Mineral Availability as a Key Regulator of Soil Carbon Storage

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Mineral Availability as a Key Regulator of Soil Carbon Storage Guanghui Yu, Jian Xiao, Shuijin Hu, Matthew L. Polizzotto, FangJie Zhao, Steve P. Mcgrath, Huan Li, Wei Ran, and Qirong Shen Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.7b00305 • Publication Date (Web): 12 Apr 2017 Downloaded from http://pubs.acs.org on April 13, 2017

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Environmental Science & Technology

1

Mineral Availability as a Key Regulator of Soil Carbon Storage

2

Guanghui Yu,†,ǁ Jian Xiao,† Shuijin Hu,†,¶ Matthew L. Polizzotto,‡ Fangjie Zhao,†,ǂ

3

Steve P. McGrath,ǂ Huan Li,†,¶ Wei Ran,† Qirong Shen†,*

4

†

Jiangsu Provincial Key Lab for Organic Solid Waste Utilization, Jiangsu

5

Collaborative Innovation Center for Solid Organic Waste Resource Utilization,

6

Nanjing Agricultural University, Nanjing 210095, PR China.

7 8 9 10 11 12 13

¶

Department of Plant Pathology, North Carolina State University, Raleigh, NC 27695,

USA. ‡

Department of Crop and Soil Sciences, North Carolina State University, Raleigh,

NC 27695, USA. ǂ

Sustainable Soils and Grassland Systems, Rothamsted Research, Harpenden,

Hertfordshire AL5 2JQ, UK. ǁ

Department of Crop and Soil Science, Oregon State University, ALS Building 3017,

14

Corvallis, Oregon 97331, USA.

15

Corresponding Author

16

*Phone: +86 25 84396291; fax: +86-25-84395212; e-mail: [email protected]

1

ACS Paragon Plus Environment


17

Abstract

18

Mineral binding is a major mechanism for soil carbon (C) stabilization, and mineral

19

availability for C binding critically affects C storage. Yet, the mechanisms regulating

20

mineral availability are poorly understood. Here, we showed that organic amendments

21

in three long-term (23, 154, and 170 yrs, respectively) field experiments significantly

22

increased mineral availability, particularly of short-range-ordered (SRO) phases. Two

23

microcosm studies demonstrated that the presence of roots significantly increased

24

mineral availability and promoted the formation of SRO phases. Mineral

25

transformation experiments and isotopic labelling experiments provided direct

26

evidence that citric acid, a major component of root exudates, promoted the formation

27

of SRO minerals, and that SRO minerals acted as "nuclei" for C retention. Together,

28

these findings indicate that soil organic amendments initialize a positive feedback

29

loop by increasing mineral availability and promoting the formation of SRO minerals

30

for further C binding, thereby possibly serving as a management tool for enhancing

31

carbon storage in soils.

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33

TOC Art

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■INTRODUCTION

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Soils are the largest and most stable terrestrial carbon (C) pool, and they are often

37

assumed to be a major sink for future C storage.1, 2 Globally, soil organic matter

38

(SOM) contains more than three times as much C as either the atmosphere or

39

terrestrial vegetation.1 Recent isotopic and spectroscopic studies indicate that

40

microbial accessibility to substrates rather than chemical complexity of organic C

41

dominantly controls long-term C stability in soils1, 3-5 and that a significant proportion

42

of stable SOM is derived from simple C rather than chemically resistant compounds.1,

43 44

6, 7

Such stable SOM mainly results from physical occlusion in microaggregates and

chemical sorption in organo-mineral complexes.1, 8-10

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The majority of studies represent organo-mineral complexes as ‘biogeochemical

46

black boxes’, where inputs and outputs of organics and minerals are estimated but the

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underlying mechanisms controlling C stabilization and storage are rarely explored.11

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This is partly due to the inherent physical and biogeochemical complexity of soil

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systems, fluctuation of environmental conditions,1 and the existence of nano-scale

50

(~1–100 nm) minerals that may dominate C binding.12 Recently, available minerals

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have been shown to correlate strongly with soil C and its long-term stabilization

52

because they are accessible to SOM.13 Here, available minerals are referred to as the

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mineral surfaces available for C binding, and the concentration of a metal in

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water-dispersible colloids is a good proxy for the availability of a mineral. More

55

importantly, the availability of mineral surfaces for C binding can be affected by soil

4


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moisture content,14 organic amendments,15, 16 or land-use change,17 suggesting that

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management practices may in return affect mineral availability for further C binding.

