Article pubs.acs.org/est
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*,† †
Jiangsu Provincial Key Lab for Organic Solid Waste Utilization, Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, Nanjing Agricultural University, Nanjing 210095, PR China ‡ Department of Plant Pathology, North Carolina State University, Raleigh, North Carolina 27695, United States § Department of Crop and Soil Sciences, North Carolina State University, Raleigh, North Carolina 27695, United States ∥ Sustainable Soils and Grassland Systems, Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, U.K. ⊥ Department of Crop and Soil Science, Oregon State University, ALS Building 3017, Corvallis, Oregon 97331, United States S Supporting Information *
ABSTRACT: Mineral binding is a major mechanism for soil carbon (C) stabilization, and mineral availability for C binding critically affects C storage. Yet, the mechanisms regulating mineral availability are poorly understood. Here, we showed that organic amendments in three long-term (23, 154, and 170 yrs, respectively) field experiments significantly increased mineral availability, particularly of short-range-ordered (SRO) phases. Two microcosm studies demonstrated that the presence of roots significantly increased mineral availability and promoted the formation of SRO phases. Mineral transformation experiments and isotopic labeling experiments provided direct evidence that citric acid, a major component of root exudates, promoted the formation of SRO minerals, and that SRO minerals acted as “nuclei” for C retention. Together, these findings indicate that soil organic amendments initialize a positive feedback loop by increasing mineral availability and promoting the formation of SRO minerals for further C binding, thereby possibly serving as a management tool for enhancing carbon storage in soils.
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are accessible to SOM.13 Here, available minerals are referred to as the mineral surfaces available for C binding, and the concentration of a metal in water-dispersible colloids is a good proxy for the availability of a mineral. More importantly, the availability of mineral surfaces for C binding can be affected by soil moisture content,14 organic amendments,15,16 or land-use change,17 suggesting that management practices may in return affect mineral availability for further C binding. Two major mechanisms critically control mineral availability for C binding. First, soil physiochemical conditions, such as pH18−20 and redox potential,20−22 and dissolution−precipitation processes regulate the release of mineral elements from primary minerals.22 Second, both plants and microbes also affect mineral availability through their exudates and metabolic compounds.20,22 By delivering a continuous supply of individual exudate solutions through an artificial root into unperturbed soil, low molecular weight (LMW) acids have been shown to have strong metal-complexing abilities, changing mineral
INTRODUCTION
Soils are the largest and most stable terrestrial carbon (C) pool, and they are often assumed to be a major sink for future C storage.1,2 Globally, soil organic matter (SOM) contains more than three times as much C as either the atmosphere or terrestrial vegetation.1 Recent isotopic and spectroscopic studies indicate that microbial accessibility to substrates rather than chemical complexity of organic C dominantly controls long-term C stability in soils1,3−5 and that a significant proportion of stable SOM is derived from simple C rather than chemically resistant compounds.1,6,7 Such stable SOM mainly results from physical occlusion in microaggregates and chemical sorption in organo−mineral complexes.1,8−10 The majority of studies represent organo−mineral complexes as “biogeochemical black boxes”, where inputs and outputs of organics and minerals are estimated but the underlying mechanisms controlling C stabilization and storage are rarely explored.11 This is partly due to the inherent physical and biogeochemical complexity of soil systems, fluctuation of environmental conditions,1 and the existence of nanoscale (∼1−100 nm) minerals that may dominate C binding.12 Recently, available minerals have been shown to correlate strongly with soil C and its long-term stabilization because they © 2017 American Chemical Society
Received: Revised: Accepted: Published: 4960
January 17, 2017 April 2, 2017 April 12, 2017 April 12, 2017 DOI: 10.1021/acs.est.7b00305 Environ. Sci. Technol. 2017, 51, 4960−4969
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Environmental Science & Technology
