Industrial Crops & Products 195 (2023) 116420

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Industrial Crops & Products

journal homepage: www.elsevier.com/locate/indcrop

Anaerobic digestion of lignocellulosic waste for enhanced methane

production and biogas-digestate utilization
Omayma A. Awadalla a, Walaa A. Atawy b, Mohamed Y. Bedaiwy a, Sameh S. Ali a, c, *,
Yehia A.-G. Mahmoud a
a
Botany Department, Faculty of Science, Tanta University, Tanta 31527, Egypt
b
Agriculture Research Center, Soil, Water and Environment Institute, Cairo, Egypt
c
Biofuels Institute, School of the Environment and Safety Engineering, Jiangsu University, Zhenjiang 212013, China

A R T I C L E I N F O A B S T R A C T

Keywords: Lignocellulosic biomass is an important source for nutrient management in agricultural systems and has a largely
Anaerobic digestion unexploited potential for biogas production. The digestates from the anaerobic digestion (AD) process are widely
Industrial crops used in agriculture systems due to their nutrient composition and organic matter, making them a valuable source
Fusarium oxysporum
for plants. As a result, methane (CH4) production from AD of lignocellulosic biomass waste, such as rice straw,
Methane
corn stalk, and grape stalk, was determined in this study, and their anaerobic digester residues were studied at
Tomato fruits
Biomass waste various concentrations to investigate their potential on tomato plant growth and fruit yield. The biogas and CH4
yields of the pretreated rice straw, corn stalk, and grape stalk were determined through the AD process for 72
days, and the results revealed a gradual increase in the cumulative biogas and CH4 production until the end of the
AD process (72 days). The cumulative biogas from rice straw, corn stalk, and grape stalk was 359.3, 309.9, and
215.1 L/kg VS, respectively. However, the biogas production of rice straw was higher than that of corn stalk, and
grape stalk by 15.6% and 67%, respectively. The cumulative CH4 yield of rice straw was higher than that of corn
stalk, and grape stalk by 21.1% and 76.3%, respectively. The results also showed that tomato growth signifi­
cantly increased under grape stem residue (GSR) more than under rice straw residue (RSR) and corn stalk residue
(CSR), as well as under untreated control and control infected with Fusarium oxysporum f. sp. lycopersici (FOL).
The increase in bioreactor residue concentration resulted in a significant increase in tomato growth parameters,
crop yield, and tomato quality. The results confirmed that 20% of GSR increased the tomato’s physical and
chemical properties compared with control, RSR, and CSR. The soil content of total nitrogen, phosphorus, and
potassium gradually increased with the increase in residue concentrations before and after AD, and the maximum
concentration was obtained at 25% of GSR. Therefore, anaerobic digestate could be economically viable, which
can be a good solution for sustainable lignocellulosic biomass waste management and plant growth.

1. Introduction agricultural country where the agricultural sector contributes nearly

Bioenergy from lignocellulosic biomass is a viable alternative to
fossil fuels (Ali et al., 2023, 2021h; Danso et al., 2022; González-Gloria
et al., 2022; Koutra et al., 2021). Lignin is the most abundant organic
matter on earth, with various quantities, properties, and shapes, and
therefore it is a promising raw material for bioenergy production
(Madadi et al., 2022; Murillo Morales et al., 2020; Nawaz et al., 2023;
Wang et al., 2020c). Most developed nations consider agricultural waste
an essential resource for biogas production (Ali et al., 2017, 2019c,
2020, 2021f; Ali and Sun, 2015, 2019). On the other hand, Egypt is an
40% of the total national income (Swain, 2011). The Egyptian agricul­
tural area is 3.3 million hectares; despite the narrowness of this area,
agricultural residues are considered one of the main problems in rural
Egyptian regions (Nour et al., 2021). Data on environmental protection
in Egypt confirms that 33.4 million tons of agricultural waste are
generated annually. The distribution of these residues varies among the
different crops, where the amount of rice crop residue and corn residue
is 3.6 and 4.5 million tons, respectively (Abou Hussein and Sawan,
2010). About 52% of agricultural residues are burned inefficiently,
which causes air pollution and the loss of organic matter. However, 18%

* Corresponding author at: Botany Department, Faculty of Science, Tanta University, Tanta 31527, Egypt.
E-mail addresses: samh@ujs.edu.cn, samh_samir@science.tanta.edu.eg (S.S. Ali).