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Two major mechanisms critically control mineral availability for C binding. First,

59

soil physiochemical conditions, such as pH18-20 and redox potential,20-22 and

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dissolution-precipitation processes regulate the release of mineral elements from

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primary minerals.22 Second, both plants and microbes also affect mineral availability

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through their exudates and metabolic compounds.20, 22 By delivering a continuous

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supply of individual exudate solutions through an artificial root into unperturbed soil,

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low molecular weight (LMW) acids have been shown to have strong

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metal-complexing

66

short-range-ordered (SRO) minerals and metal-organic complexes in the affected

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zone next to roots.23 However, a single LWM acid in artificial root systems is far from

68

a real root system. Therefore, direct evidence illustrating the linkage among real root

69

exudates and the formation of SRO minerals in soils is still lacking.

abilities,

changing

mineral

availability

by

decreasing

70

Here, we present direct evidence from four independent but complementary

71

experiments demonstrating that organic acids resulting from long-term organic

72

amendments increase soil mineral availability and the formation of SRO minerals, and

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that SRO minerals facilitate C retention. First, we assessed the impacts of long-term

74

organic amendments on mineral availability and organic-acid production in three (one

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in China24 and two in England25, 26) well-controlled, long-term (23 yrs, 154 yrs, and

76

170 yrs, respectively) field experiments. Second, we designed two microcosm studies

5



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to test the role of root exudates and organic amendments in the enhancement of

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mineral availability and SRO mineral formation. Third, we conducted an incubation

79

experiment to examine the mechanistic role of organic acids in the formation of SRO

80

minerals. Finally, we used

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available

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synchrotron-based X-ray absorption fine structure (XAFS) spectroscopy and scanning

83

transmission X-ray microscopy (STXM) imaging, as well as nano-scale secondary ion

84

mass spectrometry (NanoSIMS) were integrated to identify the composition and

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distributions of organic C and soil minerals. Collectively, our results indicate that soil

86

organic amendments initialize a positive feedback loop by increasing mineral

87

availability and promoting the formation of SRO minerals for further C binding.

88

■MATERIALS AND METHODS

minerals.

13

C to directly trace the retention capacity of labile C by

Throughout

our

experiments,

advanced

techniques

of

89

Field Studies and Soil Colloid Extraction. The Qiyang Experiment was set up

90

on a Ferralic Cambisol soil in 1990 in Hunan Province, China.24 The top soil in 1990

91

contained approximately 61.4% clay, 34.9% silt, and 3.7% sand. The Park Grass

92

Experiment, the oldest field experiment on permanent grassland in the world, was set

93

up in 1856 at the Rothamsted Research Station in Hertfordshire, England.25, 26 The top

94

soil (0–23 cm) is a silty clay loam containing 22% clay, 29% silt and 49% sand. The

95

Broadbalk Experiment, the oldest continuously running field wheat experiment in the

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world, was set up in 1843 at the Rothamsted Research Station, England.25,

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According to the Food and Agriculture Organization of the United Nations (FAO)

6


26

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classification, the soil at Rothamsted Research Station is classified as a Chromic

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Luvisol.25 Soil samples to 0–20 cm depth, 0–10 cm depth, and 0–23 cm depth were

100

collected in September 2013 at the Qiyang Experiment, 2008 at the Park Grass

101

Experiment, and 2013 at the Broadbalk Experiment, respectively, using a 5-cm

102

internal diameter auger. Each plot was evenly separated into three regions, and 10

103

cores were randomly sampled from each region. Fresh soil was thoroughly mixed,

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air-dried, and sieved through a 5-mm screen for further analysis. In all three

105

Experiment stations, swine manure, or farmyard manure was used as a long-term

106

organic amendment (M). The other fertilization regimes were selected for

107

comparison: i) no fertilizer input (Control) and ii) chemical fertilizers of nitrogen,

108

phosphorus and potassium only input (NPK). In this study, both manure alone and

109

manure plus NPK treatments are collectively called organic fertilization treatments.

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The numbers of plots of a given amendment treatment were 2 and 1 for Qiyang and

111

Rothamsted Experiments, respectively. Other detailed information about soil

112

sampling and the Experiment stations can be found in Supplementary Information

113

(SI).