were 2 and 1 for Qiyang and Rothamsted Experiments, respectively. Other detailed information about soil sampling and the Experiment stations can be found in Supporting Information (SI). Soil colloids were isolated using the following procedure.27 Briefly, air-dried soil was suspended in deionized water at the ratio of 1:5 (W/V), shaken for 8 h at 25 °C, and centrifuged for 6 min at 2500g. Aliquots of the supernatant suspensions containing the soil colloids were transferred into 50 mL glass vials, stored in the dark at 4 °C, and analyzed within 1 week. The isolated water-dispersible colloids represent one of the most reactive components in soils.28,29 Microcosm Experiments. One microcosm experiment with three replicates was conducted to determine the effect of root and Arbuscular Mycorrhizal Fungi (AMF) exudates on mineral availability in the USDA-ARS Plant Science Research CO2 facility at North Carolina State University, Raleigh, NC. The experimental microcosm was divided into six compartments with each compartment measuring 13 × 14 × 15 cm (width × depth × height). Three compartments in a row were designated as host compartments (containing host plants and AM) and the three adjacent compartments were designated test compartments to assess mycorrhizal functioning. The host and test compartments were separated by a replaceable 0.45, 20, or 1000 μm mesh fabric panel (Tetko/Sefar mesh, Sefar America, NY) that allowed nothing (-Root-AMF), AM fungal hyphae (-Root+AMF), or both roots and AM fungal hyphae (+Root +AMF) to grow into the test compartments, respectively.30 Effectiveness of the 20 mm mesh fabric in preventing root growth into the test compartment was visually assessed at the completion of each experiment. Each compartment of the microcosm unit was filled with 3.5 kg of an autoclaved quartz sand and sandy loam soil (1:1 w/w) mixture. Ten seeds of Triticumaestivum Linn. (Wheat) were sown into each host cell. Microcosms were watered with deionized water daily. Plants were allowed to grow for 4 months, and then the soils in the test cells were air-dried. Another microcosm experiment with three replicates was conducted to determine the effect of root and fertilization treatments on mineral availability in a greenhouse at Nanjing Agricultural University. PVC pots (20 cm high, 7.8 cm internal diameter) were filled with red soils collected at the Qiyang Experiment in 2014. Each pot was filled with 1.5 kg of equivalent dry red soil. The pots were sown with corn and every treatment had three replicates. Each pot was put into two pore sizes of mesh (30 and 1000 μm).31 The pore sizes 1000 and 30 μm would permit and not permit the entry of roots, respectively. The pots were watered with deionized water daily. Plants were allowed to grow for 10 weeks, and then the soils were air-dried. Incubation Studies for Fe Mineral Transformations. Citric acid solutions (SIGMA-Aldrich, ACS reagent, ≥ 99.5%) were added to the soil colloid suspensions from the Qiyang Experiment and stirred. The final concentrations of citric acid in the soil colloid suspensions were 10 and 100 mg L−1, and the pH values were adjusted to 6.7, which was the same as that of the raw soil colloid solutions. After 1 day of incubation, the suspensions in the series of reaction solutions and the control solutions (i.e., without the addition of citric acid) were analyzed by Fe K-edge extended X-ray absorption fine structure (EXAFS) spectroscopy. The incubation study was performed in duplicate.
availability by decreasing short-range-ordered (SRO) minerals and metal−organic complexes in the affected zone next to roots.23 However, a single LWM acid in artificial root systems is far from a real root system. Therefore, direct evidence illustrating the linkage among real root exudates and the formation of SRO minerals in soils is still lacking. Here, we present direct evidence from four independent but complementary experiments demonstrating that organic acids resulting from long-term organic amendments increase soil mineral availability and the formation of SRO minerals, and that SRO minerals facilitate C retention. First, we assessed the impacts of long-term organic amendments on mineral availability and organic-acid production in three (one in China24 and two in England25,26) well-controlled, long-term (23 yrs, 154 yrs, and 170 yrs, respectively) field experiments. Second, we designed two microcosm studies to test the role of root exudates and organic amendments in the enhancement of mineral availability and SRO mineral formation. Third, we conducted an incubation experiment to examine the mechanistic role of organic acids in the formation of SRO minerals. Finally, we used 13C to directly trace the retention capacity of labile C by available minerals. Throughout our experiments, advanced techniques of synchrotron-based X-ray absorption fine structure (XAFS) spectroscopy and scanning transmission X-ray microscopy (STXM) imaging, as well as nanoscale secondary ion mass spectrometry (NanoSIMS) were integrated to identify the composition and distributions of organic C and soil minerals. Collectively, our results indicate that soil organic amendments initialize a positive feedback loop by increasing mineral availability and promoting the formation of SRO minerals for further C binding.
