A Mini Review on Persulfate Activation by Sustainable Biochar for the Removal of Antibiotics

Antibiotic contamination in water bodies poses ecological risks to aquatic organisms and humans and is a global environmental issue. Persulfate-based advanced oxidation processes (PS-AOPs) are efficient for the removal of antibiotics. Sustainable biochar materials have emerged as potential candidates as persulfates (Peroxymonosulfate (PMS) and Peroxydisulfate (PDS)) activation catalysts to degrade antibiotics. In this review, the feasibility of pristine biochar and modified biochar (non-metal heteroatom-doped biochar and metal-loaded biochar) for the removal of antibiotics in PS-AOPs is evaluated through a critical analysis of recent research. The removal performances of biochar materials, the underlying mechanisms, and active sites involved in the reactions are studied. Lastly, sustainability considerations for future biochar research, including Sustainable Development Goals, technical feasibility, toxicity assessment, economic and life cycle assessment, are discussed to promote the large-scale application of biochar/PS technology. This is in line with the global trends in ensuring sustainable production.


Introduction
Antibiotics are used as medicines to protect human and animal health from bacterial infections [1]. The global antibiotics consumption increased from 21.1 to 34.8 billion tons daily from 2000 to 2015 [2]. Based on the chemical structure of antibiotics, the common classes of antibiotics are sulfonamides, tetracyclines, fluoroquinolones, macrolides, and β-lactams [3]. The antibiotics are partially metabolized in vivo, and a significant fraction are released into wastewater with urines and feces. However, the treatment capacity of antibiotics in wastewater treatment plants is limited because of the antibacterial property of antibiotics [4,5]. Residual antibiotics result in the emergence of antibiotic-resistant bacteria, threatening public healthcare [6]. Therefore, it is essential to effectively remove them from wastewater.
Various approaches have been used to remove antibiotics from wastewater, such as biological degradation, adsorption (e.g., plants, materials), membrane filtration, and oxidation processes [7][8][9]. Biological degradation has a low removal efficiency owing to the antibacterial activities of antibiotics. The process of adsorption and membrane filtration can only transfer antibiotics to solid matrices but cannot degrade antibiotics into small molecules [10]. Persulfate-based advanced oxidation processes (PS-AOPs) can induce the generation of highly reactive radicals (sulfate radicals (SO 4 •− ), hydroxyl radicals (•OH), and superoxide radicals (O 2 •− )) to degrade antibiotics into other compounds, water (H 2 O), and carbon dioxide (CO 2 ). The persulfates (peroxymonosulfate (PMS) and peroxydisulfate (PDS)) can be activated via ultraviolet light, heat, ultrasound, carbon materials, and transition metals, generating active radicals [11,12]. To overcome the disadvantages of additional

Mechanism of PS Activation
The mechanism of PS activation by biochar materials mainly includes free radical (SO 4 •− , •OH and O 2 •− ) and non-radical pathways (singlet oxygen ( 1 O 2 ) and surface electron transfer) [24]. The active sites, such as persistent free radicals (PFRs), oxygen-containing groups (C=O, C-OH, C-OOH, C-O-C, etc.), free-flowing electrons in biochar, structural defects, oxygen vacancy, and the redox cycle of metal ions, can activate PS to produce free radicals (Table 2). SO 4 •− with a redox potential of 2.5-3.1 V shows a strong oxidation capacity in comparison with •OH (1.9-2.7 V). SO 4 •− can also react with -OH to form •OH. Biochar materials may deliver an electron to O 2 to produce O 2 •− , which can be an intermediate product for 1 O 2 formation [25]. Table 2. Active sites on biochar catalysts for PS activation to remove antibiotics.