114

Soil colloids were isolated using the following procedure.27 Briefly, air-dried soil

115

was suspended in deionized water at the ratio of 1:5 (W/V), shaken for 8 hrs at 25°C,

116

and centrifuged for 6 min at 2,500 g. Aliquots of the supernatant suspensions

117

containing the soil colloids were transferred into 50-mL glass vials, stored in the dark

118

at 4°C, and analyzed within one week. The isolated water-dispersible colloids

119

represent one of the most reactive components in soils.28, 29 7



120

Microcosm Experiments. One microcosm experiment with three replicates was

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conducted to determine the effect of root and Arbuscular Mycorrhizal Fungi (AMF)

122

exudates on mineral availability in the USDA-ARS Plant Science Research CO2

123

facility at North Carolina State University, Raleigh, NC, USA. The experimental

124

microcosm was divided into six compartments with each compartment measuring 13

125

× 14 × 15 cm (width × depth × height). Three compartments in a row were designated

126

as host compartments (containing host plants and AM) and the three adjacent

127

compartments were designated test compartments to assess mycorrhizal functioning.

128

The host and test compartments were separated by a replaceable 0.45, 20 or 1000 µm

129

mesh fabric panel (Tetko/Sefar mesh, Sefar America, NY) that allowed nothing

130

(-Root-AMF), AM fungal hyphae (-Root+AMF) or both roots and AM fungal hyphae

131

(+Root+AMF) to grow into the test compartments, respectively.30 Effectiveness of the

132

20 mm mesh fabric in preventing root growth into the test compartment was visually

133

assessed at the completion of each experiment. Each compartment of the microcosm

134

unit was filled with 3.5 kg of an autoclaved quartz sand and sandy loam soil (1 : 1

135

w/w) mixture. Ten seeds of Triticumaestivum Linn. (Wheat) were sown into each host

136

cell. Microcosms were watered with deionized water daily. Plants were allowed to

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grow for 4 months, and then the soils in the test cells were air-dried.

138

Another microcosm experiment with three replicates was conducted to determine

139

the effect of root and fertilization treatments on mineral availability in a greenhouse at

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Nanjing Agricultural University. PVC pots (20 cm high, 7.8 cm internal diameter)

141

were filled with red soils collected at the Qiyang Experiment in 2014. Each pot was 8


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filled with 1.5 kg of equivalent dry red soil. The pots were sown with corn and every

143

treatment had three replicates. Each pot was put into two pore sizes of mesh (30 and

144

1000 µm).31 The pore sizes 1000 µm and 30 µm would permit and not permit the

145

entry of roots, respectively. The pots were watered with deionized water daily. Plants

146

were allowed to grow for 10 weeks, and then the soils were air-dried.

147

Incubation Studies for Fe Mineral Transformations. Citric acid solutions

148

(SIGMA-ALDRICH, ACS reagent, ≥ 99.5%) were added to the soil colloid

149

suspensions from the Qiyang Experiment and stirred. The final concentrations of

150

citric acid in the soil colloid suspensions were 10 and 100 mg L−1, and the pH values

151

were adjusted to 6.7, which was the same as that of the raw soil colloid solutions.

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After 1 d incubation, the suspensions in the series of reaction solutions and the control

153

solutions (i.e., without the addition of citric acid) were analyzed by Fe K-edge

154

extended X-ray absorption fine structure (EXAFS) spectroscopy. The incubation

155

study was performed in duplicate.

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Isotopic Labelling Experiment. Soil colloids with organic amendments in the 13

157

Qiyang Experiment were incubated with a

C-labeled amino acid mixture (algal

158

amino acids, Isotec, Miamisburg USA; C/N ratio: 2.8; min. 99 atom%

159

readily bioavailable C isotopic tracer. The amino acid mixture was suspended in

160

deionized water at a concentration of 10 mg L−1. After addition of 13C enriched amino

161

acids the samples were incubated for 24 hrs at 20°C and then used for NanoSIMS

162

analysis. The incubation study was performed in duplicate.

9


13

C) as a


163

Analysis Techniques. The soil colloids were mixed with 10% nitric acid at a

164

ratio of 1:1 (v/v) on a heating plate;32 then, the mixture was digested at 150°C for 2

165

hrs. After the digestion, the mixture was filtered through a filtration membrane (0.45

166

µm) and the metal ions in the supernatant were quantified by inductively coupled

167

plasma atomic emission spectroscopy (710/715 ICP-AES, Agilent, Australia)..

168

Mineral dissolution in the microcosm experiments was determined by suspending

169

air-dried soil in deionized water at the ratio of 1 : 5 (w/v), putting the mixture on a

170

horizontal shaker (170 rpm) for 24 h at room temperature, and then centrifuging it at

171

3000 g for 10 min. The supernatant was passed through a 0.45-µm

172

polytetrafluoroethylene filter. Quantitation of SRO minerals was performed using the

173

acid ammonium oxalate extraction method.28 In brief, soil was extracted using 0.275

174

M ammonium oxalate at pH 3.25 with a soil : extractant = 1 : 100 (w/v) ratio. The

175

main mineral elements, namely Fe and Al, were quantified by ICP-AES (710/715

176

ICP-AES, Agilent, Australia). Dissolved organic carbon (DOC) was measured using a

177

TOC/TN analyser (multi N/C 3000, Analytik Jena AG, Germany).

