Environmental Chemistry Letters (2023) 21:2707–2727

https://doi.org/10.1007/s10311-023-01618-x

REVIEW ARTICLE

Bioenergy production from chicken manure: a review

Ahmed Tawfik1 · Mohamed Eraky2 · Ahmed I. Osman3 · Ping Ai2 · Zhongbo Zhou4,5 · Fangang Meng6,7 ·
David W. Rooney3

Received: 24 May 2023 / Accepted: 31 May 2023 / Published online: 12 June 2023
© The Author(s) 2023

Abstract
Adopting waste-to-wealth strategies and circular economy models can help reduce biowaste and add value. For instance,
poultry farming is an essential source of protein, and chicken manure can be converted into renewable energy through
anaerobic digestion. However, there are a number of restrictions that prevent the utilization of chicken manure in bioenergy
production. Here, we review the conversion of chicken manure into biomethane by anaerobic digestion with focus on limiting
factors, strategies to enhance digestion, and valorization. Limiting factors include antibiotics, ammonia, fatty acids, trace
elements, and organic compounds. Digestion can be enhanced by co-digestion with sludge, lignocellulosic materials, food
waste, and green waste; by addition of additives such as chars, hydrochars, and conductive nanoparticles; and by improving
the bacterial community. Chicken manure can be valorized by composting, pyrolysis, and gasification. We found that the
growth of anaerobic organisms is inhibited by low carbon-to-nitrogen ratios. The total biogas yield decreased from 450.4
to 211.0 mL/g volatile solids in the presence of Staphylococcus aureus and chlortetracycline in chicken manure. A chlo-
rtetracycline concentration of 60 mg/kg or less is optimal for biomethanization, whereas higher concentrations can inhibit
biomethane production. The biomethane productivity is reduced by 56% at oxytetracycline concentrations of 10 mg/L in the
manure. Tylosin concentration exceeding 167 mg/L in the manure highly deteriorated the biomethane productivity due to
an accumulation of acetate and propionate in the fermentation medium. Anaerobic co-digestion of 10% of primary sludge
to 90% of chicken manure increased the biogas yield up to 8570 mL/g volatile solids. Moreover, chemicals such as biochar,
hydrochar, and conducting materials can boost anaerobic digestion by promoting direct interspecies electron transfer. For
instance, the biomethane yield from the anaerobic digestion of chicken manure was improved by a value of 38% by sup-
plementation of biochar.

Keywords Chicken manure · Anaerobic digestion · Mono-digestion · Co-digestion · Biochar

4
* Ahmed Tawfik College of Resources and Environment, Southwest
prof.tawfik.nrc@gmail.com University, Chongqing 400715, China
5
* Ahmed I. Osman Chongqing Engineering Research Center of Rural Cleaner
aosmanahmed01@qub.ac.uk Production, Chongqing 400715, China
6
1 School of Environmental Science and Engineering, Sun
Water Pollution Research Department, National Research
Yat-Sen University, Guangzhou 510275, China
Centre, P.O. Box 12622, Giza, Egypt
7
2 Guangdong Provincial Key Laboratory of Environmental
College of Engineering, Huazhong Agricultural University,
Pollution Control and Remediation Technology (Sun Yat-Sen
Wuhan 430070, China
University), Guangzhou 510275, China
3
School of Chemistry and Chemical Engineering, David Keir
Building, Queen’s, University Belfast, Stranmillis Road,
Belfast BT9 5AG, Northern Ireland, UK

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2708 Environmental Chemistry Letters (2023) 21:2707–2727

Introduction However, several challenges limit the anaerobic digestion

of chicken manure (Jurgutis et al. 2020). One such limita-
In recent decades, the production and consumption of tion is the presence of high concentrations of ammonia and
energy in relation to urbanization, modernization, and volatile fatty acids in the chicken manure, along with anti-
industrialization have become increasingly significant in a biotics and heavy metals that are added to the animal feed,
variety of economic, scientific, and social sectors. In addi- which can negatively affect the anaerobic microorganisms
tion, the anticipated 10-billion-person global population (Mahdy et al. 2020). To overcome these limitations, sev-
by 2050 is a significant and pressing issue that necessitates eral practices have been reported to enhance the anaerobic
increased food security and energy production (Allam digestion of chicken manure. One such approach is the
et al. 2015; Manogaran et al. 2020; Osman et al. 2022). anaerobic co-digestion technology, in which other feed-
Therefore, investigating alternative solutions is crucial for stocks are added to the chicken manure. It has been found
resolving the impending global energy crisis and rising that the addition of other feedstocks can enhance biogas
biofuel demands while also taking environmental issues productivity and alleviate inhibitory factors by diluting
and their mitigation into account (Ji et al. 2015; Elsayed the ammonia in the substrate and providing more nutrients
et al. 2020). The vast majority of the world's energy needs required for the anaerobes (Magbanua et al. 2001; Wang
are met by fossil fuels, but their greenhouse gas emis- et al. 2022). The addition of some substances, such as
sions pose a serious environmental threat (Tawfik et al. biochar, hydrochar, and conductive materials, can enhance
2022a). In accordance with the Paris roadmap agreement the anaerobic digestion and enhance the direct interspecies
from December 2015, greenhouse gas emissions must be electron transfer process. Great attention has been paid to
reduced by 50% by 2050 if the average global temperature the following reviews for treatment processes of chicken
rise is to be limited to 2 ℃ (Eraky et al. 2022). manure (Manogaran et al. 2022), anaerobic digestion of
In addition, animals, particularly chickens, have played chicken litter, animal manure and green policy(Bhatnagar
a crucial role in providing protein sources and promoting et al. 2022), ammonia inhibition (Fuchs et al. 2018). How-
global food security. Farming manure is one of the most ever, no comprehensive review focuses on the limiting fac-
prevalent organic wastes produced globally, and improper tors affecting the anaerobic digestion process, i.e., antibi-
disposal could lead to eutrophication and contamination of otics and aromatic substances (phenol and catechol) that
water bodies, which raises grave environmental concerns. is extensively addressed here. Furthermore, this review
Several operators have adopted anaerobic digestion, which article thoroughly examines the appropriate methods for
converts carbon waste into biogas, an important source handling chicken manure and explores potential applica-
of renewable energy, in order to address this issue (Sobhi tions to maximize its benefits. Specifically, it highlights
et al. 2019; Elsayed et al. 2022). Untreated chicken waste the use of chicken manure as a substrate in anaerobic
emits an offensive odor that attracts vermin and rodents, digestion technology while addressing the limitations and
spreads infections, and poses a significant threat to human possible solutions for improving the process.
health. Therefore, it is necessary to investigate feasible and
cost-effective options for the management and application
of chicken manure (Duan et al. 2019). Waste-to-wealth is Chicken manure characteristics
a waste management strategy that aims to recover and add
value to waste streams while fostering new technologies, Chicken manure characteristics play a big role in choosing
job creation, and environmental benefits (Elreedy et al. the proper management method to save energy and chemical
2015). The waste-to-wealth strategy is closely related to consumption and optimize the bioenergy productivity from
the circular economy model, which aims to reduce waste such waste (Meky et al. 2021). Chicken manure is rich in
through resource regeneration and recycling (Mostafa organics, ammonia–nitrogen, pathogens, and microorgan-
et al. 2017). Adopting this paradigm can lead to waste- isms degrading bacteria, as shown in Fig. 1 and reported
free value chains and the use of renewable energy and by Ibrahim et al. (2022). The total solids are 59.16 ± 0.06%;
natural resources. It is crucial to modernize systems for the volatile solids are 48.19 ± 0.24%, and the volatile solids-
managing chicken manure because it can generate circu- to-total solids ratio is 80.15%. Chicken manure is a suit-
lar economy outputs such as energy (Nasrollahzadeh et al. able substrate for bioenergy production strategies such
2019; Manogaran et al. 2022). as biogas production technologies due to the high total
Due to the high content of total and volatile solids as solids content and high biodegradability within chicken
well as highly biodegradable substances, chicken manure manure. Furthermore, the high nutrient contents of chicken
has a high potential for bioenergy production via the manure increased the wide range of exploitation methods.
anaerobic digestion process (Elsamadony et al. 2015). For example, carbon, nitrogen, sulfur, and hydrogen con-
tents of 38.91% ± 0.78, 9.39% ± 0.21, 0.47% ± 0.02, and

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Environmental Chemistry Letters (2023) 21:2707–2727 2709

Fig. 1  Characteristics of chicken manure that can aid in selecting the tion process. The unfavorable components of chicken manure, such
most effective management strategies. Due to an abundance of biode- as ammonia, antibiotics, heavy metals, and fatty acids, may hinder
gradable materials, high total solids, and essential nutrients, chicken anaerobic digestion
manure presents a significant advantage for the anaerobic diges-

