Professional Documents
Culture Documents
Review
H I G H L I G H T S G R A P H I C A L A B S T R A C T
A R T I C L E I N F O A B S T R A C T
Editor: Qilin Wang The preparation of biochar from digestate is one of the effective ways to achieve the safe disposal and resource
utilization of digestate. Nevertheless, up to now, a comprehensive review encompassing the factors influencing
Keywords: anaerobic digestate-derived biochar production and its applications is scarce in the literature. Therefore, to fill
Characteristics of digestate this gap, the present work first outlined the research hotspots of digestate in the last decade using bibliometric
Biochar
statistical analysis with the help of VOSviewer. Then, the characteristics of the different sources of digestate were
Modification method
summarized. Furthermore, the influencing factors of biochar preparation from digestate and the modification
Anaerobic digestion
Resistance genes methods of digestate-derived biochar and associated mechanisms were analyzed. Notably, a comprehensive
synthesis of anaerobic digestate-derived biochar applications is provided, encompassing enhanced anaerobic
digestion, heavy metal remediation, aerobic composting, antibiotic/antibiotic resistance gene removal, and
phosphorus recovery from digestate liquor. The economic and environmental impacts of digestate-derived bio
char were also analyzed. Finally, the development prospect and challenges of using biochar from digestate to
combat environmental pollution are foreseen. The aim is to not only address digestate management challenges at
the source but also offer a novel path for the resourceful utilization of digestate.
* Corresponding authors.
E-mail addresses: zhaojianwei@qut.edu.cn (J. Zhao), yjsun1971@126.com (Y. Sun).
https://doi.org/10.1016/j.scitotenv.2023.168822
Received 5 September 2023; Received in revised form 21 November 2023; Accepted 22 November 2023
Available online 1 December 2023
0048-9697/© 2023 Elsevier B.V. All rights reserved.
Z. Fu et al. Science of the Total Environment 912 (2024) 168822
2
Z. Fu et al. Science of the Total Environment 912 (2024) 168822
Fig. 1. Statistical analysis of digestate bibliometrics (a Distribution of annual number of digestate publications and changes in citation frequency, 2013–2022; b
Distribution of hotspots of digestate keywords, 2013–2022; c Distribution of top 10 disciplines of digestate research, 2013–2022; d Top 25 countries and regions in
terms of number of citations in digestate literature, 2013–2022).
3
Z. Fu et al. Science of the Total Environment 912 (2024) 168822
(Kabaivanova et al.,
(Kabaivanova et al.,
2020)
2022)
2022)
to treat digestate poses a severe challenge to the traditional biogas in
dustry. Incineration and landfilling are common methods for solid waste
disposal, also applicable to digestate, but these approaches come with
high environmental risks and low resource utilization efficiency (Luo
carbon
Fixed
2.54
14.9
21.6
20.2
et al., 2020).
/%
–
–
–
–
–
–
–
–
Considering the nutrient-rich composition of digestate, it can be used
as animal feed, crop fertilizer, and more (Song et al., 2021; Ham
merschmiedt et al., 2021). For instance, Xu et al. (2017) indicated that
solids
Total
24.8
9.63
/%
34
fermented digestate can be used as raw materials for feeding pigs, and
–
–
–
–
–
–
–
–
the addition of ≤15 % fermented digestate to diet of pigs can increase
NH4+-
(g/kg)
the weight gain. However, because of many inputs derived human and
0.234
0.244
0.177
0.175
4.7
–
–
–
–
–
–
–
–
–
using it as fertilizer directly without proper treatment, as it could in
34.3–53.5
40.3–56.5
42.6–50.6
crease soil salinization risks and negatively impact on the crop growth
20.331
15.942
22.72
34.83
31.9
/%
TC
livestock feed can lead to excessive heavy metal content in manure, and
–
heavy metals are also present in organic household waste and sludge
57.87
60.18
74.38
60.21
63.46
(Bernardo et al., 2020; Eid et al., 2017). These factors contribute to the
58.8
50.1
85.1
78.4
79.8
/%
VS
–
–
0.39
1.35
1.09
0.3
0.4
/%
S
0.23
1.15
1.18
3.67
2.84
–
–
–
2.07
1.01
0.86
0.39
0.94
0.71
/%
–
–
–
1.9
2.1
2.0
/%
TN
2022). Moreover, HTC does not require a drying step and has a higher
biochar yield compared to pyrolysis. However, the preparation of solid
8960
(mg/
COD
688
591
–
–
–
–
–
–
–
–
–
–
–
Wet fermentation
fermentation
fermentation
–
–
35.8
28.7
15.7
Ash
/%
–
–
digestate pyrolysis
80.27
87.84
85.62
/%
–
–
–
–
7.62
7.88
8.4
8.9
pH
–
–
–
–
Chicken manure
Swine manure
Raw materials
Kitchen waste
Kitchen waste
Kitchen waste
Energy crops
Cow manure
Wheat straw
Wheat straw
2022; Ahmed and Hameed, 2020; Das et al., 2021). Generally, feed
waste
Table 1
Sludge
Straw
stocks with high cellulose and hemicellulose content tend to promote the
formation of oxygen-rich groups on biochar. In contrast, source
4
Z. Fu et al. Science of the Total Environment 912 (2024) 168822
materials with high lignin content may lead to a highly aromatic internal pores within the feedstock, subsequently leading to an
structure within the biochar (Das et al., 2021; Hassan et al., 2020; Ortiz augmentation in both surface roughness and porosity (Liu et al., 2020).
et al., 2020). Table 2 presents the structural characteristics of biochar derived from
In their work, Wang et al. (2021) discovered that under identical various digestate feedstocks at different pyrolysis temperatures. How
conditions, biochar produced from straw digestate exhibited a larger ever, it is not always the case that higher pyrolysis temperatures result in
specific surface area when compared to biochar derived from pig and larger specific surface areas of biochar. In certain scenarios, biochar
chicken manure digestate. Furthermore, the biochar produced from produced through high-temperature pyrolysis exhibits lower specific
straw digestate had a higher carbon content, but a lower hydrogen surface areas. Liu et al. (2022b) found that when the pyrolysis temper
content. Yu et al. (2016) compared the specific surface area of biochar ature increased from 800 ◦ C to 1000 ◦ C, the specific surface area of food
from two different feedstocks, swine manure digestate and straw waste digestate-derived biochar decreased from 76.72 m2/g to 68.95
digestate, and the results showed that the specific surface area of swine m2/g. Wang et al. (2021) prepared biochar from pyrolysis of straw
manure digestate-derived biochar prepared by pyrolysis at 550 ◦ C for 2 h digestate, swine manure digestate and chicken manure digestate,
was significantly smaller than straw digestate-derived biochar. These respectively, and the results showed that when the pyrolysis tempera
may be due to the fact that straw digestate is enriched with more lignin ture increased from 550 ◦ C to 600 ◦ C, the specific surface area of biochar
and cellulose. Studies have shown that feedstocks with more lignin, prepared from straw, swine manure, and chicken manure digestate
cellulose and hemicellulose are more likely to form pores and higher decreased from 36.2869 m2/g, 31.7341 m2/g and 30.8243 m2/g to
surface area during pyrolysis (Cong et al., 2022). Usually, lignin-rich 32.9237m2/g, 29.2719m2/g and 29.2335m2/g, respectively. This phe
digestate-derived biochar has higher carbon content, larger specific nomenon may be caused by the high temperature that causes part of the
surface area and stronger aromaticity, which is favorable for pollutant pore structure of the digestate-derived biochar to begin to collapse and
removal (Huang et al., 2019). Biochar prepared from biomass with high gradually melt, the formation of the liquid phase in the pore space is
lignin content has higher yield and the higher heating value (HHV). filled and thus leads to a reduction in the specific surface area.
Usually, the HHV of biomass components follow the order, lignin > In addition, the pH of digestate-derived biochar varies with pyrolysis
cellulose > hemicellulose > ash (Kumar et al., 2020). To sum up, temperature. It is shown that the pH of biochar increases with pyrolysis
digestate with higher lignin content can be preferred for the preparation temperature, and at 400–600 ◦ C, >80 % of the unstable component
of biochar. carbon in the biochar was converted to difficult-to-degrade aromatic
carbon with increasing temperature (Das et al., 2021). Cong et al. (2022)
4.2. Pyrolysis temperature found that the pH of digestate-derived biochar gradually increased with
increasing temperature, and when the pyrolysis temperature increased
Pyrolysis refers to the thermal decomposition of dried biomass under from 300 ◦ C to 700 ◦ C, the pH of the sludge digestate-derived biochar
anaerobic or oxygen-deficient conditions at temperatures ranging from increased from 7.05 to 9.29. The increased pH may be due to the
300 to 900 ◦ C. During this process, isomerization, cleavage of chemical decomposition and volatilization of nitrogen compounds and sulfides in
bonds, and small molecule aggregation reactions occur (Cha et al., the digestate at 700 ◦ C. Alghashm et al. (2018) prepared biochar from
2016). Pyrolysis is a thermal disposal technique that simultaneously food waste digestate and the pH of digestate-derived biochar increased
accomplishes the treatment of complex waste components and the from 9.19 to 12.52 as the pyrolysis temperature increased from 400 ◦ C to
production of high-value added products. It offers advantages of low 900 ◦ C. This may be related to the polymerization or condensation re
energy consumption and minimal emissions (Ding et al., 2016). Previous action of aliphatic compounds on the surface of biochar (Stefaniuk and
studies indicates that pyrolysis was effective in achieving high conver Oleszczuk, 2015). Studies have shown that at lower pyrolysis tempera
sion rates when applied to digestate, with most of the digestate being tures the functional groups on the surface of biochar are mainly domi
transformed into resources such as biochar for beneficial utilization nated by hydroxyl, phenolic hydroxyl groups and carboxyl groups, but
(Neumann et al., 2015). Temperature, as the most critical control vari with increasing pyrolysis temperatures, the functional groups on the
ables in the pyrolysis process, has a significant effect on the yield and surface of biochar continue to deoxygenate, dehydrate and condense to
quality of pyrolysis products. Generally, pyrolysis temperature is an form carbonyl and quinone groups and other functional groups (Zhang
important factor affecting the yield of biochar, with the increase of et al., 2019). As the temperature rises, the organic components in bio
temperature gases such as CH4, CO, and CO2 are emitted more, and the char begin to decompose in large quantities, while the increase of
bound water and volatile organic compounds (VOCs) in the biomass are inorganic components, i.e., the ash content. Ash in biochar is rich in
gradually decomposed and precipitated to form biochar with porous mineral elements such as potassium, calcium, sodium, and magnesium,
structure (Yuan et al., 2015). To further investigate the effect of pyrol as well as carbonates that become alkaline when dissolved in water.
ysis temperature on the biochar yield of digestate, Liu et al. (2020) Generally, a higher ash content in biochar corresponds to a higher pH in
conducted an experimental investigation using kitchen waste anaerobic the biochar (Zheng et al., 2022). In addition, the increase in pH may be
fermentation digestate, and it was shown that the yield of biochar caused by the enrichment of alkaline inorganic components and the
showed a decreasing trend with increasing pyrolysis temperature, from elimination of organic matter in biochar. As the temperature increases,
44.26 % at 400 ◦ C to 36.13 % at 800 ◦ C. Alghashm et al. (2018) prepared acidic functional groups such as carboxylic acids in the biomass matrix
biochar from kitchen waste digestate, and when the pyrolysis temper are eliminated, leading to an increase in the concentration of alkaline
ature was increased from 400 ◦ C to 600 ◦ C, the yield of biochar from functional groups, which increases the pH of the digestate-derived bio
digestate decreased from 70.35 % to 66.02 %. This trend may be char (Al-Wabel et al., 2013).
attributed to the continuous increase in temperature, leading to the In summary, within a certain temperature range, the increase in
gradual gasification and secondary decomposition of organic substances pyrolysis temperature leads to an augmentation in the specific surface
within the biochar, formed from initial decomposition (Al Afif et al., area, porosity, carbon content, thermal stability, pH, and ash content of
2020). Consequently, this results in a decreasing biochar yield. digestate-based biochar. However, the yield, polarity, and acidic oxygen
The porosity and specific surface area of biochar are also affected by functional groups decrease with the elevation of pyrolysis temperature.
the pyrolysis temperature. Numerous studies indicate that as the py By analyzing the effect of different pyrolysis temperatures on the per
rolysis temperature increases, the porosity of biochar increases, formance of digestate-derived biochar in the literature, pyrolysis tem
accompanied by an enlargement of its specific surface area. This phe perature in the range of 550 ◦ C to 900 ◦ C is recommended for digestate-
nomenon is primarily attributed to the release of substantial heat from derived biochar production depending on the properties of digestate-
the feedstock during heating, causing gaseous products to escape from derived biochar, such as specific surface area, pH, etc.
the solid phase. This process results in the expansion and disordering of
5
Z. Fu et al. Science of the Total Environment 912 (2024) 168822
Table 2
Structural characteristics of biochar at different digestate feedstocks and pyrolysis temperatures.