178

Diffusive gradients in thin films (DGT) were prepared by placing a Chelex-100

179

disc on a support, followed by a diffusive gel disc (DGT Research Ltd, Lancaster,

180

UK), and then filtering samples through a membrane filter. The upper cover, with a

181

window exposed to the sample, was affixed lightly. The calculated concentration

182

represents the effective available concentration of Fe in soil. A detailed description of

183

analysis techniques is found in the SI.

10


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Iron K-edge absorption spectra were collected using a Si (111) double crystal

185

monochromator at the XAFS station of the BL14W1 beamline of the Shanghai

186

Synchrotron Radiation Facility (SSRF). The storage ring was working at 3.5 GeV

187

with 200 mA as an average storage current. The prepared samples and standard

188

samples were recorded in transmission mode. All the samples were mounted in a thin

189

custom-built plastic sample holder covered with Kapton tape and placed at 45° to the

190

incident X-ray beam. Ten scans were averaged for each sample to obtain a good

191

signal-to-noise ratio. The X-ray energy scale was calibrated to the iron K-edge

192

(7112.0 eV) using an iron metal foil before XAFS measurements were performed.

193

The XAFS data were processed and analyzed using ATHENA software (version

194

2.1.1).33 A detailed description of analysis techniques is found in the SI.

195

Carbon 1s near edge X-ray absorption fine structure (NEXAFS) spectra were

196

obtained on the BL08U1 beamline of the SSRF. For specimen preparation, one

197

droplet of suspension was deposited at a 100-nm thickness onto a Si3N4 window,

198

which was previously glued onto the detection plate of the microscope. The sample

199

thickness is important to obtain a good signal-to-noise ratio when using NEXAFS

200

spectroscopy.34 The main 1s-p and Rydberg/mixed valence transitions in the fine

201

structure regions of the C K-edge spectra were recorded in the energy range from

202

284–310 eV. A detailed description of analysis techniques is found in the SI.

203

NanoSIMS analyses were performed with a NanoSIMS 50L (Cameca,

204

Gennevilliers, France) at the Institute of Geology and Geophysics, Chinese Academy

11



205

of Sciences, China. Prior to the analysis, the gold coating layer (~10 nm) and possible

206

contamination of the sample surface were sputtered using a high primary beam

207

current (pre-sputtering).28, 29 During the pre-sputtering step, reactive Cs+ ions were

208

implanted into the sample to enhance the secondary ion yields. Secondary ion images

209

of

210

multipliers with an electronic dead time of 44 ns. We compensated for the charging

211

that resulted from the non-conductive mineral particles by employing the electron

212

flood gun of the NanoSIMS instrument. For every sample, 4–6 spots were analyzed to

213

obtain reliable data. A detailed description of analysis techniques is found in the SI.

12

C−,

13

C−,

27

Al16O− and

56

Fe16O− were simultaneously collected by electron

214

Statistical Analyses. Differences between the data were assessed with one-way

215

analysis of variance (ANOVA) using the SPSS software version 16.0 for Windows

216

(SPSS, Chicago, IL). Significance was determined using one-way ANOVA’s

217

followed by Tukey’s HSD post hoc tests, where conditions of normality and

218

homogeneity of variance were met. Means ± SE (n = 3) followed by different letters

219

in figures and tables indicate significant differences between treatments at P < 0.05.

220

Data were log transformed to attain normality and homoscedasticity for regression

221

analysis. Regression analyses were performed between two log-transformed variables

222

using the OriginPro 9.0 software. Similar to most analyses, a value of P < 0.05 is

223

typically considered significant.

