Abstract
Production of liquid fertilizers containing nitrogenous nutrients and biostimulants from sewage sludge (SS-NB) has been attracting increasing attention due to its excellent fertilization effect and resource recycling attributes. To better understand the functional effects of nutrients and biostimulants in SS-NB on soil, the adsorption capacity and mechanism of straw biochar (SB) and wood chip biochar (WCB) for alkaline and neutral SS-NB components were investigated. The adsorption of total organic carbon (TOC) from alkaline and neutral SS-NB by WCB was 61.14% and 89.73%, respectively, higher than that by SB, which was 56.25% and 83.36%. Moreover, TOC from neutral SS-NB was more readily adsorbed, especially for fulvic and humic acids. SB had a strong adsorption capacity for calcium ions and nitrogen (TKN, nitrate N, protein, amino acid) and released large amounts of P. In addition, WCB and SB showed a strong affinity for macromolecules (proteins) and reducing substances (lignin and lipids) and excellent fixation ability for phytohormones and allelochemicals. However, WCB adsorbed more types of molecular substances than SB while maintaining a high immobilization rate. Analysis of the adsorption mechanism showed that surface amino groups of the biochar were involved in adsorption, while WCB had additionally high adsorption efficiencies through pore adsorption, hydrogen bonding adsorption and pore size-exclusion effects. The study revealed that biochar can be used as an efficient adsorption carrier for SS-NB to improve soil fertility management.
Graphical Abstract
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Highlights
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SB was better able to fix N (TKN, NO3−−N, proteins, amino acids) than WCB.
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More humic acid fluorescent substances from neutral SS-NB adsorbed on biochar.
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WCB and SB had excellent immobilization capacity for phytohormones and allelochemicals.
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WCB had higher adsorption efficiencies for N-, P-, and S-containing molecules.
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Hydrogen bonding and pore size-exclusion effect enhanced the adsorption of WCB.
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1 Introduction
The current annual output of sewage sludge in China is more than 70 million tons (80% water content) (Xiao and Zhou 2020). Activated sludge is a complex mixture of various types of microorganisms, apoptotic cells, organic and inorganic substances, and extracellular polymers, and it comprises 50% of proteins, 20% to 30% of humic acid, and 10% to 30% of carbohydrates (Wilen 1999). It has thus significant resource properties. In the context of resource recovery and sustainable agricultural development, the utilization of resource materials such as carbon (C), nitrogen (N), and phosphorus (P) in activated sludge for the production of organic molecules that promote plant growth has raised attention (He et al. 2015; Soobhany 2019; Tang et al. 2022a).
Alkaline thermal hydrolysis accelerates the rupture of activated sludge cells and the decomposition of extracellular polymer flocs, which can significantly increase the rate of protein solubilization (Liu et al. 2008; Cho et al. 2013). Sewage sludge-derived nutrient biostimulants (SS-NB), obtained through flash evaporation, solid–liquid separation, and concentration of the supernatant mixture, not only contains the basic nutrients N, P, and potassium (K), but also humic acids, polypeptides, proteins, and amino acids (Lu et al. 2021). It can achieve inactivation of pathogenic bacteria, removal of heavy metals, and stabilization of refractory organic matter (Dewil et al. 2006; Barber 2016; Wang et al. 2021). Studies have shown that humic and fulvic acids (Canellas et al. 2015), along with chitosan (Pichyangkura and Chadchawan 2015), plant or animal protein hydrolysis products (Colla et al. 2015), algal extracts (Battacharyya et al. 2015), and inter-root beneficial microorganisms (Ruzzi and Aroca 2015), are the main stimulant components. Stimulants improve N assimilation and C metabolism, increase growth hormone and gibberellin-like activities, and enhance antioxidant enzyme activities and secondary metabolite production, which can improve soil quality and ultimately enhance crop yield and quality (Cai et al. 2021; Ceccarelli et al. 2021). In addition, sludge contains phytohormone analogs and chemosensory substances that have good leverage effects in regulating plant nutrient uptake and tolerance to abiotic stresses (Cozzolino et al. 2016; Li et al. 2018). Although SS-NB, as a water-soluble nitrogen-containing liquid fertilizer, has great potential in agricultural applications (Hao et al. 2023, 2024), nutrient and stimulant substances tend to be trapped on the soil surface and lost with rainwater runoff during land use. Therefore, a biomass carrier is needed to enhance the distribution of nutrients and stimulant substances in the soil, and thus enhance uptake and utilization by crop roots. Biochar has received increasing attention due to its extensive agricultural benefits. Biochar shows excellent adsorption capacity, and studies have shown that biochar-based fertilizers have strong adsorption capacity for ammoniacal N and nitrate N after being applied to soil, which reduces the loss of N from soil and thus increases N availability (Mantovi et al. 2003). The presence of functional groups (hydroxyl and amino groups) on the surface of biochar can increase its hydrophilicity, which endows it with excellent properties for adsorption of organic matter and trace elements (Kasera et al. 2022). Biochar has also many benefits in improving soil quality. Studies have shown that biochar not only improves the attachment properties of soil microbial cells and promotes the growth of some specific groups of soil microorganisms (Thies and Rillig 2009), but also enhances the activity of the soil microflora and N-fixing capacity (Xiu et al. 2021). In addition, coupling of biochar with high C content and SS-NB with high N content can balance the C/N ratio, which plays an important role in improving plant growth efficiency and yield (Sanchez et al. 2004). Therefore, biochar appears to be an ideal carrier, and it is necessary to explore the adsorption characteristics and mechanism of biochar with respect to nutrients, organic molecules, and biostimulants in SS-NB so as to guide biochar SS-NB coupling to better utilize its functional role in soil.