Pristine Biochar with Desirable Active Sites for PS Activation to Degrade Antibiotics
Pristine biochar is produced via pyrolysis at >500 • C under inert conditions. Pristine biochar serves as an excellent catalyst for PS activation owning to the high specific surface area, persistent free radicals (PFRs), defects, oxygen-containing functional groups, graphitization properties, and a small quantity of metal components (Table 3). Studies have shown that pollutant degradation may occur on the biochar surface [38,62]. The high specific surface area of biochar can provide sufficient space for the reaction and enhance the loading of active sites and the adsorption capacity for pollutants [63][64][65]. Adsorption of PS on biochar was reported as the essential step for PS activation, due to the facilitated electron transfer between biochar and PS [55]. The adsorption capacity of biochar for PS (Figure 1a) was consistent with the specific surface area, and so was ofloxacin degradation, indicating that the adsorption of PS on biochar may promote PS activation and ofloxacin degradation.
PFRs are free radicals on the surface or interior of biochar, which have a lifetime of hours to months. PFRs can provide electrons to oxidants for organic pollutant degradation, thus endowing pristine biochar with catalytic capacity [66]. As shown by Zhang et al. [26], PFRs were verified on the biochar surface. The PFRs and defects were the active sites for PMS activation to generate radicals (SO 4 •− , •OH), which were responsible for the degradation of tetracycline antibiotics. Intrinsic defects could also contribute to the electron transfer non-radical process. Miao et al. [49] used in situ Raman spectroscopy to indicate the formation of metastable surface species (biochar-PDS*) (Figure 1b), which could subsequently oxidize the adsorbed tetracycline via a direct electron transfer pathway [67]. Together with the reduction in the current in chronoamperometry tests after adding PDS or tetracycline solution, electron transfer was achieved in the co-presence of tetracycline molecules and biochar-PDS*. On the surface of biochar, oxygen-containing functional groups with an electron-rich nature are desirable for the mediation and promotion of redox reactions. Wang et al. [19] revealed graphite N and C=O were the active sites using the linear correlations between values of log (k) and active sites (Figure 1c,d). Graphitic N played an essential role in PMS activation by promoting electron transfer from biochar to O 2 to produce 1 O 2 [68]. C=O on the edge of biochar could activate PMS to produce 1 O 2 [69]. Together with defects which contributed to the radical pathway and surface electron transfer, free radicals and the non-radical pathways were involved in the biochar/PMS system for sulfamethoxazole degradation (Figure 1e). The existence of metal ions in biochar could facilitate PS activation. Fang et al. [70] reported that the C=O and Fe 2+ /Fe 3+ on the sludge biochar samples were the main active sites for PDS activation to produce a large amount of 1 O 2 . 1 O 2 was found to be reactive to degrade the tertiary amine of enrofloxacin. Piperazine ring cleavage (P1 and P2), quinolone ring decomposition (P7 and P8), decarboxylation, and defluorination (P10) ( Figure 1f) were proposed as the degradation pathways of enrofloxacin. The other products were produced by further oxidization. The toxicity of degraded enrofloxacin products decreased during the oxidation process ( Figure 1g). Materials 2022, 15, x FOR PEER REVIEW 6 of 16

Biochar with Surface Modification for PS Activation to Degrade Antibiotics
In order to enhance the catalytic performance of pristine biochar, pristine biochar needs to be treated by functionalization processes. Non-metal heteroatom-doped biochar, and metal-loaded biochar can attach more functional groups to the biochar surface. The abundant active sites, such as PFRs, defects, oxygen-containing functional groups, heteroatom species, metal ions, oxygen vacancy, and graphitized carbon boost the catalytic capacity of biochar for the degradation of antibiotics (Table 3). The amounts of persulfate (PS) adsorbed on cellulose and lignin-derived biochar prepared at 500 or 1000 • C (C500, C1000, L500 and L1000). Reproduced with permission from [55]. (b) In situ Raman spectra of graphitic biochar prepared at 1000 • C (GBC-1000). Reproduced with permission from [49]. Sulfamethoxazole degradation rate in a log (k) versus (c) C=O content; (d) graphite N content. (e) Mechanism scheme of sulfamethoxazole removal in dairy manure digestate-derived biochar (DMDB)/PMS system. Reproduced with permission from [19]. (f) Possible degradation pathways of enrofloxacin in sludge-derived biochar (SDBC)/PDS system. (g) The toxicity of enrofloxacin and degraded products in an oxidation reaction. Reproduced with permission from [70].

Biochar with Surface Modification for PS Activation to Degrade Antibiotics
In order to enhance the catalytic performance of pristine biochar, pristine biochar needs to be treated by functionalization processes. Non-metal heteroatom-doped biochar, and metal-loaded biochar can attach more functional groups to the biochar surface. The abundant active sites, such as PFRs, defects, oxygen-containing functional groups, heteroatom species, metal ions, oxygen vacancy, and graphitized carbon boost the catalytic capacity of biochar for the degradation of antibiotics (Table 3).