5.68% ± 0.16, respectively, encourage the land application viability from an economic standpoint (Ran et al. 2022).
of chicken manure as fertilizer (Wang et al. 2022). Using anaerobic digestion, a type of biorefinery technology,
Due to the high protein and fat content, chicken manure is multiple biowaste streams can be converted into digestate
utilized in the animal feed industry. However, these protein and biogas that are rich in nutrients and energy. Additionally,
fractions result in high ammonia concentrations and a low it may reduce the odor and greenhouse gas emissions that
carbon-to-nitrogen ratio, which pose significant technologi- biowaste causes. However, the sustainability of anaerobic
cal obstacles to biogas production (Bhatnagar et al. 2022). digestion is contingent on its capacity to control the sub-
Li et al. (2022) characterized the chicken manure harvested stantial amount of digestate produced during the process, as
from a company with the following characteristics: total inefficient treatment of it could result in significant environ-
solids (% fresh matter) of 22.82% ± 0.03, volatile solids mental problems (Eraky et al. 2022). Chicken manure is a
(%fresh matter) of 19.94% ± 0.1, carbon (%total solids) of viable option for generating renewable energy due to its high
39.42% ± 0.9, hydrogen (% total solids) of 5.53% ± 0.01, biomethane potential, which is one of the highest among
nitrogen (% total solids) of 7.32% ± 0.6, and carbon/nitro- all livestock manures. Each kilogram of organic matter in
gen ratio of 5.4 ± 0.5. chicken manure is estimated to produce around 0.5 ­m3 of
In conclusion, considering the composition of chicken biogas containing about 58% methane. According to a com-
manure can improve the effectiveness of an application strat- monly used biogas handbook, the methane yield for chicken
egy. It has high biodegradable solid components, which sup- manure falls within the range of 200–360 mL/g volatile sol-
ports the use of chicken manure as a substrate for biogas pro- ids (Fuchs et al. 2018).
duction; however, high ammonia and lower carbon/nitrogen Although there has been little research on using chicken
are significant obstacles to the application of the anaerobic manure as a sole substrate for anaerobic digestion, it has a
digestion process (Table 1). substantial degree of biodegradability (Song et al. 2019**).
This is due to the high ammonia content in chicken manure,
which can raise pH levels and impair the anaerobic diges-
Anaerobic digestion as a bioenergy tion process. Moreover, the antibiotics in chicken manure
production strategy can inhibit the growth of anaerobic organisms, and the low
carbon-to-nitrogen ratio makes it difficult for these organ-
Anaerobic digestion is a challenging technology with enor- isms to survive. Additionally, volatile fatty acids in chicken
mous potential for treating organic waste (Tawfik and Salem manure can inhibit anaerobic digestion (Nie et al. 2015;
2012). In addition to lowering greenhouse gas emissions, Alhajeri et al. 2022). There are numerous ways to improve
it has the capacity to produce biogas and organic fertilizer. the anaerobic digestion of chicken manure through pro-
Large-scale operations have demonstrated the technology’s cessing. For instance, diluting the substrate can reduce the

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2710 Environmental Chemistry Letters (2023) 21:2707–2727

Table 1  Basic characteristics of chicken manure

Parameters Units Wang et al. (2019) Hassan et al. (2016) Wang et al. (2022) Li et al. (2022); Zhao et al. (2022)
Linsong et al.
(2022)

Total solids wt% 33.2 ± 0.2 29.56 59.16 ± 0.06 22.82 ± 0.03 27.19
Volatile solid wt% 25.6 ± 0.2 67.04 48.19 ± 0.24 19.94 ± 0.1 16.51
Volatile solids -to- total solids wt% 77.1 – 80.15 87.3 60.7
Total nitrogen wt% – 4.23 9.39 ± 0.21 7.32 ± 0.6 3.12
Carbon wt% – – 38.91 ± 0.78 39.42 ± 0.9 40.20
Hydrogen wt% – – 5.68 ± 0.16 5.53 ± 0.01 5.49
Sulfur wt% – – 0.47 ± 0.02 – 0.68
Total ammonia nitrogen mg/Kg 2240 ± 11.4 1343.33 – – –
Total organic carbon wt% 321,800 ± 9700 35.95 – 5.4 ± 0.5 –
Carbon-to-nitrogen ratio - – 8.51 – – –
Cellulose wt% – –
Hemicellulose wt% – – – – –
Lignin wt% – 10.13
pH – 7.71 ± 0.2 7.78 8.66 – –
Alkalinity mg/L 6270 ± 24.5 – - – -

The volatile organics are significant in the chicken manure that increased the biodegradability. The carbon-to-nitrogen ratio is an important
parameter affecting the biogas productivity. The anaerobic digestion process type, either dry or wet, highly depends on the biosolids composi-
tion. Trace elements are essential for the anaerobic digestion process that should be considered for the analysis of chicken manure

toxicity of ammonia, and adjusting the hydrolytic retention populations in chicken manure (Kirby et al. 2019). How-
time can enhance anaerobe performance (Vanwonterghem ever, the anaerobic digestion process is highly affected due
et al. 2015; Karki et al. 2021). However, it has been demon- to the presence of both chlortetracycline and Staphylococcus
strated that the co-digestion of chicken manure with other aureus in the manure feedstock resulting in a lower total
organic waste can reduce the negative effects of mono-diges- biogas yield. Total biogas productivity was 450.4 mL/g vola-
tion and increase biogas production. tile solids fed for chicken manure and reduced to 434.0 and
In conclusion, anaerobic digestion is a promising method 416.9 mL/g volatile solids fed for chicken manure contain-
for treating chicken manure and producing biogas and ing Staphylococcus aureus and chicken manure containing
organic fertilizer. Although chicken manure has a high biom- Staphylococcus aureus and chlortetracycline, respectively.
ethane potential, its low carbon-to-nitrogen ratio and other Likely, chicken manure containing Staphylococcus aureus
factors can impede anaerobic digestion. Co-digestion of and chlortetracycline produced the lowest methane yield
chicken manure and other organic waste can help overcome of 211.0 mL/g volatile solids fed. The chicken manure
these obstacles and increase biogas production. and chicken manure-rich Staphylococcus aureus provided
methane yields of 223.5 and 220.1 mL/g volatile solids fed,
respectively.
Anaerobic digestion limiting factors Sorption of the chlortetracycline onto the sludge would
occur, reducing the inhibition effect of antibiotics (Yin et al.
Antibiotics 2016). However, the sorption of chlortetracycline onto the
sludge could be reversible and depends on the operational
Chlortetracycline conditions and antibiotic concentration (Spielmeyer 2018).
Furthermore, chlortetracycline could be biodegraded by
The infected chicken flocks produce manure contaminated anaerobes existing in the sludge where some anaerobic bac-
with pathogenic Staphylococcus aureus and antibiotic chlo- teria have the capability to remove the hydroxyl (OH) and
rtetracycline. Antibiotics, primarily chlortetracycline, are amino ­(NH2) groups of the chlortetracycline compound (Yin
prescribed at the flock level in poultry farms to prevent et al. 2016). Some bacteria could use the antibiotic as a car-
and control the common disease. Thus, significant quanti- bon and nitrogen source for their growth and metabolism
ties of manure containing antibiotics are excreted daily by (Liao et al. 2017). It was reported that 100 μg/L chlortetra-
infected birds into the effluent manure. The anaerobic diges- cycline was removed by 48.7–84.9% in the anaerobic culture
tion process could highly destroy Staphylococcus aureus bacteria. Firmicutes, Bacteroidetes, and Proteobacteria were

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Environmental Chemistry Letters (2023) 21:2707–2727 2711