In this study, straw biochar (SB) and wood chip biochar (WCB) were used to explore the adsorption characteristics of nutrients, organic molecules, and biostimulants in alkaline and neutral SS-NB. In addition, FT-ICR-MS was used to distinguish changes in the molecular composition of organics during adsorption at the molecular level, and changes in biostimulant substances during adsorption were determined using gas chromatography coupled to time-of-flight mass spectrometry (GC/TOF–MS). To better understand the adsorption of components and the related mechanisms, FTIR, BET, SEM and XPS were also used to discover the surface states and pore channels of the biochar. The findings will be conducive to promote the application of biochar and SS-NB in agricultural production and efficient management of soil fertilizer and soil quality.
2 Materials and methods
2.1 Preparation of materials
Sewage sludge-derived nutrients and biostimulants were obtained from an alkaline thermal hydrolysis practical project that treats 500 t d−1 of excess sludge (Shanxi Jinlian Environmental Technology Co., Ltd.). In this study, straw biochar (SB) and wood chip biochar (WCB) were selected to investigate their adsorption effect of SS-NB nutrients under alkaline and neutral conditions. The biochar was purchased from Pingdingshan Tanuo Environmental Protection Material Co., Ltd., Henan Province, China, and was obtained from straw and wood chips at a temperature of 450 ℃. The grain sizes of SB and WCB were 50–100 mesh and 200 mesh, respectively. The surface area and pore volume of SB were 762.93 m2 g−1 and 0.66 cm3 g−1, respectively, while the surface area and pore volume of WCB were 557.49 m2 g−1 and 0.40 cm3 g−1.
2.2 Batch adsorption experiments
To investigate the effect of contact time between SS-NB nutrients and biochar adsorbents, 1 g of SB and WCB were added to 300 mL of alkaline SS-NB (Dilute 800X, pH = 10.49) and neutral SS-NB (Dilute 800X, pH = 6.93), respectively, and then shaken at 25 °C and 180 rpm. Samples were collected at intervals of 1, 5, 10, 15, 60, and 240 min; 1 ml sample was collected each time and filtered through a 0.45-µm membrane. Total organic carbon (TOC) was used to represent the adsorption capacity of SB and WCB for SS-NB nutrients. The adsorption capacity was calculated as follows:
where C0 and Ct are the TOC concentrations at the initial time and time t (mg TOC/g), respectively, Qt defines the amount of TOC adsorbed by SB and WCB at time t (mg TOC/g), m represents the mass of SB and WCB (g), and V denotes the volume of the SS-NB solution (L). When adsorption reaches equilibrium, Ct is represented by the equilibrium TOC concentration Ce, and the equilibrium adsorption amount Qe is subsequently obtained. To investigate the effects of the SB and WCB dosage on the adsorption of SS-NB nutrients, 50 mL of alkaline and neutral SS-NB were mixed with SB and WCB at concentrations ranging from 0.2–8 g L−1, respectively, and shaken at 180 rpm for 24 h at 25 °C.
2.3 Nutritional component analysis
To study changes of nutrients in SS-NB solution after adsorption equilibrium with SB and WCB, 1 g of SB and WCB were mixed with 300 ml of alkaline and neutral SS-NB diluent (diluted 800 times), respectively, and the supernatant was used to analyze nutrient indices and molecular composition after natural precipitation for 48 h. Solution pH and conductivity (EC) were determined using pH meter (STARTER3100, OHAUS Instruments, Shanghai, China) and portable conductivity meter (Multi 3630 IDS, WTW Instruments, Munich, Germany), respectively. The SS-NB supernatant before and after adsorption was treated by using the microwave digestion method (Multiwave Eco, Anton Par, Austria), and mineral elements were determined by using inductively coupled plasma mass spectrometry (ICP-MS, PerkinElmer Optima 8300), with more details provided in a previous study (Hao et al. 2023). TOC was measured using a total organic carbon analyzer (TOC V CPH, Shimadzu, Japan). Molybdenum blue colorimetry was used to determine total phosphorus (TP) and phosphate (PO43−−P) (DR6000, HACH, Loveland, USA). Total kjeldahl nitrogen (TKN) was determined via the Automatic Kjeldahl apparatus (K9840, Hanon Instruments, Dezhou, China), and the conversion coefficient of crude protein was 6.25. In addition, analysis of ammonium and nitrate N was performed in accordance with standard methods (Rice et al. 2012). The SS-NB solution before and after adsorption was diluted with the same amount of trichloroacetic acid solution, filtered, and centrifuged, and finally, the content of free amino acids was determined (HPLC, Agilent 1100).
2.4 EEM-PARAFAC and FT-ICR-MS analysis
The three-dimensional fluorescence characteristic of SS-NB solution before and after biochar adsorption was analyzed using an RF-6000 analyzer (Shimadzu, Japan). SS-NB solution was diluted using ultrapure water to a final dissolved organic carbon concentration below 1 mg L−1, and the background fluorescence was deducted. An excitation wavelength (Ex) of 200–450 nm and an emission wavelength of 200–600 nm were used to determine the properties of dissolved substances in the sample solution. Regional integration of the PARAFAC model was achieved using MATLAB 2018b with the DOM Fluor Toolbox.