https://doi.org/10.1016/j.indcrop.2023.116420
Received 19 November 2022; Received in revised form 27 January 2023; Accepted 9 February 2023
Available online 20 February 2023
0926-6690/© 2023 Elsevier B.V. All rights reserved.
O.A. Awadalla et al.
of agricultural waste was used as fertiliser and 30% as animal feed (Jat
et al., 2022; Srinivas et al., 2019).
The only type of vegetable crop that is grown commercially every­
where in the world is tomatoes, which are members of the family Sol­
anaceae and contain more than three thousand species (Srinivas et al.,
2019; Sun et al., 2023). This crop, which is consumed both in its natural,
unprocessed form and in a wide variety of manufactured goods, is an
essential component of the food that people eat regularly (Pędzik et al.,
2021). One of the most common diseases that affect tomatoes is called
tomato wilt, and it is caused by a fungus called Fusarium oxysporum f. sp.
lycopersici (FOL) (Borisade et al., 2017). When the FOL gets into the
epidermis of the root, it eventually spreads through the vascular tissue
and inhabits the xylem vessels of the plant. This causes the vessels to get
clogged, which leads to significant water stress, which in turn causes
wilt-like symptoms to occur (Singh et al., 2017).
The conversion of various waste streams into biogas can be accom­
plished by a process known as anaerobic digestion (AD) in the presence
of microorganisms (Ali et al., 2019a, 2021a, 2021g). The production of
biogas, which consists mostly of methane (CH4; 50–70%) and carbon
dioxide (CO2; 30–50%), has several advantages, both financially and
environmentally (Ali et al., 2021c; Ali et al., 2021d). Although CH4 is the
end product of AD, the digestate that is also produced can be valorized
into fertilizer. It has been demonstrated that industrial digesters can
achieve greater economic viability when the digestate is recycled for use
as a soil amendment (Fernández-Rodríguez et al., 2021).
Biogas slurry and digestate are secondary products generated by AD
process of biowastes, which have been extensively applied as a fertilizer
in agricultural activities. Biogas slurry and digestate are eco-friendly
organic fertilizers and efficiently utilized waste by-products (You
et al., 2019). The digestate is a semi-stabilized by-product that has a high
moisture content and is produced during the AD process (Li et al., 2020).
Nitrogen and phosphorus are both mineralized during the digestion
process, but they are not removed from the system. As a result, the
digestate has a high concentration of nitrogen and phosphorus, which
contributes to its enormous potential for use as a soil amendment or
fertilizer (Akhiar et al., 2017; Ali et al., 2021b, 2021e). Notably, the
carbon, nitrogen, and phosphorus contents of the digestate are found to
be between 15% and 55%, 0–8%, and 1–4%, respectively (Chozha­
vendhan et al., 2023). Animal dung and food waste contain between 1%
and 3% ammonia as a source of nitrogen (Luo et al., 2020; Pecchi et al.,
2020). The phosphorus content in fruit and vegetable wastes is
approximately 2.5%, while swine dung digestate contains 4.5% (Parmar
and Ross, 2019). The application of 30 m3 of dried biogas digester res­
idue significantly increased the vegetative growth, yield, and fruit
quality of the tomato crop (Youssef and Saleh, 2016). The application of
biogas plant residues at 50 t/ha produced the highest shoot and root dry
weights and plant heights at 30 and 45 days after transplantation (Kibria
et al., 2016). The maximum number of fruits/plant, the weight of
fruits/plant, and yield (t/ha) were also found with the same treatment.
Several studies investigated biogas and CH4 production from agri­
cultural wastes (Ali et al., 2019b, 2021d). However, to the best of our
knowledge, this study might be the first to explore the potential of cattle
dung co-digested with different chemically pretreated agricultural
wastes to improve biogas and CH4 production yield simultaneously with
biogas residues properties as a fertilizer to enhance soil and fruit phys­
icochemical properties. The utilization of anaerobic co-digestion of
organic wastes could potentially pave a new avenue toward developing
a competitive system for agricultural waste management while also
increasing biofuel production and soil fertility.
2. Materials and methods
2.1. Feedstock collection and preparation
Rice straw (RS), corn stalks (CS), and fresh cattle dung (CD) were
collected from Etay El-Baroud, El-Behera Agriculture Research Farm.
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Industrial Crops & Products 195 (2023) 116420
Grape stems (GS) were collected from El-Gemeza Agriculture Research
Farm, El-Gharbia Governorate. All plant materials were air-dried,
chopped, and sieved using a mesh sieve (2 mm) to attain a uniform
particle size before pretreatment to attain a large surface for liquid
adhesion and direct contact with microorganisms. Digested cattle dung
was derived from an active household biogas digester located at the
Training Center for Recycling of Agricultural Residues (TCRAR),
Moshtohor, Qualubia Governorate, and used as a seeding inoculum