224

■RESULTS

12


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Long-term Organic Amendments Increased Soil Mineral Availability and

226

SRO Phases. Compared to no fertilizer and chemical fertilizer inputs, long-term

227

organic amendments significantly (Tukey’s HSD post hoc tests; P < 0.05) increased

228

available minerals (i.e., Al and Fe) (Figure 1) in soil colloids by over two orders of

229

magnitude at the Qiyang Experiment and 2–12 times at the Park Grass and Broadbalk

230

Experiments. Similarly, results from DGT experiments confirmed that long-term

231

organic amendments significantly (Tukey’s HSD post hoc tests; P < 0.05) increased

232

bioavailable Fe at the Qiyang Experiment (Figure S1). Based on the results of Fe

233

K-edge X-ray absorption near edge structure (XANES) (Figure S2a) and Al 2p3/2 XPS

234

(Figure S2b), we found that approximately 17–57% of Fe minerals and 13–28% of Al

235

minerals in soil colloids with long-term organic amendments at the three field

236

Experiments were SRO minerals (i.e., ferrihydrite and allophane, respectively); these

237

values were higher than those in samples receiving no fertilizer and chemical fertilizer

238

inputs. In addition, the extracted minerals and organic carbon in soil colloids

239

accounted for approximately 0.02–1.8% and 0.2–1.5% of total soils, respectively

240

(Tables S1), with the biggest percentages found in samples from the organic

241

amendment treatments, followed by those receiving no fertilizer and chemical

242

fertilizer inputs. Taken together, these findings show that long-term organic

243

amendments significantly increase the presence of SRO phases.

244

The Presence of Roots and the Application of Organic Exudates Increased

245

Mineral Availability and Promoted the Formation of SRO Minerals. To explore

246

the factors that increase mineral availability, we conducted two microcosm studies 13



247

that allowed us to investigate the contribution of root and AMF exudates as well as

248

fertilizers on mineral availability and SRO mineral formation (Figure 2). The presence

249

of roots increased the release of Al and Fe from soils (P < 0.05) over 2 times for mean

250

values with or without the application of fertilizers (Figure 2a,b), but AMF had no

251

significant impact on Al and Fe release (P > 0.05) (Figure 2a). Interestingly, both

252

microcosm studies demonstrated that the presence of roots also markedly increased

253

the concentration of SRO minerals (Figure 2c,d).

254

Compared to chemical fertilizers, organic amendments significantly decreased

255

mineral mobilization (Figure 2b) but increased (> 20%, p < 0.05) the concentration of

256

SRO minerals from 3.7 to 3.9 g kg-1 in the presence of roots (Figure 2d). These results

257

indicate that roots, in concert with organic amendments, may be responsible for

258

increasing mineral availability and the formation of SRO minerals.

259

Citric Acid—One of the Most Abundant Exudate Classes—Promoted the

260

Formation of SRO Minerals. Addition of LMW organic acids (e.g., citric acid—one

261

of the most abundant exudate classes) to soils benefits the formation of SRO

262

minerals.23 We used C 1s NEXAFS spectroscopy to identify the composition of

263

organic C in soil colloids from all three field Experiments (Figures 3a and S3).

264

Carboxyl C (1–π∗ transition of COOH) was dominant in soluble organic C,

265

accounting for approximately 61% of the organic C at the Qiyang Experiment, while

266

aromatic C (1s–π∗ transition of conjugated C=C) only constituted less than 5% of the

267

organic C in the three field Experiments (Figure 3a, Tables S2 and S3). For the Park

14


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Grass and Broadbalk Experiments, carboxyl C and aromatic C accounted for 35–44%

269

and approximately 3–11% of the organic C, respectively (Figure S3, Table S3). The

270

other C forms were present as phenolic C, alkyl C, O-alkyl C, and carbonyl C (Table

271

S3). In addition, long-term organic amendments also markedly increased the

272

concentration of dissolved organic C when compared to chemical fertilization in all of

273

the three Experiments (Figure S4). LMW organic acids have in other experiments

274

shown to consist of approximately 0.5–5% of C in soil solution.35,

275

long-term organic amendments may increase production of organic acids, especially

276

with LMW components, in soils.

36

Therefore,

277

To test the critical role of root exudates in the formation of SRO minerals, we

278

designed a simulated study by adding citric acid to soil colloids. The colloids were

279

derived from soils with long-term organic amendments at the Qiyang Experiment.

280

Iron k3-weighted EXAFS spectra (Figure 3b) showed that two peaks at k = 5.7−6.0 Å

281

and 8.0−8.8 Å, were observed in the raw soil colloids and those with 10 mg L−1 citrate

282

addition but disappeared in the soil colloids with 100 mg L−1 citrate addition. These

283

two peaks could be observed in goethite mineral standards but were not present in

284

ferrihydrite (Figure 3b). Linear combination fitting (LCF) results (Table S4) of the Fe

285

k3-weighted EXAFS spectra further demonstrated that incubation of soil colloids with

286

citric acid at a concentration of 10 and 100 mg L−1 for 1 d could decrease goethite

287

from 27.6% to 13% and 5.1% of the total Fe mineralogy but increase ferrihydrite from

288

39.4% to 49.9% and 74.6% of the iron mineralogy, respectively. The results from no

289

fertilizer inputs also support the observation that citric acid drives transformation of 15



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Fe minerals in soil colloids (Figure S5). Because ferrihydrite is more mobile and has a

291

higher specific surface area than goethite,37 these results provide spectroscopic

292

evidence that citric acid can increase mineral mobilization and promote

293

transformation of goethite to ferrihydrite, the most reactive SRO iron (oxyhydr)oxide.