The molecular composition of SS-NB diluents was analyzed with Fourier transform ion cyclotron resonance mass spectrometry (FT-ICR-MS, Bruker, Germany) before and after biochar adsorption. To extract organic molecules from the SS-NB solution, a modified styryl-divinylbenzene polymer extraction column (500 mg in 6 mL, Bond Elut PPL, Agilent) was utilized in solid phase extraction (SPE) (Shi et al. 2020). The concentrated sample was analyzed in negative electrospray ionization (ESI) mode with a 9.4T FT-ICR-MS Bruker solariX (Bruker, Germany). The measurement accuracy was less than 1.0 ppm, and the molecular formula was 12C1H16O1‑3014N0‑1531P0‑232S0‑4 (Kind and Fiehn 2007).
2.5 Determination of phytohormones and allelopathic substances
Phytohormones and allelopathic substances in SS-NB were extracted according to previous reports on dissolved organic samples (Scaglia et al. 2015, 2017; Tang et al. 2022b). A weight of 0.4 g of SB and WCB was added to 30 ml of alkaline and neutral SS-NB dilutions (Dilute 200X), respectively, and stirred at 25 °C and 180 rpm for 24 h. After adsorption and standing for 24 h, the supernatant and the unadsorbed dilutions of SS-NB (alkaline and neutral) were used for the determination of phytohormones and allelopathic substances. Details on target substance extraction, GC/TOF–MS determination, and concentration quantification are provided in the Additional file 1: Text S1.
2.6 Adsorption mechanism analysis
To explore changes in the characteristics of SB and WCB before and after adsorption, the two types of biochar after adsorption equilibrium were dried for further analysis. The surface morphologies of biochar adsorbed were observed by scanning electron microscopy (SEM, ZEISS Sigma 300, Germany). A trace biomass sample was directly glued to the conductive adhesive, and gold was sprayed with Quorum SC7620 sputtering coater. Then the sample morphology was photographed with a ZEISS Sigma 300 scanning electron microscope with an accelerated voltage of 3 kV. Spectral properties were detected using a Fourier Transform infrared spectrometer (IRTracer-100, Shimadzu, Japan) with attenuated total reflection (ATR) (Pike Technologies Inc., MIRacle™ single reflection). Spectra were obtained in a wavelength range of 4000–520 cm−1 with 16 successive scans at a resolution of 2 cm−1. In addition, the surface composition and chemical state of SB and WCB were analyzed using an X-ray photoelectron spectrometer (Thermo Scientific K-Alpha) with an Al Ka radiation source (hv = 1486.6 eV at 12 kV and 6 mA under 5.0E-7 mbar). The binding energies were calibrated with reference to the C1s peak at 284.6 eV. Deconvolution of C1S, N1S, and O1S peaks was conducted using the Avantage software. The specific surface areas of SB and WCB were determined using an ASAP 2460 Surface area analyzer (Micromeritics, USA) at 77 K liquid N, and the samples were desorbed at 110℃ for 8 h before N2 adsorption. The total specific surface area of the materials was obtained by the BET method (Brunauer et al. 1938). The contents of C, H, N, and S in SB and WCB samples were determined by using an elemental analyzer (vario MICRO cube, ELEMENTAR, Germany).
3 Results and discussion
3.1 Adsorption capacity and efficiency
The sorption capacity of SB and WCB for TOC was investigated in alkaline and neutral SS-NB by contact time (Fig. 1a). The sorption of SB in alkaline and neutral SS-NB was consistent, reaching the highest value at 60 min. The adsorption capacity of SB in neutral SS-NB solution (64.48 ± 2.17 mg TOC/g) was 1.45 times higher than that in alkaline SS-NB solution (44.33 ± 1.67 mg TOC/g). Additionally, the adsorption capacity of WCB in neutral SS-NB solution (52.35 ± 3.53 mg TOC/g) was 1.35 times higher than that in alkaline SS-NB solution (38.82 ± 2.17 mg TOC/g). SB adsorbed 14.19−23.17% more TOC than WCB for both alkaline and neutral SS-NB. However, when the adsorption time reached 240 min, the adsorption capacity of WCB (43.10 ± 0.41 mg TOC/g) was higher than that of SB (38.98 ± 3.52 mg TOC/g) in alkaline SS-NB, while the adsorption capacity of WCB (60.31 ± 0.86 mg TOC/g) was comparable to that of SB (62.04 ± 1.95 mg TOC/g) in neutral SS-NB. The experimental results showed that WCB and SB were able to effectively adsorb more TOC in neutral SS-NB. The SEM results also showed that more substances were stacked on the surface of SB and WCB after adsorption in neutral SS-NB compared to alkaline SS-NB (Additional file 1: Fig. S1). A similar study confirmed that the surface of biochar has a positive charge at low pH, which results in more adsorption sites and favors the adsorption of organic pollutants (Ambaye et al. 2021). The adsorption capacity of SB decreased with an increase in adsorption time, which may indicate that SB only adsorbs TOC on its surface. In contrast, the adsorption capacity of WCB increased with increasing adsorption time, indicating that WCB not only adsorbs TOC on its surface, but that TOC also diffuses into pores (Yao et al. 2020). In addition, in order to further analyze the adsorption process, pseudo-first-order kinetics, pseudo-second-order kinetics and in-particle diffusion models were fitted to the data in Fig. 1a, as shown in Additional file 1: Table S1. The R2 fitted by the pseudo-first-order kinetic model and the in-particle diffusion model was low, and the maximum adsorption capacity predicted by the pseudo-second-order kinetic model was far from the actual value. The results showed that the adsorption process of TOC in SS-NB by biochar did not conform to the adsorption kinetic model, possibly because TOC represents a type of complex organic substance and the adsorption process of various organic substances is inconsistent. Therefore, the adsorption process of TOC does not show specific regular characteristics.
