 24 hours at pH 4.3 (Fig 2c). This is faster than suggested by the in-situ mean residence time of

244

38 months (Fig 2b), but these two numbers are not directly comparable. First, the hydrolysis was determined at

245

23°C, which is much warmer than average in situ soil temperatures during the active months, which was 6°C11.

246

Second, soil colloids probably act as strong adsorbers of the trichloroacetyl molecules. Since the negatively

247

charged colloids attract hydrogen ions, the difference in acidity between colloid surfaces and the bulk solution

248

may be up to two pH units. Adsorbed molecules therefore ”experience” much lower pH than molecules in the

249

bulk solution28,29. As the pH dependence (Fig 2c) was determined under laboratory conditions, where the soil

250

was diluted 25-fold in 1M buffer, sorption equilibrium would presumably be shifted and more of the

251

trichloroacetyl compounds would be present in the bulk liquid due to dilution and high ionic strength.

252

Consequently, the trichloroacetyl compounds would be more labile than in-situ even at the same bulk pH.

253 254

Co-emission of brominated chloroform analogues

9 ACS Paragon Plus Environment

Environmental Science & Technology

Page 10 of 23

255

The formation of trichloroacetyl compounds requires nonspecific halogenation by free, reactive chlorine

256

species such as HOCl16, equation (1). The formation of HOCl by either chloroperoxidases or the fenton reaction

257

is, however, unspecific and other halides than chloride may be oxidized by both reaction mechanisms. This

258

means that HOBr (reactive bromine) would also be formed, if bromide ions were present18,19,30. Furthermore,

259

HOCl may react spontaneously with bromide and convert into HOBr due to the higher standard oxidation

260

potential of bromide compared to chloride31. If the proposed reaction mechanisms were correct (equation 1),

261

then brominated chloroform analogues would be formed along with chloroform when bromide is present. The

262

concentration of free bromide was below the detection limit (