Biochar DOM for plant promotion but not residual biochar for metal immobilization depended on pyrolysis temperature

Science of the Total Environment 662 (2019) 571–580

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Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv

Biochar DOM for plant promotion but not residual biochar for metal immobilization depended on pyrolysis temperature Rongjun Bian a,b, Stephen Joseph a,c, Wei Shi a, Lu Li a, Sarasadat Taherymoosavi c, Genxing Pan a,b,⁎ a b c

Institute of Resources, Ecosystem and Environment of Agriculture and Center of Biomass and Biochar Green Technology, Nanjing Agricultural University, 1 Weigang, Nanjing, 210095, China Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, Nanjing Agricultural University, 1 Weigang, Nanjing 210095, China School of Materials Science & Engineering, University of New South Wales, Australia

H I G H L I G H T S

G R A P H I C A L

A B S T R A C T

• DOM and nutrients content in BE was varied with the pyrolysis temperature. • Spraying BE350 showed greatest value for plant yield and quality promotion. • DOM may regulate gene expression and stimulate nitrogen assimilation in cabbage. • DOM-free biochar can be used for metal immobilization in soil. • Biochar can be recycled with valueadded applications in agriculture.

a r t i c l e

i n f o

Article history: Received 20 October 2018 Received in revised form 21 January 2019 Accepted 21 January 2019 Available online 22 January 2019 Editor: Daniel CW Tsang Keywords: Biochar Water extract Dissolved organic matter Pyrolysis temperature Plant growth promoter Heavy metal immobilization

a b s t r a c t While biochar on metal immobilization was well understood, a small pool of dissolvable organic matter (DOM) from biochar was recently recognized as a bioactive agent for plant growth promotion. However, how the molecular composition and plant effects of this fraction and the performance for metal immobilization of the DOMremoved biochar could vary with pyrolysis temperature had been not well addressed. In this study, wheat straw biochar pyrolyzed at a temperature of 350 °C, 450 °C, 550 °C were extracted with hot water to separate the DOM fraction. The obtained biochar extracts (BE350, BE450, and BE550) were tested as foliar amendment to Chinese cabbage while the extracted (DOM-removed) biochars were tested for heavy metal immobilization in a contaminated soil. The results showed that BE350 was higher in organic matter content, abundance of organic molecules and mineral nutrients than BE450 and BE550. Compared to control, foliar application of BE350 significantly enhanced the shoot biomass (by 89%), increased leaf soluble sugar content (by 83%) but reduced leaf content of nitrate (by 34%) and of potential toxic metals (by 49% for Cd and by 30% for Pb). Moreover, BE350 treatment increased gene expression of nitrate reductase and glutamine synthetase enzyme activity of the tested plant. Meanwhile, soil amendment of DOM-extracted biochars significantly decreased soil CaCl2 extractable pool of Cd, Pb, Cu and Zn in a range of 27%–78%. Thus, the performance of DOM extract of biochar on plant growth promotion was indeed dependent of pyrolysis temperature, being greater at 350 °C than at higher temperatures. In contrast, metal immobilizing capacity of biochar was regardless of pyrolysis temperature and

Abbreviations: BE, biochar extract; BBC, bulk biochar; DOC, dissolvable organic carbon; DOM, dissolvable organic matter; EBC, DOM-extracted biochar; LMW, low molecular weight; TOC, total organic carbon. ⁎ Corresponding author at: Institute of Resource, Ecosystem and Environment of Agriculture and Center of Biochar and Green Agriculture, Nanjing Agricultural University, 1 Weigang, Nanjing 210095, China. E-mail address: [email protected] (G. Pan).

https://doi.org/10.1016/j.scitotenv.2019.01.224 0048-9697/© 2019 Published by Elsevier B.V.

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DOM removal. Therefore, pyrolyzing wheat straw at low temperature could produce a biochar for valorized separation of a significant DOM pool for use in vegetable production, leaving the residual biochar for amendment to metal contaminated soil. © 2019 Published by Elsevier B.V.

1. Introduction Biochar is a carbon-rich solid product derived from biomass pyrolysis under limited oxygen conditions, its use for soil amendment had been widely recommended to improve soil fertility, immobilize soil contaminants, reduce greenhouse gas emission while enhance soil carbon sequestration (Lehmann, 2007; Beesley et al., 2010; He et al., 2017). These beneficial functions had been attributed to the high porosity and surface area (Ahmad et al., 2014), high content of recalcitrant carbon (Inyang et al., 2016), existence of reactive mineral components as well as the redox activity (Hagemann et al., 2017), associated with biochar particles. However, use of biochar in dozens of tons for soil amendment would raise the cost concerns against for the beneficiary from crop improvement, often causing uncompetitive with other inputs (Fidel et al., 2017). For metal immobilization to ensure Cd-safe rice cultivation practiced in China, for example, the cost for biochar amendment at 20 t ha−1 (Bian et al., 2016a) could not balance the income from increased grain production (Chen et al., 2016) even over four or more years (Bian et al., 2014; L. Wang et al., 2018), compared to the conventional lime amendment (Bian et al., 2016a). This high cost could make biochar soil amendment less competitive among independent farming inputs in China's agriculture (Clare et al., 2014). Therefore, technology for value-added biochar use should be urged to make biochar production and application viable (Clare et al., 2015). In other words, cost of biochar used for soil amendment should be lower via separated use of value biochar portion for application to valued products in agriculture or other sectors. Recent studies had shown that labile organic molecules dissolved from biochar could result in an increase in plant growth and in resistance to disease as well as an increase in abundance of beneficial micro-organisms in amended soils (Graber et al., 2014; Qu et al., 2016; Sun et al., 2017; Yuan et al., 2017). A study by Qu et al. (2016) indicated higher concentrations of oxygen-rich and polar functional groups and lower aromaticity of the DOM fraction, compared to organics persistent in the solid bulk, of rice or bamboo biochar. Biochar extracts as a DOM fraction had been known of a composition of organic compounds as biopolymers, humics, building blocks, low molecularweight acids, and low molecular-weight neutrals as well as hydrophobic organic carbon (Lin et al., 2012; Lou et al., 2016). E et al. (2015) reported an improvement of plant metabolic processes by labile organic molecules from fast pyrolysis of rice husks. Lou et al. (2016) isolated with hot water the smaller DOM pool from maize or wheat biochar, and applied to valued vegetable production. They found a very significant improvement of growth and nutrition quality of Chinese cabbage with the extracts and recommended for commercial use as a liquid organic fertilizer in agriculture. In a recent study by P. Wang et al. (2018), an extract using the pyroligneous solution, instead of hot water, of maize biochar significantly improved (by 39%) pepper productivity and nutrition quality with diluted spraying. Whereas, the composition of humic-like supramolecular compounds and the plant germination effect of an acid water extracts of biochar pyrolyzed at 450 °C differed between wheat and maize feedstock (Sun et al., 2017). However, a DOM fraction of biochar could vary with pyrolysis temperature. In a study by Lin et al. (2012), the DOM pool of sawdust biochar pyrolyzed at 450 °C was larger than at 550 °C. In a previous study (Bian et al., 2018), wheat biomass from contaminated was pyrolyzed at different pyrolysis temperatures ranging from 350 °C to 550 °C, and the respective biochar hot-water extracts, were shown different effective for promoting cabbage yield and quality, without potential environmental risk. Regardless