(starter).
2.2. Pretreatment and experimental design
Lignocellulosic wastes (RS, CS, and GS) were soaked in a combina­
tion of 2.5% NaOH and 2.5% NH4OH at 25ºC for 2 days in a closed
plastic container to improve delignification levels (Ali and Sun, 2019).
After chemical pretreatment, pH was adjusted to 7.0 using dilute 1 N HCl
to maintain a suitable medium for the AD process. For CD preparation,
water was added to obtain 10% TS content and then kept in anaerobic
conditions for 5 days before digester feeding in each constructed
digester to enrich the anaerobic microbial populations. Concerning feed
rate, the ratio of investigated substrate to CD was 4:1 on a dry weight
basis. For CD preparation, water was added to obtain 10% TS content
and then kept in anaerobic conditions for 5 days before digester feeding
to enrich the anaerobic microbial populations. The prepared mixtures
(RS: CD, CS: CD, and GS: CD) were subjected to a batch digester for 72
days of hydrolytic retention time (HRT). The prepared mixture was
separately loaded into a biogas reactor with an 8 L working volume and
a 2 L headspace containing N2/CO2 (80/20; v/v) and kept at mixed
mesophilic conditions on an incubator shaker (35 ◦ C, 120 rpm). The
three constructed bioreactors were encoded as RS-D, CS-D, and GS-D, as
shown in Fig. 1.
2.3. Biogas and its component measurements
The volume of gas generated was measured according to the water
displacement method as described previously (Ali and Sun, 2015; Ali
et al., 2015). CH4 content was determined daily by gas chromatography
(Gow-MAC gas chromatograph Model 750p). The column was made of
stainless steel and packed with Porapak-Q 60–80 mesh. The operation
temperatures were 50, 100, and 120ºC for a column, detector, and
injector, respectively. However, CO2 was evaluated by the method for
Orsats apparatus, utilizing a 33% potassium hydroxide solution for CO2
absorption (Wypych, 2018).
2.4. Biogas and CH4 yield kinetics
The biogas kinetics were investigated using two different kinetic
models. The modified Gompertz model (MGPM) was used to study the
production of biogas (Eq. 1). The MGPM presents a classic sigmoidal
curve and is expected to be a function of microbial growth (Deepanraj
et al., 2015). The logistic growth model (LOGM) (Eq. 2) was applied to
determine the biogas production potential, lag-phase, and maximum
biogas production rate, which are also essential for the evaluation of the
AD process (Thakur et al., 2022).
[
2.718282
]}
p(t) = pm ∗ exp{ − exp R ∗ (L − t) + 1 (1)
pm
/ [ ]}
4R
p(t) = pm {1 + exp (L − t) + 2 (2)
pm
where, p(t) is the cumulative production at digestion time (L/kg VS), pm
is the production potential (L/kg VS), R is the maximum production rate
(L/kg VS/day), L is the lag-phase period (days), and t is the cumulative
time for production (days).
O.A. Awadalla et al.
Fig. 1. Experimental set up for exploring the potential of anaerobic digestion of lignocellulosic wastes for enhanced methane production and the application of their
digestate to improve plant growth and tomato fruit yield.
2.5. Analytical methods
Analyses of samples were carried out according to standard methods
(APHA, 2012). For the determination of total solids (TS) content, sam­
ples were put into pre-weighed porcelain crucibles. Then, the samples
were dried in an oven at 105ºC until a constant weight was obtained for
the TS content (Ali and Sun, 2015). Total Kjeldahl nitrogen (TKN) was
measured by an automatic Kjeldahl nitrogen analyzer (VELP, UDK159,
Italy). The pH of the sample was measured by a pH instrument (INESA,
China). NH+ 4 -N was measured by Nessler’s reagent colorimetric method
(Wei et al., 2021). VFAs were determined by gas chromatography
(TECHCOMP, GC7900, China), according to Wang et al. (2020a). Total
VFAs and acetic acid were calculated using the following equations.
Reading of titration × Normality of NaOH × 1000
Total VFAs =
Volume of sample
Reading of titration × Normality of NaOH × 60 × 1000
Acetic acid =
Volume of sample × 0.7
2.6. FOL inoculum preparation
The cultures of FOL were maintained on potato dextrose agar (PDA)
at 25 oC with a 12 h photoperiod to induce sporulation and were sub­
cultured on fresh PDA every 30 days. Isolates were subcultured on a PDA
slant at 25–27 oC for 7 days. Sterilized water agar (10 mL; 0.1%) was
added to each slant and spores were released by shaking for a few mi­
nutes. The spore suspensions were filtered using sterilized Whatman
No.1 filter paper to remove the mycelium fragments. The filtrate was
received in a sterile Erlenmeyer flask, and the number of spores was
adjusted to 106/mL in sterilized water by a haemocytometer slide.
2.7. Tomato production using anaerobic fermentation residues
Tomato seedlings were purchased from the greenhouse in Kom-
Hamada (El-Behiara, Egypt). As depicted in Fig. 1, three tomato seed­
lings were transplanted into a 30 cm plastic pot containing three kilo­
grams of natural soil and used as a control. The infected tomato
seedlings were prepared similarly to the control experiment, with the
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Industrial Crops & Products 195 (2023) 116420