Types of digestate Pyrolysis temperature Yield Specific surface area Average pore size Micropore volume Reference
(◦ C) (%) (m2/g) (nm) (cm3/g)
Wine lees digestate 300 – 2.442 1.195 0.0016 (Cong et al., 2022)
500 4.452 1.189 0.0029
700 5.531 1.191 0.0028
Mushroom digestate 300 – 2.102 1.191 0.0011 (Cong et al., 2022)
500 6.631 1.190 0.0036
700 70.271 1.176 0.0553
Sludge digestate 300 – 2.493 1.196 0.0010 (Cong et al., 2022)
500 3.122 1.191 0.0021
700 29.874 1.183 0.0237
Food waste digestate 400 70.35 17.91 – – (Alghashm et al., 2018)
500 68.25 19.05
600 66.02 21.68
Pig manure digestate 400 85.51 10.7435 – – (Wang et al., 2021)
500 84.58 22.6527
550 84.46 31.7341
Chicken manure digestate 400 86.73 10.3792 – – (Wang et al., 2021)
500 86.61 24.2949
550 86.47 30.8243
Straw digestate 400 86.96 12.8362 – – (Wang et al., 2021)
500 82.23 27.392
550 81.37 36.2896
Studies have shown that pyrolysis time affects the yield and Heating rate plays an important role in the pyrolysis process because
carbonization of biochar, and longer residence time during pyrolysis the rate of change in heat affects the properties of the pyrolysis products,
leads to more carbonized biochar with less unstable organic matter, especially the biochar, such as porosity, surface area, volatile compound
which is less susceptible to microbial attack (Leng and Huang, 2018). content and biochar yield (Rangabhashiyam and Balasubramanian,
Furthermore, at the same pyrolysis temperature, the yield of biochar 2019). It has been shown that as the heating rate increases, the biochar
tends to decrease with an increase in residence time (Zhang et al., yield decreases while the gas production increases, suggesting that the
2015a). In a work examining the influence of residence time on the higher heating rate promotes the cleavage of organic components and
specific surface area and pore characteristics of biochar, Lu et al. (1995) volatiles in the biochar to form gaseous products (Li et al., 2021). Py
reported that within the range of 500–900 ◦ C, both specific surface area rolysis can be categorized into three types based on the rate of heating:
and pore area increase with longer residence times. However, when the slow pyrolysis, fast pyrolysis and flash pyrolysis (Fahmy et al., 2020).
residence time exceeds 2 h, both specific surface area and pore area start Slow pyrolysis usually occurs in slow heating rate (5–7 ◦ C/min), with
to diminish. Particularly, at high temperatures, a residence time high biochar yield (<35 %) and low yield of bio-oil and syngas (Feng and
exceeding 2 h leads to a rapid reduction in both specific surface area and Lin, 2017). In this process, long residence time (several hours or days)
pore area. Li et al. (2018) explored the effect of different pyrolysis time results in a fully pyrolyzed biochar product with highly stabilized car
on biochar from digestate and found that the adsorption of ammonia bon, which does not undergo microbial degradation over long periods of
nitrogen by biochar increased firstly and then decreased with the in time (Mukherjee et al., 2022). The main characteristic of fast pyrolysis is
crease of pyrolysis time. In addition, the maximum adsorption capacity thermal degradation at high heating rate (300 ◦ C/min) with short resi
was reached at the pyrolysis temperature of 550 ◦ C and pyrolysis time of dence time (<5 s), so that lignocellulosic components and organic
2 h (Li et al., 2018). The reason for this may be since under the short matter decompose rapidly during thermal treatment. This conversion
pyrolysis time, the digestate is not sufficiently pyrolyzed, resulting in provides the high bio-oil yield (75 %) followed by low yield of syngas
incomplete carbonization. This may result in a small specific surface and biochar (Feng and Lin, 2017). Flash pyrolysis is performed at high
area of the biochar, which could not have enough ammonia nitrogen temperature process using higher heating rate (1000 ◦ C/s) and shorter
adsorption sites, and ultimately lead to a lower ammonia nitrogen residence time (30 ms-1.5 s), and the product is mainly bio-oil (<70 %)
adsorption capacity. Excessive pyrolysis time, on the other hand, may (Feng and Lin, 2017). Considering the stability and yield of biochar,
result in a decrease in surface organic functional groups of the biochar, slow heating rate is always the favorable option.
which can also have adverse effects on the adsorption of ammonia In conclusion, the characteristics of biochar prepared from digestate
nitrogen. are affected by the raw material of digestate, pyrolysis temperature,
However, it has also been shown that pyrolysis temperature is the pyrolysis time, heating rate and other factors. Pyrolysis temperature in
most important process parameter in determining the characterization the range of 550–900 ◦ C, slow heating rate (5–7 ◦ C/min), long reaction
of the resulting biochar compared to heating rate and residence time residence time, and digestate feedstock with high lignin content are the
(Tsai et al., 2018). The effect of residence time is usually dominated by preferred choices to enhance the stability and yield of biochar.
pyrolysis temperature, and it is sometimes difficult to give a direct
indication of the role of residence time on biochar stability (Leng and 5. Modification of biochar from digestate
Huang, 2018). In conclusion, strictly control the anaerobic conditions
and pyrolysis temperature, and appropriately prolong the residence time After anaerobic digestion, the complex and three-dimensional
can help the formation of good spatial structure of digestate-derived structure of lignin, cellulose and hemicellulose interconnection is
biochar. broken to a certain extent (Chen et al., 2019). Although digestate-
derived biochar exhibits larger specific surface area, pore volume, and
a highly chemically stable molecular structure, pure digestate-derived
biochar still possesses certain limitations and has room for
6
Z. Fu et al. Science of the Total Environment 912 (2024) 168822
improvement. To enhance the physicochemical properties of digestate- modification can increase the porosity, specific surface area, and
derived biochar, numerous researchers have employed various oxygen-containing functional groups (such as -OH) of biochar (Peng
methods to modify its characteristics. Studies indicate that modification et al., 2023). Alkaline modification similarly enhances the adsorption
of biochar can significantly enhance its activity and increase its potential performance of digestate-derived biochar. Yu et al. (2016) used KOH to
application in environmental remediation (Mohan et al., 2014). The modify swine manure digestate-derived biochar and straw digestate-
modification mechanism of biochar is shown in Fig. S1. Biochar modi derived biochar, and the experimental results showed that the modi
fication can be categorized into physical, chemical, and biological fied swine manure digestate-derived biochar and straw digestate-
modification, with chemical modification being the most common derived biochar both exhibited well ammonium adsorption perfor
approach. Depending on the modifying reagents employed, chemical mance in liquid fraction of digestate with the adsorption capacities of
modification includes acid treatment, alkaline treatment, modification 26.82 mg/g and 19.16 mg/g, respectively. Wongrod et al. (2018b) used
with metal salts or metal oxides, organic reagents, nanomaterials, KOH to modify sewage sludge digestate-derived biochar, and the results
oxidizing agents. indicated that the modified digestate-derived biochar increased the
adsorption capacity of As (V) by four times compared to unmodified
5.1. Acid modification biochar. However, if a careful washing procedure (column washing) is
not implemented, a strong release of inorganic and organic compounds
The common acid-modifying reagents mainly include HNO3, H2SO4, occurs in the biochar after KOH treatment, altering the adsorption
H3PO4, HCl, citric acid, acetic acid and so on. The acid modification can properties and affecting As (V) adsorption. It was shown that KOH
be accomplished in two ways: (1) the raw materials are mixed with acid modification effectively enhanced the adsorption capacity of digestate-
reagents and then pyrolyzed to synthesize biochar (Kumar et al., 2022); derived biochar, but also promoted As (III) oxidation, especially in the
(2) the raw materials are pyrolyzed to produce biochar, and then soaked case of incomplete washing (Wongrod et al., 2019). Therefore, contin
the biochar with acid reagents (Dong et al., 2017). Acid modification is uous and adequate washing of KOH-modified digestate-derived biochar
the most commonly used method to alter the surface properties of ad is crucial.
sorbents. Acid modification primarily involves promoting the dissolu
tion of soluble substances and generating a substantial amount of gas, 5.3. Metal salt solution, metal oxide modification
thereby increasing the porosity of biochar, enlarging its specific surface
area, and consequently enhancing its adsorption capacity (Cheng et al., The common metal salt and metal oxide modification reagents
2021). In addition, oxygen-containing functional groups formed by acid include FeCl3, MgCl2, AlCl3, ZnCl2, FeSO4, MgO, etc. The modification of
modification play an important role in adsorption (Hu et al., 2018). For metal salts or metal oxides can be accomplished in two ways: (1) the raw
example, HNO3 can increase the amount of -COOH on the surface of materials are mixed with metal salts or metal oxides and then pyrolyzed
biochar, and H3PO4 and H2SO4 can introduce functional groups such as to synthesize biochar; (2) the raw materials are pyrolyzed to produce
-SO3H, -P=OOH and -P=O (Jin et al., 2018; Xiong et al., 2018; Cheng biochar, and then soaked the biochar with metal salts or metal oxides
et al., 2017). Ma et al. (2023) employed HCl solution for the modifica (Wang and Wang, 2019). The addition of metal salt reagents or metal
tion of digestate-derived biochar. In comparison to the unmodified oxides can increase the metal element content in biochar, and the doping
biochar, the HCl-modified biochar exhibited a rougher surface, an of metal elements can lead to significant changes in the properties of
increased specific surface area, and a more enriched and oxygen- biochar. For instance, FeSO4/FeCl3 modification can generate γ-Fe2O3 or
functionalized porous structure. Furthermore, the acid-modified bio Fe3O4 on the surface of the biochar thus making the biochar magnetic
char demonstrated higher efficiency in the degradation of pollutants. and contributing to the recycling of the biochar (Wang and Wang,
Sheng et al. (2022) used citric acid reagent to modify biochar from 2019). ZnCl2 modification can be used as a dehydrating agent to lower
digestate, and the modified biochar from digestate showed excellent the carbonization temperature, inhibit tar production and promote
adsorption capacity for tetracycline, with an adsorption capacity of stomatal formation and fiber expansion, leading to an increase in the
58.25 mg/g, and the adsorption performance was increased by 6 times pore structure and specific surface area of the biochar (Liu et al., 2015).
compared with that of the original digestate-derived biochar. However, It has been shown that metal oxides or metal salts modified biochar has
acid modification also has certain drawbacks. Studies have shown that good electrostatic attraction, precipitation and anion exchange capacity
modified by acid washing not only removes minerals (K+, Ca2+, Mg2+, (Wu et al., 2019).
Fe3+, Al3+, etc.) from the ash in the biochar, but also releases potentially Metal salt solution, metal oxide modification similarly enhances the
toxic substances (VOCs, polycyclic aromatic hydrocarbons, etc.) that can adsorption performance of digestate-based biochar. Liu et al. (2019)
be harmful to the microbial community as the biochar ages (He et al., produced a magnetic digestate-derived biochar loaded with MgO by
2021a; Wang and Wang, 2019). pyrolysis through chemical co-precipitation of MgCl2/FeCl3 on mixed
In conclusion, acid modification increases the specific surface area of digestate from the garden and vegetables. It was found that the
biochar and enriches the surface functional groups of biochar, but it also adsorption of PO3−4 by the modified digestate-derived biochar at 600 C
◦
causes negative impacts on the environment. Therefore, the above was about 70 mg/g and it was about 3.5 times higher than that of the
possible problems should be considered when acid modification is car unmodified biochar, and the maximum adsorption capacity was up to
ried out. 149.25 mg/g. Xia et al. (2016) experimentally found that the maximum
specific surface area of digestate-derived biochar was prepared by
5.2. Alkali modification mixing swine manure digestate with ZnCl2 solution pyrolysis, and its
surface area was increased by 4.2 times compared with unmodified
In addition to acid modification, alkaline modification is also a digestate-derived biochar, and it had the maximum capacity of
commonly employed strategy. In comparison to acid modification, adsorption for As3+.
alkaline modification contributes to the improvement of H/C (stability), Modification with metal oxides or metal salt solutions can lead to the
N/C (alkalinity) and lower O/C (hydrophilicity) of biochar (Kumar partial blockage of pores in biochar. However, the specific surface area
et al., 2022). Common alkaline modifying agents include NaOH and of metal oxides is higher than that of low-specific-surface-area biochar
KOH. Alkali modification can be divided into two methods. In one (Trakal et al., 2016). Therefore, for biochar with low specific surface
method, alkali reagents are mixed with raw materials and then pyro area, modification with metal oxides or metal salt reagents can increase
lyzed to synthesize biochar (Balahmar et al., 2017). In another method, its specific surface area. On the other hand, high-specific-surface-area
biomass is mixed with alkali reagent and then pyrolyzed to synthesize biochar may experience a reduction in specific surface area due to
biochar under the anoxic conditions (Dong et al., 2017). Alkaline pore blockage. In addition, metal modification may cause the risk of
7
Z. Fu et al. Science of the Total Environment 912 (2024) 168822
leaching of metal ions. Study has shown that metal-modified biochar specific surface area and pore volume. Additionally, the tetracycline
could cause pollution of water bodies by shedding metal ions (Du et al., could form complexes with Cu (II) and attach to the biochar, further
2023). Moreover, functional agents used for metal-modified biochar improving the adsorption and degradation efficiency of tetracycline in
could release secondary pollutants such as metal ions, which has the water.
negative impact on the environment (Yang et al., 2021a).
5.6. Oxidizer modification
5.4. Organic reagent modification
The principle of oxidative modification involves oxidizing the sur
The common organic modifying reagents include chitosan, poly face substances of biochar and forming oxygen-containing functional
ethyleneimine, methanol, glutaraldehyde, urea, etc. Organic reagent groups on the biochar surface, thereby enhancing its adsorption capacity
modification can be divided into two ways: In one method, organic re for pollutants (Wang et al., 2019). The common oxidizing agents are
agent is mixed with raw materials and then pyrolyzed to synthesize H2O2, KMnO4, etc. Typically, oxidation-modified biochar is prepared by
biochar (Qiao et al., 2020). In another method, biomass is mixed with soaking the biochar in oxidizing agents, followed by filtration, washing
organic reagent and then pyrolyzed them to synthesize biochar (Kumar and drying (Hassan et al., 2020). Wongrod et al. (2018a) used H2O2 to
et al., 2022). Organic reagent modification plays an important role in modify the biochar from sewage sludge digestate, and the results
altering the properties of biochar and can cause changes in many aspects showed that the modified biochar had a strong adsorption capacity for
of biochar properties. Firstly, organic reagent modification can effec Pb in water. Jiang et al. (2018) modified swine manure digestate-
tively increase the abundance of functional groups on the surface of derived biochar with KMnO4, and it was found that the modified
biochar. It has been shown that chitosan can increase the content of -OH digestate-derived biochar had a larger specific surface area and pore
and -NH2 functional groups on the surface of biochar after modification volume, which were increased by 11.225 and 4.31 times, respectively,
due to the abundance of -OH and -NH2 (Shi et al., 2020). The cross- compared with that before modification. Moreover, the digestate-
linking reaction during the modification of polyethyleneimine also in derived biochar modified by KMnO4 formed the structure of MnOx,
troduces nitrogen-containing groups (Liu et al., 2015). In addition, which produced a strong adsorption effect on heavy metals and antibi
organic reagents can change the elemental composition of biochar and otics through the combination of the oxidation state of Mn (such as Mn3+
affect the aromaticity, polarity and hydrophilicity of the biochar surface and Mn4+) and different phases (such as β-MnO2, δ-MnO2, etc.) (Jiang
(Liu et al., 2015; Shi et al., 2020). Qiao et al. (2020) prepared modified et al., 2018).
biochar by mixing urea with digestate and then pyrolyzing it. The results Different types of modification approaches have indeed increased the
showed that the addition of urea introduced nitrogen-containing func biochar’s specific surface area and pore volume, as well as enriched the
tional groups into the biochar, which could strengthen and promote the variety and concentration of functional groups. However, these modi
interaction between the biochar and CO2, and thus significantly fications also come with certain drawbacks. Among them, the advan
improved the CO2 uptake of biochar from digestate. The maximum CO2 tages and drawbacks of each biochar modification methods are shown in
uptake (1.22 mmol g− 1) of the biochar prepared by pyrolysis was ach Table 3. Alkaline modification leads to higher surface aromaticity ratios
ieved when the mixing ratio of urea and digestate was 1:1. It has also and higher nitrogen to carbon ratios but lower oxygen to carbon ratios
been shown that organic reagents can promote the dissolution of compared to acid modification (Kumar et al., 2022). It is important to
harmful compounds such as polycyclic aromatic hydrocarbons and di note that acid or alkaline solution needs to be handled after modifica
oxins in biochar and reduce the environmental risks of biochar (Lyu tion, which complicates the biochar preparation process. Oxidizer
et al., 2016). modification can increase the oxygen-containing groups on the surface
of biochar. However, the cost and handling of oxidizers limit their
5.5. Nanomaterial modification application. To promote recycling of the oxidizer solution would be a
way to reduce costs. Compared with other chemical modifications,
Nanomaterials such as metal nanoparticles, graphene, graphene metal or metal oxide modifications are mainly used to increase the
oxide, carbon nanotubes, and magnetite nanoparticles are characterized active sites for adsorption and catalysis. However, studies have shown
by large specific surface area and high capacity for the adsorption of that metal-modified biochar could cause pollution of water bodies by
pollutants, but they are costly and have some environmental risks shedding metal ions (Du et al., 2023; Rajapaksha et al., 2016). There
(Anjum et al., 2019). The modification of biochar by nanomaterials has fore, further research measures should be taken to improve the stability
the characteristics of reducing the environmental risks and economic of metal ions on biochar. To sum up, when considering the modification
costs of nanomaterials, inhibiting their agglomeration, and preventing of biochar, various factors need to be taken into account, including costs,
them from being oxidized by air, while retaining the excellent properties byproducts, and the efficiency of pollutant remediation.
of nanomaterials (Zhu et al., 2018). Nanomaterial modification can be
divided into two ways: (1) the biomass feedstock is mixed with nano 6. Applications of digestate-derived biochar
particles and then pyrolyzed in the presence of nitrogen to synthesize
biochar; (2) the raw materials are pyrolyzed to produce biochar, and 6.1. Promotion of anaerobic digestion processes
then impregnated the biochar with nanoparticles (Hassan et al., 2020).