of this, the extracted biochars exerted similar capacity to immobilize toxic metals when amending to contaminated fields. Therefore, the DOM pool size and abundance of the organic compounds or C bond groups, as well as agronomic effects of a biochar extract, could be a function of pyrolysis temperature, in addition to feedstock, pre or postprocessing. Pyrolysis temperature had been considered thoroughly as a driver for biochar property and functioning in biochar science and technology (Lehmann and Joseph, 2015). It had been well known that biochars pyrolyzed at low temperatures were high in volatile matter and N content (Hagner et al., 2016) but low in aromaticity (Mcbeath et al., 2014). This could be due to the collapse of biomass tissue microstructure, escape of functional groups or elements on their surface with increasing pyrolysis temperature (Chen et al., 2014). Accordingly, increasing pyrolysis temperature could lead to an increase in carbon recalcitrance or stability and surface reactivity but decrease in soil microbial use (Tushar et al., 2012). Generally, biochar capacity to depress soil carbon emissions increased with pyrolysis temperature (Rittl et al., 2018) though opposite for manure biochar (Subedi et al., 2016). High pyrolysis temperatures biochars were generally effective in sorption of organic contaminants whereas those at low temperatures tended to immobilize inorganic and polar organic contaminant (Ahmad et al., 2014). In a metaanalysis by Chen et al. (2018), biochar's potential to reduce soil metal availability and plant uptake varied in a wide range with metal species and feedstock. Thus, pyrolysis temperature effects on biochar plant productivity were very uncertain, depending on feedstock types (Liu et al., 2013). On crop productivity assessed thereby, biochars from crop residue pyrolyzed at temperature over 350 °C were all positive while those at lower temperature negative. In a study by Hagner et al. (2016), with pyrolysis temperature increased from 300 °C to 475 °C, birch-derived biochar effect was negative to neutral on seed germination but marginal on soil pH and microbial activity when amended to a Finnish poor sandy soil. Igalavithana et al. (2017) compared biochars from vegetable residue between different pyrolysis temperatures within 200–500 °C and concluded that low temperature (200 °C) only provided significant improvement of soil quality in a heavy metal contaminated field. Similarly, low temperature (b300 °C) pyrolyzed biochar could tend to preserve nutrients available in poultry manure and perform soil fertility improvement (Gunes et al., 2015). Particularly, biochars from wood and vegetable waste pyrolyzed at low (350 °C) and high (600 °C) temperatures exerted similar effects on Rhizoctonia solani suppression and plant growth promotion of cucumber (Jaiswal et al., 2014). Overall, pyrolysis temperature played a varying role in the soil and plant effects by the bulk (unextracted) biochars reported in the literature and its effect on biochar DOM and the DOM-removed biochar had not yet been clearly understood. Therefore, this study is to address whether the size, chemical and agronomic properties of a biochar DOM pool and its plant promotion effect would vary with the pyrolysis temperature and whether the DOMremoved biochars could be still effective on metal immobilization. The hypotheses included: (1) The size, abundance and composition of organic compound and inorganics, and thus the agronomic effect of the DOM pool of a biochar could be a function of pyrolysis temperature; (2) The extracted biochars could be effective on metal immobilization without at the cost of DOM removal, regardless of pyrolysis temperature. For these, wheat straw biochar was used with pyrolysis at temperature sequence and the hot-water extract of biochars was chemically characterized and pot culture tested, in line with a soil amendment experiment of the extracted biochars. Finally, the study is to provide an