the dominant phyla for the biodegradation of chlortetracy- harvesting during the anaerobic digestion (Ince et al. 2013).
cline. Chlortetracycline isomerization could have occurred Biogas harvesting from anaerobic digestion of manure con-
under anaerobic conditions. Yin et al. (2016) found that taining oxytetracycline levels of 20, 50, and 80 mg/L was
biomethanization of chicken manure has occurred at chlo- reduced by 43.83, 65.1, and 77.79%, respectively (Ke et al.
rtetracycline concentration of less than 60 mg/kg total solids. 2014). Likely, the biomethane productivity was reduced by
However, (Álvarez et al. 2010) observed that a significant values of 56, 60, and 62% at oxytetracycline concentrations
drop in biogas yields of more than 62% is taking place at of 10, 50, and 100 mg/L in the manure, respectively (Álvarez
60 mg/kg total solids. The stoichiometry of the biomethane et al. 2010).
fermentation of chlortetracycline is presented in Eq. (1), Yin et al. (2016) found that the biochemical methane
where 1.0 g of chlortetracycline could produce 0.43 L of potential of the anaerobic digestion of manure-rich oxytet-
biomethane. However, increasing the concentration of chlo- racycline is feasible at a concentration not exceeding 40 mg/
rtetracycline from 60 to 500 mg/kg total solids reduced the kg total solids where the antibiotic could be completely
biomethane harvesting due to an inhibition effect of the anti- eliminated and converted into biomethane. However, oxy-
biotics on the methane-producing archaea. tetracycline above the thresholds inhibited manure biom-
ethanization, and the antibiotic removal rate exponentially
C22 H23 ClN2 O8 + 4H2 O → 10CH4 + 9CO2 + 2NH+4 + HCO−3 + Cl−
decreased at levels of 40–100 mg/kg total solids. Oxytet-
(1)
racycline negatively affects gram-negative microorganisms
Therefore, chicken manure from infected flocks contains (methanogen archaea) by combining with the A location of
Staphylococcus aureus and antibiotics (chlortetracycline), bacterial ribosomes preventing the coupling of tRNA and
which can reduce the amount of biogas produced during aminoacyl on the A location. This would inhibit protein syn-
anaerobic digestion. However, if chlortetracycline is bio- thesis and peptide growth leading to failure of the anaero-
degraded by anaerobic bacteria and absorbed by sludge, bic digestion process and bacterial death (Stone et al. 2009;
its inhibitory effect can be diminished. A chlortetracycline Huang et al. 2014).
concentration of 60 mg/kg or less is optimal for biometha-
nization, whereas higher concentrations can inhibit methane C22 H24 N2 O9 + 15H2 O → 11CH4 + 9CO2 + 2NH+4 + 2HCO−3
production. (2)
In conclusion, due to the high concentration of oxytetra-
cycline present in animal husbandry, 60–90% of antibiot- Tylosin
ics are excreted in urine and feces, posing health concerns
to humans and preventing the production of biogas from To protect chickens from common diseases, antimicrobials
manure. In addition to preventing protein synthesis and pep- such as tylosin are added to their food. Tylosin is a gram-
tide development in gram-negative bacteria, oxytetracycline positive bacteria-active antibiotic. The most effective anti-
inhibits manure biomethanization when used more than the biotic is Tylosin A, which is commonly used in farms. Ani-
recommended dose of 40 mg/kg total solids. mal manure excretes greater than 40% of the administered
tylosin. Tylosin inhibits protein synthesis by interacting with
Oxytetracycline 50S ribosomal subunits during the anaerobic digestion of
manure (Mazzei et al. 1993). However, archaea, particularly
Sixty to 90% of antibiotics are excreted daily in animals’ acetate-utilizing Methanosaeta spp., are not suppressed and
urine and feces, posing risks to human health and negatively are sensitive to high tylosin concentrations due to the pre-
impacting agricultural activities. However, anaerobes can vailing differences in 23S rRNA binding sites (Shimada
biodegrade this antibiotic into methane bioenergy (Eq. 2). et al. 2008). The effect of tylosin on the anaerobic degrada-
Theoretically, 1.0 g of oxytetracycline could produce 0.49 tion of manure was limited; nevertheless, the relative abun-
L of biomethane. However, increasing oxytetracycline lev- dance of Methanosarcinaceae sp. was quite low.
els from 40 mg/kg total solids to 500 mg/kg total solids An anaerobic sequencing batch reactor fed with wastewa-
reduced the biomethane productivity due to an inhibition of ter containing tylosin concentrations (0, 1.67, and 167 mg/L)
the antibiotic (Yin et al. 2016). Oxytetracycline concentra- was investigated by Shimada et al. (2008). 1.67 mg/L tylosin
tions in manure varied from 0 to 121.8 mg/kg total solids addition did not affect the reactor performance. However,
(Agga et al. 2020). The application of anaerobic digestion adding tylosin (167 mg/L) to the reactor highly reduced the
for biogas harvesting from manure could be inhibited due biomethane productivity and accumulation of acetate and
to the presence of high concentrations of oxytetracycline propionate. Biogas harvesting from butyrate-rich wastewater
(Ince et al. 2013). was fully inhibited in the presence of tylosin. This indicates
Oxytetracycline levels in the manure slurry decreased tylosin inhibited butyrate and propionate oxidizing syn-
from 20 to 0 mg/L and exhibited 50% inhibition in methane trophic bacteria and, subsequently, methanogenesis process.

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2712 Environmental Chemistry Letters (2023) 21:2707–2727

In conclusion, chicken manure contains the antibiotic Fatty acids

tylosin, which is added to chicken feed and inhibits pro-
tein synthesis during anaerobic digestion. Tylosin inhib- The lipid portion of the substrate is hydrolyzed by hydro-
its butyrate and propionate, thereby oxidizing syntrophic lytic enzymes during the anaerobic digestion stages. In this
bacteria and decreasing biomethane production, both of stage of hydrolysis, long-chain fatty acids are produced. Due
which affect the methanogenesis process. to their toxicity toward anaerobic bacteria, fatty acids have
inhibiting effects (Alhajeri et al. 2022). In addition to lower-
ing the pH, fatty acids can inhibit anaerobic digestion’s aci-
Ammonia dogenesis and acetogenesis phases (Elsamadony et al. 2021).
Furthermore, the long-chain fatty acids could need more
Nitrogen is abundant in chicken manure in urea and time to by hydrolyzed by the hydrolytic anaerobes, hence
protein forms, accounting for 30 and 70% of total nitro- increasing the anaerobic digestion time and decreasing the
gen contents, respectively. During anaerobic digestion, biogas production rates (Meng et al. 2022).
chicken manure's organic nitrogen and uric acid are con- The substrate's carbohydrates and proteins also degraded
verted into ammonium–nitrogen, which exists as ions anaerobically, leading to the formation of pyruvic acids and
and unionized ammonia. Temperature and pH increase subsequent volatile fatty acids. The accumulation of these
the proportion of ammonia, which is toxic to bacteria by fatty acids inhibits the activity of anaerobes and causes
diffusing across their cell membranes (Shapovalov et al. a decline in pH levels. It was reported that the inhibitory
2020). Numerous stages of anaerobic digestion are shown threshold of volatile fatty acids is 6.0 g/L (Zhang et al. 2022;
to be inhibited by a high concentration of total ammonia Ketsub et al. 2022). Propionate accumulation is a common
nitrogen. Particularly sensitive to ammonia are aceto- inhibitory event. Because propionate has a slow degradation
clastic methanogens. Aquatic environments contain both rate into biogas, the acidification of the anaerobic digestion
ionized ammonium nitrogen and unionized free ammo- system takes place, resulting in the failure of the system
nia nitrogen, which makes up total ammonia nitrogen. (Samarasiri et al. 2019).
According to the literature, total and free ammonia nitro- In conclusion, the anaerobic digestion of substrates pro-
gen suppressed mesophilic anaerobic digestion of chicken duces long-chain fatty acids. These fatty acids accelerate
manure at concentrations of 4.5 and 0.7 g/L, respectively. acidogenesis and acetogenesis, damage bacteria, and reduce
Methane yield declines under ammonia inhibition, and biogas production. Carbohydrates and proteins produce
volatile fatty acid accumulation has been seen as a result pyruvic acids and volatile fatty acids, but their accumula-
(Fuchs et al. 2018; Bi et al. 2020). tion above 6.0 g/L is inhibitive; propionate accumulation is
The mechanism of ammonia toxicity is that high con- a common cause of system failure due to its slow breakdown
centrations of extracellular ammonia cells can diffuse rate into biogas and pH decline.
into methanogenic bacterial cells and produce ammo-
nium ions, leading to an increase in protons and a pH Trace elements
imbalance. The procedure also requires the cell to expend
additional energy in order to pump potassium ions out of Chicken manure lacks trace elements such as cobalt, nickel,
the cell, resulting in potassium depletion. This can lead selenium, molybdenum, and tungsten that highly deterio-
to cytotoxicity (Jiang et al. 2019). Even though ammo- rate the biomethanization process. Those elements play a
nia inhibits anaerobic digestion, Wang et al. (2018a, b) necessary role in metabolizing microorganisms degrading
reported the role of free ammonia nitrogen in boosting organics into bioenergy. Cobalt (1 mg/L), nickel(1.0 mg/L),
hydrogen production. The authors discovered that free (0.2 mg/L), molybdenum (0.2 mg/L) and tungsten
ammonia inhibited all bioprocesses except for acetogen- (0.2 mg/L) supplementation increased the biomethaniza-
esis but that its inhibition of the hydrogen consumption tion of chicken manure from 0.017 ± 0.01 to 0.27 ± 0.03 L/g
processes such as homoacetogenesis, methanogenesis, volatile solids removed at ammonium concentration exceed-
and the sulfate-reducing process was much more severe ing 6000 mg/L due to the promoting the growth of hydrog-
than that of the hydrolysis and acidogenesis processes. enotrophic methanogens, i.e., Methanoculleus bourgensis
In conclusion, the high ammonia concentrations in (Molaey et al. 2018a). The biomethane yield from chicken
chicken manure pose a significant challenge to anaerobic manure was increased by a value of 50% and reached
digestion due to its toxic effects on the anaerobes. How- 0.27 ± 0.01 L/g of volatile solids added with selenium addi-
ever, the free ammonia could direct the anaerobic diges- tion (Molaey et al. 2018b). This was due to the selenium
tion process toward biohydrogen production. supplementation enhanced the digestion process stability
and increased the number of Methanoculleus bourgensis
genera. The addition of cobalt (1 mg/L), nickel (1.0 mg/L),

