Excess sludge biochar facilitates persulfate activation for highly efficient tetracycline removal

As environmental pollution becomes increasingly serious, the combined pollution of antibiotics (Wang et al. 2020a) and heavy metal (Arslan et al. 2022) has caused widespread concern among many environmental problems. Tetracycline (TC) is one of the most common antibiotics, which is widely used for treating bacterial infections and as a feed additive in a variety of animal husbandry and aquaculture, due to its low cost, effectiveness, and wide antimicrobial spectrum (Wang et al. 2018). In China, nearly 100,000 tons of TC are manufactured every year (Liu et al. 2012), however, most TC is poorly metabolized and ends up in the environment through human and animal faeces (Xie et al. 2018). This not only results in serious environmental pollution which endangers human health, but also accelerates the emergence of drug-resistant bacteria that may lead to more serious disasters (Duan et al. 2022). All over the world, urban wastewater is a major source of metals and antibiotics in the environment (Senta et al. 2019), and there is an urgent need to discover methods to remove typical antibiotics and metals from the wastewater effectively.

Many technologies have been proved effective to remove TC, including membrane technology, bioremediation, and anaerobic biodegradation, but the costs are relatively expensive and the procedures are usually complicated (Scaria et al. 2021). Among these, adsorption techniques have the virtues of simplicity, low consumption, high removal efficiency, and nontoxicity, and have been widely used throughout environmental restoration (Ma et al. 2021). A series of adsorbents have been applied to remove contaminants, particularly biochar (Krasucka et al. 2021). Its adsorption of metals included the coordination of hydroxyl and carboxyl groups, and the precipitation of complexes on the mineral surface (Ma et al. 2021). The main mechanism of antibiotic adsorption by biochar included EDA π-π interactions and electrostatic interactions (Fan et al. 2018). Besides, biochar has also been proved to contain abundant electron-donating and electron-accepting groups on the surface, which could serve as preferred carriers for many catalysts with the additional function of strengthening the catalytic performance (Shen et al. 2020). However, the main precursors (such as rice and straw) used for biochar were biogenic substances which has more valuable application than becoming the raw material of biochar, such as fermentation for biogas (Wei et al. 2020). Therefore, it is necessary to choose some precursors which are low-quality and cost-efficient.

Because of their powerful radical-driven processes and direct electron transfer property, persulfate-based advanced oxidation processes have attracted increasing attention for their application in the degradation of antibiotics which is abundant in urban wastewater and groundwater (Pan et al. 2018). The persulfate reactivity depends on the activating agents heavily, including thermal catalysis (Yabalak et al. 2022), transition metals (Song et al. 2021), and carbon materials (Wu et al. 2018). Among these activating agents, the high efficiency of transition metals has been reflected in the persulfate activation, with Fe(II) or Cu(I) having a better activation effect than other metals (Li et al. 2017). It's worth noting that common water treatment processes generally involve iron ions, resulting in the output solid waste (excess sludge) containing a certain amount of residual Fe(II) and Fe(III) (Wang et al. 2020b). From an engineering point of view, in situ utilization of residual Fe²⁺ and Fe³⁺ in solid waste for persulfate activation is highly desirable but also very challenging, which relies on the continuous generation of Fe²⁺ from Fe³⁺.

In this study, biochar (BC500) was prepared from excess sludge. Through its self-contained variable valence metal, BC500 can conduct electrons which may result in its stronger catalytic properties for PS than biochar made from conventional materials. In addition, water bodies contaminated by the combined pollution of antibiotics and heavy metal were simulated with the most common contaminants (TC and Fe) as representatives. Thus, the original adsorption and catalytic properties of BC500 were investigated, as well as the effectiveness of its activation of PS for the degrading antibiotics after synergistic metal contamination. Therefore, this study not only provided a feasible idea for the resource utilization of excess sludge, but also offered an efficient solution for some environmental pollution.

Excess sludge (moisture content of 80%, pH of 8) taken from the Kuihe Sewage Treatment Plant in Xuzhou, China, was air-dried to a constant weight, then ground and passed through an 80-mesh nylon sieve. The pretreated sludge was then carbonized in a high-temperature furnace with a pure Ar atmosphere for 2 h at different temperatures (300 °C, 500 °C, and 700 °C), at a heating rate of 2 °C/min. The prepared biochar was first washed with 1 M HCl for 12 h, followed by deionized water until a neutral pH was reached. Finally, the biochar samples were dried in an oven at 60 °C for 24 h. All biochars were named BCX, where X was substituted with the pyrolysis temperatures of individual samples.