Studies have shown that biochar modified with nanomaterials usually Biochar, as a carbon-rich material, has the advantages of high carbon
exhibits great improvement in terms of functional groups, specific sur content, high cation exchange capacity, large specific surface area, and
face area, pore size distribution, surface active sites, catalytic degrada good stability compared to other carbon materials (Lee et al., 2017;
tion, and ease of separation, and has a strong pollutant removal capacity Rizwan et al., 2016; Zhao et al., 2022). Biochar used to enhance
(Tan et al., 2016). Wang et al. (2023d) used nanomagnetite to modify anaerobic digestion performance is mostly exogenously added, and the
digestate-derived biochar, and it was found that the specific surface area common feedstock for biochar production includes straw, wood, and
of digestate-derived biochar was increased by about 81.8 % after the livestock manure. In comparison with exogenous biochar, digestate-
modification. The larger specific surface area provided more attachment derived biochar offers geographical advantages. Digestate-derived bio
sites for microorganisms, facilitated the enrichment of microorganisms, char can be directly produced from digestate and utilized within local
favored the rapid establishment of direct interspecies electron transfer biogas systems, thereby further enhancing anaerobic digestion. This
(DIET), and promoted the production of methane. Fu et al. (2017) approach promotes system circularity, cost savings, and reduction in
loaded nano-Cu onto digestate-derived biochar, and the modified greenhouse gas (GHGs) emissions (Li et al., 2022a; Zhao et al., 2021b).
digestate-derived biochar was experimentally found to have a larger Moreover, digestate-derived biochar is easier to obtain than other
8
Z. Fu et al. Science of the Total Environment 912 (2024) 168822
Table 3
Advantages, drawbacks and suitable conditions of chemical modification methods.
Modification Advantages Drawbacks Suitable conditions Reference
methods
Acid modification Improve the porosity of biochar, increase Microporous walls corrode due to acidic Chen et al. (2021) mixed biochar with 0.2 (Sajjadi et al.,
the specific surface area, and introduce treatment; as biochar ages, it releases mol/L H2SO4 in a thermostatic oscillator 2019; Chen et al.,
acidic oxygen-containing functional groups potentially toxic substances for 24 h at 60 ◦ C at 200 r⋅min− 1 and the 2021; Lu et al.,
ratio of biochar to acid reagent was 1:50. 2021)
Lu et al. (2021) mixed dried eucalyptus
powder with 40 wt% H3PO4 solution for 10
h, and the impregnation ratio was 1:2, then
dried and pyrolyzed it.
Alkali modification Increase the porosity of biochar, increase KOH modification requires an Yu et al. (2016) immersed 1 g digestate in 1 (Xu et al., 2022a;
the specific surface area, introduce unavoidable washing process, and the g/L KOH solution for 24 h, then dried and Kumar et al.,
hydroxyl functional groups; increase the H/ pore size is prone to collapse at high pyrolyzed it. 2022; Yu et al.,
C, N/C and lower O/C of biochar pyrolysis temperatures Xu et al. (2022a) mixed 10 g biochar with 2016)
500 mL KOH (80 g/L) in a magnetic stirrer
for 24 h.
Metal salt solution, Increase the active sites for adsorption and Block part of the pores of the biochar, Wu et al. (2019) mixed 50 g biochar with 1 (Wu et al., 2019;
metal oxide catalysis of biochar and has good and the high specific surface area M MgCl2 solution, then dried and pyrolyzed Trakal et al.,
modification electrostatic attraction, precipitation and biochar will be reduced due to the it. 2016; Long et al.,
anion exchange capacity blockage of the pores Long et al. (2019) impregnated the biochar 2019)
in 1 mol/L metal salt solution for 24 h and
the impregnation ratio was 3 g:1 g.
Organic reagent Enrich the functional groups on the surface Chitosan-modified biochar is subject to Qiao et al. (2020) mixed urea with (Gao et al., 2022;
modification of biochar; promote the dissolution of ionic inhibition digestate and then pyrolyzing it. The Shi et al., 2020;
harmful compounds in biochar and reduce optimal weight ratio of urea and digestate Qiao et al., 2020)
the environmental risk of biochar was 1:1
Nanomaterial Show great improvement in terms of Biochar modified with metal Fu et al. (2017) dissolved biochar (2.16 g) (Akhil et al., 2021;
modification functional groups, specific surface area, nanoparticles, leaching of metal ions in 250 mL of 27 mmol/L CuCl2⋅2H2O Tan et al., 2016;
pore size distribution, surface active sites, easily leads to secondary pollution solution with stirring and then added 250 Fu et al., 2017)
catalytic degradation and ease of separation mL of 54 mmol/L Cu nanoparticles
Oxidizer Oxidize the surface material of biochar and The adsorption capacity of oxidant- Wongrod et al. (2018b) placed 2 g biochar (Xu et al., 2022a;
modification form oxygen-containing functional groups modified biochar varied with the target in 20 mL 10 % H2O2 solution and oscillated Wongrod et al.,
on the surface of biochar pollutant and exhibited a low at 25 ◦ C for 2 h 2018b)
adsorption capacity for methylene blue Xu et al. (2022a) mixed 10 g biochar with
100 mL KMnO4 (0.5 g/L) in a magnetic
stirrer for 24 h
9
Z. Fu et al. Science of the Total Environment 912 (2024) 168822
10
Z. Fu et al. Science of the Total Environment 912 (2024) 168822
dissolved substrates, effectively alleviated ammonia nitrogen inhibition, prepared at 800 ◦ C had excellent performance and the maximum
and improved the buffering capacity of the anaerobic digestion system. adsorption capacity of As (III) was up to 69.03 mg/g as determined by
In conclusion, biochar can effectively alleviate the toxicity inhibition the Langmuir isotherm model. Characterization revealed that the
caused by ammonia nitrogen in anaerobic digestion systems, thereby mechanism of action involved precipitation, redox, electrostatic effect
enhancing anaerobic digestion capacity. However, further clarification and surface complexation.
is needed regarding the mechanisms by which digestate-derived biochar However, it has been shown that although the application of swine
mitigates the toxic effects of ammonia inhibition. manure digestate-derived biochar to the soil significantly reduced the
heavy metal content of the plants, it also increased the heavy metal
6.2. Remediation of heavy metals content of the soil due to the heavy metal richness of swine manure
digestate-derived biochar (Ayaz et al., 2022). Therefore, when using
In the process of rapid industrialization and development, heavy digestate-derived biochar for heavy metal remediation, the type and
metal pollution has become a significant ecological and environmental content of heavy metals in the biochar should be tested and considered
issue that cannot be underestimated. Due to its well-developed porous for possible problems such as heavy metal leaching.
structure, abundant surface functional groups, and strong cation ex
change capacity, biochar possesses significant advantages and potential 6.3. Enhanced aerobic composting
applications in heavy metal remediation (Qiu et al., 2021). Currently, a
considerable amount of research has focused on the remediation efficacy Aerobic composting is a cost-effective and socially acceptable
of digestate-derived biochar for pollutants such as lead, cadmium, method for treating solid or semi-solid biodegradable wastes. It can not
copper, arsenic, mercury, and nickel in contaminated soils and water only effectively solve the environmental problems of waste, but also the
bodies. The application and remediation effects of different types of final compost product can be used to rehabilitate the soil and contribute
digestate-derived biochar on heavy metals are summarized in Table S2. to the development of green economy (Ramzani et al., 2017; Yuan et al.,
In general, biochar directly affects heavy metals mainly through 2017; Zhao et al., 2021c). However, during aerobic composting, if good
electrostatic action, complexation, precipitation, ion exchange, physical ventilation and timely turning of the heap are not done, the heap will
adsorption, and redox action (Liu et al., 2022c). The mechanism of ac locally agglomerate, resulting in an anaerobic zone, when the activity of
tion is shown in Fig. 4. Heavy metal ions can undergo various in methanogenic bacteria will produce CH4. In addition, the heap may also
teractions with the surface of biochar. They can exchange ions with release H2S, NH3, VOCs and other malodorous substances, which not
surface ions like Ca2+, Mg2+, Na+. They can also form co-precipitates only pollute the environment but also pose a serious threat to people’s
with metal hydroxides. Additionally, they can complex with functional health (Chen et al., 2017; Yuan et al., 2023).
groups present on the surface, such as CO2− 3− 2−
3 , PO4 , SO4 and oxygen- Recently, the selection of biochar as an additive in aerobic com
containing functional groups (e.g., -COOH, -OH). Moreover, since the posting has become a hot research topic due to its good physical and
surface of biochar is often negatively charged, positively charged metal chemical adsorption properties, stable porous structure and low cost. It
ions like Hg2+, Cd2+ and Cu2+ are easily adsorbed onto the surface of mainly affects the physical and chemical properties, GHGs emissions
digestate-based biochar. and other factors in the composting process, thus improving the envi
From the characterization analysis, Liu et al. (2022f) found that Hg2+ ronmental conditions of the pile, increasing microbial activity and
was attached to digestate-derived biochar mainly through pore accelerating the decomposition process. It was shown that biochar cre
adsorption, electrostatic interactions and surface complexation. Ho et al. ates a favorable microbial environment for nitrifying bacteria, aiding in
(2017) successfully prepared biochar from sewage sludge digestate the conversion of ammonia to nitrate and thus reducing nitrogen loss
under pyrolysis at 600 ◦ C for 90 min, and the adsorption capacity of six during the composting process (Wang et al., 2023a). Adding biochar can
heavy metals was in the order of Pb2+ > Cd2+ > Cu2+ > Zn2+ > Ni2+ > also improve the porosity of the compost pile, increase oxygen con
Cr6+. Among them, the adsorption of Pb2+ was as high as 51.20 mg/g. centration, and thereby inhibit the growth of methane-producing bac
Liu et al. (2022b) pyrolyzed food waste digestate at 400 ◦ C–1000 ◦ C for teria, leading to a reduction in CH4 production (Liu et al., 2017).
100 min to obtain digestate-derived biochar for heavy metal remedia Additionally, biochar provides a suitable protective space and essential
tion of As (III) in water. It was showed that the digestate-derived biochar nutrients (such as potassium, calcium, sodium, magnesium) for
11
Z. Fu et al. Science of the Total Environment 912 (2024) 168822
thermophilic microorganisms during the active phase (Lv et al., 2023). increase the temperature of food waste composting, accelerate the
This improves the composting environment and ensures the quality of degradation of aromatic proteins, and form humic acids quickly, which
the compost product. In addition, biochar, with its strong adsorption led to rapid humification of the composting process. Furthermore, the
capacity and well-developed pore structure, can adsorb NH+ 4 to reduce addition of food waste digestate-derived biochar reduced the total vol
its availability, thereby reducing NH3 production and emissions (Qu atile sulfur gas emissions by 15–20 %.
et al., 2022). Relevant studies have found that, compared with other These studies have shown that digestate-derived biochar improves
additives, the application of biochar to compost can significantly the maturity and fertility of composted products and significantly
shorten the warming time and effectively extend the duration of the modulates the structure and function of microbial communities during
high-temperature period (Yuan et al., 2015; Czekała et al., 2016). Thus, the composting process. Furthermore, the growth of anaerobic bacteria
it is beneficial to increase the decomposition rate of organic matter in was inhibited by the digestate-derived biochar, thus effectively reducing
compost feedstock. It can also effectively control the GHGs such as CO2, GHGs emissions and nitrogen loss.
CH4, N2O, and odor gases such as NH3 and H2S due to the strong
decomposition of carbon and nitrogen substances during aerobic com
posting (Ouyang et al., 2022; He et al., 2021b). 6.4. Removal of antibiotic/resistance genes
In addition, the dosages of biochar could have an effect on the
composting process. Studies have shown that the impact of biochar on Antibiotics have a wide range of applications both in healthcare and
reducing greenhouse gas emissions is significantly correlated with the livestock and aquaculture due to their good antibacterial, antimicrobial
dosages of biochar added (Yin et al., 2021). Table 4 summarizes the and bactericidal effects (Sengupta et al., 2013). According to statistics,
effect of biochar dosage on composting effectiveness. Notably, biochar China’s antibiotic production and use in 2013 were about 248,000 tons
additions generally range from 0 to 25 % (w/w), with approximately 10 and 162,000 tons, of which 48 % was used for humans and the rest for
% being effective. In general, small doses of biochar had no significant animal husbandry, the amount of use was 9 times that of the United
effect on reducing GHG emissions of compost. Awasthi et al. (2017) States and 150 times that of the United Kingdom (Zhang et al., 2015b).
found that the addition of 2–6 % biochar dosages had little effect on the However, due to the poor metabolism of antibiotics, 30 % to 90 % of
emissions of these greenhouse gases. In addition, adding excessive doses their residual components are excreted in their original forms and ulti
of biochar could negatively affect the composting process. Liu et al. mately enter water bodies, soils, and sediments, leading to accumulation
(2017) found that adding >10 % biochar can lead to significant water (Akhtar et al., 2021; Yuan et al., 2022; Chen et al., 2022). This accu
loss and heat dissipation in the compost, negatively affecting the com mulation has significant impacts on the surrounding environment and
posting process. ecosystems. More importantly, long-term exposure to antibiotic stress
The application of biochar in aerobic composting can also improve generates resistant bacteria and resistance genes (ARGs). They can
the quality of compost products, particularly by increasing their nitro spread and diffuse in the environment in a variety of ways (Fig. 5a) (Du
gen content. The addition of biochar can facilitate the transformation et al., 2023), posing a risk of genetic contamination of public health,
and fixation of nitrogen, thereby enhancing the presence of nitrogenous food and drinking water, and posing an even greater hazard to ecosys
substances in the compost. It can serve as a nitrogen source and carrier, tems and human health (Kunhikannan et al., 2021).
providing favorable conditions for nitrogen’s biological cycling and The digestate-derived biochar is considered to be an ideal material
aiding in its absorption and utilization. Wang et al. (2022a) investigated for the removal of this new type of pollutant due to its large specific
the effect of digestate-derived biochar on the mixed compost of swine surface area, obvious pore structure, rich functional groups, environ
manure and wolfberry twigs composting, and it was found that mentally friendly and efficient. The mechanisms of antibiotic adsorption
digestate-derived biochar could improve the composting environment on biochar are mainly pore filling, hydrophobic interactions, hydrogen
and increase the content of nitrogen in the final product. The loss of bonding interactions, π-π electron donor acceptor interactions, electro
nitrogen in the form of NH3 and N2O during composting decreased from static interactions, surface complexation, and ion exchange (Fig. 5b) (Du
10.78 % to <5.73 % and from 0.34 % to <0.041 %, respectively, as et al., 2023). In addition, electrostatic interactions, π-π electron donor
compared to the non-addition of digestate-derived biochar. Wang et al. receptor interactions, hydrophobic interactions, surface complexation,
(2022b) found that the addition of digestate-derived biochar could and pore filling are the main mechanisms for the adsorption of ARGs on
biochar (Fig. 5b) (Shao et al., 2022). Yao et al. (2018) prepared
Table 4
Effect of biochar dosage on the effectiveness of compost.