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MATERIALS AND METHODS Field Studies and Soil Colloid Extraction. The Qiyang Experiment was set up on a Ferralic Cambisol soil in 1990 in Hunan Province, China.24 The top soil in 1990 contained approximately 61.4% clay, 34.9% silt, and 3.7% sand. The Park Grass Experiment, the oldest field experiment on permanent grassland in the world, was set up in 1856 at the Rothamsted Research Station in Hertfordshire, England.25,26 The top soil (0−23 cm) is a silty clay loam containing 22% clay, 29% silt, and 49% sand. The Broadbalk Experiment, the oldest continuously running field wheat experiment in the world, was set up in 1843 at the Rothamsted Research Station, England. 25,26 According to the Food and Agriculture Organization of the United Nations (FAO) classification, the soil at Rothamsted Research Station is classified as a Chromic Luvisol.25 Soil samples to 0−20 cm depth, 0−10 cm depth, and 0−23 cm depth were collected in September 2013 at the Qiyang Experiment, 2008 at the Park Grass Experiment, and 2013 at the Broadbalk Experiment, respectively, using a 5 cm internal diameter auger. Each plot was evenly separated into three regions, and 10 cores were randomly sampled from each region. Fresh soil was thoroughly mixed, air-dried, and sieved through a 5 mm screen for further analysis. In all three Experiment stations, swine manure, or farmyard manure was used as a long-term organic amendment (M). The other fertilization regimes were selected for comparison: (i) no fertilizer input (Control) and (ii) chemical fertilizers of nitrogen, phosphorus and potassium only input (NPK). In this study, both manure alone and manure plus NPK treatments are collectively called organic fertilization treatments. The numbers of plots of a given amendment treatment 4961
DOI: 10.1021/acs.est.7b00305 Environ. Sci. Technol. 2017, 51, 4960−4969
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Environmental Science & Technology Isotopic Labeling Experiment. Soil colloids with organic amendments in the Qiyang Experiment were incubated with a 13 C-labeled amino acid mixture (algal amino acids, Isotec, Miamisburg USA; C/N ratio: 2.8; min. 99 atom % 13C) as a readily bioavailable C isotopic tracer. The amino acid mixture was suspended in deionized water at a concentration of 10 mg L−1. After addition of 13C enriched amino acids the samples were incubated for 24 h at 20 °C and then used for NanoSIMS analysis. The incubation study was performed in duplicate. Analysis Techniques. The soil colloids were mixed with 10% nitric acid at a ratio of 1:1 (v/v) on a heating plate;32 then, the mixture was digested at 150 °C for 2 h. After the digestion, the mixture was filtered through a filtration membrane (0.45 μm) and the metal ions in the supernatant were quantified by inductively coupled plasma atomic emission spectroscopy (710/715 ICP-AES, Agilent, Australia).. Mineral dissolution in the microcosm experiments was determined by suspending air-dried soil in deionized water at the ratio of 1:5 (w/v), putting the mixture on a horizontal shaker (170 rpm) for 24 h at room temperature, and then centrifuging it at 3000g for 10 min. The supernatant was passed through a 0.45 μm polytetrafluoroethylene filter. Quantitation of SRO minerals was performed using the acid ammonium oxalate extraction method.28 In brief, soil was extracted using 0.275 M ammonium oxalate at pH 3.25 with a soil: extractant = 1:100 (w/v) ratio. The main mineral elements, namely Fe and Al, were quantified by ICP-AES (710/715 ICP-AES, Agilent, Australia). Dissolved organic carbon (DOC) was measured using