294

Retention of Labile C by Available Minerals. To verify the strong retention

295

capability for C by the mobilized Al and Fe minerals, we then designed an isotopic

296

labeling experiment (using

297

observation (Figure 4). Here

298

newly added C (i.e., animal manure) in soils. After 24 hrs of incubation with a

299

amino acid mixture, the composite NanoSIMS image showed a profound enrichment

300

of newly added

301

'nuclei'

302

hue-saturation-intensity (HSI) image of

303

that colloid particles were surrounded by these

13 −

304

further indicated that the distribution patterns of

13 − 12

305

were similar (Figure S6). However, for large soil particles (i.e., approximately 15

306

µm), a part of newly added C was present at the edges of particles (Figure S6). These

307

large particles seemed to retain much more C than small particles. It should be noted

308

that 12C− represents the native C (Figure S6) and it does not impact sorption of amino

309

acids based on the similar slopes between

310

S7). Compared to no fertilizer or chemical fertilizer inputs, the total sorption capacity

for

13

the

C− on

27

13

C-labelled amino acid) combined with NanoSIMS

13

C-labelled amino acids were used as a precursor of

Al16O− and

retention

of

56

13

C

Fe16O− (Figures 4a and S6), which served as

13 −

C. 13

This

is

further

supported

by

the

C/12C− (Figure 4b), which clearly showed C enriched spots. Line profiles C,

13 − 12 −

C,

C−,

C and

27

16


27

Al16O−, and

Al16O−,

56

56

Fe16O−

Fe16O− (Figure

Page 17 of 42


311

of organic carbon by soil colloids was significantly increased with organic

312

amendments (Figure 4c).

313

■DISCUSSION

314

Drivers of Mineral Availability and SRO Mineral Formation. Our long-term

315

field studies demonstrate that organic amendments significantly increase the

316

availability of Al and Fe minerals, particularly their SRO phases (Figures 1 and S2).

317

The available Al and Fe minerals decrease C mineralization and increase the potential

318

for SOC sequestration.19, 21 The percentage of SRO minerals in organic-amended soil

319

was higher than that of no fertilizer and chemical fertilizer inputs based on the

320

previous results achieved from selective extraction methods38 and transmission

321

electron microscopy (TEM) analysis24,

322

selective extraction methods give only operationally defined pool of SROs and suffer

323

from intrinsic limitations due to artifacts associated with reagent selectivity and the

324

inability to differentiate specific SROs.40 X-ray absorption fine structure (XAFS)

325

spectroscopy complements sequential extraction techniques,41 and in our study

326

provided direct identification of important SROs (Figure S2). These SRO minerals

327

possess structural defects, high specific surface area and charge density, and variably

328

charged surfaces, enabling them to bind and thereby potentially chemically stabilize

329

organic matter.42, 43 Although the importance of SRO minerals in protecting soil C has

330

increasingly been recognized,13, 23, 43 the information about their regulation is still very

39

at the Qiyang Experiment. However,

17



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331

limited. In this study, having a well-controlled long-term field system and advanced

332

technologies allowed us to identify the formation of SRO minerals.

333

Microbial- or plant-driven increases to mineral availability are believed to be

334

important steps in the formation of SRO minerals in soil.44 Our microcosm

335

experiments show that plant roots and their exudates may play a bigger role than

336

mycorrhiza in the development of mineral availability and subsequent formation of

337

SRO minerals (Figure 2). This result also challenges the long-standing conceptual

338

view that the weathering of minerals and the formation of SRO minerals are very slow

339

processes and cannot be detected in short-term systems.22, 45 We therefore suggest that

340

the formation of SRO minerals can be accelerated or regulated by plant roots and

341

some agricultural practices (e.g., organic amendments), a notion which is also

342

supported

343

exudate-induced effects on SRO minerals.23

by

previous

microcosm

experiments

that

have

demonstrated

344

Furthermore, our mineral transformation experiments provide direct evidence that

345

the formation of SRO minerals is promoted by LMW organic acids (Figure 3), which

346

may be produced by roots or the degradation of organic amendments. Similarly,

347

oxalate, another common root exudates or intermediate of soil microbes, was also

348

found to have the same effect on the dissolution of goethite20, 46 and Al minerals47.