Composting Periods Biochar Preparation Dosages Effectiveness Reference
feedstock conditions
Pig manure and 50 solid 500 ◦ C 2.5 %, 5.0 %, Biochar mitigated NH3 and N2O emissions and protected nitrogen (Wang et al.,
Lycium chinensis days digestate 7.5 % (dry 2022a)
branch filings weigh)
Food waste digestate 50 Food waste 600 ◦ C 6.25 %, 12.5 %, Biochar promoted the humification of the composting, decreased (Wang et al.,
and sawdust days digestate 25 % (dry the NH3 and volatile sulfur compounds emissions and it was 2022b)
weigh) recommended that 25 % biochar was added to reduce odor
emissions.
Food waste digestate 50 Food waste 600 ◦ C 6.25 %, 12.5 %, The group with 25 % biochar promoted the growth of nitrifying (Wang et al.,
days digestate 25 % (dry bacteria, and was beneficial for both nitrogen conversion and 2023a)
weigh) humification during the composting
Food waste digestate 42 Tobacco 450 ◦ C, 2 h 2.5 %, 5 %, 10 Biochar improved carbon degradation and humification rates and (Manu et al.,
and sawdust days stalk % (dry weight) adding 10 % biochar reduces NH3 emissions by 58 % and nitrogen 2021)
losses by 50 %.
Sewage sludge and 11 Rice straw 500 ◦ C, 2 h 5 %, 10 %, 20 % Biochar at 10 % and 20 % dosages strengthened the relationship (Du et al.,
sawdust days (wet weight) between enzyme activity and bacterial communities, further 2019)
increasing the contribution of functional bacterial communities to
composting.
Wheat straw and 58 Wheat straw – 2 %, 4 %, 6 %, 8 Biochar promoted the humification of the composting, decreased (Awasthi
sewage sludge days %, 12 %, 18 % the CH4, N2O and NH3 emissions and it was recommended that 12 % et al., 2017)
(dry weight) biochar was used in sewage sludge compost.
12
Z. Fu et al. Science of the Total Environment 912 (2024) 168822
Fig. 5. (a) Sources of antibiotic resistance genes and pathways into the environment (Du et al., 2023) (b) Mechanism of antibiotic and resistance gene removal by
biochar (Du et al., 2023).
sugarcane digestate-derived biochar at 600 ◦ C and found that its the soil-plant system (Fu et al., 2021).
maximum adsorption capacity for sulfamethoxazole and sulfapyridine The above results suggest that in different environmental systems,
was 54.38 mg/g and 8.60 mg/g, respectively. Jiang et al. (2018) used biochar can reduce the environmental risk of the spread of ARGs and
swine manure digestate to prepare biochar. Among them, the biochar antibiotics by influencing system elements (including bacterial com
from digestate modified with KMnO4 solution showed the maximum munities and environmental factors) or by directly adsorbing and
removal of antibiotics with 83.76 % and 77.34 % for sulfadimethoxine destroying them.
and tylosin, respectively.
Biochar was found to directly or indirectly influence the removal of 6.5. Recovery of phosphate from liquid fraction of digestate
ARGs from the environment. Wu et al. (2020) found that β-cyclodextrin-
functionalized biochar significantly reduced all detectable ARGs Most of the phosphorus currently used in global agriculture comes
(including tetW, tetM, sul1, sul2, blaTEM, oxa1, qnrS, ermB and intI1) in from non-renewable sources, so phosphorus recycling will be key to
an anaerobic reactive system for wastewater under the combined stress meeting the growing demand for agricultural fertilizers (Alberto et al.,
of heavy metals and dyes in the wastewater treatment system. Study has 2021). Liquid fraction of digestate, as a recyclable agricultural waste
shown that biochar affects the distribution of ARGs mainly by influ resource, is rich in phosphorus resources. The recovery of phosphorus
encing Firmicutes and Proteobacteria (Sun et al., 2018). Moreover, the and other nutrients from liquid fraction of digestate can not only purify
persistent free radicals in biochar and the produced ⋅OH can directly water quality, but also realize the recovery and utilization of phosphorus
destroy the structure of ampicillin resistance gene structure by oxidation and other nutrients, and solve the problem of phosphorus shortage
(Wu et al., 2022). Lian et al. (2020) found that the nano-biochar can (Wang et al., 2020).
remove ARGs by adsorption and fragmentation (hydroxyl radicals The adsorption of phosphorus in liquid fraction of digestate by bio
generated by persistent free radicals on nano-biochar play an important char is mainly affected by physical adsorption and chemical adsorption.
role in the destruction of ARGs). In addition, biochar could improve Physical adsorption is mainly due to the large specific surface area and
environmental factors (carbon sequestration, water, nutrients, soil abundant pore structure on the surface of biochar, which provides
porosity structure) in soil and reduce the selective pressure of Cd and abundant adsorption sites for the adsorption of PO3− 4 and promotes the
hygromycin on plant endophytes, thus inhibiting the spread of ARGs in physical adsorption of PO3−4 on the surface of biochar (Nobaharan et al.,
13
Z. Fu et al. Science of the Total Environment 912 (2024) 168822
2021). Chemisorption is due to the extremely rich hydrogen bond, hy the mineralization of nitrogen during anaerobic digestion, ammonia is
droxyl and other functional groups on the surface of biochar, which can produced, and higher ammonia concentrations combined with an in
be hydrogen bonded and complexed with PO3− 4 , and promote the crease in pH facilitates the conversion of NH+4 to free ammonia (Guilayn
adsorption of PO3− 4 on the surface of biochar (Luo et al., 2023). In et al., 2020). This effect leads to an increased risk of ammonia volatili
addition, metal ions (Ca2+, Mg2+, Fe3+, Al3+, etc.) bound on the surface zation during digestate transportation and processing. In addition,
of biochar can not only serve as adsorption sites but also combine with ammonia nitrogen entering the air from the digestate drying process
PO3−4 to form phosphate precipitation to achieve phosphorus removal should be paid attention, because the drying process is often considered
(Dai et al., 2020). Luo et al. (2022) used digestate-derived biochar to an integral step in pyrolysis. During the drying process, the digestate
recover phosphorus from liquid fraction of digestate. Under the optimal releases most of the ammonia nitrogen into the air. After pyrolysis of
conditions of OA-HCl leaching and precipitation of ammonium magne digestate, combustion of syngas, bio-oil or biochar as fuel will be
sium phosphate, the recovery rate of PO34-P was as high as 99.3 %. detrimental to the natural carbon and nitrogen cycle (Peng et al., 2020).
Alberto et al. (2021) prepared biochar by mixing digestate with food Another problem with digestate pyrolysis is that the PAHs is inevitably
waste and cow dung and found that digestate-derived biochar could formed and presents on the surface of biochar (Wang et al., 2017). In
adsorb 20 % of phosphate in liquid fraction of digestate. The application addition, HCN and heterocyclic-N are produced during the pyrolysis of
of biochar for the recovery of phosphate from liquid fraction of digestate nitrogenous organic wastes (e.g. digestate), which may lead to second
is also a promising use of biochar. ary contamination (Zhang et al., 2014b).
The economic viability of biochar production systems depends The recovery of carbon materials from digestate can effectively
largely on the feedstock, production costs and value generated (Mar promote the efficient utilization of waste and the preparation of new
oušek et al., 2023). The cost of digestate is low and during the produc materials. Compared with other treatment technologies, the preparation
tion of biochar, bio-oil and syngas (mainly CO2, H2 and CO) are of biochar from digestate is worth promoting because it can realize its
produced. Bio-oil is characterized by low calorific value, high viscosity harmlessness, minimization and resourcing while meeting the devel
and water fraction, but it can be upgraded for utilization in a variety of opment trend of high efficiency, greenness, recycling and sustainability.
chemically and fuel lucrative applications, thus reducing the cost of Currently, experimental validations have been conducted on the use
biochar production to a certain extent (Cavali et al., 2022; Cheng et al., of anaerobic digestion and pollutant adsorption by digestate-derived
2021). However, pre-treatment (drying), pyrolysis and modification of biochar. However, there are still certain challenges and gaps to bridge
the digestate can be costly and energy intensive. before the practical industrial application of digestate-derived biochar.
Biogas from anaerobic digestion is often used to generate electricity Therefore, in the future, attention should be focused on the following
and heat in combined heat and power (CHP) plants (Monlau et al., aspects:
2015). Nevertheless, the thermal energy available for biogas enhance
ment may be much lower than the value needed to operate the drying (1) Efforts should be directed towards the comprehensive utilization
unit (González et al., 2020). The cost of capital investment is excessive of anaerobic digestion byproduct, digestate waste, through
when considering the integration of anaerobic digestion and pyrolysis. research experiments. This will facilitate the transformation of
The high initial capital investment in these plants is a major inhibiting innovative outcomes in digestate-derived biochar production
factor. González et al. (2020) pointed out that unless additional financial technology.
incentives are provided, a market for such power is not in any case (2) Due to the varied sources of digestate, there might be concerns
viable. From an energy point of view, the digestate conversion route about excess salt content and heavy metal pollution. Biochar
through HTC represents an innovative technology that enables the direct produced from thermal decomposition of digestate may contain
utilization of digestate at high water contents without any drying (Wang certain levels of pollutants, which could pose leaching risks
et al., 2023b). However, a study on the economic aspects associated with during processing and application. Therefore, in the future, it is
digestate-derived hydrochar showed that the price of hydrochar pro important to prioritize the selection of digestate-derived biochar
duction was almost double that of natural gas (Suwelack et al., 2016). feedstock and optimize manufacturing processes. Emphasis
Therefore, there is an ongoing necessity for specialized incentives and should be placed on researching the safe and stable application of
further technological development to promote the commercial appli digestate-derived biochar in the environment, aiming to reduce
cation of biochar. or eliminate the potential release of toxic pollutants into the
Regarding the environment, pyrolysis stabilizes harmful substances environment.
and fixes heavy metals in digestate (Feng and Lin, 2017). In addition, the (3) Currently, research on digestate-derived biochar has primarily
use of biochar as an energy recovery medium can reduce the use of fossil focused on its pollutant removal performance under laboratory
fuels, and the application of biochar as an adsorption medium may have conditions, and effective validation for large-scale practical ap
a lower environmental impact than other removal methods based on plications is still lacking. Therefore, in the future, it is necessary
fossil materials (Catenacci et al., 2022). to expand the scale of experiments and clearly define the appli
However, there are also potential environmental risks associated cation prospects of digestate-derived biochar in actual treatment
with digestate-derived biochar. After anaerobic digestion, the charac scenarios.
teristics of the digestate are very different from the biomass before (4) The digestate-derived biochar as an adsorbent should be further
digestion. During anaerobic digestion, microorganisms convert the studied, and research and discussion on environmental samples
organic fraction into CO2 and CH4 (Tayibi et al., 2021). In addition, with complex pollutant systems should be encouraged. The reli
many inorganic reagents are added to the digestate coagulation, dew ability and stability of digestate-derived biochar as an adsorbent
atering and stabilization processes. These could result in the higher need to be further clarified.
concentration of inorganic matter in digestate than in feedstock. Study (5) Efforts should be made to optimize the process of preparing
has shown that the inorganic components in digestate affect the for biochar from digestate, and pay close attention to the treatment
mation, molecular structure and surface properties of biochar, which and disposal of waste generated in the preparation process, as
further affects its performance as an adsorbent (Yang et al., 2023). In well as metal ion leaching in the modification process of
addition, higher ash content may cause problems such as slagging, digestate-derived biochar.
scaling and corrosion of plant equipment (Catenacci et al., 2022). Due to
14
Z. Fu et al. Science of the Total Environment 912 (2024) 168822
CRediT authorship contribution statement Bernardo, M., Correa, C.R., Ringelspacher, Y., Becker, G.C., Lapa, N., Fonseca, I.,
Esteves, L.A., Kruse, A., 2020. Porous carbons derived from hydrothermally treated
biogas digestate. Waste Manag. 105, 170–179. https://doi.org/10.1016/j.
Zhou Fu: Conceptualization, Methodology. Jianwei Zhao: Funding wasman.2020.02.011.
acquisition, Writing – review & editing. Dezheng Guan: Software. Bogusz, A., Nowak, K., Stefaniuk, M., Dobrowolski, R., Oleszczuk, P., 2017. Synthesis of
Yuxin Wang: Validation. Jingliang Xie: Project administration. Hua biochar from residues after biogas production with respect to cadmium and nickel
removal from wastewater. J. Environ. Manag. 201, 268–276. https://doi.org/
wei Zhang: Project administration. Yingjie Sun: Supervision. Jiangwei 10.1016/j.jenvman.2017.06.019.
Zhu: Supervision. Liang Guo: Supervision. Cai, Y., Zhu, M., Meng, X., Zhou, J.L., Zhang, H., Shen, X., 2022. The role of biochar on
alleviating ammonia toxicity in anaerobic digestion of nitrogen-rich wastes: a
review. Bioresour. Technol. 126924 https://doi.org/10.1016/j.
Declaration of competing interest biortech.2022.126924.
Cao, Z., Jung, D., Olszewski, M.P., Arauzo, P.J., Kruse, A., 2019. Hydrothermal
The authors declare that they have no known competing financial carbonization of biogas digestate: effect of digestate origin and process conditions.
Waste Manag. 100, 138–150. https://doi.org/10.1016/j.wasman.2019.09.009.
interests or personal relationships that could have appeared to influence Catenacci, A., Boniardi, G., Mainardis, M., Gievers, F., Farru, G., Asunis, F., Malpei, F.,
the work reported in this paper. Goi, D., Cappai, G., Canziani, R., 2022. Processes, applications and legislative
framework for carbonized anaerobic digestate: opportunities and bottlenecks. A
critical review. Energy Convers. Manag. 263, 115691 https://doi.org/10.1016/j.
Data availability enconman.2022.115691.
Cavali, M., Junior, N.L., de Almeida Mohedano, R., Belli Filho, P., da Costa, R.H.R., de
Data will be made available on request. Castilhos Junior, A.B., 2022. Biochar and hydrochar in the context of anaerobic
digestion for a circular approach: An overview. Sci. Total Environ. 822, 153614
https://doi.org/10.1016/j.scitotenv.2022.153614.
Acknowledgements Cha, J.S., Park, S.H., Jung, S.C., Ryu, C., Jeon, J.K., Shin, M.C., Park, Y.K., 2016.
Production and utilization of biochar: a review. J. Ind. Eng. Chem. 40, 1–15. https://
doi.org/10.1016/j.jiec.2016.06.002.