Adsorption capacity and efficiency. a Effect of contact time for SB and WCB on adsorption capacity of alkaline and neutral SS-NB; b Effects of the amount of SB on the adsorption capacity and removal rate of alkaline SS-NB; c Effects of the amount of WCB on the adsorption capacity and removal rate of alkaline SS-NB; d Effects of the amount of SB on the adsorption capacity and removal rate of neutral SS-NB; e Effects of the amount of WCB on the adsorption capacity and removal rate of neutral SS-NB; f The maximum adsorption capacity and maximum TOC removal rate of alkaline and neutral SS-NB by SB and WCB adsorption (f)
The effects of the WCB and SB dosage on adsorption in alkaline and neutral SS-NB are shown in Fig. 1b–e. With an increase in the WCB and SB dosage, the TOC removal from SS-NB increased, while the adsorption capacity of the adsorbents decreased. Therefore, the growth rate of the removal efficiency gradually slowed down and finally stagnated. The result is similar to that of adsorption of DOC in biotreated coking wastewater by chitosan modified straw biochar (Shi et al. 2020). This may be because at a constant SS-NB concentration, higher WCB and SB dosages would provide excess adsorption sites that are not utilized (Shi et al. 2020). The stability of the maximum removal efficiency indicates that some substances in SS-NB could not be adsorbed efficiently. Under the same experimental conditions, the TOC removal rates of WCB and SB in neutral SS-NB were 89.73% and 83.36%, respectively, which were higher than those of WCB (61.14%) and SB (56.25%) in alkaline SS-NB. In addition, the TOC removal rates of WCB in alkaline and neutral SS-NB were higher than those of SB (by 7.64−8.70%). These results imply that a neutral environment is more conducive to SS-NB adsorption on biochar than an alkaline environment. The significantly higher adsorption efficiency of WCB over SB for SS-NB was most likely due to differences in the surface structure and pore channels between the two types of biochar. It is thus necessary to explore the effect of structural differences of biochar on the adsorption of nutrients in SS-NB.
3.2 Nutrients adsorption characteristics
3.2.1 Mineral elements
Interactions between biochar and SS-NB modify nutrient composition, which subsequently impacts nutrient uptake and utilization by the soil. Changes in pH and EC in the SS-NB solution are illustrated in Additional file 1: Fig. S2. Following WCB and SB adsorption, the pH of the alkaline SS-NB solution fluctuated while that of the neutral SS-NB solution increased. The EC increased in both alkaline and neutral SS-NB solutions. The above results may be related to the alkaline properties of biochar mineral elements dissolved in water and the electrical conductivity of oxygen-containing functional groups (Liu et al. 2015; Qian et al. 2015). Therefore, the variations in the mineral elements Ca, Fe, K, Mg, Na, P, and S in the SS-NB solutions were explored, as shown in Table 1. The higher elemental Ca content of the SS-NB solution was related to the input of slaked lime by alkaline thermal hydrolysis. In both SS-NB solutions (alkaline and neutral), the Ca content increased by 5.13–8.21% after WCB adsorption, while it decreased by 58.87–78.98% after SB adsorption, indicating that Ca may be released or adsorbed based on the structural composition of biochar. In addition, after adsorption on WCB and SB, the Fe content in the alkaline SS-NB solution decreased by 43.02–49.86%, while that in the neutral SS-NB solution decreased by 16.88%–23.13%. The difference in adsorption performance under different pH conditions may be due to the easier precipitation of Fe under alkaline conditions, which enhanced the adsorption and fixing of Fe by biochar. After adsorption on WCB and SB, the contents of Mg, K, and P in the alkaline and neutral SS-NB solutions increased, especially after adsorption on SB, the content of P in SS-NB solution increased by 48–606 times. The results indicate differences in the source and structure of biochar will have an impact on the content of mineral elements in SS-NB solution.
3.2.2 Phosphorus and nitrogen
P and N are necessary for photosynthesis, synthesis and breakdown of carbohydrates and amino acids, and energy transfer within plants (Zekri and Obreza 2003). The adsorption of P on WCB and SB in both SS-NB solutions is shown in Fig. 2a. After adsorption on WCB, PO43−P and TP in the alkaline SS-NB solution decreased by 29.63% and 61.99%, respectively, indicating that WCB can adsorb various forms of P in alkaline SS-NB solution, especially organophosphorus. However, in the SB adsorption group, PO43−P and TP contents in alkaline SS-NB solution significantly increased (10.78–20 times), which may be caused by the PO43−P that contained in SB (Jiang et al. 2015). Similar results were observed for the adsorption experiments with WCB and SB in the neutral SS-NB solution. In summary, WCB mainly fixed organic P in SS-NB solution, while SB released significant amounts of P. The use of different sources of biochar in combination with SS-NB can thus be used to guide agricultural P fertilizer application strategies.