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insight to separate valuable pools from biochar for profit-raising use of biochar products in agriculture. 2. Materials and methods 2.1. Biochar preparation and separation of DOM Wheat straw biomass was collected from a local farm in Yixing Municipality, Jiangsu Province, China. After air-drying at room temperature, the biomass was chopped and pyrolyzed at temperature respectively of 350 °C, 450 °C and 550 °C under oxygen-limited condition in a bench scale pyrolyzer (SSBP-5000A, China). The pyrolyzer consisted of a biomass feeder, a closed and electrically heated reactor, a condenser for bio-oil collection and outlets for gas, liquid and biochar collection (Bian et al., 2016b). For biochar production, 4 kg of biomass was fed into the reactor and heated in a rate of 3 °C min−1 to reach a target temperature for 2 h. Compressed nitrogen (N2) was pumped into the reactor to maintain anoxic conditions during the pyrolysis process. After cooling to room temperature, biochar was ground to pass a 1 mm sieve. The bulk biochar was coded as BBC350, BBC450, and BBC550 representing pyrolysis temperature at 350 °C, 450 °C, and 550 °C, respectively. A DOM pool of the produced biochar was separated as per Lou et al. (2016). In detail, 10 g of a biochar was added into 200 mL distilled water and heated in a 100 °C water bath for 3 h. Subsequently, the mixture was shaken at 160 rpm for 24 h at room temperature before filtering through a 3 μm filter paper (Grade 44 Whatman). The obtained biochar extract (BE) was stored in a refrigerator at 4 °C prior to analysis. Hereafter, the BE was coded as BE350, BE450, and BE550 and the extracted biochar (DOM-removed biochar) as EBC350, EBC450, and EBC550, respectively. 2.2. Characterization of DOM and the extracted biochar Physico-chemical properties were analyzed following our previous studies (Bian et al., 2016b; Lou et al., 2016) and the procedure was supplied in supplementary materials. A portion of BE was filtered through a 0.45 μm PES-filter (Millipore, #SLHP033RB) and diluted by 100 x and the pH value adjusted to 7.0 with a 30% HCl solution. The resultant solution was injected to a Liquid Chromatography-Organic Carbon Detection (LC-OCD, DOC Labor, Germany) for organic fraction characterization (Taherymoosavi et al., 2016). The freeze-dried extract was lyophilized at −70 °C using a MODULYOD-230 unit (Thermo Electron Corporation, USA) and examined using XPS, and JOELARM scanning transmission electron microscope with incorporate electron energy loss spectroscopy (EELS) and X-ray energy dispersive analyzer (EDS) (Archanjo et al., 2017). The bulk biochar and biochar after treatment with hot water was examined using FEI NanoSEM 450 scanning electron microscope and EDS analysis was undertaken. Details of equipment and methods were given in Archanjo et al. (2017). 2.3. Pot experiment with DOM (BE) for plant growth A topsoil sample was collected in a vegetable farm from suburb of Nanjing. After shipping to the lab, the soil sample was air dried and ground to pass a 2 mm sieve. The contents of soil organic carbon (SOC), N, P, and K as well as soil pH were determined following the method described by Lu (2000). To determine the total concentration of toxic metals both of soil and biochar, a portion (0.5 g) of oven-dried soil/biochar sample was digested with a mixture of HF-HClO4-HNO3. The soil sample was also extracted with a solution (1:5, w/w) of 0.01 M CaCl2 solution or of 0.005 mol L−1 DTPA for determination of available pool of heavy metals. Metals in all the digestions were detected with a graphite furnace atomic absorption spectrometry (A3, Persee Analytical Instruments, China). The soil properties were detailed in Table S1.

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A pot of 20 cm in height and 25 cm in diameter was used for growing Chinese cabbage in a greenhouse. A portion of topsoil (3 kg dry equivalent) was placed in a pot and 0.6 g N, 0.45 g P2O5 and 0.6 g K2O was added respectively in the form of urea, mono-ammonium phosphate and potassium chloride. The soil and fertilizer were thoroughly mixed and homogenized and supplied with water to attain 30% of field water holding capacity. Four days after, 20 seeds of Chinese cabbage (Brassica rapa subsp. chinensis) were evenly sown on soil surface and five seedlings in similar size retained in each pot 10 days after germination. A portion of a BE (biochar DOM) was diluted by 50 times and sprayed on the cabbage leaves twice a week till harvest (14 times, each 100 mL per pot). Water instead of BE solution, in same amount, was sprayed for the control. The experiment was performed in four replicates and all pots arranged in a randomized complete block design. The total content of macro and micronutrients applied to each pot is given in Table S2. The aboveground shoot biomass from all 5 plants in a pot was collected as a bulk plant sample. After washing with deionized water and weighing for biomass yield, one portion was stored in a refrigerator at 4 °C prior to chemical analysis, and the remaining portion was ovendried at 105 °C for 15 min, followed by 65 °C for another 12 h (Lu, 2000). The dried samples were ground to pass through a 1-mm sieve and homogenized for further chemical analysis. For cabbage quality analysis, a portion of fresh shoot biomass was milled and blended using a plant crusher. For N, P and K measurement of the shoot biomass, 0.5 g of dried sample was wet-digested with H2SO4-H2O2 mixture and analyzed as outlined above. Another portion was digested with HNO3HClO4 (4:1, v:v) mixed solution and contents of metals determined using methods outlined above. Moreover, the content of vitamin C, soluble sugar, protein and nitrite was measured using the protocols described by Wang (2006). The total RNA was extracted from the newest leaves of Chinese cabbage using Trizol (Invitrogen, Waltham, MA, USA) according to the manufacturer's instructions. The real-time quantitative reverse transcriptionpolymerase chain reaction (qRT-PCR) was selected to quantify the expression levels of the genes related to nitrate reductase (BcNR) and glutamine synthetase (BcGS) of Brassica rapa subsp. Chinensis. The first-strand cDNA synthesized with the PrimeScript® RT reagent kit (TaKaRa, Kusatsu, Japan) was used as template for qRT-PCR analysis (Applied Biosystems 7500 Fast Real-Time PCR System, LifeTechnologies™, Carlsbad, USA). A 112 bp internal standard fragment of Chinese cabbage Actin was amplified from the samples. The primer sequences for Actin are 5′-GTTGCTATCCAGGCTGTTCT-3′ (sense) and 5′-AGCGTGAGGAA GAGCATAAC-3′ (antisense). For amplifying the target genes as per Sun et al. (2008), the primer sequence for BcNR was BcNR (EU662272), forward 5′-ACGACGAGGACGAGAGCC-3′ and reverse 5′-CAGTTGTCAGCCGT GGATTC-3′; and for BcGS was BcGS (EU239243), forward 5′-CCGTGA CATTTCAGATGCTC-3′ and reverse 5′-TGCTTCGATTCCTACGCTC-3′. The thermal cycling program was: 2 min denaturation at 95 °C for amplification and quantification, 40 cycles of 10 s at 95 °C, 20 s at 58 °C (the annealing temperature varied depending on the gene specific primers), 20 s at 72 °C; 10 min extension at 72 °C and then a melt curve from 60 °C to 95 °C. 2.4. Experiment of metal immobilization with DOM-removed biochar The DOM-removed biochar (Subsection 2.1) was air dried and homogenized before soil amendment. A topsoil (0–15 cm) sample was collected from a paddy field contaminated with heavy metals (31°24′28.88″ N and 119°41′36.43″ E) since the 1970s. Wheat straw was collected from an area nearby that was not contaminated by heavy metals. Total concentration of Cd, Pb, Cu, and Zn of the sample was 41.6 mg kg−1, 655.1 mg kg−1, 89.7 mg kg−1, and 522.5 mg kg−1, respectively. After air-drying at room temperature, the soil sample was ground to pass a 2 mm sieve and homogenized before treatment with the bulk biochar (BBC) and extracted (DOM-removed) biochar (EBC). In detail, a portion of 100 g (dry equivalent) soil was placed in a 200 mL plastic jar, mixed