Non-Metal Heteroatom-Doped Biochar
Researchers found that non-metal heteroatom-doped biochar could tune the electronic properties and enhance the catalytic performance of pristine biochar [71]. N atoms can easily substitute the carbon (C) atoms in biochar due to the similar molecular properties to C atoms. N can reconstruct the electron arrangement and enhance the active sites (Pyridinic N, graphitic N, and pyrrolic N) of biochar materials. Ye et al. [42] found that the efficient catalytic performance was due to the facilitated electron transfer originating from graphitization and N functionalization, in which the non-radical pathways (surface electron-transfer and 1 O 2 ) were the dominant pathways for the degradation of tetracycline. Moreover, pyridinic N and graphitic N were the potential active sites for PMS activation (Figure 2a). Liang et al. [40] prepared N-doped biochar from sewage sludge and red mud. Sulfanilamide degradation was enhanced in the N-doped biochar (NSRCBs)/PMS system (Figure 2b), reflecting the important role of N dopants. The as-prepared biochar had abundant catalytic sites for PMS activation to degrade sulfanilamide (Figure 2c). Specifically, the redox cycle of Fe 2+ /Fe 3+ could generate SO 4 •− and •OH. The pyridinic N could activate PMS to generate O 2 •− . The electronic properties of biochar could be regulated by the edge nitrogen. Hence the biochar samples could act as electron mediators to promote electron transfer from sulfanilamide to metastable PMS. Pyridinic N and the C=O group were responsible for the non-radical pathway of 1 O 2 .
In addition to the N heteroatom, sulfur (S) and boron (B) heteroatoms could also be doped in biochar to improve its catalytic activity. Zhang et al. [39] synthesized N/Sdoped moso bamboo biochar. N/S doping increased the concentration of PFRs in biochar, which played the key role in activating PMS. The antibiotic removal efficiency was 92.23%, 88.86%, and 70.97% in 30 min in N-biochar/PMS, S-biochar/PMS, and N/S-biochar/PMS systems, respectively, which were higher than that in the biochar/PMS system (79.86%). The degradation efficiency was consistent with the concentration of PFRs. Dou et al. [17] showed that N and B co-doped biochar not only enhanced the catalytic performance but also switched the radical pathway into the electron transfer-dominated non-radical pathway, as confirmed by theoretical calculations. Due to the narrowest energy gap of N and B co-doping biochar, the electrons of tetracycline (HOMO, −8.202 eV) tended to transfer to BC-PDS* (LUMO, 2.806 eV) via an N/B co-doped biochar bridge (Figure 2d), triggering PDS decomposition without the generation of free radicals. In the catalytic reaction, it was proven that pyridinic N and BC 3 species were the main contributors in PDS activation to degrade tetracycline.

Metal-Loaded Biochar
Doping with transition metal/metal oxides (Mn, Ce, Cu, ZnO, Cr 2 O 3 , Fe 0 , Fe 3 O 4 , etc.) was also reported to enhance the catalytic performance via synergetic effects [13,72]. The composites can also avoid the aggregation of metal/metal oxides [73] and the potential risk of metal ion leaching. As shown by Xu et al. [13], benefiting from the synergistic effect between biochar and ZnO nanoparticles, more PFRs were created to improve catalytic efficiency. They extrapolated that the molecules with one phenolic hydroxyl, or two adjacent phenolic hydroxyls would produce PFRs through dehydration and electron transport with Zn. Then, PFRs in ZnO/biochar provided electrons to PS to produce SO 4 •− and •OH to remove tetracycline hydrochloride (Figure 3a).