a TOC/TN analyzer (multi N/C 3000, Analytik Jena AG, Germany). Diffusive gradients in thin films (DGT) were prepared by placing a Chelex-100 disc on a support, followed by a diffusive gel disc (DGT Research Ltd., Lancaster, UK), and then filtering samples through a membrane filter. The upper cover, with a window exposed to the sample, was affixed lightly. The calculated concentration represents the effective available concentration of Fe in soil. A detailed description of analysis techniques is found in the SI. Iron K-edge absorption spectra were collected using a Si (111) double crystal monochromator at the XAFS station of the BL14W1 beamline of the Shanghai Synchrotron Radiation Facility (SSRF). The storage ring was working at 3.5 GeV with 200 mA as an average storage current. The prepared samples and standard samples were recorded in transmission mode. All the samples were mounted in a thin custom-built plastic sample holder covered with Kapton tape and placed at 45° to the incident X-ray beam. Ten scans were averaged for each sample to obtain a good signal-to-noise ratio. The X-ray energy scale was calibrated to the iron K-edge (7112.0 eV) using an iron metal foil before XAFS measurements were performed. The XAFS data were processed and analyzed using ATHENA software (version 2.1.1).33 A detailed description of analysis techniques is found in the SI. Carbon 1s near edge X-ray absorption fine structure (NEXAFS) spectra were obtained on the BL08U1 beamline of the SSRF. For specimen preparation, one droplet of suspension was deposited at a 100 nm thickness onto a Si3N4 window, which was previously glued onto the detection plate of the microscope. The sample thickness is important to obtain a good signal-to-noise ratio when using NEXAFS spectroscopy.34 The main 1s-p and Rydberg/mixed valence transitions in the fine structure regions of the C K-edge spectra were recorded in the energy range from 284−310 eV. A detailed description of analysis techniques is found in the SI.
NanoSIMS analyses were performed with a NanoSIMS 50L (Cameca, Gennevilliers, France) at the Institute of Geology and Geophysics, Chinese Academy of Sciences, China. Prior to the analysis, the gold coating layer (∼10 nm) and possible contamination of the sample surface were sputtered using a high primary beam current (presputtering).28,29 During the presputtering step, reactive Cs+ ions were implanted into the sample to enhance the secondary ion yields. Secondary ion images of 12C−, 13C−, 27Al16O− and 56Fe16O− were simultaneously collected by electron multipliers with an electronic dead time of 44 ns. We compensated for the charging that resulted from the nonconductive mineral particles by employing the electron flood gun of the NanoSIMS instrument. For every sample, 4−6 spots were analyzed to obtain reliable data. A detailed description of analysis techniques is found in the SI. Statistical Analyses. Differences between the data were assessed with one-way analysis of variance (ANOVA) using the SPSS software version 16.0 for Windows (SPSS, Chicago, IL). Significance was determined using one-way ANOVA’s followed by Tukey’s HSD post hoc tests, where conditions of normality and homogeneity of variance were met. Means ± SE (n = 3) followed by different letters in figures and tables indicate significant differences between treatments at P < 0.05. Data were log transformed to attain normality and homoscedasticity for regression analysis. Regression analyses were performed between two log-transformed variables using the OriginPro 9.0 software. Similar to most analyses, a value of P < 0.05 is typically considered significant.