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Table 1 Physicochemical properties of biochar. BC350

BC450

BC550

Proximate analysis (%) Ash 20.3 VM 66.8 Fixed C 13.0

Feedstock

16.2 34.7 49.1

20.4 25.9 53.7

18.6 14.0 67.4

Ultimate analysis (%) C H N O N (g kg−1) P (g kg−1) K (g kg−1) Cu (mg kg−1) Zn (mg kg−1) Ca (mg kg−1) Mg (mg kg−1) Fe (mg kg−1) Mn (mg kg−1) pH CEC

59.8 3.8 1.6 18.6 7.7 3.4 11.3 19.8 63.8 8393.4 3041.7 2375.0 335.2 8.3 32.5

62.2 3.0 1.6 12.9 10.0 4.5 12.2 21.0 81.0 6506.4 2902.8 2560.0 422.0 9.1 23.5

67.4 2.7 1.5 9.8 9.1 5.6 24.5 22.3 82.9 9423.1 4243.1 3483.7 433.5 9.5 11.7

41.6 5.3 1.6 31.2 5.7 3.0 6.9 5.6 20.7 2378.2 1105.6 781.7 142.4 – –

BC350, BC450 and BC550: biochar produced at 350 °C, 450 °C and 550 °C, respectively.

with 2.0 g biochar and homogenized before the moisture adjusted to 60% of the water holding capacity (WHC). The treated jars were incubated at room temperature under a consistent soil moisture at 60% of soil WHC throughout one year. Moisture content was weekly adjusted by adding distilled water to maintain a constant mass. At the end of incubation, all soil samples were taken out from the jars and processed for lab analysis (outlined in Subsection 2.2). 2.5. Data processing and statistics All the data were given as mean ± standard deviation. Differences between biochar samples and treatments were analyzed by ANOVA using Tukey's test for means comparison (p b 0.05). All statistical analyses were carried out using SPSS, version16.0 (SPSS Institute, USA, 2007). 3. Results and discussions 3.1. Variation of biochar property with pyrolysis temperature The results of the ultimate analysis, proximate analysis and ash analysis for the feedstock and biochars are listed in Table 1. Clearly, the chemical composition of biochar varied with pyrolysis temperature. There was a decrease in volatile matter, H and O contents of biochar as the temperature increased from 350 °C to 550 °C. As shown in previous studies (Lin et al., 2012; Wu et al., 2012; Taherymoosavi et al., 2016), higher pyrolysis temperature resulted in greater decomposition of lignocelluloses and in releases of lower molecular weight byproducts. Enders et al. (2012) noted that as temperature increased, the volatile and N content of the biochar decreased while content of fixed carbon, metals and nonmetals (ash) increased. The decrease in H/C ratio reflected an increase in the aromaticity and stability of the organic carbon in biochar (Hale et al., 2012). Thermo-chemical conversion