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Environmental Chemistry Letters (2023) 21:2707–2727 2713

molybdenum (0.2 mg/L), tungsten (0.2 mg/L), and selenium a whole than the specific process of methanogenesis from
(0.2 mg/L) significantly increased the biomethane yield from acetate. Aromatic chemicals disrupt the processes preceding
0.13 to 0.32 ± 0.01 L/g volatile solids added due to the grow- methanogenesis, thereby reducing biogas production. Over-
ing Methanobrevibacter. Anaerobic co-digestion of chicken all, aromatic chemicals inhibit hydrolysis and acetogenesis
manure with corn straw and food waste alleviated the defi- more effectively than methanogenesis (Ali et al. 2021; Ibra-
ciency of trace metals and increased the biomethane produc- him et al. 2022).
tivity, yield by 125.3% and microbial composition of Metha- In conclusion, numerous organic compounds can inhibit
nothermobacter and Methanoculleus (Zhu et al. 2022). Corn anaerobic digestion, including hydrophobic substances and
stover was co-digested with chicken manure to eliminate polar contaminants that can damage bacterial membranes.
the problem of trace metals deficiency by (Wei et al. 2021). Aromatic substances, such as phenol and catechol, have
Iron, cobalt, manganese, molybdenum, and nickel addition been found to inhibit all stages of anaerobic digestion, with
increased the biomethane yield by 34.5% from co-digestion hydrolysis and acetogenesis being impacted more severely
of corn stover with chicken manure. Likely, the biomethane than methanogenesis.
yield was increased by 20–39.5% from anaerobic digestion
of chicken manure rich with 6000 mg/L with supplementa-
tion of 1.0 mg/L for nickel, 1.0 mg/L for cobalt, 0.2 mg/L Enhancement of chicken manure anaerobic
for molybdenum, 0.2 mg/L for selenium, 0.2 mg/L for tung- digestion
sten, and 5 mg/L for iron(Molaey et al. 2018a). Anaerobic
digestion of chicken manure without trace element addition Co‑digestion
provided a methane yield of 0.12 ­m3 /kg of volatile sol-
ids added due to an accumulation of acetic and propionic Several studies indicate that co-digesting animal manure
acid. This biomethane yield was increased up to 0.26 ± 0.03 with different feedstocks increases methane production and
­m3/ kg of volatile solids added with the addition of trace is more economically advantageous than anaerobic diges-
elements(Molaey et al. 2018c). tion of animal manure alone, as shown in Fig. 2. During
In conclusion, microelements such as trace metals are co-digestion, the increased methane yields are attributable
essential for anaerobic digestion. It enhances the metabo- to the improved feed-substrate degradability and higher vola-
lism of the organics-rich wastes by anaerobes. However, tile solids concentration, both of which result in a higher
chicken manure suffers from a deficiency of trace elements methane potential (Rabii et al. 2019). Additional advantages
that negatively affect the biomethanization process. The co- of co-digestion with manure include its use as a carrier for
digestion with other substrates-rich trace elements still rep- drying feedstocks, the maintenance of the digester’s pH, the
resents a promising option for valorizing chicken manure. provision of essential nutrients for microbes, and the provi-
The addition of trace metals enhanced the microbial commu- sion of the essential anaerobic microorganisms required to
nity structure for anaerobic digestion of the chicken manure initiate the process (Montoro et al. 2019). Hence, co-diges-
containing a high ammonia concentration of 6000 mg/L. tion of complementary feedstocks can greatly improve the
stability of microbial communities and subsequent microbial
Organic compounds augmentation (Ma et al. 2020).

Many organic substances could prevent the anaerobic pro- Co‑digestion of untreated primary sludge with raw chicken
cess from occurring. Anaerobic digesters can serve as a manure under mesophilic environmental conditions
collection point for hydrophobic or sludge-bound organic
materials. Polar pollutants have the potential to harm bac- The yearly chicken manure production in Egypt is 2.3 mil-
terial membranes. By disrupting ion gradients, membrane lion tons (Mahmoud et al. 2022). Furthermore, huge amounts
swelling and permeability may ultimately result in cell lysis. of excess sludge from wastewater treatments are produced
Anaerobic processes are known to be sensitive to halogen- daily in Egypt. The authors investigated the biogas harvest-
ated aliphatic alkanes, alcohols, halogenated alcohols, alde- ing from mesophilic anaerobic cofermentation of untreated
hydes, ethers, ketones, acrylates, carboxylic acids, amines, primary sludge and chicken manure at different ratios. The
nitriles, amides, and pyridine and its derivatives. In addition, highest biogas yield of 8570 mL was obtained from cofer-
a few long-chain fatty acids, surfactants, and detergents have mentation of 10:90 primary sludge: chicken manure, while
been found to be detrimental to anaerobic digestion (Hernan- the yield was reduced to 5600 mL at a ratio of 90:10 (pri-
dez and Edyvean 2008). Several types of bacteria involved mary sludge:chicken manure). Excess sludge from waste-
in anaerobic digestion are shown to be inhibited to varying water treatment plants poses a serious problem for devel-
degrees by aromatic compounds. For instance, phenol and oping nations. However, the sludge contains volatile fatty
catechol were more detrimental to the digestive system as acids, less ammonia and is rich in microorganism-degrading

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2714 Environmental Chemistry Letters (2023) 21:2707–2727

Fig. 2  Anaerobic co-digestion of chicken manure with different feed- anaerobic digestion process. Co-digestion process maintains the pH at
stocks. Adding lignocellulosic materials, primary sludge, food waste, a neutral level. Co-substrate fermentation greatly improves the stabil-
or green waste could improve the properties of the chicken manure. ity of microbial communities and subsequent microbial augmentation
The supply of essential nutrients for microbes is essential for the

organics (El-Kamah et al. 2010). However, solely anaerobic play a big role in the acidogenesis of organics and pro-
digestion of sewage sludge yielded low energy productivity duce volatile fatty acids in the fermentation medium(Ali
due to the limitation of the biodegradable substrate and high et al. 2021). Thermotogae bacteria highly metabolize car-
carbon/nitrogen ratio, which caused a drop in the microbial bohydrates into fatty acids, and a proper mixing ratio of
producing energy (El-Bery et al. 2013). chicken manure and sewage sludge promotes the micro-
Adding chicken manure would enhance bioenergy pro- bial metabolism of Synergistetes and Thermotogae (Tawfik
ductivity due to a balanced carbon-to-nitrogen ratio, buffer- et al. 2014). The archaeal communities at thermophilic
ing capacity and supply of sufficient hydrogen and methane- conditions were Methanosaeta (57.1–84.2%), Methano-
producing microorganisms. Solely anaerobic digestion of spirillum (3.7–9.0%), Methanobacterium (5.0–12.9%),
sewage sludge provided a biomethane yield of 82.4 mL/g Methanobrevibacter (0.5–2.1%), and Methanolinea
volatile solids added under mesophilic conditions and (0.4–5.9%). Methanosaeta is known to be a strict aceti-
33.9 mL/g volatile solids added under thermophilic condi- clastic organism, and it cannot utilize molecular hydrogen
tions (Wang et al. 2022). Those values were highly increased for methane productivity (Farghaly et al. 2019). Metha-
with the addition of chicken manure at ratios (1 sewage nolinea and Methanospirillum are methanogens neces-
sludge: 1.5–2 chicken manure) up to 123.1 mL/g volatile sary for hydrogen scavenging into biomethane and play a
solids added under mesophilic and 171.3 mL /g volatile sol- role in volatile fatty acid conversion (Qyyum et al. 2022).
ids added under thermophilic conditions, respectively. Methanobacterium is mainly a hydrogenotrophic metha-
The bacterial communities dominating at thermo- nogen that has the capability to convert carbon dioxide
philic temperatures were Firmicutes (26.4– 37.6%), Pro- and hydrogen into methane (Tawfik et al. 2022a). Metha-
teobacteria (5.2–15.7%), Actinobacteria (13.5–29.1%), nosarcina is an efficient archaea methanogen at high total
Thermotogae (0.6–6.7%), Chloroflexi (3.5–15.0%), and ammonium nitrogen compounds which could highly make
Synergistetes (0.5–4.4%). The Firmicutes are mainly a synergism effect between aceticlastic and hydrogeno-
responsible for organics metabolism, particularly hydroly- trophic organisms. The combination of hydrogenotrophic
sis and acidogenesis (Elreedy et al. 2019). Actinobacteria methanogenesis and syntrophic acetate oxidation is the