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RESULTS Long-Term Organic Amendments Increased Soil Mineral Availability and SRO Phases. Compared to no fertilizer and chemical fertilizer inputs, long-term organic amendments significantly (Tukey’s HSD post hoc tests; P < 0.05) increased available minerals (i.e., Al and Fe) (Figure 1) in soil colloids by over 2 orders of magnitude at the Qiyang Experiment and 2−12 times at the Park Grass and Broadbalk Experiments. Similarly, results from DGT experiments confirmed that long-term organic amendments significantly (Tukey’s HSD post hoc tests; P < 0.05) increased bioavailable Fe at the Qiyang Experiment (SI Figure S1). Based on the results of Fe K-edge X-ray absorption near edge structure (XANES) (SI Figure S2a) and Al 2p3/2 XPS (SI Figure S2b), we found that approximately 17−57% of Fe minerals and 13− 28% of Al minerals in soil colloids with long-term organic amendments at the three field Experiments were SRO minerals (i.e., ferrihydrite and allophane, respectively); these values were higher than those in samples receiving no fertilizer and chemical fertilizer inputs. In addition, the extracted minerals and organic carbon in soil colloids accounted for approximately 0.02−1.8% and 0.2−1.5% of total soils, respectively (SI Tables S1), with the biggest percentages found in samples from the organic amendment treatments, followed by those receiving no fertilizer and chemical fertilizer inputs. Taken together, these findings show that long-term organic amendments significantly increase the presence of SRO phases. The Presence of Roots and the Application of Organic Exudates Increased Mineral Availability and Promoted the Formation of SRO Minerals. To explore the factors that increase mineral availability, we conducted two microcosm studies that allowed us to investigate the contribution of root and AMF exudates as well as fertilizers on mineral availability and SRO mineral formation (Figure 2). The presence of roots 4962
DOI: 10.1021/acs.est.7b00305 Environ. Sci. Technol. 2017, 51, 4960−4969
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organic C, accounting for approximately 61% of the organic C at the Qiyang Experiment, while aromatic C (1s−π* transition of conjugated CC) only constituted less than 5% of the organic C in the three field Experiments (Figure 3a, SI Tables S2 and S3). For the Park Grass and Broadbalk Experiments, carboxyl C and aromatic C accounted for 35−44% and approximately 3−11% of the organic C, respectively (SI Figure S3, Table S3). The other C forms were present as phenolic C, alkyl C, O-alkyl C, and carbonyl C (SI Table S3). In addition, long-term organic amendments also markedly increased the concentration of dissolved organic C when compared to chemical fertilization in all of the three Experiments (SI Figure S4). LMW organic acids have in other experiments shown to consist of approximately 0.5−5% of C in soil solution.35,36 Therefore, long-term organic amendments may increase production of organic acids, especially with LMW components, in soils. To test the critical role of root exudates in the formation of SRO minerals, we designed a simulated study by adding citric acid to soil colloids. The colloids were derived from soils with long-term organic amendments at the Qiyang Experiment. Iron k3-weighted EXAFS spectra (Figure 3b) showed that two peaks at k = 5.7−6.0 Å and 8.0−8.8 Å, were observed in the raw soil colloids and those with 10 mg L−1 citrate addition but disappeared in the soil colloids with 100 mg L−1 citrate addition. These two peaks could be observed in goethite mineral standards but were not present in ferrihydrite (Figure 3b). Linear combination fitting (LCF) results (SI Table S4) of the Fe k3-weighted EXAFS spectra further demonstrated that incubation of soil colloids with citric acid at a concentration of 10 and 100 mg L−1 for 1 day could decrease goethite from 27.6% to 13% and 5.1% of the total Fe mineralogy but increase ferrihydrite from 39.4% to 49.9% and 74.6% of the iron mineralogy, respectively. The results from no fertilizer inputs also support the observation that citric acid drives transformation of Fe minerals in soil colloids (SI Figure S5). Because ferrihydrite is more mobile and has a higher specific surface area than goethite,37 these results provide spectroscopic evidence that citric