of the raw feedstock also led to a significant increase in the pH value from 8.3 in BC350 to 9.5 in BC550, which is an effect of the increase in calcium carbonate and other alkaline salts being present in biochar (Prakongkep et al., 2015). 3.2. Variation of pool size, mineral and organic composition of biochar DOM with pyrolysis temperature The data of extracts (separated DOM fractions) of the produced biochars are presented in Table 2. Clearly, the content of DOC, N, P, Mn, Ca, and Mg was significantly higher in the BC350 than in BC450 and BC550. A DOM pool size was as large as 4% of biochar pyrolyzed at 350 °C while decreased to 2% of biochar pyrolyzed at 550 °C. This confirmed the observation of larger pool size in high-temperature biochars than in low temperature biochars from sawdust (Lin et al., 2012) and greenhouse waste (Graber et al., 2014). All the macronutrient of N and P and the meso- and micro-nutrients followed the trend of DOC except for K, which was not markedly changed. This could suggest that lower pyrolysis temperature could provide better removal from biochar and enrichment of beneficial nutrients along with DOC in the extract (particularly in BC350). These could help the extract of BC350 to play a significant role in soil nutrient supply and biological activity when use in agriculture. Fig. 1 presented the data of total OC and carbon groups derived from LC-OCD measurement of the biochar extracts as the separated DOM pool. Total OC content was 691 mg L−1 for BE350 but decreased dramatically to only 97 mg L−1, with the carbon groups composition significantly altered with increasing pyrolysis of the biochar. With increasing pyrolysis temperature, the content of hydrophobic carbons together with humics and building blocks decreased in arithmetic series, but those of biopolymers and LMW molecules decreased in geometric progression. This trend was reflected by the arithmetic increase in the abundance of hydrophobic carbons and the geometric decline in the hydrophilic carbons. As shown in Table S3, while the abundance of biopolymers with molecular weight N20 kDa (including polysaccharides, proteins, and amino sugars) was low in all the samples, its abundance was not seen changed with pyrolysis temperature. However, the abundance of low molecular weight (LMW) acids (protic organic acids) and the ratio of acids to neutrals of LMW carbons (alcohols, aldehydes, ketones, sugars and LMW amino acids), and the ratio of biopolymers and LWM acids to hydrophobic carbon showed a sharp decline with increasing pyrolysis temperature. Clearly, among the biochar extracts, BE350 was not only in TOC concentration but also in the abundance of low molecular weight (LMW) organic acids and the ratio of acids to neutrals of LMW carbons, and the ratio of biopolymers and LWM acids. Also, dissolved organic nitrogen was only detected in the humics with the highest concentration being a factor of 30 times higher in the BE350 (3 ppm) compared with 0.06 ppm and 0.17 ppm in BE450 and BE550, respectively (Table S4). Under pyrolysis at low temperatures, polysaccharides from cellulose and hemicellulose depolymerize to mainly form low molecular weight organic compounds (Lin et al., 2012). The humic-like fraction, similar in structure and molecular weight to humic and fulvic acids from soil, could contribute in part to the cation exchange capacity of biochar (Table 1). As addressed by Sun et al. (2017), the dissolved humic-like supramolecular materials from maize straw biochar could deliver

Table 2 Elemental content of biochar extracts. Sample

pH

DOC

N

K

(mg kg−1 of biochar) BE350 BE450 BE550

7.9 ± 0.1b 8.3 ± 0.1a 8.5 ± 0.0a

40.40 ± 2.11a 32.79 ± 6.36b 19.20 ± 2.16c

1.55 ± 0.04a 1.38 ± 0.03b 0.54 ± 0.02c

P

Ca

Mg

Mn

Cu

Zn

Fe

279 ± 4a 211 ± 8b 80 ± 12c

12.8 ± 0.20a 5.23 ± 0.38b 4.04 ± 0.40b

2.3 ± 0.5a 1.3 ± 0.2b 1.5 ± 0.4ab

4.7 ± 0.5a 8.0 ± 0.4a 5.6 ± 0.3a

0.55 ± 0.01b 0.23 ± 0.03b 1.23 ± 0.18a

(μg kg−1 of biochar) 22.86 ± 0.30b 24.84 ± 0.60a 25.98 ± 0.30a

499 ± 85a 297 ± 20b 197 ± 34c

2432 ± 60a 784 ± 51b 603 ± 73b

Values are mean ± standard deviation (n = 3). Different letters in a single column indicate a significant difference between the BEs (p b 0.05). BE350, BE450 and BE550: extract of biochar produced at 350 °C, 450 °C and 550 °C, respectively.

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pyrolyzing temperature (Table S5). Using the NIST library, 63 compounds were identified in BE350 while 45 and 32 compounds respectively in BE450 and BE550. Graber et al. (2015) noted that these soluble organic components on biochar surface could have a direct influence on the abundance of various micro-organisms and on plant's ability to take up specific nutrients and resist pathogenic disease. In this study, 27 compounds were detected only in BE350. Among these compounds, 6-epi-shyobunol, Hexadecanoic acid, and Hexadecane had been associated with antimicrobial activity (Bonaventure et al., 2003; Rubalcava et al., 2007; Preethi et al., 2010); Furan, 2,5-dimethyl, Dodecane, and Undecane was identified to play an important positive role in plant growth promotion (Farag et al., 2006; Reda et al., 2017). 3.3. Microscopic structure of freeze-dried DOM from biochars with varying pyrolysis temperatures

Fig. 1. LC-OCD quantitative analysis of dissolved organic carbon fraction of biochar extract.

bioactive molecules to boost plant germination and growth. As seen in the study by Lou et al. (2016), LMW acid and LMW neutrals could be beneficial for soil microbial community and plant root growth. In a study of compost extracts (Valdrighi et al., 1996), biological activity of organic substances in compost depend on their molecular dimension, with the LMW portions of the extracts being the most active. Decreasing numbers of organic compounds and their concentrations were detected putatively by GC–MS in the DOM with increasing

STEM/EELS/EDS analysis indicates existence of tiny biochar particles in size b3 μm in the freeze-dried DOM fraction (biochar extract). Fig. 2 illustrates a typical biochar particle that has a range of submicron inorganic compounds/minerals and organic compounds around its surface. EDS spectra that the inorganic particles have a range of elements including K, Si, Al, P, and a small concentration of Fe. The EELS spectrum was used to determine the type and relative intensity of different C and C/ O functional groups. The EELS spectrum of Fig.2 shows peaks at approximately 298 eV and 291 eV which indicates that the principle carbon compound in the agglomerate is CaCO3. Peaks at between 286 eV and 287.5 eV indicated the presence of C\\C and C\\O compounds, and from 288 eV to 289.5 eV was C_O and COOH. Compounds were binding

Fig. 2. Scanning transmission electron microscopy and electron energy loss spectroscopy of freeze-dried biochar extract produced at 350 °C. a, Secondary electron image of the extract produced at 350 °C; b, C K edge spectra of biochar; c, High angle area dark field (HAADF) image; d, EDS spectrum of the particle. The Cu is from the grid not the particle.