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Environmental Chemistry Letters (2023) 21:2707–2727 2715

main microbial pathway of biomethane generation from Furthermore, the co-digestion boosts buffering abil-
organics degradation. ity, dilutes potentially harmful substances, makes use of
Hydrogenotrophic reaction by Methanoculleus, Methano- nutrients and a variety of microorganisms, and reduces the
brevibacter, and Methanobacterium (Eq. 3) chance of ammonia inhibition. The high water content of
animal manures can dilute the concentrated organic chemi-
4H2 + CO2 → CH4 + 2H2 OΔG◦ −135 KJ∕mol CH4 (3)
( )
cals in lignocellulosic waste, thereby reducing the inhibi-
tory effect on the process. Numerous anaerobic digestion
Methanogenesis process by Methanoculleus and Metha-
processes that combine animal manure with lignocellulosic
nobrevibacter (Eq. 4) and by Methanoculleus and Methano-
by-products or other carbon-rich materials as co-substrates
bacterium (Eq. 5).
are examined in this context.
Wheat straw is a common agricultural waste that has
( )
4HCOOH → CH4 + 3CO2 + 2H2 O −130 KJ∕mol CH4
(4) the potential to be used in the generation of biogas. Due to
( ) its high lignocellulose content, the material produces little
CO2 + 4 CH3 2CHOH → CH4 + 4CH3 COCH3 methane since wheat straw degrades slowly and performs
(5)
poorly during anaerobic digestion. The wheat straw’s inef-
( )
+ 2H2 O −37 KJ∕mol CH4
fectiveness is further constrained by its high carbon-to-nitro-
The methylotrophic reaction by Methanomassiliicoccus gen ratio, which is too high for anaerobic digestion, and its
and Methanobacterium (Eq. 6) low trace element levels (Chen et al. 2020).
In conclusion, lignocellulosic materials produce little
(6)
( )
CH3 OH + H2 → CH4 + H2 O −113 KJ∕mol CH4
methane and degrade slowly; however, co-digestion with
Aceticlasitic reaction by Methanothrix (Eq. 7) chicken manure can increase biogas production and preserve
nutrient-rich residue. Wheat straw, a common agricultural
(7) waste, has the potential to produce biogas due to its slow
( )
CH3 COOH → CH4 + CO2 −33 KJ∕mol CH4
decomposition and high carbon-to-nitrogen ratio, but its use
In conclusion, according to research conducted in Egypt alone is ineffective.
on the potential for biogas production by cofermentation
of chicken manure and untreated primary sludge at various Food waste
ratios, the maximum biogas yield was found to be generated
from a 10:90 ratio of primary sludge to chicken manure. Several studies have examined the benefits and difficulties of
Due to a balanced carbon-to-nitrogen ratio and the presence managing food waste through anaerobic digestion compared
of microorganisms, the addition of chicken manure to the with landfills and incineration. Hegde and Trabold (2019)
anaerobic digestion of sewage sludge enhanced bioenergy contend that anaerobic digestion is a more environmentally
production. During the fermentation process, communities benign method of managing food waste. Although it is com-
of bacteria and archaea were discovered, with diverse spe- mon to combine the digestion of animal manure with food
cies participating in various aspects of organics metabolism waste, there is growing interest in just the digestion of food
and biomethane production. waste. Researchers have investigated the use of mixed res-
taurant food waste and other substrates in anaerobic diges-
Lignocellulose materials tion and discovered that stability and methane yield could be
affected by factors such as the loading rate of organic mate-
Lignocellulosic materials have a high carbon content and rial and the addition of trace elements (Zhang et al. 2019;
cannot be used for anaerobic digestion alone due to their de Jonge et al. 2020).
slow decomposition and low methane production. Although Anaerobic digesters may benefit from the co-digestion of
pretreatments can increase the potential for biogas produc- food waste, and pretreating animal manure with activated
tion, they may not be economically viable because cellu- carbon and microwave energy before digestion may increase
lose hydrolysis is the rate-limiting step in the process. (Peng methane production and decrease the genes associated with
et al. 2019; Ran et al. 2022). Co-digestion of lignocellulosic antibiotic resistance (Paranjpe et al. 2023).
materials and chicken manure can balance the carbon-to- Zhu et al. (2022) found that co-digestion of food waste,
nitrogen ratio for anaerobic digestion, produce biogas while corn straw, and chicken manure in two-stage anaerobic
retaining a nutrient-rich residue, and produce bioenergy. Co- digestion significantly increased hydrogen and methane
digestion also has advantages such as improving bacterial production compared to mono-substrate digestion. The
variety, optimizing nutrient utilization, decreasing the risk dominant hydrogen production pathways were butyrate and
of ammonia inhibition, and enhancing buffering capacity ethanol fermentation, with FW as the main substrate. The
(Karki et al. 2021). highest methane co-digestion efficiency was observed at a

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2716 Environmental Chemistry Letters (2023) 21:2707–2727

foods waste:(corn straw:chicken manure) ratio of 8:2 with activity and a larger relative abundance of methanobacte-
a fixed corn straw:chicken manure ratio of 3:1. The easily rium, co-digestion of all three substrates, thereby increased
bioavailable part of trace elements positively correlated with biomethanization by 49.9%.
co-digestion efficiency. The increased relative abundance of
obligate hydrogenotrophic methanogens, specifically Meth- Additives
anoculleus and Methanothermobacter, suggested positive
co-digestion efficiency in the two-stage anaerobic digestion. The addition of chars mitigates the ammonium inhibition
In conclusion, the anaerobic digestion of food waste has and biogas productivity
advantages as well as disadvantages, which have been the
focus of numerous studies. Food waste can produce more Chars were reported to highly reduce the inhibition effect of
methane and hydrogen when co-digested with other sub- ammonia, and metal ions, with improving methane yields
strates, whereas stability and methane yield can be affected (Yang et al. 2017; Masebinu et al. 2019). The biochar and
by factors such as loading rate and trace element addition. hydrochar addition improves methane yields from manures
Additionally, pretreatment of animal manure with activated by values ranging from 17 to 500% (Hurst et al. 2022). Bio-
carbon and microwave energy may increase methane pro- char derived from rice husk and wood was efficiently used
duction and decrease antibiotic resistance genes before for ammonium elimination from anaerobic digestate (Kizito
digestion. et al. 2015). The maximum adsorption capacity of wood and
rice-husk-derived biochar was 44.64 and 39.8 mg/g, respec-
Anaerobic co‑digestion of chicken manure tively. The adsorption was increased due to an increase in
with Enteromorpha and green waste biochar adsorption sites. The adsorption efficiency of both
biochars was highly increased with an increase in ammo-
Enteromorpha prolifera is one of the harmful algal blooms nium ­(NH4) concentration, temperature, contact time, and
that resulted from pollution and formed during sea tides pH. However, increasing the biochar particle size led to a
(Tawfik et al. 2006). Huge quantities of green waste, such substantial reduction in adsorption capacity (Linville et al.
as grass clippings, are annually produced and mainly incin- 2017).
erated, releasing harmful oxides. Furthermore, anaerobic Increasing the biochar dosage from 0.1 to 1.0 g enhanced
digestion of solely green waste and Enteromorpha prolifera ammonium adsorption from the digestate. At dosages greater
produced low quantities of biogas due to the difficulty of than 1.0 g, however, the ammonium adsorption rate degraded
hydrolysis and the low nitrogen content (Tawfik and Salem dramatically. Lü et al. (2016) investigated the effect of bio-
2014). Anaerobic co-digestion with chicken manure that char particle size on biogas productivity and ammonium
is rich with easily biodegradable organics and nitrogenous adsorption capacity. The lag phase of ammonium adsorp-
compounds would promote microbial activities and subse- tion on biochar was highly reduced by 23.9, 23.8, and 5.9%
quently increase the biogas yield. Co-substance of chicken with biochar particle sizes of 2.5–5, 0.5–1, and 75–150 μm,
manure was anaerobically digested with Enteromorpha pro- respectively. Furthermore, the biomethane productivity
lifera and green waste to improve biomethanization (Zhao was increased by 47.1, 23.5, and 44.1% for biochar particle
et al. 2022). Anaerobic mono-digestion of chicken manure, sizes of 2.5–5, 0.5–1, and 75–150 μm, respectively, due to
Enteromorpha prolifera and green waste produced biom- the increased Methanosarcina community. This indicates
ethane yield of 1.162, 0.948, and 0.963 mL/g volatile solids that biochar particle size is the major parameter affecting
per hour. Co-digestion of chicken manure: Enteromorpha adsorption and promoting microbial growth. Taghizadeh-
prolifera at a ratio of 2:1 improved biomethane productivity Toosi et al. (2012) found that the ammonium was adsorbed
by 32.7%. Further biomethanization improvement of 49.9% by biochar due to the large adsorbent surface area.
was achieved for co-digestion of three substrates of chicken The biochar has the ability to adsorb free ammonia during
manure, Enteromorpha prolifera, and green waste. This was the anaerobic digestion process of citrus waste, as reported
mainly due to the enhancement of cellulase enzyme activi- earlier (Chen et al. 2008; Solé-Bundó et al. 2019). Torri
ties and increased the relative abundance of methanobacte- and Fabbri (2014) found that methane content in the biogas
rium from 12.0 to 43.7%. composition increased from 34 to 60% with the addition
In conclusion, the co-digestion of chicken manure with of biochar derived from corn stalks. The biochar addi-
green waste and Enteromorpha prolifera was investigated tion reduced the lag phase from 10 days to 5.5–5.9 days in
to enhance biomethanization. Little biogas yields were the anaerobic digester (Sunyoto et al. 2016). This further
obtained from anaerobic mono-digestion of these substrates, resulted in an increase in biomethane productivity by 41.6%.
but biomethane productivity was increased by the co-diges- However, the reactors ceased to produce methane at biochar
tion of chicken manure and Enteromorpha prolifera at a dosage exceeding 16.6 g/L. The biochar encourages volatile
2:1 ratio. Due to primarily the enhanced cellulase enzyme fatty acids productivity during the hydrolysis process and