acid can increase mineral mobilization and promote transformation of goethite to ferrihydrite, the most reactive SRO iron (oxyhydr)oxide. Retention of Labile C by Available Minerals. To verify the strong retention capability for C by the mobilized Al and Fe minerals, we then designed an isotopic labeling experiment (using 13C-labeled amino acid) combined with NanoSIMS observation (Figure 4). Here 13C-labeled amino acids were used as a precursor of newly added C (i.e., animal manure) in soils. After 24 h of incubation with a 13C amino acid mixture, the composite NanoSIMS image showed a profound enrichment of newly added 13C− on 27Al16O− and 56Fe16O− (Figure 4a and SI Figure S6), which served as “nuclei” for the retention of 13C−. This is further supported by the hue-saturationintensity (HSI) image of 13C/12C− (Figure 4b), which clearly showed that colloid particles were surrounded by these 13C− enriched spots. Line profiles further indicated that the distribution patterns of 13C−, 12C−, 27Al16O−, and 56Fe16O− were similar (SI Figure S6). However, for large soil particles (i.e., approximately 15 μm), a part of newly added C was present at the edges of particles (SI Figure S6). These large particles seemed to retain much more C than small particles. It should be noted that 12C− represents the native C (SI Figure S6) and it does not impact sorption of amino acids based on the similar slopes between 13C−, 12C−, and 27Al16O−, 56Fe16O−
Figure 1. Effects of long-term organic amendments on the Al and Fe concentrations in soil colloids at the Qiyang (a), Park Grass (b), and Broadbalk (c) Experiments. Control, no fertilizer inputs; NPK, chemical fertilizer inputs; NPK1, (NH 4 ) 2 PKNaMg; NPK2, (NO3)2PKNaMg; M, manure inputs; NPKM, chemical fertilizer plus manure inputs; NPKS, chemical fertilizer plus straw inputs; NPKMS, chemical fertilizer plus manure plus straw inputs. Significant differences between fertilization practices were determined using one-way ANOVA’s followed by Tukey’s HSD post hoc tests at P < 0.05, where conditions of normality and homogeneity of variance were met (n = 3).
increased the release of Al and Fe from soils (P < 0.05) over 2 times for mean values with or without the application of fertilizers (Figure 2a,b), but AMF had no significant impact on Al and Fe release (P > 0.05) (Figure 2a). Interestingly, both microcosm studies demonstrated that the presence of roots also markedly increased the concentration of SRO minerals (Figure 2c,d). Compared to chemical fertilizers, organic amendments significantly decreased mineral mobilization (Figure 2b) but increased (>20%, p < 0.05) the concentration of SRO minerals from 3.7 to 3.9 g kg−1 in the presence of roots (Figure 2d). These results indicate that roots, in concert with organic amendments, may be responsible for increasing mineral availability and the formation of SRO minerals. Citric AcidOne of the Most Abundant Exudate ClassesPromoted the Formation of SRO Minerals. Addition of LMW organic acids (e.g., citric acidone of the most abundant exudate classes) to soils benefits the formation of SRO minerals.23 We used C 1s NEXAFS spectroscopy to identify the composition of organic C in soil colloids from all three field Experiments (Figure 3a and SI Figure S3). Carboxyl C (1−π* transition of COOH) was dominant in soluble 4963
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Figure 2. Effect of the presence of roots and organic amendments on mineral dissolution and the formation of SRO minerals. (a) Effect of the presence of roots on the mobilized minerals. (b) Effect of the presence of roots and organic amendments on the mobilized minerals. (c) Effect of the presence of roots on the formation of SRO minerals. (d) Effect of the presence of roots and organic amendments on the formation of SRO minerals. −Root−AMF, not allowing either AMF hyphae or roots growing into the test compartments; −Root+AMF, allowing AM hyphae but not roots growing into the test compartments; +Root+AMF, allowing both AMF hyphae and roots growing into the test compartments; Control, no fertilizer inputs; NPK, chemical fertilizer inputs; M, manure inputs. Significant differences between treatments were determined using one-way ANOVA’s followed by Tukey’s HSD post hoc tests at P < 0.05, where conditions of normality and homogeneity of variance were met (n = 3).