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BE350

BE550

Fig. 3. SEM images of the biochar extracts. BE350, the extract of biochar produced at 350 °C; BE550, the extract of biochar produced at 550 °C.

the mineral particles in the agglomerate and had been identified using LC-OCD and the GC–MS. Other particles were agglomerations of many small particles with varying concentrations of organic and inorganic compounds or specific minerals with a wide range of compositions (Fig. S1). These agglomerates, appearing porous, could have formed during the freeze-drying process. Fig. S1(d) is a Fe EELS spectrum of the bright area in Fig. 2c. The EELS spectrum indicates that agglomerated iron oxide particles, probably being composed of ferrihydrite, Fe3O4, and Fe2O3. Fig. S2 illustrates a porous agglomerate consisting of a mixture of sub 1–2 nm SiO2 and Fe/O particles bound together with organic molecules. Data in Fig. 3 could suggest a significant difference in both the morphology and composition of the DOM free biochars between different pyrolysis temperatures. Results of SEM/EDS analysis of the freeze-dried biochar extracts (Fig. 3) shows that most of the agglomerates have a low carbon content

and a high mineral content. BE550 could have a higher concentration of Na, Si and P mineral particles with dimensions b1 μm. Table 3 clearly shows a difference in the concentration and type of functional groups on the surface of the crushed freeze-dried extract. BE350 contains highest amino-acid N. BE550 alone had a small concentration of C-NH4/NO, probably associated with N in the carbon matrix of the biochar. BE550 had a much higher concentration of nitrates that probably were held tightly in sub ten-nanometer pores (as illustrated in Fig. S2) as has been found by Kammann et al. (2015) and Joseph et al. (2016). Amino type N (N-COOH) was detected only in the BE450 and BE350, suggesting potential transformation and escape of biomass N during pyrolysis at temperatures over 450 °C. The difference in the type and concentration of O/N functional groups can change the ability of the biochar to bind heavy metals (Uchimiya et al., 2011; Sun et al., 2017).

Table 3 C 1s, N 1s, O 1s, S 2p and Si 2p bonding state and its relative atomic percentage on the freeze-dried biochar extracts surfaces as determined by X-ray photoelectron spectroscopy (XPS). Sample

BE350 BE450 BE550

N1s B

N1s C

C1s A

C1s B

C1s C

C1s D

O1s A

O1s B

S2p

Si2p

Amino Acids

N1s A N-COOH

C-NH4/NO

Nitrate

C=C/C-H

C-O

O-C-O

O=C-O(N)

C=O

COO

Sulphate

Si–O–C

2.19 2.81 1.9

0.16 0.34 n.d

n.d n.d 0.84

0.27 0.42 1.71

41.32 31.68 26.21

16.07 13.96 6.61

3.78 2.75 5.7

5.15 5.06 n.d

16.07 13.96 6.61

17.01 22.24 24.93

0.58 1.79 2.54

0.87 2.79 7.9

n.d. non-detected. BE350, BE450 and BE550: extract of biochar produced at 350 °C, 450 °C and 550 °C, respectively.

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Table 4 Effect of biochar extract spraying on yield and quality of Chinese cabbage. Treatments

CK BE350 BE450 BE550

Fresh yield

Soluble sugar

Soluble protein

Vitamin C

Nitrate

(g pot−1)

(g kg−1)

(g kg−1)

(mg kg−1)

(mg kg−1)

49.2 ± 12.5c 93.1 ± 6.0a 77.6 ± 4.7ab 60.3 ± 7.1bc

2.24 ± 0.24c 4.10 ± 0.38a 2.93 ± 0.08b 2.53 ± 0.09bc

8.56 ± 0.41b 9.06 ± 0.14a 8.62 ± 0.62ab 8.36 ± 0.58ab

266.6 ± 17.2b 308.8 ± 15.5a 271.4 ± 10.2b 261.9 ± 12.2b

1043.2 ± 64.4a 687.85 ± 26.8c 807.31 ± 36.9b 1016.08 ± 45.9a

Values are mean ± standard deviation (n = 4). Different letters in a single column indicate a significant difference between the BEs (p b 0.05). BE350, BE450 and BE550: extract of biochar produced at 350 °C, 450 °C and 550 °C, respectively.

3.4. Variation of plant promotion effect of biochar extract with pyrolysis temperatures Data of cabbage yield, leaf quality indices of soluble sugar, soluble protein, vitamin C and nitrate content under biochar extracts treatments in pot experiment are presented in Table 4. Cabbage yield was significantly increased under BE spraying with BE 350 and BE 450 but not significantly changed with BE 550. Compared to the control, the content of soluble sugar and protein, and vitamin C of cabbage was significantly increased under BE350 but unchanged under BE 450 and BE550. Whereas, nitrate content was unchanged with BE550 but decreased greatly under BE350 and moderately under BE450. However, the gene expression both of nitrate reductase and glutamine synthetase was seen with foliar spray of BE350 only (Fig. S3). Data in Table S6 showed no remarkable change in the major nutrient in cabbage leaf with BE spraying treatment. However, BE spraying caused changes in the heavy metals content of the cabbage leaf (Table 5). Cabbage leaf concentrations of Cd and Pb decreased while Zn and Mn more or less increased, with BE spraying at increasing pyrolysis temperature. Data of DTPA-extractable pool of metals in soil samples collected at harvest evidenced a significant immobilization of Cd and Pb by over 25% under all BE treatments (Table S7) although the soil was metal contaminated as soil concentration of Cd (1.1 mg kg−1) was far beyond the guideline limit of 0.3 mg kg−1 for Chinese agricultural soils (MEE, 2018). In this study, first of all, the major and micronutrients of cabbage leaf under spraying treatments were not remarkably affected by the BEs, in which these nutrient contents generally decreased with pyrolysis temperature, particularly of N, P, Ca and Mg (Table 2). Particularly Nitrate and Mn content in the treated cabbage leaf was even the reverse trend to those in the BEs. Again, the changes of Cd and Pb content in leaf was not fully explained with the soil immobilization (all BE treatments reduced their availability, Table S7) or by dilution with increased biomass (the metal decrease extent much smaller than yield increase under BE 350). These could indicate that some other mechanisms other than their content in soil or in BEs was in action. Among these, the reduction of leaf nitrate content was seen negatively following the trend of atom abundance of nitrate bonds but positively following the trend of ratio of amino acids to nitrate and organic N to nitrate, on surface of the BE particles (Table 3). This seemed overweighted the role the gene expression both of nitrate reductase and glutamine synthetase, which was seen with foliar spray of BE350 only (Fig. S3). Increased input of nitrate, a dominant N source for Chinese cabbage (Ullrich, 2002), with spraying of BE450 and particularly BE550 poor in organic N could have negated the reduction in plant. Also, the reduction could not be limited for the smaller abundance of amino acids, proteins, and nucleic acids to incorporate the produced NH4+ (Tang et al., 2013). In contrast, the most significant reduction of nitrate under BE350 could suggest a multiple mechanisms responsible. BE350 was poor in nitrate but high in organic N to nitrate ratio as well as the plant tissue rich in soluble protein treated. The increased gene expression of nitrate reduction enzymes only with BE 350 could support high reduction capacities of DOM from biochar produced at low temperature (Graber et al., 2014). For these, spraying of BE350 reduced leaf