addition of 20 mL of FOL spore suspension per seedling. Three biogas
residues with concentrations of 10% (RS), 20% (CS), and 25% (GS) were
mixed with soil and seedlings individually (Fig. 1). The pots were irri­
gated and maintained at 25–30 oC and 70% relative humidity. The
inoculated tomato plants were monitored for wilt signs for 60 days after
inoculation.
2.8. Physico-chemical composition of soil and tomatoes
Standard procedures were used to determine the soil’s chemical
composition (macronutrients), including TKN, total potassium (TK), and
total phosphate (TP) (APHA, 2012). The chlorophyll content was
determined following the method described by Li et al. (2018). Using a
digital force Shimpo pressure tester, fruit hardness (Newton) was
measured on both sides of the fruit (Gouge Model, Nidec, Japan). The
tomato’s total soluble solids (TSS) content was evaluated using Abbe’s
refractometer. A drop of tomato juice extracted from the fruit pulp was
placed on the refractometer’s prism, and TSS was measured as a per­
centage of Brix. The titratable acidity of tomato pulp was measured
using the technique described by Tyl and Sadler (2017). Ascorbic acid
was tested by titrating against a standard alkaline solution (0.1 N NaOH)
with a phenolphthalein indicator.
2.9. Statistical analysis
The data were visualized and interpreted using GraphPad version
(V.8.0.2) and NCSS 2021 statistical analysis software. A one-way
ANOVA with unpaired and paired t-tests was used to compare mean
values between groups. All data were carried out in triplicate are pre­
sented as a mean ± standard deviation. P value ≤ 0.05 was considered
significant. The kinetic studies were performed by PASW software
(V.18.0.0) using the modified Gompertz model and the logistic growth
model.
O.A. Awadalla et al.
3. Results and discussion
3.1. Biogas and CH4 production
Three bioreactors were constructed to study the productivity of
biogas and CH4 from RS, CS, and GS. The obtained data showed that the
maximum daily biogas production from RS-D, CS-D, and GS-D bio­
reactors was 19.3, 18.3, and 16.3 L/kg VS on the 38th, 36th, and 42nd
days, respectively (Fig. 2A). Moreover, the daily maximum biogas yield
of RS-D was significantly (P < 0.05) higher than that of CS-D
(P = 0.0024) and GS-D (P < 0.0001) by 5.6% and 18.7%, respectively
(Fig. 2B). Furthermore, the daily maximum production of CS-D was
significantly (P < 0.05) higher than GS-D (P = 0.0056) by 12.5%.
However, the cumulative biogas production from RS-D, CS-D, and GS-D
bioreactors was 359.3, 309.9, and 215.1 L/kg VS, respectively, as shown
in Fig. 2C. Insignificant increase in biogas produced from RS-D over that
from CS-D (P = 0.5630) and a significantly increased biogas level over
GS-D (P = 0.0020) by 15.6% and 67%, respectively. Furthermore, the
biogas yield by CS-D was significantly higher than that of GS-D by 44.1%
(P = 0.0074) (Fig. 2D).
In terms of CH4 production, the maximum daily CH4 production of
RS-D, CS-D, and GS-D bioreactors was 13.9, 14.5, and 12.2 L/kg VS on
the 38th, 36th, and 40th days, respectively (Fig. 3A). The daily
maximum CH4 production by CS-D was significantly higher than that of
RS-D and GS-D by 4.3% (P=0.0013) and 18.9% (P=0.0070), respec­
tively. The daily maximum CH4 production by RS-D was significantly
higher than that of GS-D by 13.9% (P<0.0001) (Fig. 3B). The cumulative
CH4 yield of RS-D, CS-D, and GS-D was 261.7, 216.1, and 148.4 L/kg VS,
respectively (Fig. 3C). The cumulative CH4 yield of RS-D was insignifi­
cantly higher than CS-D and significantly higher than GS-D by 21.1%
(P=0.3942) and 76.3% (P=0.0012), respectively. However, cumulative
CH4 production by RS-D was significantly higher than that of GS-D by
45.6% (P=0.0102) (Fig. 3D). The obtained data also confirmed that
biogas and CH4 production gradually increased with the extent of HRT
4
Industrial Crops & Products 195 (2023) 116420
until achieving maximum production, then gradually decreased for all
investigated feedstocks. In this context, Gaby et al. (2017) reported that
HRT can influence the AD process and microbial activity. The operation
of the methanogenic stage at HRT for less than 8–10 days can cause
instability in CH4 production (Gaby et al., 2017). Dareioti and Kornaros
(2014) found that the methanogenic reactor showed better stability after
25 days of HRT. After 20 days, the accumulation of volatile fatty acids
(VFAs) was determined, which could be the reason for the reduction of
biogas and CH4 production based on the acidification of the medium (Ali
et al., 2022).
As depicted in Fig. 4, the maximum daily CH4 content of RS-D, CS-D,
and GS-D bioreactors was 78.8%, 78.7%, and 79.8% on the 28th, 36th,
and 26th days, respectively. However, the average CH4 content of RS-D,
CS-D, and GS-D was 66.7%, 63.8%, and 65.0%, respectively. The CH4
content produced by RS-D was significantly higher than that of CS-D
(3.4%; P < 0.0001); but it was insignificantly higher than that of GS-D
by 2.6% (P = 0.2325). In addition, the CH4 content of GS-D was insig­
nificantly higher than that of CS-D by 1.9% (P = 0.4423). The findings