Variations in NO3−−N, NH4+−N, and TKN are shown in Fig. 2b. After adsorption on WCB, the contents of NO3−−N and TKN were reduced by 34.86–81.61% and 17.42–51.96% in both SS-NB solutions, respectively. In contrast, after adsorption on SB, the contents of NO3−−N and TKN were reduced by 76.82–93.61% and 32.30–65.49% in both SS-NB solutions, respectively. These results indicate that the adsorption ability of SB for NO3−−N and TKN was stronger than that of WCB. However, in both the WCB and SB adsorption experiments, the content of NH4+−N in both SS-NB solutions increased, which may have been caused by reaction of amino groups leached from biochar with Nessler's reagent (Feit 1994). The initial protein content of the neutral SS-NB solution was higher than that of the alkaline SS-NB solution, but after adsorption on WCB and SB, the protein content decreased in both solutions, and the adsorption capacity of SB for protein (47.37−57.09%) was higher than that of WCB (42.11−53.12%) (Fig. 2c). Amino acids, as the source of organic N available to plants, can improve crop yield and quality, enhance crop resistance, and improve soil quality (Calvo et al. 2014). The content of free amino acids (FAA) in both SS-NB solutions did not decrease significantly during the WCB and SB adsorption processes (Fig. 2d), and there was no significant change in the composition of amino acid fractions, indicating the weak adsorption capacity of biochar for FAA (Fig. 2e). However, the adsorption capacity of SB for amino acids was still higher than that of WCB. Overall, biochar does not only reduce the loss of N from SS-NB, but as a carrier, together with NO3−−N, TKN, and proteins, also promotes multiplication of soil microorganisms, which in turn promotes plant growth (Masiello et al. 2013). Although biochar has a weak ability to fix amino acids, amino acids can easily be taken up by plants and utilized as fast-acting fertilizers (Chen et al. 2014).
Changes in elemental composition were determined after biochar adsorption, as shown in Table 2. The C/N ratios of SB and WCB before adsorption were as high as 137.78 and 492.4, respectively. Studies have shown that if the C/N ratio is remarkably wide, microbial decomposition and mineralization are slow and active N in the soil is consumed, which is not conducive to the management of soil nutrients (Brust 2019). The C/N ratios of SB and WCB decreased to 43.31–43.35 and 50.78–51.37 after adsorption in both SS-NB solutions, indicating that a large amount of N in SS-NB was immobilized on the biochar. Therefore, biochar coupling with SS-NB reduced the C/N ratio to a range more beneficial to crop growth.
3.3 Fixed characteristics of functional substances
3.3.1 Biostimulants
Phytohormones and allelochemicals are crucial signaling factors that participate in the entire growth and development process of plants, playing significant roles in their life cycle (Niharika et al. 2021). In the present study, the substantial amounts of phytohormones (indole acetic acid and hydroxyphenylacetic acid) and allelochemicals (indole derivatives and aromatic amino acids) were detected in SS-NB (Fig. 3). The concentrations of indole acetic acid, hydroxyphenylacetic acid, indole derivatives, and aromatic amino acids were higher in the alkaline than in the neutral SS-NB solution. Specifically, the concentration of aromatic amino acids in the alkaline SS-NB was 1.81 times that in the neutral SS-NB, suggesting that alkaline SS-NB contains more biostimulants and allelopathic substances. After adsorption by WCB and SB, phytohormones (indoacetic acid and allelopathic substances) were detected in neither SS-NB solution, indicating that phytohormones were completely fixed on the biochar. Moreover, the concentrations of indole derivatives decreased by 31.40−62.86% and 74.12−100% after adsorption on WCB and SB, respectively, indicating that SB had a higher fixation efficiency for indole derivatives. The fixation efficiency of both WCB and SB for aromatic amino acids in the neutral SS-NB solution was higher (89.29−99.34%) than that in the alkaline SS-NB solution, which was consistent with the higher TOC removal rate in the neutral SS-NB solution (Fig. 1a). Overall, WCB and SB efficiently adsorbed and fixed phytohormones and allelopathic substances from both SS-NB solutions.
3.3.2 Fluorescent components
The fluorescence components in the SS-NB solutions were characterized by EM-PARAFAC before and after WCB and SB adsorption. Through PARAFAC modeling, six groups of fluorescent components were finally decomposed from the EEM data set, including soluble microbial by-products (280/370, Ex/Em), humic acid-like organics (320–360/420–460, Ex/Em), visible marine humic-like organics (290–310/370–410, Ex/Em), fulvic acid-like organics (260/400–460, Ex/Em), tryptophan-like protein (275/340, Ex/Em), and tyrosine-like protein (275/305, Ex/Em) (Coble et al. 1998). The fluorescence intensity (FI) of each component in both SS-NB solutions after WCB and SB adsorption were shown in Fig. 4a, b. The initial fluorescence intensity (FI) of each component in the alkaline SS-NB solution was stronger than that in the neutral SS-NB solution, indicating that the alkaline SS-NB solution contained more dissolved organic matter, which was consistent with the TOC contents measured in solution (Additional file 1: Fig. S3). Overall, biochar was more effective in immobilizing fluorescent substances. WCB immobilized 74.35–93.49% and 82.48–97.42% of fluorescent components in alkaline and neutral SS-NB, respectively, while SB immobilized 82.15–91.79% and 81.63–99.71% of fluorescent components in alkaline and neutral SS-NB, respectively. There was no significant difference in the adsorption efficiency of fluorescent components by biochar type. The high affinity of the two types of biochar to hydrophobic tyrosine and tryptophan-like protein substances suggests that the hydrophobic interaction may be involved in the adsorption process (Yang et al. 2018). However, biochar adsorbed more fluorescent substances in the neutral SS-NB solution, perhaps due to the higher abundance of adsorption sites on the biochar surface at a lower solution pH. WCB and SB maintained high adsorption rates for both fulvic acid-like (91.00−97.42%) and humic acid-like organics (85.64−99.71%), in which the adsorption efficiency in the neutral SS-NB solution was relatively higher. Humic acid has been reported to have a large average molecular weight and abundant N- and oxygen-containing functional groups (Ateia et al. 2017; Bhatnagar and Sillanpää 2017), the results thus indicate that the surface functional groups of WCB and SB favored the adsorption of high molecular weight organic compounds. Changes in the fluorescence composition ratio for each component before and after adsorption for both SS-NB solutions are shown in Fig. 4c, d. In the alkaline SS-NB solution, the ratio of fluorescence components before and after adsorption did not show obvious variation, while in the neutral SS-NB solution, more tyrosine-like and tryptophan-like proteins remained after adsorption, which further confirmed that the biochar had a strong adsorption capacity for humic acid.