and thereby potentially chemically stabilize organic matter.42,43 Although the importance of SRO minerals in protecting soil C has increasingly been recognized,13,23,43 the information about their regulation is still very limited. In this study, having a wellcontrolled long-term field system and advanced technologies allowed us to identify the formation of SRO minerals. Microbial- or plant-driven increases to mineral availability are believed to be important steps in the formation of SRO minerals in soil.44 Our microcosm experiments show that plant roots and their exudates may play a bigger role than mycorrhiza in the development of mineral availability and subsequent formation of SRO minerals (Figure 2). This result also challenges the long-standing conceptual view that the weathering of minerals and the formation of SRO minerals are very slow processes and cannot be detected in short-term systems.22,45 We therefore suggest that the formation of SRO minerals can be accelerated or regulated by plant roots and some agricultural practices (e.g., organic amendments), a notion which is also supported by previous microcosm experiments that have demonstrated exudate-induced effects on SRO minerals.23 Furthermore, our mineral transformation experiments provide direct evidence that the formation of SRO minerals is promoted by LMW organic acids (Figure 3), which may be produced by roots or the degradation of organic amendments. Similarly, oxalate, another common root exudates or
(SI Figure S7). Compared to no fertilizer or chemical fertilizer inputs, the total sorption capacity of organic carbon by soil colloids was significantly increased with organic amendments (Figure 4c).
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DISCUSSION Drivers of Mineral Availability and SRO Mineral Formation. Our long-term field studies demonstrate that organic amendments significantly increase the availability of Al and Fe minerals, particularly their SRO phases (Figure 1 and SI Figure S2). The available Al and Fe minerals decrease C mineralization and increase the potential for SOC sequestration.19,21 The percentage of SRO minerals in organic-amended soil was higher than that of no fertilizer and chemical fertilizer inputs based on the previous results achieved from selective extraction methods38 and transmission electron microscopy (TEM) analysis24,39 at the Qiyang Experiment. However, selective extraction methods give only operationally defined pool of SROs and suffer from intrinsic limitations due to artifacts associated with reagent selectivity and the inability to differentiate specific SROs.40 X-ray absorption fine structure (XAFS) spectroscopy complements sequential extraction techniques,41 and in our study provided direct identification of important SROs (SI Figure S2). These SRO minerals possess structural defects, high specific surface area and charge density, and variably charged surfaces, enabling them to bind 4964
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Figure 4. Isotopic labeling experiment illustrated retention of labile C by Al and Fe minerals. (a) Composite element distribution map of 13 − C (red), 27Al16O− (green), and 56Fe16O− (blue) following 24 h incubation of 13C-labeled amino acid with soil colloids from long-term organic amendment samples of the Qiyang Experiment. Colors reflect the proportion of each species. (b) These 13C− enrichment images are shown as hue-saturation-intensity image (HSI) images, where the color scale indicates the 13C−/12C− ratio. (c) The mass balance of the 13 − C in the different fertilization treatments. Note that residuals are referred to the soils after removing soil colloids.