349

Although these organic acids only account for a small percentage of soil soluble C,36

350

they represent the most reactive forms of organic matter and exist widely in soils,

351

especially in the rhizosphere.47 Since ferrihydrite is more available than goethite,37

18


Page 19 of 42


352

this transformation is particularly important because the absence of iron in an

353

available form limits C storage in many soils.

354

Newly formed SRO minerals may adsorb or precipitate on soil aggregates and

355

promote soil aggregation.48 The aggregation role of newly formed SRO minerals is

356

also supported by the results from high-resolution TEM combined with EDS analysis

357

that Al and Fe are enriched on the surface of soil particles with long-term organic

358

amendments.24, 29, 39 The driving force for this aggregation may be the decrease in

359

surface energy that appears to be low enough for SRO minerals.49 This increased soil

360

aggregation lowers rates of respiration per unit of soil C, one of the main mechanisms

361

of soil C storage and preservation.19

362

In addition to microbes or plants, other parameters, i.e., pH, complexation or,

363

most important, redox variation, also affect mineral availability19, 21 and the formation

364

of SRO minerals39. Our previous results from the Qiyang Experiment indicated that

365

compared with chemical fertilization, organic fertilization significantly (P < 0.05)

366

increased soil pH, the concentration of Al and Fe, and amorphous Al, but decreased

367

exchangeable Al.24,

368

treatments ondesert soil and showed that compared to a Control, an NPK treatment

369

significantly decreased the soil pH (P < 0.05), whereas a manure treatment maintained

370

the soil pH.50 Meanwhile, the addition of manure significantly (P < 0.05) increased

371

the content of SOC, with SOC content ranked by descending order as M > NPKM >

372

NPK > Control.50 In addition, our unpublished data (paper in review) show that there

38

Wang et al. (2016) investigated the effect of fertilization

19



373

was a significantly positive relationship between poorly crystalline Fe minerals and

374

SOC, as well as aromatic C, in gray desert soil; attachment of aromatic functional

375

groups to the poorly crystalline Fe minerals could also protect the poorly crystalline

376

Fe minerals from transforming to their more crystalline counterparts.51

377

Impacts of Organic Amendments on Carbon Retention in Soils. We

378

hypothesized that the mobilized mineral particles in soils with organic amendments

379

have a strong capability to retain C in soils. To test this hypothesis, we examined the

380

distribution patterns of native C, newly added C, and minerals in soil colloids to

381

support the C storage potential of the mobilized mineral particles in soil colloids. Our

382

NanoSIMS results indicate that native C and newly added C are co-localized with

383

minerals (Figure 4). Also, we provide direct evidence demonstrating that these

384

mineral particles can act as 'nuclei' to preferentially retain new labile C (Figures 5 and

385

S6). By contrast, it has recently been shown that only a limited proportion (< 19%) of

386

the clay-sized surfaces contributes to organic C stabilization,52 indicating that using

387

the amount of clay as a proxy to predict the storage potential of soil C is not

388

sufficient. Meanwhile, some authors demonstrated that the particle surface area

389

covered by SOM decreased with increasing fraction density, as the proportion of

390

aggregated particles decreased.53 Together, our NanoSIMS results indicate that the

391

mobilized mineral particles in soil colloids have a strong capability to retain labile C

392

in soils.

20


Page 20 of 42

Page 21 of 42


393

By combining long-term data from a grassland biodiversity experiment and

394

radiocarbon (14C) modelling, some investigators demonstrated that the increase in soil

395

C storage is mainly limited by the integration of new C into soil and less by the

396

decomposition of pre-existing soil C,54 suggesting that the protection of new C plays a

397

major role in soil C storage. This mineral binding of labile C has recently been shown

398

to markedly contribute to the formation of SOM,55 and it has been described in terms

399

of a layer-by-layer 'onion' model.56 Due to the surface reactivity of mineral particles

400

varying as a function of particle size,12 we suggest that soil colloids, composed of the

401

mobilized submicron- and nano- scale mineral particles with high reactivity, deserve

402

more attention.