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Environmental Chemistry Letters (2023) 21:2707–2727 2717

promotes the methanogenesis process. Sunyoto et al. (2016) In conclusion, adding biochar during anaerobic digestion
indicated that biochar adding enhanced the acidogenesis pro- increases methane production by mitigating the inhibitory
cess at a pH of 5 and improved hydrogen productivity and effects of ammonia and metal ions. Wood and rice husk bio-
yield by 32.5 and 31%. Similarly, methanogenesis at a pH of char effectively remove ammonium from anaerobic diges-
7 and the supplement of biochar increased methane produc- tate; however, the adsorption capacity decreases as biochar
tion and yield by 41.6 and 10%, respectively. particle size increases. In addition, biochar accelerates the
Furthermore, the biochar highly reduced the lag phase acidogenesis and methanogenesis processes, shortens the lag
period by a value of 36% during acidogenesis and 41% dur- phase, and promotes the growth of archaea and methano-
ing the methanogenesis process. This can be attributed to gens. Moreover, biochar facilitates the direct interspecies
increased archaea with adding biochar (Luo et al. 2015). electron transfer process during biomethanization and has a
Shanmugam et al. (2018) compared biochar with activated high carbon dioxide adsorption capacity.
carbon for the biomethanization of glucose-rich wastewater
in batch anaerobic digestion. The authors found that both Addition of hydrochar
biochar and activated carbon promoted a direct interspecies
electron transfer process. However, biochar increased the Agriculture wastes subjected to acid hydrolysis yielded a
yield of methane by 72%; and activated carbon improved the solid residue primarily composed of lignin and recalcitrant
yield of methane by 40%. This indicates that the biochar has lignocellulose. Particularly, these residues are humins. As a
high redox-active species compared with activated carbon, byproduct of biorefinery processes, macromolecular humins
thereby facilitating the transfer of electrons between fermen- are produced from carbon-based materials, specifically sac-
tative bacteria utilizing substrate and methanogens, convert- charide-based ones. Humins are comparable to hydrochars.
ing volatile fatty acids, hydrogen, and carbon dioxide. Hydrochars are residues-rich carbonaceous materials result-
Likely, biochar supply enhanced the direct interspecies ing from hydrothermal carbonization of biomass using a cat-
electron transfer process and, subsequently, the biometha- alyst under free aqueous conditions. The utilized hydrochar
nization of wastewater in an upflow anaerobic sludge blan- can be used for the anaerobic digestion of chicken manure
ket reactor (Zhao et al. 2016). The biochar-amended upflow for enhancement of bio methane productivity. Supplying
anaerobic sludge blanket reactor showed an increase in hydrochar and/or biochar to the fermentation medium could
methane by 16–25% compared with the control digester adsorb the fermentation inhibitors existing in the chicken
due to the growing of Geobacter and Methanosaeta. Due manure and promotes the growth of degrading archaeal and
to the promotion of the direct interspecies electron transfer bacterial organics (Nasr et al. 2021). Hydrochar from wood-
phenomenon, the addition of biochar during the anaerobic derived improved biomethane yields by 10% at ammonium
digestion process significantly reduces the rate of carbon concentrations of 4 g/L in the chicken manure (Ganesh
dioxide production. The removal of carbon dioxide during et al. 2014). Hurst et al. (2022) found that adding hydrochar
anaerobic digestion of food waste by adding walnut shell- (2–10 g/L) increased the methane yields by 14.1% from the
derived biochar was investigated by Linville et al. (2017). anaerobic digestion of chicken manure. 6 g/L of hydrochar
The biochar-amended anaerobic digester improved methane adsorbed 20% of ammonium concentrations and highly
content harvesting by 77.5–98.1% and the carbon dioxide promoted the growth of microbial diversity, particularly
reduction by 40 and 96%. Biochar has a high capacity for Firmicutes and Bacteroidetes phyla. Nevertheless, archaea
the adsorption of carbon dioxide. (Euryarchaeota) abundance was decreased with the addition
The pine and corn-stover-derived biochar-amended anaer- of hydrochars. Likely, the biomethane yield from anaerobic
obic digesters fed sewage sludge provided an increase in digestion of chicken manure was improved by a value of
methane content by 9.1 and 25.3%, respectively (Shen et al. 38% by supplementation of biochar. Hydrochar derived from
2017). Likely, both biochars at a dosage of 1.75 g/g volatile sewage sludge highly enhanced the methane productivity
solids increased the biomethane yield by 16.6% for pine- from glucose by 37% (Ren et al. 2020). Hydrochar increases
derived biochar and 36.9% for corn-stover-derived biochar. the biomethane productivity from acetate fermentation and
This indicates that biochar improves the anaerobic diges- promotes hydrogenotrophic methanogenesis by direct inter-
tion stability and enables carbon dioxide adsorption. Wheat species electron transfer where proton, electron, and carbon
straw-derived biochar improved biomethane productivity dioxide are converted into methane (Fig. 3). The hydrochar
and yield by 46 and 31% (Mumme et al. 2014). Vegetable accepts electrons from anaerobic bacteria by organic oxida-
waste-derived biochar cleaned biogas from carbon dioxide tion and donates those electrons to methanogens for harvest-
by a value of 84.2% within 25 min in an adsorption tower ing of methane from fermentation of wastes. The electrons
(Sahota et al. 2018). Likely, the removal of hydrogen sulfide are shuttled for direct interspecies electron transfer process
from biogas exceeded 98% by the addition of biochar during to promote the methanogenesis process.
the anaerobic digestion process (Kanjanarong et al. 2017).

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2718 Environmental Chemistry Letters (2023) 21:2707–2727

Fig. 3  Hydrochar's contribu-

tion to the enhancement of
methane production. Hydro-
char accepts electrons from
anaerobic bacteria via organic
oxidation and donates these
electrons to methanogens in
order to harvest methane from
waste fermentation. To promote
the methanogenesis process,
electrons are transferred directly
between anaerobic species.
­NH4+ and OH refer to ammo-
nium and hydroxyl groups. The
Methanosaeta (Methanothrix)
was involved in the direct inter-
species electron transfer process

Further, the redox activity of biochar served as an elec- transformation process of alcohols and volatile fatty acids
tron transfer shuttle and accelerated the process between into biomethane via direct interspecies electron trans-
bacteria and methanogens in the fermentation system. The fer process using methanosarcina barkeri and Geobacter
Trichococcus and Methanosaeta were abundant with hydro- metallireducens (Rotaru et al. 2014; Tawfik et al. 2022c).
char added into the fermentation medium. Methanosaeta was Luo et al. (2015) found that the biochar established a direct
highly involved in the direct interspecies electron transfer interspecies electron transfer process between anaerobic bac-
process, where protein upregulation was involved in the teria and methanogens for the biomethanization of organ-
hydrogenotrophic methanogenesis process. The Methanos- ics. Magnetite and granular activated carbon as conductive
aeta (Methanothrix) was involved in the direct interspecies materials were used to accelerate and stabilize the organic
electron transfer process, where they utilized protons and waste conversion into a biomethane batch digester (Zhao
electrons but not molecular hydrogen for enhancing hydrog- et al. 2017). The results showed that magnetite enhanced
enotrophic methanogenesis (Rotaru et al. 2014; Holmes et al. the decomposition of the complex organic into simple struc-
2017). The authors (Ren et al. 2020) attempted to produce ture components, and the conductive carbon-based materials
hydrochars from activated carbon, corn straw, poplar wood, highly promoted the syntrophic conversion of volatile fatty
and Enteromorpha algae and examined them in anaerobic acids, hydrogen, and carbon dioxide into biomethane via
digestion. Supplement of sewage sludge, Enteromorpha direct interspecies electron transfer process.
algae, and corn straw-derived hydrochar increased methane The biomethane productivity was increased by 16% with
productivity by 39, 20, and 15%, respectively, compared magnetite addition due to stimulating the methanogenesis.
with the control experiment. This was mainly due to hydro- Magnetite-granular activated carbon supplement increased
char's redox property, electrical conductivity, and abundant biomethane productivity by up to 80%. This was due to a
surface functional groups (oxygen-containing). couple of mechanism actions of the direct interspecies elec-
tron transfer process and methanogens growing. Magnetite is
Addition of conductive nanoparticles materials a crystalline and insoluble form of ferric and ferrous oxides
with a high electrical conductivity that serves as an electron
As shown in Fig. 4, conductive carbon and non-carbon- conduit to enhance and improve the direct interspecies elec-
based materials served as highly electrical conduits, thereby tron transfer between syntrophs activities and methanogens
facilitating direct interspecies electron transfer between the archaeal. Methanobacterium species or hydrogen-utilizing
bacterial degrading substrate and methanogen organism’s methanogens have the capability of maintaining the hydro-
activities. Granular activated carbon, graphite rod, biochar, gen balance and partial pressure in the anaerobic digester
and carbon cloth could highly accelerate the syntrophic that was only 10% of the relative abundance communities in