This work was financially supported by the project of Taishan
Chen, D., Kuang, Y., Wang, H., Liang, J., Zhao, J., 2022. Insights into the mechanism of
Scholar Engineering Program (NO. tsqn202306235), China Postdoctoral naproxen inhibiting biohydrogen production from sludge dark fermentation.
Science Foundation (No. 2023T160349 and No. 2019M660162), Process. Saf. Environ. Prot. 167, 390–397. https://doi.org/10.1016/j.
Shanghai Key Lab for Urban Ecological Processes and Eco-Restoration psep.2022.09.015.
Chen, G., Guo, X., Liu, F., Ma, Z., Cheng, Z., Yan, B., Ma, W., 2019. Gasification of
(SHUES2022A09), Shanghai Engineering Research Center of Biotrans lignocellulosic biomass pretreated by anaerobic digestion (AD) process: an
formation of Organic Solid Waste (SERC2020C05). experimental study. Fuel 247, 324–333. https://doi.org/10.1016/j.
fuel.2019.03.002.
Chen, M., Wang, F., Zhang, D.L., Yi, W.M., Liu, Y., 2021. Effects of acid modification on
Appendix A. Supplementary data the structure and adsorption NH+ 4 -N properties of biochar. Renew. Energy 169,
1343–1350. https://doi.org/10.1016/j.renene.2021.01.098.
Supplementary data to this article can be found online at https://doi. Chen, W., Liao, X., Wu, Y., Liang, J.B., Mi, J., Huang, J., Zhang, H., Wu, Y., Qiao, Z.,
Li, X., Wang, Y., 2017. Effects of different types of biochar on methane and ammonia
org/10.1016/j.scitotenv.2023.168822. mitigation during layer manure composting. Waste Manag. 61, 506–515. https://
doi.org/10.1016/j.wasman.2017.01.014.
References Cheng, B.H., Zeng, R.J., Jiang, H., 2017. Recent developments of post-modification of
biochar for electrochemical energy storage. Bioresour. Technol. 246, 224–233.
https://doi.org/10.1016/j.biortech.2017.07.060.
Ahmed, M.J., Hameed, B.H., 2020. Insight into the co-pyrolysis of different blended
Cheng, N., Wang, B., Wu, P., Lee, X., Xing, Y., Chen, M., Gao, B., 2021. Adsorption of
feedstocks to biochar for the adsorption of organic and inorganic pollutants: a
emerging contaminants from water and wastewater by modified biochar: a review.
review. J. Clean. Prod. 265, 121762 https://doi.org/10.1016/j.
Environ. Pollut. 273, 116448 https://doi.org/10.1016/j.envpol.2021.116448.
jclepro.2020.121762.
Cheong, J.C., Lee, J.T., Lim, J.W., Song, S., Tan, J.K., Chiam, Z.Y., Yap, K.Y., Lim, E.Y.,
Akhil, D., Lakshmi, D., Kartik, A., Vo, D.V.N., Arun, J., Gopinath, K.P., 2021. Production,
Zhang, J., Tan, H.T., Tong, Y.W., 2020. Closing the food waste loop: food waste
characterization, activation and environmental applications of engineered biochar: a
anaerobic digestate as fertilizer for the cultivation of the leafy vegetable, xiao bai cai
review. Environ. Chem. Lett. 19, 2261–2297. https://doi.org/10.1007/s10311-020-
(Brassica rapa). Sci. Total Environ. 715, 136789 https://doi.org/10.1016/j.
01167-7.
scitotenv.2020.136789.
Akhtar, L., Ahmad, M., Iqbal, S., Abdelhafez, A.A., Mehran, M.T., 2021. Biochars’
Chiappero, M., Norouzi, O., Hu, M., Demichelis, F., Berruti, F., Di Maria, F., Mašek, O.,
adsorption performance towards moxifloxacin and ofloxacin in aqueous solution:
Fiore, S., 2020. Review of biochar role as additive in anaerobic digestion processes.
role of pyrolysis temperature and biomass type. Environ. Technol. Innov. 24, 101912
Renew. Sust. Energ. Rev. 131, 110037 https://doi.org/10.1016/j.rser.2020.110037.
https://doi.org/10.1016/j.eti.2021.101912.
Chozhavendhan, S., Karthigadevi, G., Bharathiraja, B., Kumar, R.P., Abo, L.D., Prabhu, S.
Al Afif, R., Anayah, S.S., Pfeifer, C., 2020. Batch pyrolysis of cotton stalks for evaluation
V., Balachandar, R., Jayakumar, M., 2022. Current and prognostic overview on the
of biochar energy potential. Renew. Energy 147, 2250–2258. https://doi.org/
strategic exploitation of anaerobic digestion and digestate: a review. Environ. Res.
10.1051/e3sconf/201911600001.
114526 https://doi.org/10.1016/j.envres.2022.114526.
Alberto, D.R., Tyler, A.C., Trabold, T.A., 2021. Phosphate adsorption using biochar
Concari, A., Kok, G., Martens, P., 2022. Recycling behaviour: mapping knowledge
derived from solid digestate. Bioresour. Technol. Rep. 16, 100864 https://doi.org/
domain through bibliometrics and text mining. J. Environ. Manag. 303, 114160
10.1016/j.biteb.2021.100864.
https://doi.org/10.1016/j.jenvman.2021.114160.
Alghashm, S., Qian, S., Hua, Y., Wu, J., Zhang, H., Chen, W., Shen, G., 2018. Properties of
Cong, P., Song, S., Song, W., Dong, J., Zheng, X., 2022. Biochars prepared from biogas
biochar from anaerobically digested food waste and its potential use in phosphorus
residues: temperature is a crucial factor that determines their physicochemical
recovery and soil amendment. Sustainability 10 (12), 4692. https://doi.org/
properties. Biomass Convers. Biorefin. 1–14. https://doi.org/10.1007/s13399-022-
10.3390/su10124692.
03229-y.
Al-Wabel, M.I., Al-Omran, A., El-Naggar, A.H., Nadeem, M., Usman, A.R., 2013. Pyrolysis
Czekała, W., Malińska, K., Cáceres, R., Janczak, D., Dach, J., Lewicki, A., 2016. Co-
temperature induced changes in characteristics and chemical composition of biochar
composting of poultry manure mixtures amended with biochar–the effect of biochar
produced from conocarpus wastes. Bioresour. Technol. 131, 374–379. https://doi.
on temperature and C-CO2 emission. Bioresour. Technol. 200, 921–927. https://doi.
org/10.1016/j.biortech.2012.12.165.
org/10.1016/j.biortech.2015.11.019.
Anjum, M., Miandad, R., Waqas, M., Gehany, F., Barakat, M.A., 2019. Remediation of
Dai, Y., Wang, W., Lu, L., Yan, L., Yu, D., 2020. Utilization of biochar for the removal of
wastewater using various nano-materials. Arab. J. Chem. 12 (8), 4897–4919.
nitrogen and phosphorus. J. Clean. Prod. 257, 120573 https://doi.org/10.1016/j.
https://doi.org/10.1016/j.arabjc.2016.10.004.
jclepro.2020.120573.
Awasthi, M.K., Wang, M., Chen, H., Wang, Q., Zhao, J., Ren, X., Li, D., Awasthi, S.K.,
Das, S.K., Ghosh, G.K., Avasthe, R.K., Sinha, K., 2021. Compositional heterogeneity of
Shen, F., Li, R., Zhang, Z., 2017. Heterogeneity of biochar amendment to improve
different biochar: effect of pyrolysis temperature and feedstocks. J. Environ. Manag.
the carbon and nitrogen sequestration through reduce the greenhouse gases
278, 111501 https://doi.org/10.1016/j.jenvman.2020.111501.
emissions during sewage sludge composting. Bioresour. Technol. 224, 428–438.
Ding, K., Zhong, Z., Zhang, B., Wang, J., Min, A., Ruan, R., 2016. Catalytic pyrolysis of
https://doi.org/10.1016/j.biortech.2016.11.014.
waste tire to produce valuable aromatic hydrocarbons: an analytical Py-GC/MS
Ayaz, M., Stulpinaite, U., Feiziene, D., Tilvikiene, V., Akthar, K., Baltrėnaitė-Gedienė, E.,
study. J. Anal. Appl. Pyrolysis 122, 55–63. https://doi.org/10.1016/j.
Striugas, N., Rehmani, U., Alam, S., Iqbal, R., Toleikiene, M., Doyeni, M., 2022. Pig
jaap.2016.10.023.
manure digestate-derived biochar for soil management and crop cultivation in heavy
Dong, H., Deng, J., Xie, Y., Zhang, C., Jiang, Z., Cheng, Y., Hou, K., Zeng, G., 2017.
metals contaminated soil. Soil Use Manag. 38 (2), 1307–1321. https://doi.org/
Stabilization of nanoscale zero-valent iron (nZVI) with modified biochar for Cr (VI)
10.1111/sum.12773.
removal from aqueous solution. J. Hazard. Mater. 332, 79–86. https://doi.org/
Balahmar, N., Al-Jumialy, A.S., Mokaya, R., 2017. Biomass to porous carbon in one step:
10.1016/j.jhazmat.2017.03.002.
directly activated biomass for high performance CO2 storage. J. Mater. Chem. A 5
(24), 12330–12339. https://doi.org/10.1039/C7TA01722G.
15
Z. Fu et al. Science of the Total Environment 912 (2024) 168822
Du, J., Zhang, Y., Qu, M., Yin, Y., Fan, K., Hu, B., Zhang, H., Wei, M., Ma, C., 2019. Jiang, B., Lin, Y., Mbog, J.C., 2018. Biochar derived from swine manure digestate and
Effects of biochar on the microbial activity and community structure during sewage applied on the removals of heavy metals and antibiotics. Bioresour. Technol. 270,
sludge composting. Bioresour. Technol. 272, 171–179. https://doi.org/10.1016/j. 603–611. https://doi.org/10.1016/j.biortech.2018.08.022.
biortech.2018.10.020. Jiang, Y., McAdam, E., Zhang, Y., Heaven, S., Banks, C., Longhurst, P., 2019. Ammonia
Du, L., Ahmad, S., Liu, L., Wang, L., Tang, J., 2023. A review of antibiotics and antibiotic inhibition and toxicity in anaerobic digestion: a critical review. J. Water Process Eng.
resistance genes (ARGs) adsorption by biochar and modified biochar in water. Sci. 32, 100899 https://doi.org/10.1016/j.jwpe.2019.100899.
Total Environ. 858, 159815 https://doi.org/10.1016/j.scitotenv.2022.159815. Jin, H., Hanif, M.U., Capareda, S., Chang, Z., Huang, H., Ai, Y., 2016. Copper (II) removal
Dutta, S., He, M., Xiong, X., Tsang, D.C., 2021. Sustainable management and recycling of potential from aqueous solution by pyrolysis biochar derived from anaerobically
food waste anaerobic digestate: a review. Bioresour. Technol. 341, 125915 https:// digested algae-dairy-manure and effect of KOH activation. J. Environ. Chem. Eng. 4
doi.org/10.1016/j.biortech.2021.125915. (1), 365–372. https://doi.org/10.1016/j.jece.2015.11.022.
Eid, E.M., El-Bebany, A.F., Alrumman, S.A., Hesham, A.E.L., Taher, M.A., Fawy, K.F., Jin, J., Li, S., Peng, X., Liu, W., Zhang, C., Yang, Y., Han, L., Du, Z., Sun, K., Wang, X.,
2017. Effects of different sewage sludge applications on heavy metal accumulation, 2018. HNO3 modified biochars for uranium (VI) removal from aqueous solution.
growth and yield of spinach (Spinacia oleracea L.). Int. J. Phytoremediation 19 (4), Bioresour. Technol. 256, 247–253. https://doi.org/10.1016/j.biortech.2018.02.022.
340–347. https://doi.org/10.1080/15226514.2016.1225286. Johnravindar, D., Kaur, G., Liang, J., Lou, L., Zhao, J., Manu, M.K., Kumar, R.,
Fahmy, T.Y., Fahmy, Y., Mobarak, F., El-Sakhawy, M., Abou-Zeid, R.E., 2020. Biomass Varjani, S., Wong, J.W., 2022. Impact of total solids content on biochar amended co-
pyrolysis: past, present, and future. Environment. Environ. Dev. Sustain. 22, 17–32. digestion of food waste and sludge: microbial community dynamics, methane
https://doi.org/10.1007/s10668-018-0200-5. production and digestate quality assessment. Bioresour. Technol. 361, 127682
Feng, Q., Lin, Y., 2017. Integrated processes of anaerobic digestion and pyrolysis for https://doi.org/10.1016/j.biortech.2022.127682.
higher bioenergy recovery from lignocellulosic biomass: a brief review. Renew. Sust. Kabaivanova, L., Ivanova, J., Chorukova, E., Hubenov, V., Nacheva, L., Simeonov, I.,
Energ. Rev. 77, 1272–1287. https://doi.org/10.1016/j.rser.2017.03.022. 2022. Algal biomass accumulation in waste digestate after anaerobic digestion of
Fu, D., Chen, Z., Xia, D., Shen, L., Wang, Y., Li, Q., 2017. A novel solid digestate-derived wheat straw. Fermentation 8 (12), 715. https://doi.org/10.3390/
biochar-Cu NP composite activating H2O2 system for simultaneous adsorption and fermentation8120715.
degradation of tetracycline. Environ. Pollut. 221, 301–310. https://doi.org/ Kaur, G., Wong, J.W., Kumar, R., Patria, R.D., Bhardwaj, A., Uisan, K., Johnravindar, D.,
10.1016/j.envpol.2016.11.078. 2020. Value addition of anaerobic digestate from biowaste: thinking beyond
Fu, Y., Jia, M., Wang, F., Wang, Z., Mei, Z., Bian, Y., Jiang, X., Virta, M., Tiedje, J.M., agriculture. Curr. Sustain./Renew. Energy Rep. 7, 48–55. https://doi.org/10.1007/
2021. Strategy for mitigating antibiotic resistance by biochar and s40518-020-00148-2.
hyperaccumulators in cadmium and oxytetracycline co-contaminated soil. Environ. Kumar, A., Saini, K., Bhaskar, T., 2020. Hydochar and biochar: production,
Sci. Technol. 55 (24), 16369–16378. https://doi.org/10.1021/acs.est.1c03434. physicochemical properties and techno-economic analysis. Bioresour. Technol. 310,
Gao, N., Du, W., Zhang, M., Ling, G., Zhang, P., 2022. Chitosan-modified biochar: 123442 https://doi.org/10.1016/j.biortech.2020.123442.
preparation, modifications, mechanisms and applications. Int. J. Biol. Macromol. Kumar, A., Bhattacharya, T., Shaikh, W.A., Chakraborty, S., Sarkar, D., Biswas, J.K.,
209, 31–49. https://doi.org/10.1016/j.ijbiomac.2022.04.006. 2022. Biochar modification methods for augmenting sorption of contaminants. Curr.