nitrate to 687 mg kg−1, a level below 785 mg kg−1 recommended for vegetables in China (Zhou et al., 2000). Many studies addressed the potential role of the nanoparticles possibly existing in BE extracts in promoting plant growth (Gu et al., 2016) via translocation through plant stomata for stimulating plant metabolic activities (Hatami et al., 2016). However, the qualitative information shown with XPS and STEM analysis could not allow an analysis with certainty of the effects of the spraying of the BEs. Here it is still not clear if nanoparticles existed in DOM affected the Cd accumulation and toxicity as argued by Wang et al. (2015) for increased nutrients uptake and antioxidant capacity in plants with nano-particles. Nevertheless, it is worthy to note that cabbage yield increase was arithmetic but of nutritional quality improvement (soluble protein and Vc as well as leaf Cd) was in geometric trend in this study. Interestingly, the yield trend (89.2%, 57.7% and 22.6% under BE350, BE450 and BE 550 respectively) was closely following the trend of DOC concentration and number of molecules identified in it, while the quality trend closely followed that of molecular abundance of LWM organic acids and the abundance ratio of LWM acids to LWM neutrals, and of biopolymers and LWM acids to hydrophobics of the BEs used (Table S3). In a similar study comparing BEs from two biochars pyrolyzed at 450 °C (Lou et al., 2016), cabbage yield increase was 41.7% and 62.5% while increase in Vc content was 68.2% and187.9%, respectively with wheat and maize biochar BE. The BE they used had a DOC concentration of 566 and 303 g L−1, with total number of molecules of 16 and 21, but a hydrophobic carbon abundance of 0.096 and 0.097 respectively for wheat BE and maize BE. However, the molecular abundance of LWM acids, the ratio of LWM acids to LWM neutrals, and of biopolymers and LWM acids to hydrophobic carbon was respectively 0.007, 0.091 and 0.229 for wheat BE, compared to 0.030, 0.455, and 0.824 for maize BE. Their results demonstrated that cabbage quality improvement did matter with the molecular abundance of LWM acids and the ratios but cabbage yield increase seemed to matter with total molecule number though unrelated to DOC concentration of BE. Therefore, the present study revealed that plant quality responded rather than the abundance bioactive molecules of LWM organic acids and biopolymers and their ratio to hydrophobic carbons than DOC pool size, which seemed control the yield response. Thus, BE350 provided the significant improvement of yield and much greater on quality of vegetable plant as well as a reliable reduction in the leaf nitrate and toxic metals particularly of Cd.

Table 5 Change in heavy metals content of Chinese cabbage under the biochar extract spraying treatments. Treatments

Cd (mg kg−1)

Pb (mg kg−1)

Cu (mg kg−1)

Zn (mg kg−1)

CK BE350 BE450 BE550

0.097 ± 0.006a 0.046 ± 0.006c 0.055 ± 0.005bc 0.063 ± 0.005b

0.057 ± 0.007a 0.037 ± 0.001b 0.037 ± 0.002b 0.039 ± 0.001b

0.38 ± 0.02b 0.45 ± 0.01a 0.34 ± 0.01c 0.34 ± 0.01c

2.13 ± 0.10ab 1.97 ± 0.06b 2.08 ± 0.09ab 2.26 ± 0.08a

Values are mean ± standard deviation (n = 4). Different letters in a single column indicate a significant difference between the BEs (p b 0.05). BE350, BE450 and BE550: extract of biochar produced at 350 °C, 450 °C and 550 °C, respectively.

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Table 6 Changes in soil pH and CaCl2 extractable metals with bulk biochar (BBC) and extracted biochar (EBC). Treatments

Control BBC350 EBC350 BBC450 EBC450 BBC550 EBC550

pH

Cd

Pb

Zn

Cu

(H2O)

(mg kg−1)

(mg kg−1)

(mg kg−1)

(mg kg−1)

4.87 ± 0.11d 6.67 ± 0.12a 5.25 ± 0.20c 6.58 ± 0.05a 5.29 ± 0.20c 6.52 ± 0.08a 5.77 ± 0.04b

2.71 ± 0.14a 1.34 ± 0.09b 1.28 ± 0.06b 1.50 ± 0.05b 1.58 ± 0.12b 1.29 ± 0.06b 0.95 ± 0.07c

0.22 ± 0.03a 0.06 ± 0.01b 0.06 ± 0.01b 0.08 ± 0.01b 0.06 ± 0.02b 0.06 ± 0.01b 0.05 ± 0.01b

1.24 ± 0.04a 0.56 ± 0.06 cd 0.49 ± 0.05de 0.75 ± 0.07b 0.70 ± 0.07bc 0.58 ± 0.03bcd 0.37 ± 0.03e

0.24 ± 0.02c 0.53 ± 0.06a 0.16 ± 0.03d 0.33 ± 0.02b 0.14 ± 0.02d 0.38 ± 0.01b 0.10 ± 0.02d

Values are mean ± standard deviation (n = 3). Different letters in a single column indicate a significant difference between treatments (p b 0.05). BBC350, BBC450 and BBC550: bulk biochar produced at 350 °C, 450 °C and 550 °C, respectively; EBC350, EBC450 and EBC550: extracted biochar produced at 350 °C, 450 °C and 550 °C.