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Environmental Chemistry Letters (2023) 21:2707–2727 2719

Fig. 4  Conductive nanoparticles material facilitates the direct inter- ture components. The conductive carbon-based materials highly pro-
species electron transfer between electron-donating bacteria and elec- moted the syntrophic conversion of volatile fatty acids, hydrogen,
tron-accepting methanogens. The biodegradable substances are oxi- and carbon dioxide into biomethane via a direct interspecies electron
dized and generate carbon dioxide, which is converted at the end to transfer process. The relative abundance of Ruminococcaceae and
methane by the action of methanogens. The nanoparticles enhanced Clostridiaceae is increased by 30% with magnetite nanoparticles
the bacterial decomposition of the complex organic into simple struc- addition compared with the control digester

the control and increased to 80% with magnetite supplement. fatty acids, hydrogen, and carbon dioxide into biomethane.
This increase in the abundance of methanobacterium spe- Magnetite or granular activated carbon can increase the
cies is described as a magnetite supplement that accelerates number of methanogens in anaerobic digestion processes,
the bacterial complex organics decomposition into a simple such as Methanobacterium and Methanosaeta species, and
one with hydrogen generation facilitating the growth of such significantly improve biomethane productivity.
species. The relative abundance of Ruminococcaceae and
Clostridiaceae was increased by 30% with magnetite addi- Enhancement of the bacterial community
tion compared with the control digester.
Furthermore, the Methanosaeta species was increased The anaerobic digestion of chicken manure is suffered from
by 10–18% with granular activated carbon supplementation the inhibition effect of high ammonium accumulation in the
suggesting the potential occurrence of a direct interspecies fermentation medium due to the imposed high loading rate.
electron transfer process. Enhancement of biomethanization The ammonia inhibition of methanogenesis in the fermenta-
of dog food waste was taken place by supplementation of tion medium is mainly due to the accumulation of volatile
granular activated carbon (Dang et al. 2017). The biometh- fatty acids caused by imposing a high organic loading rate
ane productivity was increased by 865% due to the addition (Tawfik et al. 2022b). Solving the problem of ammonia inhi-
of granular activated carbon, which improved the volatile bition onto methanogens by dilution, co-digestion with low
solids degradation and chemical oxygen demand by 22 and carbon-to-nitrogen ratio substrate, pretreatment (sir strip-
167%, respectively. The granular activated carbon (0–5 g) ping) and trace elements addition was attempted by several
supplied onto the anaerobic digestion process treating sludge investigators (Tyagi et al. 2021; Uzair Ayub et al. 2021).
materials boosted biomethane productivity by 17.4% (Yang A culture of propionate degrading methanogenic improved
et al. 2017). biomethane productivity from chicken manure and overcame
In conclusion, conductive carbon and non-carbon materi- the ammonia inhibition by changing the imposed loading
als can promote biomethane production by facilitating direct rate (Li et al. 2022). Methanogenic culture highly promoted
electron transfer between bacteria and methanogens. Mag- the biomethane yield from chicken manure in an anaerobic
netite and granular activated carbon have been demonstrated digester by 17–26% at an imposed organic loading rate of
to enhance the decomposition of complex organics into sim- 2–4 g/ L.d compared with the control digester. This was
pler components and to facilitate the conversion of volatile due to the dominance of hydrogenotrophic methanogens

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2720 Environmental Chemistry Letters (2023) 21:2707–2727

and increasing the growth of aceticlastic Methanothrix and at a mesophilic temperature of 20–45 °C. These microbial
Syntrophobacter (syntrophic propionate oxidizing bacteria). activities cause the compost to heat up to 65–68 °C, chang-
Nevertheless, the enhancement of biomethane produc- ing the reaction medium from mesophilic to thermophilic
tivity declined to 15–18% at increasing the organic loading conditions and killing pathogens (Tuomela et al. 2000) in
rate from 4.0 to 5.0 g/ L.d, and ammonia level of 5.0–8.4 g the second step. In the third step, the compost temperature
­NH4+-N/L. (Linsong et al. 2022) found that bioaugmenta- is reduced, and fungi proliferate to degrade hemicellulose,
tion of the anaerobic digestion of chicken manure increased cellulose, and lignin, producing stable humic substances
the biomethane yield and shortened the fermentation time. (Sánchez et al. 2017).
The biomethane yield of digesters was increased by values Finally, compost-free pathogens are produced safely and
of 1.2, 1.7, 2.2, 3.4, and 3.6-fold with methanogens supple- contain sufficient nutrients for agricultural applications (Li
mentation ratios of 0.07, 0.14, 0.21, 0.27, and 0.34 g vola- 2020). The composting degree is highly dependent on the
tile solids (bioaugmentation seed)/g volatile solids (chicken temperature. (Godlewska et al. 2017) reported that an initial
manure), respectively. This was mainly due to the growing of temperature exceeding 40 °C and an oxygen of 900 mg/g
Methanothrix, Methanobacterium, and Methanomassiliicoc- volatile solids/h is required for composting. A temperature of
cus. Nevertheless, bioaugmentation of methanogenic ratio of 0–10 °C and oxygen demand of 1 mg/g volatile solids/hour
0.34 g volatile solids bioaugmentation seed/g volatile solids are needed to terminate the composting process. In-vessel
chicken manure did not highly improve the biomethaniza- reactors, aerated and/or static bins are important for accom-
tion process. plishment of composting techniques (Sánchez et al. 2017).
In conclusion, the accumulation of high levels of ammo- Temperature, carbon/nitrogen ratio, moisture, aeration rate,
nium and volatile fatty acids due to high organic loading particle size, and pH are the main factors affecting compost
rates limits the anaerobic digestion of chicken manure. quality, microbial structure community, and metabolism of
Dilution, co-digestion, and trace element addition have all bacterial degrading organics during composting process
been tried to overcome ammonia inhibition. The addition of (Wang et al. 2018b).
methanogenic cultures can boost biomethane productivity, Yu et al. (2015) found that the moisture content of the
but the effect diminishes as organic loading rates and ammo- composting process of manure and agricultural waste
nia levels rise. Methanogen bioaugmentation can increase needs to be maintained at a level of 50–60% wet basis. The
biomethane yield and reduce fermentation time, but high carbon-to-nitrogen ratio (25–30), pH (5.5–9), temperature
ratios do not result in significant improvements. (55–63 °C), and oxygen content (higher than 5%) are the
optimum conditions for producing good quality compost-
ing. Further, the pile has to be bulky to facilitate the air
Valorization of chicken manure space flowing with high water-holding capacity in the pores.
Chicken manure enjoys low porosity, alkaline pH, low car-
Waste valorization efforts have recently increased in con- bon-to-nitrogen ratio, and high moisture. The addition of
junction with the circular economy. The goal of the circular chicken manure to rice husk, wood chips, and sawdust for
economy is to transition away from the linear economy in composting reduces the carbon/nitrogen ratio and water con-
order to mitigate the negative environmental effects. The tent and increases pile porosity and aeration channels (Zhang
circular economy would reduce waste by regenerating and and Sun 2016). Composting of organic wastes is safe and
recycling resources, resulting in cleaner production. The low-cost technology compared to landfilling, which pollutes
circular economy will undoubtedly result in zero waste and, groundwater due to leachate contaminations (Ayilara et al.
as a result, value adds chains that use natural resources and 2020).
renewable energy in connected loops rather than linear flows Chicken manure compost is stable and easier to handle,
that facilitate the disposal and depletion of valuable eco- storage, and transport for soil fertilization (Akdeniz 2019).
nomic resources. One of the promising outcomes of chicken Nevertheless, the composting process is highly consuming
manure valorization could be a circular economy. time and requires from 3 to 6 months for mature compost
production. Moreover, the required footprint of the com-
Composting posting site is quite large compared with other technologies.
Composting piles generate bad odors due to the deterioration
Composting is the aerobic breaks down of chicken manure of the carbon-to-nitrogen ratio, water content, and aeration.
or any organic under thermophilic conditions to generate The piles generate ammonia at low imposed carbon-to-nitro-
stable and free pathogen digestate suitable for agricultural gen ratios where the excess nitrogen is highly volatilized,
applications (Akdeniz 2019). Four biological steps could causing a bad smell (Pardo et al. 2015). The piles could
be used to compost waste. The first step involves microor- become anoxic and rich with pathogens due to insufficient
ganisms hydrolyzing organics (proteins, sugars, and lipids)