González, R., González, J., Rosas, J.G., Smith, R., Gómez, X., 2020. Biochar and energy Pollut. Rep. 8 (4), 519–555. https://doi.org/10.1007/s40726-022-00238-3.
production: valorizing swine manure through coupling co-digestion and pyrolysis. C Kumar, M., Dutta, S., You, S., Luo, G., Zhang, S., Show, P.L., Sawarkar, A.D., Singh, L.,
6 (2), 43. https://doi.org/10.3390/c6020043. Tsang, D.C., 2021. A critical review on biochar for enhancing biogas production from
Grigatti, M., Barbanti, L., Hassan, M.U., Ciavatta, C., 2020. Fertilizing potential and CO2 anaerobic digestion of food waste and sludge. J. Clean. Prod. 305, 127143 https://
emissions following the utilization of fresh and composted food-waste anaerobic doi.org/10.1016/j.jclepro.2021.127143.
digestates. Sci. Total Environ. 698, 134198 https://doi.org/10.1016/j. Kunhikannan, S., Thomas, C.J., Franks, A.E., Mahadevaiah, S., Kumar, S., Petrovski, S.,
scitotenv.2019.134198. 2021. Environmental hotspots for antibiotic resistance genes. MicrobiologyOpen 10
Guilayn, F., Rouez, M., Crest, M., Patureau, D., Jimenez, J., 2020. Valorization of (3), e1197. https://doi.org/10.1002/mbo3.1197.
digestates from urban or centralized biogas plants: a critical review. Rev. Environ. Lee, J., Kim, K.H., Kwon, E.E., 2017. Biochar as a catalyst. Renew. Sust. Energ. Rev. 77,
Sci. Biotechnol. 19, 419–462. https://doi.org/10.1007/s11157-020-09531-3. 70–79. https://doi.org/10.1016/j.rser.2017.04.002.
Hammerschmiedt, T., Holatko, J., Sudoma, M., Kintl, A., Vopravil, J., Ryant, P., Leng, L., Huang, H., 2018. An overview of the effect of pyrolysis process parameters on
Skarpa, P., Radziemska, M., Latal, O., Brtnicky, M., 2021. Biochar and sulphur biochar stability. Bioresour. Technol. 270, 627–642. https://doi.org/10.1016/j.
enriched digestate: utilization of agriculture associated waste products for improved biortech.2018.09.030.
soil carbon and nitrogen content, microbial activity, and plant growth. Agronomy 11 Li, C., Li, J., Pan, L., Zhu, X., Xie, S., Yu, G., Wang, Y., Pan, X., Zhu, G., Angelidaki, I.,
(10), 2041. https://doi.org/10.3390/agronomy11102041. 2020. Treatment of digestate residues for energy recovery and biochar production:
Hassan, M., Liu, Y., Naidu, R., Parikh, S.J., Du, J., Qi, F., Willett, I.R., 2020. Influences of from lab to pilot-scale verification. J. Clean. Prod. 265, 121852 https://doi.org/
feedstock sources and pyrolysis temperature on the properties of biochar and 10.1016/j.jclepro.2020.121852.
functionality as adsorbents: a meta-analysis. Sci. Total Environ. 744, 140714 https:// Li, C., Hayashi, J.I., Sun, Y., Zhang, L., Zhang, S., Wang, S., Hu, X., 2021. Impact of
doi.org/10.1016/j.scitotenv.2020.140714. heating rates on the evolution of function groups of the biochar from lignin
He, A., Zhang, Z., Yu, Q., Yang, K., Sheng, G.D., 2021a. Lindane degradation in wet-dry pyrolysis. J. Anal. Appl. Pyrolysis 155, 105031. https://doi.org/10.1016/j.
cycling soil as affected by aging and microbial toxicity of biochar. Ecotoxicol. jaap.2021.105031.
Environ. Saf. 219, 112374 https://doi.org/10.1016/j.ecoenv.2021.112374. Li, D., Sun, M., Xu, J., Gong, T., Ye, M., Xiao, Y., Yang, T., 2022a. Effect of biochar
He, M., Cao, Y., Xu, Z., You, S., Ruan, R., Gao, B., Wong, H.K., Tsang, D.C., 2022. Process derived from biogas residue on methane production during dry anaerobic
water recirculation for catalytic hydrothermal carbonization of anaerobic digestate: fermentation of kitchen waste. Waste Manag. 149, 70–78. https://doi.org/10.1016/
Water-Energy-Nutrient Nexus. Bioresour. Technol. 361, 127694 https://doi.org/ j.wasman.2022.06.006.
10.1016/j.biortech.2022.127694. Li, H., Cheng, Y.R., Lin, X.S., 2018. Study of different preparation conditions and
He, X., Yin, H., Fang, C., Xiong, J., Han, L., Yang, Z., Huang, G., 2021b. Metagenomic and adsorption performance of biochar. Energy Environ. 5, 19–20 (in Chinese).
q-PCR analysis reveals the effect of powder bamboo biochar on nitrous oxide and Li, X., Chu, S., Wang, P., Li, K., Su, Y., Wu, D., Xie, B., 2022b. Potential of biogas residue
ammonia emissions during aerobic composting. Bioresour. Technol. 323, 124567 biochar modified by ferric chloride for the enhancement of anaerobic digestion of
https://doi.org/10.1016/j.biortech.2020.124567. food waste. Bioresour. Technol. 360, 127530 https://doi.org/10.1016/j.
Ho, S.H., Yang, Z.K., Nagarajan, D., Chang, J.S., Ren, N.Q., 2017. High-efficiency biortech.2022.127530.
removal of lead from wastewater by biochar derived from anaerobic digestion Li, Y., Zhang, Y., Yang, Y., Quan, X., Zhao, Z., 2017. Potentially direct interspecies
sludge. Bioresour. Technol. 246, 142–149. https://doi.org/10.1016/j. electron transfer of methanogenesis for syntrophic metabolism under sulfate
biortech.2017.08.025. reducing conditions with stainless steel. Bioresour. Technol. 234, 303–309. https://
Hu, X., Xue, Y., Long, L., Zhang, K., 2018. Characteristics and batch experiments of acid- doi.org/10.1016/j.biortech.2017.03.054.
and alkali-modified corncob biomass for nitrate removal from aqueous solution. Lian, F., Yu, W., Zhou, Q., Gu, S., Wang, Z., Xing, B., 2020. Size matters: nano-biochar
Environ. Sci. Pollut. Res. 25, 19932–19940. https://doi.org/10.1007/s11356-018- triggers decomposition and transformation inhibition of antibiotic resistance genes
2198-5. in aqueous environments. Environ. Sci. Technol. 54 (14), 8821–8829. https://doi.
Huang, Q., Song, S., Chen, Z., Hu, B., Chen, J., Wang, X., 2019. Biochar-based materials org/10.1021/acs.est.0c02227.
and their applications in removal of organic contaminants from wastewater: state-of- Liu, H., Wang, X., Fang, Y., Lai, W., Xu, S., Lichtfouse, E., 2022a. Enhancing thermophilic
the-art review. Biochar 1, 45–73. https://doi.org/10.1007/s42773-019-00006-5. anaerobic co-digestion of sewage sludge and food waste with biogas residue biochar.
Huang, X., Wang, S., Shi, Z., Fang, L., Yin, C., 2022. Challenges and strategies for biogas Renew. Energy 188, 465–475. https://doi.org/10.1016/j.renene.2022.02.044.
production in the circular agricultural waste utilization model: a case study in rural Liu, J., Jiang, J., Aihemaiti, A., Meng, Y., Yang, M., Xu, Y., Gao, Y., Zou, Q., Chen, X.,
China. Energy 241, 122889. https://doi.org/10.1016/j.energy.2021.122889. 2019. Removal of phosphate from aqueous solution using MgO-modified magnetic
Indren, M., Birzer, C.H., Kidd, S.P., Medwell, P.R., 2020. Effect of total solids content on biochar derived from anaerobic digestion residue. J. Environ. Manag. 250, 109438
anaerobic digestion of poultry litter with biochar. J. Environ. Manag. 255, 109744 https://doi.org/10.1016/j.jenvman.2019.109438.
https://doi.org/10.1016/j.jenvman.2019.109744. Liu, J., Huang, S., Chen, K., Wang, T., Mei, M., Li, J., 2020. Preparation of biochar from
Inyang, M., Gao, B., Pullammanappallil, P., Ding, W., Zimmerman, A.R., 2010. Biochar food waste digestate: pyrolysis behavior and product properties. Bioresour. Technol.
from anaerobically digested sugarcane bagasse. Bioresour. Technol. 101 (22), 302, 122841 https://doi.org/10.1016/j.biortech.2020.122841.
8868–8872. https://doi.org/10.1016/j.biortech.2010.06.088. Liu, J., Zhang, W., Mei, M., Wang, T., Chen, S., Li, J., 2022b. A Ca-rich biochar derived
Ji, M., Wang, X., Usman, M., Liu, F., Dan, Y., Zhou, L., Campanaro, S., Luo, G., Sang, W., from food waste digestate with exceptional adsorption capacity for arsenic (III)
2022. Effects of different feedstocks-based biochar on soil remediation: a review. removal via a cooperative mechanism. Sep. Purif. Technol. 295, 121359 https://doi.
Environ. Pollut. 294, 118655 https://doi.org/10.1016/j.envpol.2021.118655. org/10.1016/j.seppur.2022.121359.
Liu, M., Almatrafi, E., Zhang, Y., Xu, P., Song, B., Zhou, C., Zeng, G., Zhu, Y., 2022c.
A critical review of biochar-based materials for the remediation of heavy metal
16
Z. Fu et al. Science of the Total Environment 912 (2024) 168822
contaminated environment: applications and practical evaluations. Sci. Total sustainable biogas production. Renew. Sust. Energ. Rev. 79, 308–322. https://doi.
Environ. 806, 150531 https://doi.org/10.1016/j.scitotenv.2021.150531. org/10.1016/j.rser.2017.05.137.
Liu, N., Zhou, J., Han, L., Ma, S., Sun, X., Huang, G., 2017. Role and multi-scale Neumann, J., Binder, S., Apfelbacher, A., Gasson, J.R., García, P.R., Hornung, A., 2015.
characterization of bamboo biochar during poultry manure aerobic composting. Production and characterization of a new quality pyrolysis oil, char and syngas from
Bioresour. Technol. 241, 190–199. https://doi.org/10.1016/j.biortech.2017.03.144. digestate–introducing the thermo-catalytic reforming process. J. Anal. Appl.
Liu, W.J., Jiang, H., Yu, H.Q., 2015. Development of biochar-based functional materials: Pyrolysis 113, 137–142. https://doi.org/10.1016/j.jaap.2014.11.022.
toward a sustainable platform carbon material. Chem. Rev. 115 (22), 12251–12285. Nobaharan, K., Bagheri Novair, S., Asgari Lajayer, B., van Hullebusch, E.D., 2021.
https://doi.org/10.1021/acs.chemrev.5b00195. Phosphorus removal from wastewater: the potential use of biochar and the key
Liu, X., Du, M., Lu, Q., He, D., Song, K., Yang, Q., Duan, A., Wang, D., 2021. How does controlling factors. Water 13 (4), 517. https://doi.org/10.3390/w13040517.
chitosan affect methane production in anaerobic digestion? Environ. Sci. Technol. Ortiz, L.R., Torres, E., Zalazar, D., Zhang, H., Rodriguez, R., Mazza, G., 2020. Influence of
55, 15843–15852. https://doi.org/10.1021/acs.est.1c04693. pyrolysis temperature and bio-waste composition on biochar characteristics. Renew.
Liu, X., Lu, Q., Du, M., Xu, Q., Wang, D., 2022e. Hormesis-like effects of Energy 155, 837–847. https://doi.org/10.1016/j.renene.2020.03.181.
Tetrabromobisphenol A on anaerobic digestion: responses of metabolic activity and Ouyang, X., Lin, H., Hu, Z., Zheng, Y., Li, P., Huang, W., 2022. Effect of biochar structure
microbial community. Environ. Sci. Technol. 56, 11277–11287. https://doi.org/ on H2S emissions during sludge aerobic composting: insights into microscale
10.1021/acs.est.2c00062. characterization and microbial mechanism. Biomass Convers. Biorefin. 1-14 https://
Liu, Z., Zhen, F., Zhang, Q., Qian, X., Li, W., Sun, Y., Zhang, L., Qu, B., 2022f. doi.org/10.1007/s13399-022-03388-y.
Nanoporous biochar with high specific surface area based on rice straw digestion Pan, J., Ma, J., Liu, X., Zhai, L., Ouyang, X., Liu, H., 2019. Effects of different types of
residue for efficient adsorption of mercury ion from water. Bioresour. Technol. 359, biochar on the anaerobic digestion of chicken manure. Bioresour. Technol. 275,
127471 https://doi.org/10.1016/j.biortech.2022.127471. 258–265. https://doi.org/10.1016/j.biortech.2018.12.068.
Long, L., Xue, Y., Hu, X., Zhu, Y., 2019. Study on the influence of surface potential on the Peng, W., Lü, F., Hao, L., Zhang, H., Shao, L., He, P., 2020. Digestate management for
nitrate adsorption capacity of metal modified biochar. Environ. Sci. Pollut. Res. 26, high-solid anaerobic digestion of organic wastes: a review. Bioresour. Technol. 297,
3065–3074. https://doi.org/10.1007/s11356-018-3815-z. 122485 https://doi.org/10.1016/j.biortech.2019.122485.
Lu, G.Q., Low, J.C.F., Liu, C.Y., Lua, A.C., 1995. Surface area development of sewage Peng, Y., Li, L., Dong, Q., Yang, P., Liu, H., Ye, W., Wu, D., Peng, X., 2023. Evaluation of
sludge during pyrolysis. Fuel 74 (3), 344–348. https://doi.org/10.1016/0016-2361 digestate-derived biochar to alleviate ammonia inhibition during long-term
(95)93465-P. anaerobic digestion of food waste. Chemosphere 311, 137150. https://doi.org/
Lu, Z., Zhang, H., Shahab, A., Zhang, K., Zeng, H., Nabi, I., Ullah, H., 2021. Comparative 10.1016/j.chemosphere.2022.137150.
study on characterization and adsorption properties of phosphoric acid activated Petrovič, A., Vohl, S., Cenčič Predikaka, T., Bedoić, R., Simonič, M., Ban, I., Čuček, L.,
biochar and nitrogen-containing modified biochar employing Eucalyptus as a 2021. Pyrolysis of solid digestate from sewage sludge and lignocellulosic biomass:
precursor. J. Clean. Prod. 303, 127046 https://doi.org/10.1016/j. kinetic and thermodynamic analysis, characterization of biochar. Sustainability 13
jclepro.2021.127046. (17), 9642. https://doi.org/10.3390/su13179642.
Luo, D., Wang, L., Nan, H., Cao, Y., Wang, H., Kumar, T.V., Wang, C., 2023. Phosphorus Ponnusamy, V.K., Nguyen, D.D., Dharmaraja, J., Shobana, S., Banu, J.R., Saratale, R.G.,
adsorption by functionalized biochar: a review. Environ. Chem. Lett. 21 (1), Chang, S.W., Kumar, G., 2019. A review on lignin structure, pretreatments,
497–524. https://doi.org/10.1007/s10311-022-01519-5. fermentation reactions and biorefinery potential. Bioresour. Technol. 271, 462–472.