Metal-Loaded Biochar
Doping with transition metal/metal oxides (Mn, Ce, Cu, ZnO, Cr2O3, Fe 0 , Fe3O4, etc.) was also reported to enhance the catalytic performance via synergetic effects [13,72]. The composites can also avoid the aggregation of metal/metal oxides [73] and the potential risk of metal ion leaching. As shown by Xu et al. [13], benefiting from the synergistic effect between biochar and ZnO nanoparticles, more PFRs were created to improve catalytic efficiency. They extrapolated that the molecules with one phenolic hydroxyl, or two adja- with Zn. Then, PFRs in ZnO/biochar provided electrons to PS to produce SO4 •− and •OH to remove tetracycline hydrochloride (Figure 3a). The modified biochar with iron-based compounds (Fe 0 /biochar [58,27], Fe2O3/biochar [74], Fe3O4/biochar [57,37], Fe-Mn oxides/biochar [59]) not only enhances the catalytic activity, but also makes the material magnetism to facilitate the recycling of magnetic compounds from water. Huang et al. [57] synthesized a recyclable magnetic rape straw biochar with the saturated magnetization at 18.45 emu/g (Figure 3b). The Fe3O4 content in the composites promoted PS activation for tetracycline hydrochloride degradation in water via radical and non-radical pathways. Fe 0 on the surface of biochar acts as an activation center to produce reactive oxygen species for the removal of antibiotics in wastewater. As reported by Ma et al. [58], PDS or dissolved oxygen reacted with Fe 0 to release Fe 2+ . PDS was activated with Fe 2+ to form SO4 •− . The part of SO4 •− transformed to •OH. Fe 2+ also reacted with dissolved oxygen to generate O2 •− which could produce 1 O2. Fe 2+ was oxidized to produce Fe 3+ , which could be reduced by Fe 0 into Fe 2+ . Moreover, the electron transfer mediated by biochar also facilitated the reduction process of Fe 3+ . Overall, SO4 •− , •OH, O2 •− , and 1 O2 contributed to sulfadiazine degradation. Mn doping in magnetic biochar can further enhance the activation of PS. Huang et al. [59] [13]. (b) The magnetization curve of the magnetic rape straw biochar (MRSB). Reproduced with permission from [57]. (c) Main catalytic mechanism of PS activation on Mn-doped magnetic biochar for tetracycline degradation. (d) Proposed corresponding tetracycline degradation pathways. Reproduced with permission from [59].
The modified biochar with iron-based compounds (Fe 0 /biochar [27,58], Fe 2 O 3 /biochar [74], Fe 3 O 4 /biochar [37,57], Fe-Mn oxides/biochar [59]) not only enhances the catalytic activity, but also makes the material magnetism to facilitate the recycling of magnetic compounds from water. Huang et al. [57] synthesized a recyclable magnetic rape straw biochar with the saturated magnetization at 18.45 emu/g (Figure 3b). The Fe 3 O 4 content in the composites promoted PS activation for tetracycline hydrochloride degradation in water via radical and non-radical pathways. Fe 0 on the surface of biochar acts as an activation center to produce reactive oxygen species for the removal of antibiotics in wastewater. As reported by Ma et al. [58], PDS or dissolved oxygen reacted with Fe 0 to release Fe 2+ . PDS was activated with Fe 2+ to form SO 4 •− . The part of SO 4 •− transformed to •OH. Fe 2+ also reacted with dissolved oxygen to generate O 2 •− which could produce 1 O 2 . Fe 2+ was oxidized to produce Fe 3+ , which could be reduced by Fe 0 into Fe 2+ . Moreover, the electron transfer mediated by biochar also facilitated the reduction process of Fe 3+ . Overall, SO 4 •− , •OH, O 2 •− , and 1 O 2 contributed to sulfadiazine degradation. Mn doping in magnetic biochar can further enhance the activation of PS. Huang et al. [59] concluded that the redox cycle of Fe (Fe 2+ /Fe 3+ ) and Mn (Mn 2+ /Mn 3+ /Mn 4+ ) were present in the catalytic reaction. The results demonstrated that iron-manganese oxide, functional groups, and defects of the composites activated PS to generate free radicals (Figure 3c). Huang et al. also found that tetracycline was degraded through hydroxylation, carbon chain-breaking, ring-opening, demethylation, and hydrogen abstraction (Figure 3d). Two-dimensional metal materials (layered double hydroxides (LDH), metal-organic frameworks (MOFs)) are used to combine with biochar to improve catalytic capacity synergistically. A biochar scaffold can improve the dispersion and stability of two-dimensional materials and trigger the non-radical route in PS-AOPs [21,[75][76][77]. MgFe-LDH/biochar was fabricated using derivatives from the activated sludge and applied for PMS activation to remove aqueous doxycycline [34]. The 1 O 2 -based non-radical pathway played an important role in doxycycline removal. Biochar-loaded MIL-53(Fe) derivatives (FexC/biochar) with surface area (1685 m 2 /g) were prepared to activate PDS for norfloxacin removal [21]. SO 4 •− , •OH, and 1 O 2 were involved in the degradation of norfloxacin in the system. Moreover, the FexC/biochar/PDS system exhibited excellent stability in different water bodies.