In the present study, whereas, treatment of BE350 caused a significant but moderate increase (by 18%) cabbage leaf Cu despite a decreased under other BEs (Table 5). It was recently noticed that biochar-borne DOM had large binding affinities and the complexation capacities of Cu (Wei et al., 2019). Higher content of DOM from low temperature biochar would alter copper mobility in soil due to its large copper binding capacities (Wei et al., 2019; Huang et al., 2019). Therefore, the environmental risk of Cu caused by biochar derived DOM should be given attention while using biochar extract as liquid fertilizer in vegetable production. Of course, significant Cd reduction in cabbage leaf by 53% suggested BE350 could be still an option to use for vegetable production as Cd exposure risk from dietary intake had been given much greater attention in China and abroad (Chaney et al., 2004). Further research would deserve to determine the relative effect of the foliar spray on the leaves compared to the adsorption of the spray by the soil. 3.5. Variation of metal immobilization of DOM-removed biochar with pyrolysis temperature The changes in soil pH and CaCl2-extractable fraction of heavy metals under bulk and DOM-removed biochars (extracted biochars) treatments are given in Table 6. Soil pH was significantly elevated with amendment of both FBC and EBC, with no difference between pyrolyzing temperatures of a single biochar. Whereas, EBC caused a smaller pH increase than FBC. The amendment significantly immobilized soil Cd (by over 70%) and Pb (by over 50%), regardless of extraction and pyrolyzing temperature. This confirmed that amendment of DOM-removed biochar was effective on immobilizing toxic metals in soils, via surface adsorption and precipitation due to its porous structure and oxygen-functional groups on surface as well as its alkaline reaction (Inyang et al., 2016). In comparison to the control, the soil Zn was immobilized by 25% to 30% with the biochar amendment, regardless of extraction and pyrolyzing temperature. In contrast, soil extractable Cu was increased under FBC but significantly decreased with EBC treatments. Beesley et al. (2010) reported a significant increase in both available soil Cu and As and DOM when unextracted hardwood-derived biochar was added to a polluted soil. Similarly, soil extractable Cu was significantly increased with addition of chicken manure biochar high in leachable organic carbon (Park et al., 2011) for Cu concentration closely associated with hydrophilic fraction in DOM (Gondar and Bernal, 2009). Huang et al. (2019) argued the environmental risk of Cu due to increase in DOM hydrophobicity when applying biochar to polluted soil. Obviously, the present study demonstrated the privilege of using extracted (DOM-removed) biochar for heavy metal immobilization in soil.

were polluted by Cd (MEP and MLP, 2014). Furthermore, excessive application of nitrogen fertilizers and continuous cropping with vegetable crops has resulted in low quality and high nitrate in crop plants (Tang et al., 2016). The present study indicated a potential value of using biochar to tackle both issues. Our previous studies proved that wheat straw biochar soil amendment at 20 t ha−1 could significantly immobilize soil Cd and reduce rice grain Cd content to a safe level (Bian et al., 2013; Bian et al., 2014; Chen et al., 2016). The results of this study indicate that 20 tons wheat straw biochar could not only remediate one hectare heavy metal polluted farm land but its extracts also may use to improve the growth and quality of nearly 6 ha of Chinese cabbage. A recent field study found that the average yield increase of cabbage after applying foliar spray was 30% (P. Wang et al., 2018). It is reported that the net profit of cabbage in Nanjing is about USD 5000 per ha −1 yr −1 (Li et al., 2016). Using biochar and foliar spray farmer will increase the profit by USD 1500 per ha−1 yr−1. Thus, biochar would become more profitable than lime as a means of immobilizing heavy metals.

4. Conclusions Taking wheat residue as a feedstock, pyrolysis temperature affected the size, molecular abundance and agronomic performance of plant growth but not the performance for metal immobilization. Compared to pyrolyzed at 450 °C and 500 °C, the biochar extract produced at 350 °C had a larger DOC pool and abundance of low weight molecules and higher ratio of potentially bioactive low weight organic acids to hydrophobic substances, exerting a more significant improvement of plant yield and quality. Whereas, the effectiveness of immobilizing heavy metals of biochar was regardless of extraction and pyrolysis temperature. Consequently, biochar produced at 350 °C showed its greatest value for use of DOM extraction while could not negate its immobiliztion value. Therefore, valorizing crop production benefits from plant promotion and environment benefits from metal immobilization could allow a viable option to maximizing the economic efficiency of biochar industry, which had been urged by the state of China.

Acknowledgments This work was supported by the National Natural Science Foundation of China (41877096, 41877097, 41371298); and the Fundamental Research Funds for the Central Universities under grant nos. KJQN201671 and KYZ201713, and National Key Research and Development Program of China (2017YFD0200802).

3.6. Cost-beneficial issue of potential separation of biochar for agronomic use

Appendix A. Supplementary data

In China, approximately 26 million ha of agricultural lands were contaminated with heavy metals, and nearly 7% of total farmlands

Supplementary data to this article can be found online at https://doi. org/10.1016/j.scitotenv.2019.01.224.

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