Luo, Z., Wang, D., Zeng, W., Yang, J., 2020. Removal of refractory organics from piggery https://doi.org/10.1016/j.biortech.2018.09.070.
bio-treatment effluent by the catalytic ozonation process with piggery biogas residue Qiao, Y., Zhang, S., Quan, C., Gao, N., Johnston, C., Wu, C., 2020. One-pot synthesis of
biochar as the catalyst. Sci. Total Environ. 734, 139448 https://doi.org/10.1016/j. digestate-derived biochar for carbon dioxide capture. Fuel 279, 118525. https://doi.
scitotenv.2020.139448. org/10.1016/j.fuel.2020.118525.
Luo, Z., Wen, H., Zhang, H., Li, Y., Mai, X., Zhang, Y., Wang, J., Li, Y., Zhang, Z., 2022. Qiu, B., Tao, X., Wang, H., Li, W., Ding, X., Chu, H., 2021. Biochar as a low-cost
Biogas residue biochar integrated with phosphate from its ash for the effective adsorbent for aqueous heavy metal removal: a review. J. Anal. Appl. Pyrolysis 155,
recovery of nutrients from piggery biogas slurry. Biochar 4 (1), 23. https://doi.org/ 105081. https://doi.org/10.1016/j.jaap.2021.105081.
10.1007/s42773-022-00151-4. Qiu, L., Deng, Y.F., Wang, F., Davaritouchaee, M., Yao, Y.Q., 2019. A review on biochar-
Lv, Y., Bao, J., Liu, D., Gao, X., Yu, Y., Zhu, L., 2023. Synergistic effects of rice husk mediated anaerobic digestion with enhanced methane recovery. Renew. Sust. Energ.
biochar and aerobic composting for heavy oil-contaminated soil remediation and Rev. 115, 109373 https://doi.org/10.1016/j.rser.2019.109373.
microbial community succession evaluation. J. Hazard. Mater. 448, 130929 https:// Qu, Y., Qu, J., Yan, W., Yue, T., Zhang, Q., Yi, W., Liu, X., Sun, Y., 2022. Influence of
doi.org/10.1016/j.jhazmat.2023.130929. biochar on physico-chemical, microbial community and maturity during biogas
Lyu, H., He, Y., Tang, J., Hecker, M., Liu, Q., Jones, P.D., Codling, G., Giesy, J.P., 2016. residue aerobic composting process. Fermentation 8 (11), 623. https://doi.org/
Effect of pyrolysis temperature on potential toxicity of biochar if applied to the 10.3390/fermentation8110623.
environment. Environ. Pollut. 218, 1–7. https://doi.org/10.1016/j. Rajapaksha, A.U., Chen, S.S., Tsang, D.C., Zhang, M., Vithanage, M., Mandal, S., Gao, B.,
envpol.2016.08.014. Bolan, N.S., Ok, Y.S., 2016. Engineered/designer biochar for contaminant removal/
Ma, Z., Cheng, Z., Yang, Y., Nie, C., Wu, D., Yang, T., Wang, S., Li, D., 2023. Acid- immobilization from soil and water: potential and implication of biochar
modified anaerobic biogas residue biochar activates persulfate for phenol modification. Chemosphere 148, 276–291. https://doi.org/10.1016/j.
degradation: enhancement of the efficiency and non-radical pathway. Colloids Surf. chemosphere.2016.01.043.
A Physicochem. Eng. Asp. 663, 131121 https://doi.org/10.1016/j. Ramzani, P.M.A., Shan, L., Anjum, S., Ronggui, H., Iqbal, M., Virk, Z.A., Kausar, S., 2017.
colsurfa.2023.131121. Improved quinoa growth, physiological response, and seed nutritional quality in
Makádi, M., Tomócsik, A., Orosz, V., 2012. Digestate: a new nutrient source–review. three soils having different stresses by the application of acidified biochar and
Biogas 14, 295–312. https://doi.org/10.5772/31355. compost. Plant Physiol. Biochem. 116, 127–138. https://doi.org/10.1016/j.
Manu, M.K., Wang, C., Li, D., Varjani, S., Xu, Y., Ladumor, N., Lui, M., Zhou, J., Wong, J. plaphy.2017.05.003.
W., 2021. Biodegradation kinetics of ammonium enriched food waste digestate Rangabhashiyam, S., Balasubramanian, P., 2019. The potential of lignocellulosic biomass
compost with biochar amendment. Bioresour. Technol. 341, 125871 https://doi. precursors for biochar production: performance, mechanism and wastewater
org/10.1016/j.biortech.2021.125871. application-a review. Ind. Crop. Prod. 128, 405–423. https://doi.org/10.1016/j.
Maroušek, J., Minofar, B., Maroušková, A., Strunecký, O., Gavurová, B., 2023. indcrop.2018.11.041.
Environmental and economic advantages of production and application of digestate Rizwan, M., Ali, S., Qayyum, M.F., Ibrahim, M., Zia-ur-Rehman, M., Abbas, T., Ok, Y.S.,
biochar. Environ. Technol. Innov. 30, 103109 https://doi.org/10.1016/j. 2016. Mechanisms of biochar-mediated alleviation of toxicity of trace elements in
eti.2023.103109. plants: a critical review. Environ. Sci. Pollut. Res. 23, 2230–2248. https://doi.org/
McGlynn, S.E., Chadwick, G.L., Kempes, C.P., Orphan, V.J., 2015. Single cell activity 10.1007/s11356-015-5697-7.
reveals direct electron transfer in methanotrophic consortia. Nature 526 (7574), Sajjadi, B., Zubatiuk, T., Leszczynska, D., Leszczynski, J., Chen, W.Y., 2019. Chemical
531–535. https://doi.org/10.1038/nature15512. activation of biochar for energy and environmental applications: a comprehensive
Meng, L., Xie, L., Suenaga, T., Riya, S., Terada, A., Hosomi, M., 2020. Eco-compatible review. Rev. Chem. Eng. 35 (7), 777–815. https://doi.org/10.1515/revce-2017-
biochar mitigates volatile fatty acids stress in high load thermophilic solid-state 0113.
anaerobic reactors treating agricultural waste. Bioresour. Technol. 309, 123366 Sengupta, S., Chattopadhyay, M.K., Grossart, H.P., 2013. The multifaceted roles of
https://doi.org/10.1016/j.biortech.2020.123366. antibiotics and antibiotic resistance in nature. Front. Microbiol. 4, 47. https://doi.
Mohan, D., Sarswat, A., Ok, Y.S., Pittman Jr., C.U., 2014. Organic and inorganic org/10.3389/fmicb.2013.00047.
contaminants removal from water with biochar, a renewable, low cost and Shao, B., Liu, Z., Tang, L., Liu, Y., Liang, Q., Wu, T., Pan, Y., Zhang, X., Tan, X., Yu, J.,
sustainable adsorbent–a critical review. Bioresour. Technol. 160, 191–202. https:// 2022. The effects of biochar on antibiotic resistance genes (ARGs) removal during
doi.org/10.1016/j.biortech.2014.01.120. different environmental governance processes: a mini review. J. Hazard. Mater.
Monlau, F., Sambusiti, C., Antoniou, N., Barakat, A., Zabaniotou, A., 2015. A new 129067 https://doi.org/10.1016/j.jhazmat.2022.129067.
concept for enhancing energy recovery from agricultural residues by coupling Sheng, X., Wang, J., Cui, Q., Zhang, W., Zhu, X., 2022. A feasible biochar derived from
anaerobic digestion and pyrolysis process. Appl. Energy 148, 32–38. https://doi.org/ biogas residue and its application in the efficient adsorption of tetracycline from an
10.1016/j.apenergy.2015.03.024. aqueous solution. Environ. Res. 207, 112175 https://doi.org/10.1016/j.
Mukherjee, A., Patra, B.R., Podder, J., Dalai, A.K., 2022. Synthesis of biochar from envres.2021.112175.
lignocellulosic biomass for diverse industrial applications and energy harvesting: Shi, Y., Hu, H., Ren, H., 2020. Dissolved organic matter (DOM) removal from biotreated
effects of pyrolysis conditions on the physicochemical properties of biochar. Front. coking wastewater by chitosan-modified biochar: adsorption fractions and
Mater. 9, 870184 https://doi.org/10.3389/fmats.2022.870184. mechanisms. Bioresour. Technol. 297, 122281 https://doi.org/10.1016/j.
Neshat, S.A., Mohammadi, M., Najafpour, G.D., Lahijani, P., 2017. Anaerobic co- biortech.2019.122281.
digestion of animal manures and lignocellulosic residues as a potent approach for Song, S., Lim, J.W., Lee, J.T., Cheong, J.C., Hoy, S.H., Hu, Q., Tan, J.K., Chiam, Z.,
Arora, S., Lum, T.Q., Lim, E.Y., Wang, C.H., Tan, H.T., Tong, Y.W., 2021. Food-waste
17
Z. Fu et al. Science of the Total Environment 912 (2024) 168822
anaerobic digestate as a fertilizer: the agronomic properties of untreated digestate degradation by peroxymonosulfate activation. J. Hazard. Mater. 421, 126794
and biochar-filtered digestate residue. Waste Manag. 136, 143–152. https://doi.org/ https://doi.org/10.1016/j.jhazmat.2021.126794.
10.1016/j.wasman.2021.10.011. Wang, Y., Yu, G., Xie, S., Jiang, R., Li, C., Xing, Z., 2023c. Pyrolysis of food waste
Stefaniuk, M., Oleszczuk, P., 2015. Characterization of biochars produced from residues digestate residues for biochar: pyrolytic properties, biochar characterization, and
from biogas production. J. Anal. Appl. Pyrolysis 115, 157–165. https://doi.org/ heavy metal behaviours. Fuel 353, 129185. https://doi.org/10.1016/j.
10.1016/j.jaap.2015.07.011. fuel.2023.129185.
Stefaniuk, M., Oleszczuk, P., Bartmiński, P., 2016. Chemical and ecotoxicological Wang, Z.K., Liu, Q.H., Yang, Z.M., 2023d. Nano magnetite-loaded biochar boosted
evaluation of biochar produced from residues of biogas production. J. Hazard. methanogenesis through shifting microbial community composition and modulating
Mater. 318, 417–424. https://doi.org/10.1016/j.jhazmat.2016.06.013. electron transfer. Sci. Total Environ. 861, 160597 https://doi.org/10.1016/j.
Stoumpou, V., Novakovic, J., Kontogianni, N., Barampouti, E.M., Mai, S., Moustakas, K., scitotenv.2022.160597.
Malamis, D., Loizidou, M., 2020. Assessing straw digestate as feedstock for Wegener, G., Krukenberg, V., Riedel, D., Tegetmeyer, H.E., Boetius, A., 2015.
bioethanol production. Renew. Energy 153, 261–269. https://doi.org/10.1016/j. Intercellular wiring enables electron transfer between methanotrophic archaea and
renene.2020.02.021. bacteria. Nature 526 (7574), 587–590. https://doi.org/10.1038/nature15733.
Sugiarto, Y., Sunyoto, N.M.S., Zhu, M., Jones, I., Zhang, D., 2021. Effect of biochar Wongrod, S., Simon, S., Guibaud, G., Lens, P.N., Pechaud, Y., Huguenot, D., van
addition on microbial community and methane production during anaerobic Hullebusch, E.D., 2018a. Lead sorption by biochar produced from digestates:
digestion of food wastes: the role of minerals in biochar. Bioresour. Technol. 323, consequences of chemical modification and washing. J. Environ. Manag. 219,
124585 https://doi.org/10.1016/j.biortech.2020.124585. 277–284. https://doi.org/10.1016/j.jenvman.2018.04.108.
Sun, W., Gu, J., Wang, X., Qian, X., Tuo, X., 2018. Impacts of biochar on the Wongrod, S., Simon, S., van Hullebusch, E.D., Lens, P.N., Guibaud, G., 2018b. Changes of
environmental risk of antibiotic resistance genes and mobile genetic elements during sewage sludge digestate-derived biochar properties after chemical treatments and
anaerobic digestion of cattle farm wastewater. Bioresour. Technol. 256, 342–349. influence on As (III and V) and Cd (II) sorption. Int. Biodeterior. Biodegrad. 135,
https://doi.org/10.1016/j.biortech.2018.02.052. 96–102. https://doi.org/10.1016/j.ibiod.2018.10.001.
Sun, Z., Feng, L., Li, Y., Han, Y., Zhou, H., Pan, J., 2022. The role of electrochemical Wongrod, S., Simon, S., van Hullebusch, E.D., Lens, P.N., Guibaud, G., 2019. Assessing
properties of biochar to promote methane production in anaerobic digestion. arsenic redox state evolution in solution and solid phase during As (III) sorption onto
J. Clean. Prod. 362, 132296 https://doi.org/10.1016/j.jclepro.2022.132296. chemically-treated sewage sludge digestate biochars. Bioresour. Technol. 275,
Suwelack, K., Dostert, N., Wüst, D., Kruse, A., 2016. Economics of hydrothermal 232–238. https://doi.org/10.1016/j.biortech.2018.12.056.
carbonization of biogas digestate in a hybrid AD-HTC plant. In: Proceedings of the Wu, C., Fu, L., Li, H., Liu, X., Wan, C., 2022. Using biochar to strengthen the removal of
24th European Biomass Conference and Exhibition, pp. 6–9. https://doi.org/ antibiotic resistance genes: performance and mechanism. Sci. Total Environ. 816,
10.5071/24thEUBCE2016-3DO.9.4. 151554 https://doi.org/10.1016/j.scitotenv.2021.151554.
Tan, X.F., Liu, Y.G., Gu, Y.L., Xu, Y., Zeng, G.M., Hu, X.J., Liu, S.B., Wang, X., Liu, S.M., Wu, J.W., Wu, C.R., Zhou, C.S., Dong, L.L., Liu, B.F., Xing, D.F., Yang, S.S., Fan, J.N.,
Li, J., 2016. Biochar-based nano-composites for the decontamination of wastewater: Feng, L.P., Gao, G.L., You, S.J., 2020. Fate and removal of antibiotic resistance genes
a review. Bioresour. Technol. 212, 318–333. https://doi.org/10.1016/j. in heavy metals and dye co-contaminated wastewater treatment system amended
biortech.2016.04.093. with β-cyclodextrin functionalized biochar. Sci. Total Environ. 723, 137991 https://
Tayibi, S., Monlau, F., Marias, F., Thevenin, N., Jimenez, R., Oukarroum, A., doi.org/10.1016/j.scitotenv.2020.137991.
Alboulkas, A., Zeroual, Y., Barakat, A., 2021. Industrial symbiosis of anaerobic Wu, L., Wei, C., Zhang, S., Wang, Y., Kuzyakov, Y., Ding, X., 2019. MgO-modified biochar
digestion and pyrolysis: performances and agricultural interest of coupling biochar increases phosphate retention and rice yields in saline-alkaline soil. J. Clean. Prod.
and liquid digestate. Sci. Total Environ. 793, 148461 https://doi.org/10.1016/j. 235, 901–909. https://doi.org/10.1016/j.jclepro.2019.07.043.
scitotenv.2021.148461. Xia, D., Tan, F., Zhang, C., Jiang, X., Chen, Z., Li, H., Zheng, Y., Li, Q., Wang, Y., 2016.