Characteristics of fluorescent components. a Fluorescence intensity (FI) of each component and c PARAFAC model output for six different fluorescence components after adsorption on WCB and SB in alkaline SS-NB solution; b fluorescence intensity (FI) of each component and d PARAFAC model output for six different fluorescence components after adsorption on WCB and SB in neutral SS-NB solution
3.4 Changes in organic molecular composition
Changes in the molecular composition of the SS-NB induced by WCB and SB adsorption were analyzed by FTICR-MS. The mean molecular weight (MW), H/C, O/C, double bond equivalent (DBE), modified aromaticity (AImod), and nominal oxidation state of carbon (NOSC) are summarized in Table S2. The most significant changes after the biochar adsorption were the decrease in MW and DBE, and the increase in NOSC, indicating that biochar fixed macromolecular substances, unsaturated molecules, and reducing substances. These substances may include lignin derivatives, lipids, fatty acids, and aromatic compounds (Gunina and Kuzyakov 2022). After biochar adsorption, H/C, O/C, and molecular polarity increased in the neutral SS-NB solution, indicating that biochar has a strong affinity for molecules with low polarity (Shi et al. 2020). AImod increased and decreased in the alkaline and neutral SS-NB solutions, respectively, indicated that both types of biochar adsorbed similar molecular compounds and that the pH of SS-NB was the main factor affecting adsorption.
The van Krevelen diagram visually shows the formula for molecules in the SS-NB and the remaining molecules after adsorption on biochar (Fig. 5a, b). Major biogeochemical compounds are plotted at specific locations on the map based on H/C or O/C ratios. According to H/C, O/C, N/C, and AImod, all identified molecules were grouped into eight distinct groups, including aliphatic, nitrogen-rich (protein-like), amino sugars-like, highly unsaturated and phenolic, lignin-like, and tannin-like substances, polyphenols, and condensed aromatics (for details on the grouping criteria, refer to Additional file 1: Text S2). The number of organic molecules in the alkaline SS-NB was 8363, which was reduced to 4507 and 6737 after adsorption on WCB and SB, respectively. The number of organic molecules in the neutral SS-NB (9445) was reduced to 4306 and 7246 after adsorption on WCB and SB, respectively. The results implied that biochar adsorbed organic molecules in SS-NB and that the adsorption efficiency of WCB (46.11−54.41%) was much higher than that of SB (19.44−23.28%).
Molecular composition of SS-NB as determined by FT-ICR-MS. van Krevelen diagrams exhibiting organic molecules in a alkaline SS-NB and b neutral SS-NB (the bordered regions exhibit the rough positions of different compound categories); numbers and categories of the organic molecules identified in the SS-NB: the color schemes indicate different organic categories, namely, c the formula group and d the compound group; decreased percentage of the number of e formula groups and f compound groups by adsorption on biochar
Figure 5c, d indicate the molecular formulas and classes of organic molecules in SS-NB. The molecular formulas of organic molecules were categorized as CHO, CHON, CHOS, CHOP, CHONS, CHONP, CHOSP, and CHONSP, which are widely involved in soil N and P cycles and affect the quality of the soil and crops (Haygarth et al. 2013). After adsorption on WCB and SB, the contribution of N- (CHON, CHONS, CHONP, CHONSP), P- (CHOP, CHONP, CHOSP, CHONSP), and S-related molecular formulas (CHONS, CHOSP, CHONSP) in both SS-NB solutions ranged from 68.96 to 76.20%, 38.73 to 50.44%, and 49.95 to 54.20%, respectively. However, the immobilization rates of N-, P-, and S-related molecular formulas by WCB were 47.28−52.86%, 40.62−50.89%, and 44.47−50.53%, respectively, which was much higher than those by SB, which were 21.67−23.59% for N-, 19.22−26.32% for P-, and 18.0019.18% for S-related molecular formulas.