Tetracycline (TC, purity ≥ 98%) was purchased from the Aladdin Industrial Corporation, USA. The other chemicals, including sodium persulfate (PS) and anhydrous ferric chloride (FeCl₃) were purchased from the Sinopharm Chemical Reagent Co., Ltd, Shanghai, China.

Preliminary experiments proved that the reaction time of 720 min was sufficient to ensure contact between the absorbate and absorbent. The adsorption experiment was carried out in a 100 mL volumetric flask containing 50 mL of the reaction solution. After many preliminary tests, the reaction solution was finally prepared with 120 mg/L TC and 10 mg/L Fe³⁺ which is considered for the best results of the experiment. The solution was oscillated at 120 r/min at 25 °C. The pH value was adjusted to maintain a pH of approximately 7 (NaOH or HCl) during the course of the experiment which can best simulate the PH of natural water. The biochar content was 25 mg, and samples were collected at 5, 10, 30, 60, 120, 180, 240, 480, 600, and 720 min (Tables S1 and S2). In the isotherm study, the concentrations of TC were 60, 75, 90, 105, 120, and 135 mg/L, and the TC was oscillated for 720 min to reach equilibrium (Tables S3 and S4). After the end of the reaction, 10 mL of the supernatant using a 0.45 μm filter membrane to filtered into a clean centrifuge tube to facilitate further pretreatment and detection. Solution of 10 mg/L Fe³⁺ and 120 mg/L TC without biochar was cultured as a control group, and filtered samples were collected after complete reaction according to the above process in order to further detect the TC and Fe³⁺ contents.

The degradation experiment was carried out in a 100 mL volumetric flask containing 50 mL of the reaction solution. The free radicals produced by the activation of persulfate were used to degrade TC. Apart from the investigated parameter, the parameters of the reaction solution were fixed at an initial pH of 7, 10 mg/L Fe³⁺, 120 mg/L TC, 300 mg/L persulfate, and 25 mg biochar. The solution containing 10 mg/L Fe³⁺ and 120 mg/L TC was first oscillated at 120 r/min at 25 °C for 60 min so that the Fe³⁺ and TC could be adsorbed by the biochar. Then, the addition of persulfate triggered a degradation reaction. Solution samples were collected at 0, 60, 120, 180, 420 and 540 min after persulfate was added (Tables S5 and S6).

The 10 mL supernatant was filtered into a clean centrifuge tube with a 0.45 um filter membrane for easy detection. The biochar samples collected by filtration, and TC was further extracted and characterized. We collected the solution sample after degradation in order for detection of TC degradation intermediates by an electro-spray ionisation ultra-high performance liquid chromatography-tandem mass-spectrometry (UHPLC-MS/MS, Waters, USA). Under the same conditions, the biochar, persulfate, and BC/PS equivalent control experiments were carried out. The paper studied the influence of biochar, Fe³⁺, persulfate, and other factors on the TC removal. All the experiments were conducted in the dark.

The TC concentrations were detected through UV-vis spectrophotometer (Hitachi U-3000) at 365 nm. The Fe concentration was analyzed by using an ICP-OES spectrometer (iCAP 7200 series, Thermo Fisher Scientific Inc.). The electron paramagnetic resonance (EPR) spectra were obtained by a Bruker EMX-10/12 Spectrometer (X-band) using DMPO as spin-trapping reagents for radical detection at room temperature. Fourier transform infrared spectrometry (FTIR, Spectrum One B, Perkin Elmer Inc.) spectra of biochar were recorded in the range of 4,000–400 cm⁻¹. The spectra were obtained from 32 scans of the sample at a resolution of 4 cm⁻¹ and an interval of 1 cm⁻¹. Peak intensities in the FTIR spectra are semi-quantitatively proportional to concentrations of moieties. Powder X-ray diffraction (XRD) patterns of samples were examined using a Panalytical X'pert-pro MPD X-ray diffractometer using Cu Kα radiation (λ = 1.54056 Å). Scanning electron microscopy (SEM) equipped with an energy dispersive spectrometer (EDS) was used to characterize the surface morphological and elemental maps of biochar (Model JSM-7401, Nippon Electronics). The Brunauer-Emmett-Teller (BET) surface area was measured using the ASAP2420-4 instrument. The elemental compositions of samples were examined using X-ray photoelectron spectroscopy (XPS), and the XPS data were analyzed in the CasaXPS software.