of this study are higher than those reported by Croce et al. (2016), who
found that the yield of CH4 obtained from RS ranged from 135 to
180 L/kg VS, indicating that RS is a fertile material for biogas produc­
tion. Furthermore, Nguyen et al. (2016) found that the biogas produc­
tion of RS was 400 L/kg VS and 200 L/kg VS for CH4. Similar results
were reported by Sumardiono et al. (2022), who found that the total
biogas yield from CS was 215.77 L/kg VS after alkaline treatment and
the maximum daily biogas production was 19.86 L/kg VS on the 28th
day. Also, He et al. (2019) reported that the pretreatment of CS using
ammonium bicarbonate (8%, w/w) produced 222.6 L/kg VS of biogas.
Although the valuable utilization of GS based on the biorefinery phi­
losophy presents many challenges because of its high content of tannins
and lignin (Ping et al., 2011), few studies have investigated the pro­
duction of biogas from GS. The biogas and CH4 production from GS were
225 and 98 L/kg VS, respectively (Dinuccio et al., 2010).
Fig. 2. Daily and cumulative biogas production occurs
during the anaerobic digestion of biomass wastes,
including rice straw (RS-D), corn stalk (CS-D), and grape
stem (GS-D). Daily biogas yield (A), paired t-test of daily
biogas yield (B), cumulative biogas yield (C), and unpaired
t-test of cumulative biogas (D). Variations between groups
were analyzed using unpaired and paired t-tests according
to the type of obtained data at * P ≤ 0.05, * * P ≤ 0.01,
* ** P ≤ 0.001, and * ** * P ≤ 0.0001, while P > 0.05 is
non-significant (ns).
O.A. Awadalla et al.
Fig. 4. Percentage of methane content during the anaerobic digestion of
biomass wastes, including rice straw (RS-D), corn stalk (CS-D), and grape stem
(GS-D). Variations between groups were analyzed using unpaired and paired t-
tests according to the type of obtained data at * P ≤ 0.05, ** P ≤ 0.01,
*** P ≤ 0.001, and **** P ≤ 0.0001, while P > 0.05 is non-significant (ns).
3.2. Biogas digester performance
The AD process is a promising technique to produce biogas and
organic fertilizer. However, VFA and pH are significant process
5
Industrial Crops & Products 195 (2023) 116420
Fig. 3. Daily and cumulative methane production occurs
during the anaerobic digestion of biomass wastes,
including rice straw (RS-D), corn stalk (CS-D), and grape
stem (GS-D). Daily methane yield (A), paired t-test of daily
methane yield (B), cumulative methane yield (C), and un­
paired t-test of cumulative methane (D). Variations be­
tween groups were analyzed using unpaired and paired t-
tests according to the type of obtained data at * P ≤ 0.05,
** P ≤ 0.01, *** P ≤ 0.001, and **** P ≤ 0.0001, while
P > 0.05 is non-significant (ns).
limitations due to their effects on the stability and performance of bio­
digesters. As depicted in Fig. 5A, variations in the VFAs and pH were
observed during the 72 days of HRT. The changes in pH and VFA might
be due to the activity of the microbial population through the AD process
(Ali et al., 2019c). Insignificant changes in pH values between the RS-D,
CS-D, and GC-D (Fig. 5B). The minimum values in RS-D, CS-D, and GS-D
on the 4th–6th week of the AD process reached 5.2 ± 0.2, 5.1 ± 0.1, and
5.2 ± 0.1, respectively. The pH is one of the most influential factors in
the efficiency and content of VFA production (Chen et al., 2020). Low
pH (pH 4.0) and a short retention time are more conducive for propio­
nate production (Jankowska et al., 2015). The ideal pH range for VFA
production was reported to be between 5.3 and 11.1; this variation in pH
range depends on the type of waste used (Lee et al., 2014). As previously
documented, acidic pH values have a positive effect on the synthesis of
VFAs as well as microbial growth (Wang et al., 2020b). The acetic acid
maximum values of RS-D, CS-D, and GS-D were 2.3, 2.2, and 0.36 g/L,
respectively. The acetic acid production by RS-D was insignificantly
higher than that of CS-D (P > 0.9999); however, it was significantly
higher than that of GC-D (P= 0.0012) (Fig. 5C). Moreover, acetic acid
production by CS-D was significantly higher than that of GS-D
(P=0.0067). Acetic acid is an essential organic acid that can be used
for CH4 fermentation (Yang et al., 2008). It also plays an important in­
termediate role in the AD process and enhances lignocellulose degra­
dation (Hui et al., 2013). In this study, VFA and acetic acid
concentrations reached their maximum values in the 4th–6th weeks of
the AD process. The maximal RS-D, CS-D, and GS-D concentrations of
the VFAs were 6.8, 5.8, and 3.2 g/L, respectively. VFA production by
RS-D was insignificantly higher than that of CS-D (P=0.7117); but
significantly higher than that of GC-D (P=0.0073). Also, VFAs produc­
tion by CS-D was significantly higher than that of GS-D (P= 0.0004)
(Fig. 5D).
The MGPM, and LOGM were used to fit the biogas production data
obtained from the AD of RS-D, CS-D, and GS-D (Table 1). The maximum
biogas production rate predicted from MGPM was higher in RS-D
(362.5 L/kg VS) than that of CS-D (314.98 L/kg VS), and GS-D
O.A. Awadalla et al. Industrial Crops & Products 195 (2023) 116420