Figure 5e confirms the superior adsorption efficiency of WCB over SB for each group of molecular formulas in both solutions. The organic molecules in SS-NB were mainly proteins, lipids, and lignin, which accounted for more than 80% of the total, and the proportion of these compounds before and after adsorption did not change much for both WCB and SB (Fig. 5f). In the alkaline SS-NB, WCB exhibited a high affinity for carbohydrates (48.22%), amino sugars (58.10%), proteins and lipids (50.49%), tannins (75.43%), and lignin (40.44%), while SB had affinity for carbohydrates (43.24%), proteins and lipids (28.19%), and tannins (76.16%). Additionally, in the neutral SS-NB, WCB showed a high affinity for proteins and lipids (51.71%), lignin (80.12%), and unsaturated hydrocarbons (80.94%), while SB only had a high affinity for lignin (53.58%). These results again confirmed that the biochar presented a strong affinity for macromolecules (proteins) and reducing substances (lignin and lipids), which is consistent with the reduction in MW and NOSC (Table S1). Importantly, WCB adsorbed various types of molecular substances while maintaining a high immobilization rate. Furthermore, after the adsorption with WCB and SB in the neutral SS-NB, the content of carbohydrates (-342.04% and -214.82%), amino sugars (-44.03% and -39.34%), and tannins (-182.31% and -111.78%) notably increased, indicated that carbohydrates, amino sugars, and tannins were released from the biochar as biochar derivatives (Sun et al. 2021). This phenomenon did, however, not occur in the alkaline SS-NB, probably due to the fact that acidic groups (carboxyl and phenolic groups) of organic compounds are protonated under acidic conditions, which makes biochar derivatives more soluble (Liu et al. 2009; Enaime et al. 2020).
In summary, the FTICR-MS and EEM results were consistent, demonstrating that biochar shows a high affinity for macromolecules (humic acids and proteins). Moreover, WCB had higher adsorption efficiencies for N-, P-, and S-related molecular formulas in SS-NB, which is consistent with the better TOC removal rate of WCB. The beneficial effect of WCB adsorbing SS-NB on crop growth was further confirmed in the lettuce pot experiment (Fig. S4). Compared with the application of WCB, the biomass of lettuce increased by 29.32% after SS-NB fixed to WCB, while the biomass of lettuce only increased by 16.33% after SS-NB fixed to SB. Therefore, it is necessary to explore the adsorption mechanism of SS-NB by biochar, including the changes of surface functional groups and internal pore structure of biochar.
3.5 Adsorption mechanism
After comparing the adsorption affinity of the different types of biochar for SS-NB nutrients, the functional groups and micropores were considered to play important roles in the adsorption process, and the properties and adsorption mechanism of biochar to nutrients and biostimulants were further investigated by means of FTIR, BET, and XPS. The FTIR results before and after SB and WCB adsorption are shown in Fig. 6. The spectra of biochar before adsorption showed only a small number of peaks related to functional groups, while a large number such peaks appeared after adsorption, as shown in Table S3. The wavenumber ranges at which peaks appeared for SB and WCB after adsorption were 1339–1987 and 1329–2029, 2335, 2340, 2361 and 2364, 3513–3910, and 3437–3944 cm−1, which are mainly attributed to alkanes, alkenes, mononuclear aromatic compounds, ketones, aldehydes, carboxylic acids, esters, amine salt and fatty nitrile, and alcohol and phenol functional groups (Silverstein and Bassler 1962). Many complex functional groups emerged, which may have been related to the chemical composition of the microbiome, including proteins, nucleic acids, lipids, and sugars. Studies have shown that amino acids can synthesize amine salts (Lygo and Andrews 2004), that fatty acids can synthesize fatty nitrile (Shirazi et al. 2017), and that nucleic acids contain a large number of ester bonds (Pauling and Corey 1953).
Changes in specific surface area and pore size distribution (PSD) after SB and WCB adsorption are shown in Fig. 7. After adsorption in neutral and alkaline SS-NB solutions, the specific surface area of SB decreased from 762.92 to 674.78 m2 g−1 and 645.06 m2 g−1, while that of WCB decreased from 557.49 to 315.08 m2 g−1 and 313.84 m2 g−1, respectively, indicating that dissolved organic molecules in SS-NB adsorbed on the biochar surface. However, after adsorption in neutral and alkaline SS-NB solutions, the total pore volume of SB increased slightly from 0.61 to 0.62 cm3 g−1 and 0.66 cm3 g−1, while it decreased from 0.38 to 0.29 cm3 g−1 and 0.31 cm3 g−1 in WCB, indicating that dissolved organic molecules entered the pores of WCB during adsorption, resulting in hole blockage. It was observed that there were no visible pores on the surface of SB, while more pores were observed on the surface of WCB (Additional file 1: Fig. S1), indicated that WCB was more beneficial to the SS-NB adsorption process (Zhao et al. 2019). The PSD results of SB showed that the pore volume decreased at 1.76–3.35 nm, indicating that this part of the pore was involved in the adsorption of organic molecules in SS-NB, while the pore volume slightly increased at 3.35–54.00 nm, which was the pores left by the adsorption of organic molecules on the surface of larger pores (Liu et al. 2020). The PSD results of WCB showed that the pore volume decreased at 1.88–52.37 nm, indicating that the entire 1.88–52.37 nm pore was involved in the adsorption of organic molecules in SS-NB. The initial specific surface area, total pore volume, and average pore diameter of WCB were lower than those of SB, but the adsorption efficiency of WCB was higher than that of SB. The above results suggest that the larger pores in SB may become diffusion channels for small molecules due to the weaker adsorption force (Tan et al. 2021). In addition, larger molecules such as proteins, peptides, and organic acids may be more likely to clog in SB with slightly larger pore size than WCB with smaller pore size, and thus a large number of small molecules have the opportunity to enter WCB pores, which may be caused by the pore size-exclusion effect (Hu et al. 2023).