Non-Metal Heteroatoms and Metal Co-Modified Biochar
Non-metal and metal species can modify biochar to improve its catalytic performance synergistically. Xiao et al. [60] embedded Fe and Ce into N-enriched biochar (Fe/Ce/Nbiochar) for PMS activation to remove metronidazole. The second-order rate constant of the Fe/Ce/N-biochar/PMS system was 0.0566 min −1 , which was 10.5 times greater than that of the biochar/PMS system (0.0054 min −1 ). The Fe and Ce oxides on the biochar served as the centers to activate PMS, while N doping increased the porosity and surface area of biochar, and enhanced the PMS activation capacity. The results revealed that C=O groups and graphitic N in biochar activated PMS via a non-radical pathway, and the redox cycle of Fe (Fe 2+ /Fe 3+ ) and Ce (Ce 3+ /Ce 4+ ) participated in the radical pathway. Liu et al. [20] focused on the preparation of Fe and N co-doped biochar, due to the improved surface affinity of catalysts by N doping and the high effectiveness, recoverability, and nontoxicity of iron.

Future Perspectives Considering Sustainability
In 2015, the United Nations General Assembly proposed the Sustainable Development Goals (SDGs), containing 17 items [78]. The sustainable biochar used for antibiotic treatment in PS-AOPs assists in the partial achievement of SDGs (Figure 4). The role of valued-added biochar derived from waste biomass can promote the commercialization of biochar (SDG 11) and the creation of jobs (SDG 8) and provide a strategy for carbon footprint reduction as well as climate change (SDG 13). The biochar/PS technology can degrade antibiotics, thus reducing pollution to life below water and human health (SDG 3, 6 and 14). In addition, the biochar/PS system can serve as an alternative water treatment agent (SDG 12).

Technical Aspects
Regarding the large-scale applicability of pristine biochar and modified biochar as discussed above, biochar can be considered as a promising candidate for PS activation to efficiently degrade antibiotics ( Table 3). The performance of the biochar/PS system under A surge of interest has occurred towards the application of biochar to satisfy the sustainability requirements, which benefits the commercialization of biochar products. Although great progress has been made, the following issues need to be addressed in the future to improve the technical feasibility, economic feasibility, and environmental safety.

Technical Aspects
Regarding the large-scale applicability of pristine biochar and modified biochar as discussed above, biochar can be considered as a promising candidate for PS activation to efficiently degrade antibiotics ( Table 3). The performance of the biochar/PS system under realistic conditions is identified as an aspect of its sustainability concern, whereas most of the current reports have been conducted in simulated or artificial wastewater rather than actual wastewater. Considering the complexity of actual wastewater, the performance in multi-pollutant systems in actual wastewater needs to be investigated. The efficient catalytic activity is attributed to the abundant active sites in biochar catalysts (Tables 2 and 3). Novel technologies should be developed to further analyze the role of active sites at the molecular level, to provide direct evidence of the radical and non-radical pathways.

Toxicity Assessment
Toxicity assessments during the production and application of biochar are critical to satisfy sustainability. Risks to occupational health and safety can occur through the exposure via dermal, oral, inhalational, and ocular routes [79]. Biochar may contain toxic compounds, such as heavy metals or organics (polycyclic aromatic hydrocarbons and polychlorinated aromatic compounds, etc.) [80]. The contents of the toxic matters generally depend on the feedstock and preparation methods [14,56,81]. However, to date, the toxicity analysis of biochar catalysts used in biochar/PS system has not been well studied and documented.
Highly toxic intermediates can be generated in the water treatment process [82,83]. For example, the intermediate (m/z 477.15) of tetracycline was deemed as the molecule leading to the toxicity of the solution [84]. Additionally, 4-nitro-sulfamethoxazole as one of the sulfamethoxazole transformation products was found to be carcinogenic and mutagenic [85]. Few researchers analyzed the toxicity of products from antibiotics degradation in the biochar/PS system. For instance, Wang et al. [86] found that sulfamethoxazole significantly affected the growth of Chinese cabbage seed root. However, the N-biochar/PMS system efficiently reduced the phytotoxicity of sulfamethoxazole and its degradation products. Xiao et al. [60] evaluated the exposure risk of the degradation products of metronidazole in the Fe/Ce/N-BC/PMS system using 3-(4,5-dimethyl-2-thia-zolyl)-2, 5-diphenyl-2Htetrazolium bromide (MTT) assay (A375 skin cell line). The results showed that most cells survived in the reaction solutions. Accordingly, the ecotoxicity of biochar and degradation intermediates are indispensable research topics for the application of the biochar/PS system in the future.