Fig. 5. Performance of digesters during the anaerobic digestion of rice straw (RS-D), corn stalk (CS-D), and grape stem (GS-D). Changes in pH, VFAs, and acetic acid
(A). Statistical analysis using unpaired t-test for studying changes in pH (B), acetic acid (C), and VFAs (D). Variations between groups were analyzed using unpaired
and paired t-tests according to the type of obtained data at * P ≤ 0.05, * * P ≤ 0.01, * ** P ≤ 0.001, and * ** * P ≤ 0.0001, while P > 0.05 is non-significant (ns).

Table 1
Kinetic parameters of the modified Gompertz model and logistic growth model applied to biogas production from lignocellulosic biomass wastes.
Parameters Modified Gompertz model Logistic model

CH4 production Biogas production CH4 production Biogas production

RS-D CS-D GS-D RS-D CS-D GS-D RS-D CS-D GS-D RS-D CS-D GS-D

Experimental cumulative production 261.7 216.1 148.4 359.3 309.9 215.1 261.7 216.1 148.4 359.3 309.9 215.1
(L/Kg VS)
Expected yield 282.6 228.7 177.6 362.5 314.98 222.3 258.7 214.1 161.3 360.4 310.2 242.5
(L/Kg VS)
Difference between experimental and expected -7.98 -5.8 -19.7 -0.89 -1.6 -3.33 1.41 0.93 -8.7 -0.3 -0.09 -12.7
production (%)
Experimental maximum production (L/Kg VS) 13.9 14.5 12.2 19.3 18.3 16.3 13.9 14.5 12.2 19.3 18.3 16.3
Expected maximum production (L/Kg VS) 14.6 15.6 13.2 20.5 19.1 17.1 13.5 14.3 13.6 21.3 19.6 18.6
Difference between maximum experimental and -5.03 -7.6 -8.2 -6.2 -4.4 -4.9 2.9 1.4 -11.5 -10.4 -7.1 -14.1
expected production (%)
Expected lag phase (d) 16 14 26 18 16 30 13 11 22 14 12 25
R square 0.96 0.97 0.96 0.99 0.99 0.98 0.98 0.98 0.97 0.99 0.99 0.96

RS-D = Rice straw, CS-D = Corn stalk, GS-D, Grape stem.

(222.3 L/kg VS). While the LOGM showed an expected biogas produc­
tion rate of 360.4, 310.2, and 242.5 L/kg VS for RS-D, CS-D, and GS-D,
respectively, moreover, the predicted maximum CH4 production rate
from MGPM was also higher in RS-D (282.6 L/kg VS) than that of CS-D
(228.7 L/kg VS) and GS-D (177.6 L/kg VS). The expected CH4 produc­
tion rate for RS-D, CS-D and GS-D was 258.7, 214.1, and 161.3 L/kg VS,
respectively.
For the lag-phase time of biogas production, a range dependent on
kinetic models (LOGM and MGPM) analysis was in the range between 14
and 18 days for RS-D and 12–16 days for CS-D, while for GS-D, the lag
phase ranged from 30 to 25 days. However, the lag-phase time of CH4
production for RS-D was in the range of 13 and 16 days and 11–14 days
for CS-D, while for GS-D, the lag phase ranged from 22 to 26 days. The
LOGM also showed that the rate of biogas and CH4 generation is exactly
related to the amount of biogas produced (Çetinkaya and Yetilmezsoy,
2019; Thakur et al., 2022), indicating the significant biogas potential of
RS-D. Therefore, MGPM is a good tool for studying the kinetics of biogas
production from the investigated biomass wastes.