The adsorption kinetics of biochar were studied using the quasi-first order model and quasi-second order model. The Freundlich and Langmuir equations were used to fit the adsorption data. The removal of TC by adsorption and degradation process were also investigated by first-, second-, third-order reactions, respectively. To study the distribution of TC and Fe³⁺ in each phase, the mass ratio of TC or Fe³⁺ in the aqueous phase (A1) and biochar phase (A2) was detected. Both degradation (degraded by persulfate) and removal (adsorbed by biochar and degraded by persulfate) efficiencies were calculated to evaluate the loss of TC and Fe³⁺ (detailed information in the SI). All measurements were conducted in triplicate and reported as average values ± standard deviations.

The excess sludge was fired into biochar by a Muffle furnace at 300 °C, 500 °C, and 700 °C, and the pore surface properties were shown in Table 1. The S_BET of BC300 was 19.057 m²/g, with a small quantity of small-sized surface pores. When pyrolysis temperature reached 500 °C, the S_BET increased to 39.719 m²/g, resulting in different pore size distribution with significantly larger-sized surface pores. Thus, we can explain the increase of the specific surface area of the biochar by means of an increase in the number of micropores (Zhang et al. 2018). However, with the increasing temperature in pyrolysis from 500 °C to 700 °C, the S_BET sharply decreased to 28.898 m²/g. This decrease in the specific surface area and pore volume might be caused by an interaction between the sludge components and the pyrolysis behavior, along with other properties in terms of wall thickness, surface collapse, pore blockage at higher pyrolysis temperature (Pituello et al. 2015). Less volatile fixed carbon slag would also lose the remaining space in the matrix and form a better microporous structure after some elements were volatilized (Klasson 2017). A high specific surface area ensured the biochar had a higher adsorption capacity and more abundant persulfate activation sites.

The degradation removal efficiency of the Fe/BC500/PS system was 61.2%, which was 54.9% and 18.4% higher than those obtained in Fe/BC300/PS and Fe/BC700/PS systems. Therefore, a conclusion could be drawn that moderate pyrolysis temperature was conducive to higher persulfate activation performance mediated by biochar. The BET surface area of biochar appeared to the most direct controlling factor for degradation removal of TC, because the higher surface area could endow biochar more active sites. A significant positive correlation between BET surface area and degradation removal efficiency with an r of 99.5% (P < 0.05) was drawn out. The average pore size and pore volume of biochar prepared at pyrolysis temperature of 300 °C were lower than those of BC500 and BC700, which should be due to incomplete carbonization. However, the lamellar structure of the biochar began to collapse, appearing to have more clogged pores and leading to decreased surface area and pore volume, at higher pyrolysis temperature of 700 °C. In addition, Fe(II) is the main catalytic center, could be obtained by the Fe(III) reduction assisted by the electron-donating groups on surface of biochar to enhance the TC degradation. This result demonstrated that further increase of pyrolysis temperature contributed less to the improvement of TC degradation.

The dynamic TC removal process in the Fe/BC/PS system was investigated by addition of the persulfate after 60 min (Figure 4). The overall TC removal efficiency when applying BC500 was higher than those of BC300 and BC700, which was in agreement with above result. The TC was solely removed via the adsorption by biochar before the addition of persulfate, and the Fe³⁺ significantly enhancing the TC transferring rapidly from the aqueous phase to biochar. Afterward, the persulfate addition facilitated the TC removal without time-lag effect, indicating the higher sensitivity of persulfate to produce free radicals for TC degradation. The maximum TC removal rate was 0.66 mg/(L·min) in the Fe/BC500/PS system during 60–120 min, which was 22.2% and 11.1% higher than those obtained in Fe/BC300/PS and Fe/BC700/PS systems. However, the TC removal rate slowed down after 120 min in all test systems, and gradually ended in 600 min due to depletion of active persulfate. Based on the dynamic removal tests, the potential synergistic mechanism of biochar and Fe³⁺ on speeding up TC removal could be drawn: (1) the BC500 with higher surface area could increase the adsorption of Fe³⁺ and TC, (2) the Fe²⁺ reduced from Fe³⁺ accelerated the degradation of TC on the biochar surface, forming concentration gradient from bulk solution to biochar surface and further improving the TC exclusion from the solution.