The adsorption behavior of SB and WCB was explored using XPS, as shown in Table S3. The N1S spectra for SB showed more peaks after adsorption, including those at 397.55, 398.25, 399.08, 399.33, 399.71, 400.46, and 401.55 eV, among which the peaks near 399.5 and 401.0 eV can be attributed to hydrogen bonded-NH2 and -NH3+, respectively, which suggests that amino groups were involved in adsorption (Lanzilotto et al. 2018; Shi et al. 2018). The N1S spectra for WCB showed the same patterns. After adsorption, new peaks in the O1S spectrum for SB emerged, which were located at 530.54, 530.73, 531.63,532.16, 532.24, and 532.52 eV, and the peaks near 530.6 and 532.4 eV can be attributed to −COOH and −OH, respectively, indicating that hydrogen bonds were involved in adsorption as well (Yatsimirskii et al. 1977; Lanzilotto et al. 2018). However, WCB adsorption did not only involve hydrogen bonds, but the new peak at 533.6 eV can be attributed to C(O)O− (Shi et al. 2018). Notably, the O1S spectra for pristine WCB had −COOH(530.73 eV) and −OH (532.40 eV) peaks, which were not detected for pristine SB, suggesting that surface adsorption via hydrogen bonds was stronger for WCB than SB. This may be the reason for the higher adsorption efficiency of WCB.
These results provide a comprehensive understanding of the adsorption mechanisms involved. SB and WCB interacted with dissolved substances in SS-NB through surface functional groups, mainly including amino, hydrogen bond, and electrostatic interactions. These substances were also adsorbed within the internal pore network of the biochar. WCB exhibited a higher adsorption capacity due to its strong surface adsorption via hydrogen bonding and the pore size-exclusion effect.
4 Conclusions
SS-NB contains abundant nutrients and can exert stimulating effects, and its coupling with biochar can reduce nutrient loss and improve soil functioning. In this study, the immobilization of nutrients and biostimulants by two types of biochar in alkaline and neutral SS-NB was investigated. First, the neutral SS-NB was more favorable for the adsorption of TOC on biochar, especially for fulvic and humic acids. Although the adsorption efficiency of WCB for TOC was much higher than that of SB, the later had a higher adsorption capacity for N (TKN, NO3−−N, proteins, and amino acids) and Ca ions and released a large amount of P. Second, WCB and SB had a strong affinity for macromolecules (proteins) and reducing substances (lignin and lipids), and excellent fixation ability for phytohormones and allelochemicals. However, WCB could adsorb more types of molecular substances while maintaining a high adsorption rate. Finally, WCB showed a strong adsorption capacity for organic molecules due to its strong surface adsorption via hydrogen bonding and the pore size-exclusion effect. Therefore, biochar, as an adsorption carrier for SS-NB, may be used as a fertilization strategy to enhance soil fertility management.
Data availability
The datasets used or analyzed in this study are available from the corresponding authors upon reasonable request.
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This study received funding from National Key Research and Development Program of China (2023YFC3207602), Jiangsu Special Funding of Science and Technology Innovation for Carbon Emission Peaking and Carbon Neutrality (BE2022303), Postgraduate Research & Practice Innovation Program of Jiangsu Province (KYCX22-2382), and Jiangsu Students' Key Project (Innovation) for Innovation and Entrepreneurship Training Program (202310295011Z).
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Shuo Wang and Ji Li: Idea, Experiment design, Writing-Reviewing and Editing. Jiahou Hao: Experiment, Writing and Editing. Xi Zhang, Shaojie Zong and Yang Zhuo: Experiment. Yue Zhang, Yun Deng and Xiaokai Zhang: Formal analysis and Data Curation.
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Additional file 1:
Text S1. Detailed procedures for the determination of phytohormones and allelopathic substances. Text S2. Categories of SS-NB molecules composition. Table S1. Adsorption kinetics parameters of SS-NB by SB and WCB. Table S2. Summary of molecular attributes in SS-NB solution. Table S3. Emerging functional groups after adsorption of straw biochar (SB) and wood chip biochar (WCB). Table S4. XPS investigation of adsorption behavior of biochar: spectral changes of C1S, N1S and O1S. Fig. S1. SEM images of a SB, b SB with absorbed SS-NB (neutral), c SB with absorbed SS-NB (alkaline), d WCB, e WCB with absorbed SS-NB (neutral) and f WCB with absorbed SS-NB (alkaline). Fig. S2. Changes of a pH and b EC contents before and after adsorption of WCB and SB in SS-NB solution. Fig. S3. Changes of total organic carbon (TOC) contents before and after adsorption of WCB and SB in SS-NB solution. Fig. S4. Lettuce biomass in CK, SB, WCB, SB adsorption (alkaline) and WCB adsorption (alkaline) treatment groups.
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Hao, J., Zhang, X., Zong, S. et al. Biochar as a highly efficient adsorption carrier for sewage sludge-derived nutrients and biostimulants: component fixation and mechanism. Biochar 6, 42 (2024). https://doi.org/10.1007/s42773-024-00335-0
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DOI: https://doi.org/10.1007/s42773-024-00335-0