Trakal, L., Veselská, V., Šafařík, I., Vítková, M., Číhalová, S., Komárek, M., 2016. Lead ZnCl2-activated biochar from biogas residue facilitates aqueous As (III) removal.
and cadmium sorption mechanisms on magnetically modified biochars. Bioresour. Appl. Surf. Sci. 377, 361–369. https://doi.org/10.1016/j.apsusc.2016.03.109.
Technol. 203, 318–324. https://doi.org/10.1016/j.biortech.2015.12.056. Xiong, X., Iris, K.M., Chen, S.S., Tsang, D.C., Cao, L., Song, H., Kwon, E.E., Ok, Y.S.,
Tsai, W.T., Fang, Y.Y., Cheng, P.H., Lin, Y.Q., 2018. Characterization of mesoporous Zhang, S., Poon, C.S., 2018. Sulfonated biochar as acid catalyst for sugar hydrolysis
biochar produced from biogas digestate implemented in an anaerobic process of and dehydration. Catal. Today 314, 52–61. https://doi.org/10.1016/j.
large-scale hog farm. Biomass Convers. Biorefin. 8, 945–951. https://doi.org/ cattod.2018.02.034.
10.1007/s13399-018-0344-4. Xu, J., Zhang, Y., Li, B., Fan, S., Xu, H., Guan, D.X., 2022a. Improved adsorption
Wang, C., Wang, Y., Herath, H.M.S.K., 2017. Polycyclic aromatic hydrocarbons (PAHs) in properties of tetracycline on KOH/KMnO4 modified biochar derived from wheat
biochar–their formation, occurrence and analysis: a review. Org. Geochem. 114, straw. Chemosphere 296, 133981. https://doi.org/10.1016/j.
1–11. https://doi.org/10.1016/j.orggeochem.2017.09.001. chemosphere.2022.133981.
Wang, H., Xiao, K., Yang, J., Yu, Z., Yu, W., Xu, Q., Wu, Q., Liang, S., Hu, J., Hou, H., Xu, M., Yang, M., Song, N., Xie, D., Meng, J., Gao, M., Wang, Q., Wu, C., 2022b.
Liu, B., 2020. Phosphorus recovery from the liquid phase of anaerobic digestate Biodrying of biogas residue: maturity and microbial diversity assessment. J. Environ.
using biochar derived from iron− rich sludge: a potential phosphorus fertilizer. Chem. Eng. 10 (6), 108757 https://doi.org/10.1016/j.jece.2022.108757.
Water Res. 174, 115629 https://doi.org/10.1016/j.watres.2020.115629. Xu, X., Li, L.M., Li, B., Guo, W.J., Ding, X.L., Xu, F.Z., 2017. Effect of fermented biogas
Wang, J., Wang, S., 2019. Preparation, modification and environmental application of residue on growth performance, serum biochemical parameters, and meat quality in
biochar: a review. J. Clean. Prod. 227, 1002–1022. https://doi.org/10.1016/j. pigs. Asian-Australas. J. Anim. Sci. 30, 1464 (doi:5713.16/ajas.0777).
jclepro.2019.04.282. Yang, C., Wu, H., Cai, M., Li, Y., Guo, C., Han, Y., Zhang, Y., Song, B., 2023. Valorization
Wang, J., Pan, J., Ma, X., Li, S., Chen, X., Liu, T., Wang, Q., Wang, J.J., Wei, D., Zhang, Z., of food waste digestate to ash and biochar composites for high performance
Li, R., 2022a. Solid digestate biochar amendment on pig manure composting: adsorption of methylene blue. J. Clean. Prod. 397, 136612 https://doi.org/10.1016/
nitrogen cycle and balance. Bioresour. Technol. 349, 126848 https://doi.org/ j.jclepro.2023.136612.
10.1016/j.biortech.2022.126848. Yang, S., Wen, Q., Chen, Z., 2021a. Effect of KH2PO4-modified biochar on immobilization
Wang, L., Wang, Y., Ma, F., Tankpa, V., Bai, S., Guo, X., Wang, X., 2019. Mechanisms and of Cr, Cu, Pb, Zn and as during anaerobic digestion of swine manure. Bioresour.
reutilization of modified biochar used for removal of heavy metals from wastewater: Technol. 339, 125570 https://doi.org/10.1016/j.biortech.2021.125570.
a review. Sci. Total Environ. 668, 1298–1309. https://doi.org/10.1016/j. Yang, T., Xu, J., Zhao, Y., Gong, T., Zhao, R., Sun, M., Xi, B., 2021b. Classification
scitotenv.2019.03.011. technology of domestic waste from 2000 to 2019: a bibliometrics-based review.
Wang, M., Wang, G., Qian, L., Yong, X., Wang, Y., An, W., Jia, H., Zhou, J., 2021. Biochar Environ. Sci. Pollut. Res. 28, 26313–26324. https://doi.org/10.1007/s11356-021-
production using biogas residue and their adsorption of ammonium nitrogen and 12816-x.
chemical oxygen demand in wastewater. Biomass Convers. Biorefin. 1-12 https:// Yao, Y., Gao, B., Inyang, M., Zimmerman, A.R., Cao, X., Pullammanappallil, P., Yang, L.,
doi.org/10.1007/s13399-021-01510-0. 2011. Biochar derived from anaerobically digested sugar beet tailings:
Wang, N., Huang, D., Bai, X., Lin, Y., Miao, Q., Shao, M., Xu, Q., 2022b. Mechanism of characterization and phosphate removal potential. Bioresour. Technol. 102 (10),
digestate-derived biochar on odorous gas emissions and humification in composting 6273–6278. https://doi.org/10.1016/j.biortech.2011.03.006.
of digestate from food waste. J. Hazard. Mater. 434, 128878 https://doi.org/ Yao, Y., Zhang, Y., Gao, B., Chen, R., Wu, F., 2018. Removal of sulfamethoxazole (SMX)
10.1016/j.jhazmat.2022.128878. and sulfapyridine (SPY) from aqueous solutions by biochars derived from
Wang, N., Bai, X., Huang, D., Shao, M., Chen, Q., Xu, Q., 2023a. Insights into the anaerobically digested bagasse. Environ. Sci. Pollut. Res. 25, 25659–25667. https://
influence of digestate-derived biochar upon the microbial community succession doi.org/10.1007/s11356-017-8849-0.
during the composting of digestate from food waste. Chemosphere 137786. https:// Yenigün, O., Demirel, B., 2013. Ammonia inhibition in anaerobic digestion: a review.
doi.org/10.1016/j.chemosphere.2023.137786. Process Biochem. 48 (5–6), 901–911. https://doi.org/10.1016/j.
Wang, S., Shi, F., Li, P., Yang, F., Pei, Z., Yu, Q., Zuo, X., Liu, J., 2022c. Effects of rice procbio.2013.04.012.
straw biochar on methanogenic bacteria and metabolic function in anaerobic Yin, Y., Yang, C., Li, M., Zheng, Y., Ge, C., Gu, J., Li, H., Duan, M., Wang, X., Chen, R.,
digestion. Sci. Rep. 12 (1), 6971. https://doi.org/10.1038/s41598-022-10682-2. 2021. Research progress and prospects for using biochar to mitigate greenhouse gas
Wang, W., Lee, D.J., 2021. Valorization of anaerobic digestion digestate: a prospect emissions during composting: a review. Sci. Total Environ. 798, 149294 https://doi.
review. Bioresour. Technol. 323, 124626 https://doi.org/10.1016/j. org/10.1016/j.scitotenv.2021.149294.
biortech.2020.124626. Yu, Q., Xia, D., Li, H., Ke, L., Wang, Y., Wang, H., Zheng, Y., Li, Q., 2016. Effectiveness
Wang, W., Chang, J.S., Lee, D.J., 2023b. Digestate-derived carbonized char and activated and mechanisms of ammonium adsorption on biochars derived from biogas residues.
carbon: application perspective. Bioresour. Technol. 129135 https://doi.org/ RSC Adv. 6 (91), 88373–88381. https://doi.org/10.1039/C6RA16913A.
10.1016/j.biortech.2023.129135. Yuan, H., Lu, T., Huang, H., Zhao, D., Kobayashi, N., Chen, Y., 2015. Influence of
Wang, Y., Song, Y., Li, N., Liu, W., Yan, B., Yu, Y., Liang, L., Chen, G., Hou, L., Wang, S., pyrolysis temperature on physical and chemical properties of biochar made from
2022d. Tunable active sites on biogas digestate derived biochar for sulfanilamide sewage sludge. J. Anal. Appl. Pyrolysis 112, 284–289. https://doi.org/10.1016/j.
jaap.2015.01.010.
18
Z. Fu et al. Science of the Total Environment 912 (2024) 168822
Yuan, Q., Sui, M., Qin, C., Zhang, H., Sun, Y., Luo, S., Zhao, J., 2022. Migration, technology: a systematic review. Environ. Sci. Pollut. Res. 27, 28749–28767.
transformation and removal of macrolide antibiotics in the environment: a review. https://doi.org/10.1007/s11356-020-09282-2.
Environ. Sci. Pollut. Res. 1-18 https://doi.org/10.1007/s11356-021-18251-2. Zhang, Y., Xu, X., Zhang, P., Zhao, L., Qiu, H., Cao, X., 2019. Pyrolysis-temperature
Yuan, Q., Zhang, H., Qin, C., Zhang, H., Wang, D., Zhang, Q., Zhang, D., Zhao, J., 2023. depended quinone and carbonyl groups as the electron accepting sites in barley grass
Impact of emerging pollutant florfenicol on enhanced biological phosphorus removal derived biochar. Chemosphere 232, 273–280. https://doi.org/10.1016/j.
process: focus on reactor performance and related mechanisms. Sci. Total Environ. chemosphere.2019.05.225.
859, 160316 https://doi.org/10.1016/j.scitotenv.2022.160316. Zhao, D., Yan, B., Liu, C., Yao, B., Luo, L., Yang, Y., Liu, L., Wu, F., Zhou, Y., 2021a.
Yuan, Y., Chen, H., Yuan, W., Williams, D., Walker, J.T., Shi, W., 2017. Is biochar- Mitigation of acidogenic product inhibition and elevated mass transfer by biochar
manure co-compost a better solution for soil health improvement and N2O emissions during anaerobic digestion of food waste. Bioresour. Technol. 338, 125531 https://
mitigation? Soil Biol. Biochem. 113, 14–25. https://doi.org/10.1016/j. doi.org/10.1016/j.biortech.2021.125531.
soilbio.2017.05.025. Zhao, J., Zhang, J., Zhang, D., Hu, Z., Sun, Y., 2021c. Effect of emerging pollutant
Zhang, H., Fu, Z., Guan, D., Zhao, J., Wang, Y., Zhang, Q., Xie, J., Sun, Y., Guo, L., fluoxetine on the excess sludge anaerobic digestion. Sci. Total Environ. 752, 141932
Wang, D., 2023a. A comprehensive review on food waste anaerobic co-digestion: https://doi.org/10.1016/j.scitotenv.2020.141932.
current situation and research prospect. Process. Saf. Environ. Prot. 179, 546–558. Zhao, J., Qin, C., Sui, M., Luo, S., Zhang, H., Zhu, J., 2022. Understanding the mechanism
https://doi.org/10.1016/j.psep.2023.09.030. of polybrominated diphenyl ethers reducing the anaerobic co-digestion efficiency of
Zhang, H., Zhao, J., Fu, Z., Wang, Y., Guan, D., Xie, J., Zhang, Q., Liu, Q., Sun, Y., Sun, Y., excess sludge and kitchen waste. Environ. Sci. Pollut. Res. 29 (27), 41357–41367.
2023b. Metagenomic approach reveals the mechanism of calcium oxide improving https://doi.org/10.1007/s11356-022-18795-x.
kitchen waste dry anaerobic digestion. Bioresour. Technol. 387, 129647 https://doi. Zhao, J., Wang, Y., Guan, D., Fu, Z., Zhang, Q., Guo, L., Sun, Y., Zhang, Q., Wang, D.,
org/10.1016/j.biortech.2023.129647. 2023a. Calcium hypochlorite-coupled aged refuse promotes hydrogen production
Zhang, J., Tian, Y., Zhu, J., Zuo, W., Yin, L., 2014b. Characterization of nitrogen from sludge anaerobic fermentation. Bioresour. Technol. 370, 128534 https://doi.
transformation during microwave-induced pyrolysis of sewage sludge. J. Anal. Appl. org/10.1016/j.biortech.2022.128534.
Pyrolysis 105, 335–341. https://doi.org/10.1016/j.jaap.2013.11.021. Zhao, J., Zhang, H., Guan, D., Wang, Y., Fu, Z., Sun, Y., Wang, D., Zhang, H., 2023b. New
Zhang, J., Liu, J., Liu, R., 2015a. Effects of pyrolysis temperature and heating time on insights into mechanism of emerging pollutant polybrominated diphenyl ether
biochar obtained from the pyrolysis of straw and lignosulfonate. Bioresour. Technol. inhibiting sludge dark fermentation. Bioresour. Technol. 128358 https://doi.org/
176, 288–291. https://doi.org/10.1016/j.biortech.2014.11.011. 10.1016/j.biortech.2022.128358.
Zhang, K., Deng, Y., Liu, Z., Feng, Y., Hu, C., Wang, Z., 2023c. Biochar facilitated direct Zhao, W., Yang, H., He, S., Zhao, Q., Wei, L., 2021b. A review of biochar in anaerobic
interspecies electron transfer in anaerobic digestion to alleviate antibiotics inhibition digestion to improve biogas production: performances, mechanisms and economic
and enhance methanogenesis: a review. Int. J. Environ. Res. Public Health 20 (3), assessments. Bioresour. Technol. 341, 125797 https://doi.org/10.1016/j.
2296. https://doi.org/10.3390/ijerph20032296. biortech.2021.125797.
Zhang, Q.Q., Ying, G.G., Pan, C.G., Liu, Y.S., Zhao, J.L., 2015b. Comprehensive Zheng, X., Xu, W., Dong, J., Yang, T., Shangguan, Z., Qu, J., Li, X., Tan, X., 2022. The
evaluation of antibiotics emission and fate in the river basins of China: source effects of biochar and its applications in the microbial remediation of contaminated
analysis, multimedia modeling, and linkage to bacterial resistance. Environ. Sci. soil: a review. J. Hazard. Mater. 129557 https://doi.org/10.1016/j.
Technol. 49 (11), 6772–6782. https://doi.org/10.1021/acs.est.5b00729. jhazmat.2022.129557.
Zhang, W., Lang, Q., Wu, S., Li, W., Bah, H., Dong, R., 2014a. Anaerobic digestion Zhu, Y., Li, H., Zhang, G., Meng, F., Li, L., Wu, S., 2018. Removal of hexavalent
characteristics of pig manures depending on various growth stages and initial chromium from aqueous solution by different surface-modified biochars: acid
substrate concentrations in a scaled pig farm in southern China. Bioresour. Technol. washing, nanoscale zero-valent iron and ferric iron loading. Bioresour. Technol. 261,
156, 63–69. https://doi.org/10.1016/j.biortech.2014.01.013. 142–150. https://doi.org/10.1016/j.biortech.2018.04.004.
Zhang, W., Zhao, C., Cao, W., Sun, S., Hu, C., Liu, J., Zhao, Y., 2020. Removal of
pollutants from biogas slurry and CO2 capture in biogas by microalgae-based
19