6
O.A. Awadalla et al. Industrial Crops & Products 195 (2023) 116420

3.3. Influence of digester residues on tomato production yield and quality stem length, and blossom count. Kibria et al. (2016), who evaluated the
effects of biogas plant residues (BPR) and NPK fertilizer on the growth,
Tomato growth was considerably enhanced under grape stem res­ yield, and quality of tomatoes, obtained similar results. Compared with
idue (GSR) more than under rice straw residue (RSR) and corn stalk the control treatment, the application of BPR and NPK fertilizers
residue (CSR), as well as the control infected with FOL (CIF) (Fig. S1). considerably altered the growth and yield of tomatoes. At 30 and 45
Generally, tomato plants grown under GSR (25%) had the longest stems days after transplanting, the maximum shoot and root dry weight and
(76.3 ± 3.0 cm). At GSR (20%), the highest number of leaves/plant plant height were produced by BPR at 50 t/ha. The same treatment
(19.0 ± 2.0) and the number of flowers/plant (25.0 ± 1.0) were recor­ produced the greatest quantity of fruits per plant, fruit weight per plant,
ded. At 25% of CSR, the maximum leaf number, stem length, and flower and yield (t/ha). In another study, treatments with biogas residues, even
number were 14.0 ± 2.0, 54.3 ± 2.0 cm, and 20.0 ± 1.0, respectively when supplemented with mineral fertilizers, resulted in a significant
(Table 2). The leaf number of the control trait was significantly higher decrease in tomato fresh fruit yield compared to the control (Mupambwa
than the CIF (P=0.0179). GSR (20%) was significantly higher than et al., 2019). However, with the addition of biogas digestates, the sugar
control (P=0.0036), the CIF (P= 0.0015), 25% of RSR (P=0.0079), and content of the tomato fruits increased dramatically, although the heavy
25% of CSR (P=0.0376). The stem length of the control trait was metal concentration was below the limit indicated for irrigation water.
significantly higher than the CIF (P< 0.0001). The GSR (25%) was All tomato metrics rise significantly with increasing residual con­
significantly higher than the control (P=0.0046), the CIF (P<0.0001), centrations. However, tomato plants grown at 20% GSR had the greatest
20% of the RSR (P=0.0003), and 25% of the CSR (P=0.0005). However, leaf area (36.1 cm2), leaf total chlorophyll content (1.6 mg/g), number
the flower number of the control trait was significantly higher than CIF of fruits per plant (25), average fruit weight (77.8 g), and fruit yield per
(P= 0.0022). GSR (20%) was significantly higher than control plant (1.6 kg) (Fig. S2). Nonetheless, the highest plant height of
(P=0.0010), CIF (P=0.0002), 25% of RSR (P=0.0004), and 25% of CSR 105.3 cm was reported at 25% GSR (Table 3). At 20% GSR, tomato plant
(P=0.0036) (Fig. S1). The AD process converts organic wastes from height was not substantially lower than plant height at 25% GSR
cassava peeling residue (CPR) to biogas, and the resulting residues can (P = 0.4759); but significantly greater than control (P < 0.0001), 25%
be utilized as digestate biofertilizers (Aso et al., 2022). Utilization of RSR (P < 0.0001), and 25% CSR (P < 0.0001) (Fig. S2). In contrast, the
CPR digestate will therefore save 25% of the monetary cost of inorganic leaf area at 20% GSR was significantly higher than control (P < 0.0001),
fertilizers required for cassava root production and lower the external 25% RSR (P = 0.0011), and 25% CSR (P = 0.0005). In terms of total
expenses associated with the manufacturing and application of inor­ chlorophyll leaf content, the tomato plant leaf at 20% GSR was signifi­
ganic fertilizers. The application of biogas plant residues resulted in a cantly higher than the control (P = 0.0004), 25% RSR (P = 0.0072), and
similar number of leaves and plant height in comparison to the control 25% CSR (P = 0.0132). The number of fruits per plant at 20% GSR was
and recommended NPK fertilizer, but a significantly greater number of significantly higher than the control (P = 0.0015), 25% RSR
leaves, root length, and fresh weight of shoot and root than the control (P = 0.0056), and 25% CSR (P = 0.0213) (Fig. S2). The fruit yield per
and recommended NPK fertilizer (Hossain et al., 2014). plant at 20% GSR was significantly greater than the control
The increase in bioreactor residue concentration promoted tomato (P = 0.0116), 25% RSR (P = 0.0102), and 25% CSR (P = 0.0238). In
growth, as depicted in Fig. 6. The augmentation of tomato plant terms of fruit weight, 20% GSR was significantly (P < 0.0001) higher
development was caused by the aforementioned outcomes of leaf count, than the control, 25% RSR, and 25% CSR (Fig. S2). The digestate of the
AD process contains a number of essential components for plant growth
and increases chlorophyll content and plant dry weight. In addition,
Table 2 digestate from newly-emerging biogas facilities can be utilized as eco-
Influence of anaerobic digester residues on the tomato plant growth after friendly agricultural implements (Weimers et al., 2022). Therefore,
inoculation with Fusarium oxysporum f. sp. lycopersici. this method can be used to replace costly mineral fertilizers or replenish
Biomass Leaf no. Stem Flowers Infected Disease deficient nutrients.
residue length no. leaves index In comparison to RSR, CSR, and the control, the rise in GSR con­
(Conc.) (cm) centration improves the physical and chemical characteristics of tomato
Control 14.0 65.3 18 ± 1.0a 2.0 ± 0.0a 3 fruits (Table 4). The maximum fruit firmness (14.6 newtons), TSS (4.9
± 1.0a ± 1.2a ºBirex), titratable acidity (0.67%), fruit content of ascorbic acid (29.9 g/
b
Control 9.0 40.7 9.0 3.0 ± 0.0 3
kg of fresh weight), and extended fruit shelf life (24.5 days at room
+ FOL ± 1.0b ± 1.0b ± 2.0b
RSR (10%) 10.0 45.7 4.0 3.0 4
conditions) were observed at 20% of GSR (Fig. S3). In all treatments, the
± 1.0c ± 1.3c ± 1.0c ± 1.0abc increase in bioreactor residue concentrations resulted in a gradual in­
RSR (20%) 11.0 52.0 11.0 3.0 2 crease in all the fruit’s physical and chemical properties compared to the
± 2.0cd ± 2.0d ± 1.0b ± 1.0abc control. The physical and chemical properties of tomato fruits were
RSR (25%) 13.0 50.7 16.0 3.0 2
significantly (P < 0.05) higher at all GSR concentrations than RSR and
± 1.0ad ± 1.4cd ± 2.0a ± 1.0abc
CSR (10%) 9.0 43.0 14.0 4.0 2 CSR (Fig. S3). The application of biogas residues to the soil increases
± 1.0b ± 2.0bc ± 0.0d ± 1.0bc microbial activity and increases microbial biomass (Chen et al., 2012).
CSR (20%) 13.0 51.7 16.0 4.0 ± 0.0c 4 Biogas residue digestate application may affect soil phosphorus avail­
± 1.0ad ± 1.7d ± 3.0ad
ability and plant phosphorus nutrition directly by providing inorganic
CSR (25%) 14.0 54.3 20.0 4.0 4
± 2.0a ± 2.0de ± 2.0aeg ± 1.0bc
and organic phosphorus compounds, or indirectly by altering soil mi­
GSR (10%) 12.0 66.7 22.0 4.0 3 crobial activity as a result of organic matter supply (Insam et al., 2015).
± 1.0d ± 2.3a ± 1.0eg ± 1.0bc Positive effects of digestate on soil biological characteristics, such as
GSR (20%) 19.0 58.0 25.0 4.0 ± 0.0c 3 microbial biomass carbon and numerous enzyme activities may
± 2.0e ± 3.0e ± 1.0fg
contribute to the enhancement effect of biogas residues addition on
GSR (25%) 15.0 76.0 21.0 4.0 ± 0.0c 3
± 1.0a ± 3.0f ± 1.0g plant growth and fruit quality (Pranagal et al., 2019). In addition, biogas
P-value 0.991 0.993 0.964 0.999 residues have a high concentration of organic carbon and total nitrogen
and can enhance soil fertility (Ali et al., 2019c). Biogas digestate
RSR = Rice straw residue, CSR = Corn stalk residue, GSR = Grape stem residue,
FOL = Fusarium oxysporum f. sp. lycopersici. application significantly improved soil pH, organic carbon content, total
Values are the mean of three replicates ± SD. nitrogen, and available forms of phosphate and potassium (Stefaniuk
Different letters in the same column indicate statistically significant differences et al., 2015). The incorporation of biogas residues into the soil may
(P < 0.05). enhance carbon sequestration (Smith et al., 2014). This is the result of