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Environmental Chemistry Letters (2023) 21:2707–2727 2721

oxygen content, resulting in fermentation by-products, i.e., the pyrolysis of chicken manure are syngas (hydrogen and
alcohols and bad odor leachate (Ayilara et al. 2020). carbon monoxide) with low water quantities, tar and ash that
To summarize, composting is a process that converts depends on the feedstock type and composition. Lee et al.
organic matter into stable, pathogen-free compost suitable (2017) found that chicken manure pyrolysis in the presence
for agricultural use. The process consists of four biological of carbon dioxide provided a high productivity of carbon
steps that are affected by temperature, oxygen, moisture, pH, mono-oxide compared with the nitrogen gas source. Further-
and other factors. While composting is a less expensive and more, the addition of calcium carbonate increased the carbon
safer technology than landfilling, it requires time, space, and mono-oxide productivity up to 6.9 mol.% at a temperature of
management to prevent odor and pathogen buildup. 780 ºC in the presence of both carbon dioxide and nitrogen
gas. Pure nitrogen was utilized for chicken manure pyrolysis
Pyrolysis at 600–1000 °C (Burra et al. 2016). Catalytic pyrolysis of
chicken manure was used to produce aromatic hydrocarbons
Pyrolysis is the thermal decomposition of biomass or bio- (Shim et al. 2022).
solids in the absence of oxygen, resulting in biochar, bio- To summarize, pyrolysis is a thermal decomposition pro-
oil, and gas products. As illustrated in Fig. 5, pyrolysis of cess that produces biochar, bio-oil, and gas from biomass or
wastes and/or biomass occurs in three types: flash, slow, and biosolids in the absence of oxygen. The type of pyrolysis
fast pyrolysis. Pyrolysis is classified into three types based process used, and the products produced are determined by
on solid retention time, heating rate, biomass particle size, variables such as solid retention time, heating rate, biomass
and temperature. The products of the pyrolysis process are particle size, and temperature. Depending on the feedstock
determined by the type of biomass and the temperature (Hu size and composition, different types of reactors, such as
and Gholizadeh 2019). fixed bed, ablative, and fluidized bed, can be used for effi-
Fixed bed, ablative, and fluidized bed are the main cient pyrolysis. The catalytic effects of calcium carbonate
designed reactors for the pyrolysis process (Ore and Adebiyi combined with carbon dioxide increased carbon mono-oxide
2021). Based on the feedstock size and efficiency, the reactor productivity. Energy recovery, i.e., syngas (carbon mono-
is selected to avoid limitations and ensure functional effi- oxide and hydrogen) from chicken manure pyrolysis in the
cient of heat transfer with operational performance troubles presence of carbon dioxide, is a promising approach from a
free. Therefore, feedstock such as chicken manure should circular economy point of view.
be prepared and fractionized to be suitable for an efficient
pyrolysis process. This could be carried out using mechani- Gasification
cal machines for the grinding of wastes. The chicken manure
has to be initially dried to get feedstock with moisture con- The thermochemical conversion of carbon-rich feedstock
tent below 10 weight %. This step overcomes the implica- into combustible product gas using gasifying agents such
tions adverse of moisture on the viscosity, pH, stability, and as carbon or nitrogen is known as gasification (Yang et al.
corrosiveness of the end product. The products from the 2021; Eraky et al. 2022). Gasification consists of four stages,
pyrolysis of chicken manure are biochar, gases, and vapors as shown in Fig. 6, which are drying, devolatilization, also
(Hu and Gholizadeh 2019). The main gases produced from known as pyrolysis, combustion, and reduction. The drying

Fig. 5  Different types of pyroly-

sis processes. Three distinct
processes are used to pyrolyze
wastes and/or biomass: flash,
slow, and fast pyrolysis. Three
types of pyrolysis are distin-
guished based on temperature,
biomass particle size, heating
rate, solid retention time, and
solid retention time. The type of
feedstock and temperature have
an impact on how pyrolysis
produces its products. Syngas
(carbon mono-oxide and hydro-
gen) recovery from chicken
manure pyrolysis in the pres-
ence of carbon dioxide occurs at
a temperature of 780 ºC

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2722 Environmental Chemistry Letters (2023) 21:2707–2727

Fig. 6  Gasification of chicken

manure stages. The gasifica-
tion energy output of chicken
manure is increased by increas-
ing the temperature from 600
to 1000 °C, resulting in a high
energy yield. Carbon dioxide
is the suitable media for the
gasification of chicken manure.
Supercritical water chicken
manure gasification produces
hydrogen gas. Co-gasification of
the chicken manure waste with
other organic wastes is promis-
ing from a circular economy
point of view

stage necessitates the evaporation of free and bound water carbonaceous output as well as certain gas species produced
in the feedstock by heat often supplied by exothermic reac- by pyrolysis. The combustion reaction frequently produces
tions in the subsequent stages. The temperature is normally water, carbon dioxide, carbon monoxide, and hydrogen.
between 100 and 200 °C which satisfies the fundamental This strongly exothermic reaction is responsible for supply-
function of this stage in the overall process without ther- ing the gasifier heat required in the subsequent reduction
mally decomposing the feedstock. This is because the tem- reaction, as well as the drying and pyrolysis stages of the
perature condition does not meet the mark to execute such process, which are endothermic in nature. Gasification and
heavy duties (Yang et al. 2021). pyrolysis of chicken manure were investigated by Hussein
The emission of certain air pollutants, such as volatile et al. (2017) using carbon dioxide, nitrogen, air, and steam
organic compounds, is a disadvantage of this stage. None- and at 600–1000 °C temperatures. The energy recovery
theless, the inclusion of this step is significant in the case was increased by increasing the temperature from 600 to
of a feedstock with high moisture content. The drying stage 1000 °C. The highest energy yield was obtained from the
prevents feeding or fluidization issues such as agglomer- gasification of chicken manure by carbon dioxide, followed
ate formation and jamming, which are frequently associ- by steam. The lowest energy recovery from chicken manure
ated with feedstock with high moisture content, such as was obtained by pyrolysis and air gasification. However,
chicken manure. The reduced heating value of the product gasification reactions were the fastest, with air reducing the
gas reduces the overall energy efficiency of the gasification reaction time by a value of 75% compared with carbon diox-
reaction in the absence of the drying step. Because of the ide gasification.
decreasing reaction temperature, such conditions result in a Furthermore, energy yield was decreased by 55% at a
significantly increased tar content in the product gas (You temperature of 1000 °C. Oxygen concentrations of 21 and
et al. 2018). Essentially, the drying rate is controlled by the 10% incorporation with nitrogen were utilized to gasify
heat and mass transfer between feedstock particles and their chicken manure (Burra et al. 2016). The energy yield was
ambient atmosphere corresponding to the temperature differ- increased by increasing the oxygen content by 21%. The
ence, particle surface area, moisture, and convection veloc- maximum hydrogen yield, hydrogen and carbon gasification
ity of surrounding flows as well as diffusivity of moisture efficiency of supercritical water chicken manure gasification
within feedstock particles and moisture (Zeng et al. 2020). reached up to 22.47 mol/kg, 174.53 and 81.34%, respec-
The purpose of this stage is to further degrade the feedstock tively, at a temperature of 620 °C and reaction time of only
particles into volatile matter and solid carbonaceous resi- 12 min(Cao et al. 2022). The co-gasification of the chicken
due, also known as biochar, at high temperatures without manure waste with petroleum coke highly increased the
oxygen (Eraky et al. 2022). The following stage is the com- hydrogen gas content in the obtained syngas. The calcium
bustion, which includes the complete or partial oxidation of

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Environmental Chemistry Letters (2023) 21:2707–2727 2723

and potassium of the manure ash are highly contributed as a Economy in Northern Ireland and the Department of Business, Enter-
catalyst in the gasification process(Liu et al. 2021). prise and Innovation in the Republic of Ireland.
To summarize, gasification is a thermochemical conver- Disclaimer The views and opinions expressed in this review do not
sion process involving four stages: drying, devolatilization, necessarily reflect those of the European Commission or the Special
combustion, and reduction. The drying stage removes free EU Programmes Body (SEUPB).
and bound water from the feedstock to prevent feeding or
fluidization issues, whereas the devolatilization stage further Open Access This article is licensed under a Creative Commons Attri-
degrades the feedstock particles into the volatile matter and bution 4.0 International License, which permits use, sharing, adapta-
tion, distribution and reproduction in any medium or format, as long
carbonaceous residue. Combustion involves the complete as you give appropriate credit to the original author(s) and the source,
or partial oxidation of carbonaceous output, resulting in the provide a link to the Creative Commons licence, and indicate if changes
production of water, carbon dioxide, carbon monoxide, and were made. The images or other third party material in this article are
hydrogen, which are used to heat the gasifier in subsequent included in the article's Creative Commons licence, unless indicated
otherwise in a credit line to the material. If material is not included in
stages. The decision wise of choosing the best gasifying the article's Creative Commons licence and your intended use is not
agent is highly dependent on the resource availability and the permitted by statutory regulation or exceeds the permitted use, you will
desired output. The chicken manure was efficiently utilized need to obtain permission directly from the copyright holder. To view a
as a catalyst for the gasification of petroleum coke. copy of this licence, visit http://​creat​iveco​mmons.​org/​licen​ses/​by/4.​0/.

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