403

Based on the well-controlled long-term field experiments, microcosm

404

experiments, mineral transformation experiments, and isotopic labelling experiments,

405

we propose that soil organic amendments initialize a positive feedback loop by

406

increasing mineral availability and promoting the formation of SRO minerals for

407

further C binding (Table 1 and Figure 5). Production of root or microbial LMW

408

exudates following long-term organic amendments may be a critical step in this

409

process (Figures 2 and S3). The produced acids act as complexing and reducing

410

agents for mineral mobilization and acquisition,20 further promoting the formation and

411

stability of SRO minerals via four potential mechanisms (Figure 5). First, the

412

mobilized mineral elements (e.g., Al and Fe) can act as the precursors for formation

413

of SRO minerals.12,

414

promote transformation of minerals or oxides from more crystalline to SRO phases

37

Second, LMW organic acids, common root exudates, can

21



415

(Figure 3b), a process known as 'rejuvenation' in soil and ecology sciences.37 Third,

416

after the formation of SRO minerals, LMW organic acids can incorporate, through

417

precipitation from solution,57 into the network structure of SRO minerals58 and

418

prevent their growth or transformation to crystalline forms.59 And finally, some

419

biopolymers with soil particles can also limit the dispersal of SRO minerals that may

420

otherwise be transported away from their source via leaching, surface runoff, or

421

drainage in natural ecosystems60 adding to carbon storage (Figure S8). Although the

422

addition of organic acids to soil can lead to the release of old carbon23 or the

423

formation of SRO minerals that enhance soil carbon storage,61 it appears that a

424

long-term effect of organic-acid addition through organic amendments is increased

425

soil carbon storage.

426

Environmental Implications. Our results provide direct evidence illustrating

427

linkages among organic acids from both root exudates and organic amendments, SRO

428

minerals, and soil C stability within field and incubation experiments. Continuous

429

organic amendments initialize a positive feedback loop, in which high organic inputs

430

liberate minerals that can promote C sequestration in soils. The liberated minerals in

431

the soil colloids, and hence the high content of SRO minerals formed by organically

432

growth-limited precipitation, are therefore expected to be key factors that control the

433

storage of soil C. More importantly, our findings also provide a pathway for regulating

434

mineral availability and the formation of SRO minerals in the field, which will be

435

beneficial for managing the global C cycle. Therefore, organic amendments may

436

represent practical tools for managing and increasing global terrestrial C stocks. In 22


Page 22 of 42

Page 23 of 42


437

summary, these findings may prove vital in our understanding of C cycling in a

438

changing climate.

439

■ASSOCIATED CONTENT

440

The Supporting Information is available free of charge on the ACS Publications

441

website at http://pubs.acs.org.

442

Associated content in support of the main manuscript includes additional methods, eight

443

figures, and four data tables.

444

■AUTHOR INFORMATION

445

Corresponding Author

446

*Phone: +86 25 84396291; fax: +86-25-84395212; e-mail: [email protected]

447

Notes

448

The authors declare no competing financial interest.

449

■ACKNOWLEDGMENTS

450

We thank Xiangzhi Zhang and Lijuan Zhang for help and support at the BL08U1

451

beamline and Jingyuan Ma at the BL14W1 beamline of the Shanghai Synchrotron

452

Radiation Facility (SSRF). This work was funded by the Ministry of Science and

453

Technology of China (973 Program, 2015CB150500), the National Natural Science

454

Foundation of China (41371248 and 41371299), the Natural Science Foundation of

455

Jiangsu Province of China (BK20150059), and the Qing Lan Project. The Rothamsted

23



456

Long-term Experiments National Capability is supported by the UK Biotechnology

457

and Biological Research Council and the Lawes Agricultural Trust.

458

24


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459

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influence of low molecular weight organic acids and a soil humic acid studied by

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X-ray absorption spectroscopy. Geochim. Cosmochim. Acta 2010, 74, (22),

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6422-6435.

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Banfield, J. F., Extracellular proteins limit the dispersal of biogenic nanoparticles.

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Figures Caption

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Figure 1. Effects of long-term organic amendments on the Al and Fe concentrations

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in soil colloids at the Qiyang (a), Park Grass (b), and Broadbalk (c) Experiments.

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Control, no fertilizer inputs; NPK, chemical fertilizer inputs; NPK1, (NH4)2PKNaMg;

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NPK2, (NO3)2PKNaMg; M, manure inputs; NPKM, chemical fertilizer plus manure

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inputs; NPKS, chemical fertilizer plus straw inputs; NPKMS, chemical fertilizer plus

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manure plus straw inputs. Significant differences between fertilization practices were

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determined using one-way ANOVA’s followed by Tukey’s HSD post hoc tests at P

Mineral Availability as a Key Regulator of Soil Carbon Storage

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