Based on the results above, the potential promoting mechanism of biochar on TC removal could be summarized in sequence: (1) the Fe³⁺ and TC were firstly adsorbed by the biochar, and Fe³⁺ was reduced to Fe²⁺ under the assistance of electron-donating groups on biochar, as verified by the XPS spectrum; (2) the activation of persulfate was then enhanced by the reduced Fe²⁺, and generated free radicals for TC degradation on biochar, and (3) further movement of TC from the aqueous phase to biochar with the gradual consumption of TC on the biochar, towards a dynamic balance.

At present, most studies related to the use of biochar combined with PS tend to focus on the removal of one pollutant (e.g., antibiotics) alone without considering the presence and effects of other pollutants (e.g., metal pollution). Some studies have focused on the optimization of degradation methods to improve the efficiency of antibiotic removal, while ignoring the synergy between methods and pollutants in the advanced oxidation process. Alternatively, sewage sludge is the main solid waste in municipal wastewater plants. The current treatment methods for sewage sludge are incineration and landfilling. Although these conventional treatment methods are efficient, they cause environmental problems.

In this study, a carbonaceous material (BC500), which use excess sludge as a substrate, was prepared as a catalyst for PS activation. Meanwhile, the most common antibiotic and metal pollution (TC and Fe) were selected to form a complete synergistic degradation system in combination with the excess biochar activating persulphate. The removal rate of TC was greatly enhanced when Fe was present at the same time, far exceeding the efficiency when TC was alone as pollution. By characterising the nature of the excess biochar and analysing the free radicals in the reaction, the stability of synergistic interaction between the metal and advanced oxidation of persulfate was verified. This study provides a new approach for the treatment of sewage sludge as well as a new idea with great potential for the removal of antibiotics from sewage.

However, further studies are required to confirm the following: (1) The stability of the Fe/BC500/PS system needs to be verified in depth under other reaction conditions and aqueous environmental conditions (such as Ph, temperature and alkalinity); (2) The mechanism of antibiotic removal by the Fe/BC/PS system (such as reactive radicals and electron transfer) must be further tested and analyzed; (3) For the residual antibiotics in the system, we intend to improve the modification method of biochar. By enhancing the catalytic properties of biochar, a higher degree of PS activation will be achieved in order to generate more reactive radicals and increase antibiotic removal efficiency. At present, based on the relevant literature, we plan to combine the respective advantages of residual sludge, hydrothermal loading and special transition metals for the preparation of novel biochar. It is expected that complete removal of antibiotics will likely be achieved.

In this study, the performance of excess sludge biochar for TC removal in Fe/BC/PS system was systematically investigated and its potential degradation mechanism was explored. The main conclusions are:

• (1)

  The excess sludge biochar had a high specific surface area with numerous micropores, producing a strong adsorption capacity for TC and Fe in water.

• (2)

  The Fe(II), reduced from Fe(III) mediated by the electron-donating groups on biochar, could activate persulfate to produce free radicals of ^·OH and SO₄⁻.

• (3)

  The interaction between free radicals (^·OH and SO₄⁻) and TC was the main mechanism for TC degradation in the Fe/BC/PS system based on EPR spectra.

• (4)

  The transformation products of TC identified by UHPLC-MS/MS confirmed that TC was degraded by multiple processes including double bond oxidation, loss of dimethylamine amino group, dehydration, intramolecular condensation, aromatic epoxidation, and carbon atom ring cleavage.

Overall, in this study a novel option for the engineered disposal of large volumes of excess sludge in municipal wastewater treatment plants has been identified. The excess sludge, as well as the leftover Fe ions from the flocculation process, could be recycled into biochar to activate persulfate for TC degradation. However, its practical application performance should be further evaluated by field tests.

We are grateful for the grants for the National Natural Science Foundation of China (No. 52000153), the Xuzhou Key Research and Development Plan Project (social development) (No. KC20163), the Water Conservancy Technology Project of Jiangsu Province (No. 2021077).

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

All relevant data are included in the paper or its Supplementary Information.

The authors declare there is no conflict.