In addition to microbes or plants, other parameters, that is, pH, complexation or, most important, redox variation, also affect mineral availability19,21 and the formation of SRO minerals.39 Our previous results from the Qiyang Experiment indicated that compared with chemical fertilization, organic fertilization significantly (P < 0.05) increased soil pH, the concentration of Al and Fe, and amorphous Al, but decreased exchangeable Al.24,38 Wang et al. (2016) investigated the effect of fertilization treatments ondesert soil and showed that compared to a Control, an NPK treatment significantly decreased the soil pH (P < 0.05), whereas a manure treatment maintained the soil pH.50 Meanwhile, the addition of manure significantly (P < 0.05) increased the content of SOC, with SOC content ranked by descending order as M > NPKM > NPK > Control.50 In addition, our unpublished data (paper in review) show that there was a significantly positive relationship between poorly crystalline Fe minerals and SOC, as well as aromatic C, in gray desert soil; attachment of aromatic functional groups to the poorly crystalline Fe minerals could also protect the poorly crystalline Fe minerals from transforming to their more crystalline counterparts.51 Impacts of Organic Amendments on Carbon Retention in Soils. We hypothesized that the mobilized mineral particles in soils with organic amendments have a strong capability to retain C in soils. To test this hypothesis, we examined the distribution patterns of native C, newly added C, and minerals in soil colloids to support the C storage potential of the mobilized mineral particles in soil colloids. Our
Figure 3. Typical C 1s NEXAFS spectra for soil colloids (a) and the formation of SRO minerals following addition of citric acid (b) at the Qiyang Experiments. Note that G1−G8 represent eight Gaussian curves. Artan represents an arctangent step function. The specific C forms of G1−G8 are given in SI Table S2. Open circles indicate experimental data and solid lines show the model fits.
intermediate of soil microbes, was also found to have the same effect on the dissolution of goethite20,46 and Al minerals.47 Although these organic acids only account for a small percentage of soil soluble C,36 they represent the most reactive forms of organic matter and exist widely in soils, especially in the rhizosphere.47 Since ferrihydrite is more available than goethite,37 this transformation is particularly important because the absence of iron in an available form limits C storage in many soils. Newly formed SRO minerals may adsorb or precipitate on soil aggregates and promote soil aggregation.48 The aggregation role of newly formed SRO minerals is also supported by the results from high-resolution TEM combined with EDS analysis that Al and Fe are enriched on the surface of soil particles with long-term organic amendments.24,29,39 The driving force for this aggregation may be the decrease in surface energy that appears to be low enough for SRO minerals.49 This increased soil aggregation lowers rates of respiration per unit of soil C, one of the main mechanisms of soil C storage and preservation.19 4965
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Figure 5. Proposed mechanisms for mineral availability as the key regulator of soil C storage. Solid and dashed arrows represent positive and negative effects, respectively.
term organic amendments may be a critical step in this process (Figure 2 and SI Figure S3). The produced acids act as complexing and reducing agents for mineral mobilization and acquisition,20 further promoting the formation and stability of SRO minerals via four potential mechanisms (Figure 5). First, the mobilized mineral elements (e.g., Al and Fe) can act as the precursors for formation of SRO minerals.12,37 Second, LMW organic acids, common root exudates, can promote transformation of minerals or oxides from more crystalline to SRO phases (Figure 3b), a process known as “rejuvenation” in soil and ecology sciences.37 Third, after the formation of SRO minerals, LMW organic acids can incorporate, through precipitation from solution,57 into the network structure of SRO minerals58 and prevent their growth or transformation to crystalline forms.59 And finally, some biopolymers with soil particles can also limit the dispersal of SRO minerals that may otherwise be transported away from their source via leaching, surface runoff, or drainage in natural ecosystems60 adding to carbon storage (SI Figure S8). Although the addition of organic acids to soil can lead to the release of old carbon23 or the formation of SRO minerals that enhance soil carbon storage,61 it appears that a long-term effect of organic-acid addition through organic amendments is increased soil carbon storage. Environmental Implications. Our results provide direct evidence illustrating linkages among organic acids from both root exudates and organic amendments, SRO minerals, and soil C stability within field and incubation experiments. Continuous organic amendments initialize a positive feedback loop, in which high organic inputs liberate minerals that can promote C sequestration in soils. The liberated minerals in the soil colloids, and hence the high content of SRO minerals formed by organically growth-limited precipitation, are therefore expected to be key factors that control the storage of soil C. More importantly, our findings also provide a pathway for regulating
NanoSIMS results indicate that native C and newly added C are colocalized with minerals (Figure 4). Also, we provide direct evidence demonstrating that these mineral particles can act as ’nuclei’ to preferentially retain new labile C (Figure 5 and SI Figure S6). By contrast, it has recently been shown that only a limited proportion (