Economic and Life Cycle Assessment
Consideration of the costs in the production of biochar and application of the biochar/PS system is important for commercialization. The main production costs refer to biomass collection, chemicals, electricity, equipment maintenance, transportation, labor, and so on. Du et al. [87] calculated the economic value of biochar prepared via pyrolysis at 550 • C. The biochar yields were 42.34%. The net production cost of the biochar was estimated to be USD 0.18/kg. However, surface modifications of biochar with other chemicals are required to promote PS activation (Table 3), leading to increased production costs of the derived catalysts. Cheng et al. [88] assessed the production costs of biochar activated with potassium hydroxide (KOH). Considering the costs of biomass, KOH, electricity, and transport, the total cost of the biochar was USD 9.82/kg, which was lower than that of activated carbon (~USD 45.71/kg) sold in Henan Huasheng Charcoal Industry Ltd. (Henan, China), but higher than that of unmodified biochar. Future studies are expected to find ways to reduce the production costs of the functionalized biochar to satisfy the sustainability considerations [89]. It is also necessary to predict the cost of the biochar/PS system in application. Wang et al. [90] evaluated the cost of sodium persulfate (USD 3.87/kg) and sludge-derived biochar (USD 0.222-0.584/kg). Their calculation of biochar/PS system for treating 1 L membrane bio-reactor effluent with biochar of 5 g/L and PS of 150 mM was less than USD 0.16. Within this context, biochar can be considered as a cheap and cost-effective option for treating antibiotic-polluted water in PS-AOPs, though more studies are required to further enhance the economic feasibility of biochar materials.
Concerns have been raised in relation to the environmental sustainability of a newly proposed technology, rather than focusing solely on technical efficiency. Life cycle assessment (LCA) is one of the major tools for the analysis of environmental impacts throughout the whole life cycle of a product/process [91]. Huang et al. [92] compared the Fenton oxidation of trichloroethylene by biochar synthesized at various microwave power levels (200-400 W). According to the removal efficiency and LCA results, the microwave power level of 300 W induced the highest catalytic effect and the lowest environmental impact. However, the LCA evaluation for the use of biochar in PS-AOPs is still missing in published reports.

Conclusions
This review summarized biochar for the treatment of antibiotic-polluted water in PS-AOPs. The radical (SO 4 •− , •OH and O 2 •− ) and non-radical ( 1 O 2 and surface electron transfer) processes contribute to the degradation of antibiotics. The high specific surface area of biochar and the active sites on the biochar surface (PFRs, oxygen-containing groups, defects, sp 2 carbon network, heteroatoms, the redox cycle of metal ions, and oxygen vacancy) are responsible for PS activation to remove antibiotics. Generally, the biochar applied in the PS-AOPs is divided into pristine biochar, non-metal heteroatom-doped biochar, metal-loaded biochar, and non-metal heteroatoms and metal co-modified biochar. Pristine biochar has a relatively low catalytic efficiency, which is related to the limited active sites. The contents of active sites can be regulated through heteroatom doping and metal loading, thus enhancing the catalytic performances of pristine biochar. The synthesis and application of biochar materials can be a sustainable option for converting biomass waste into value-added biochar, resulting in the partial achievement of SDGs. The sustainable prospective of biochar applied in PS-AOPs for the treatment of antibiotics is also discussed, considering the technical aspects, toxicity assessment, and economic and life cycle assessment, to promote the further development of biochar materials. Thus, this review will improve the basic understanding of utilization of biochar in PS-AOPs to remove antibiotics and provide preliminary guidance for real-word application and commercialization of biochar products.

Conflicts of Interest:
The authors declare no conflict of interest.