7
O.A. Awadalla et al.
Fig. 6. Influence of anaerobic digester residues of rice straw (RSR), corn stalk (CSR), and grape stem (GSR) on the growth of the tomato plant. RSR (A), CSR (B), and
GSR (C).
the stability of organic materials due to the AD of organic wastes. The
application of digestate derived from agricultural waste decreased soil
bulk density while enhancing saturated hydraulic conductivity and
water retention capacity (Garg et al., 2005). Compared to NPK fertil­
ization, biogas digestate enhanced the amount of protein, wet gluten,
and phenols in wheat grain. Spring wheat biomass yields decreased after
the application of undigested pig manure but increased after the injec­
tion of digestate (Abubaker et al., 2012). The biomass digestate had a
minimal effect on the protein content and digestibility of the forage. The
application of synthetic fertilizer in conjunction with slurry resulted in
an increase in tomato yield and farmer income (Ferdous et al., 2018).
In terms of the chemical composition of the investigated soil, total
nitrogen, phosphorus, and potassium gradually increased with the
8
Industrial Crops & Products 195 (2023) 116420
increase of residue concentrations (Table 5) before and after the AD
process. The soil that was treated with 25% of GSR had the highest
contents of nitrogen (0.31% and 0.34%), potassium (1.19% and 1.27%),
and phosphorus (1.13% and 1.20%) before and after the AD process,
respectively, followed by 25% of CSR and then 20% of GSR. All residues’
concentrations significantly exceeded the control in soil content of N, P,
and K. Total nitrogen was generally significantly increased after the AD
process (P = 0.0032). Also, total potassium (P = 0.0005) and total
phosphorous (P = 0.0098) were generally significantly increased after
the AD process. It has been observed that the addition of biogas residues
to soil significantly improves its physical and chemical qualities (Fer­
dous et al., 2018). The biogas slurry treatment may also provide a more
reliable source of nutrients for the development and growth of tomatoes.
O.A. Awadalla et al. Industrial Crops & Products 195 (2023) 116420

Table 3
Influence of anaerobic digester residues on the plant growth and yield of tomato fruits.
Biomass residue (Conc.) Plant height (cm) Leaf area (cm2) Total chlorophyll (mg/g) Number of fruit /plant Fruit weight (g) Fruit yield/plant (kg)
a a a a a
Control 78.8 ± 0.8 27.4 ± 0.4 1.3 ± 0.03 15.0 ± 1.0 59.0 ± 0.3 0.9 ± 0.26a
RSR (10%) 87.7 ± 1.3b 30.5 ± 0.6b 1.4 ± 0.04b 17.0 ± 2.0ab 65.7 ± 0.3b 1.1 ± 0.10b
RSR (20%) 89.8 ± 0.8b 31.2 ± 0.3b 1.4 ± 0.04b 18.0 ± 1.0b 67.2 ± 0.2c 1.2 ± 0.23b
RSR (25%) 89.9 ± 0.9b 31.7 ± 0.9bc 1.5 ± 0.03c 18.0 ± 1.0b 67.2 ± 0.3c 1.2 ± 0.10b
CSR (10%) 88.6 ± 1.1b 30.8 ± 0.5b 1.5 ± 0.03c 18.0 ± 0.0b 66.3 ± 0.3b 1.2 ± 0.10b
CSR (20%) 92.8 ± 1.2c 32.2 ± 1.2bcf 1.5 ± 0.01c 19.0 ± 1.0b 69.4 ± 0.3d 1.3 ± 0.12bc
CSR (25%) 94.6 ± 1.3c 32.8 ± 0.5cf 1.5 ± 0.01c 19.0 ± 2.0b 70.8 ± 0.4d 1.4 ± 0.06c
GSR (10%) 98.7 ± 2.3d 34.3 ± 0.4df 1.5 ± 0.03c 20.0 ± 1.0b 73.9 ± 0.3e 1.5 ± 0.07c
GSR (20%) 103.9 ± 2.2e 36.1 ± 0.3e 1.6 ± 0.02d 25.0 ± 2.0c 77.8 ± 0.2 f 1.6 ± 0.13c
GSR (25%) 105.3 ± 1.9e 33.7 ± 0.4 f 1.5 ± 0.03c 20.0 ± 2.0b 72.6 ± 0.3e 1.4 ± 0.15c
P-value 0.962 0.942 0.844 0.939 0.999 0.912

RSR = Rice straw residue, CSR = Corn stalk residue, GSR = Grape stem residue.
Values are the mean of three replicates ± SD.
Different letters in the same column indicate statistically significant differences (P < 0.05).

Table 4 Table 5
Influence of anaerobic digester residues on the physical and chemical properties Influence of anaerobic digester residues on the soil content of nitrogen, potas­
of tomato fruits. sium, and phosphorus before and after adding residues from biogas digesters.
Biomass Fruit TSS Ascorbic Titratable Shelf Biomass Total nitrogen (%) Total potassium (%) Total phosphorus
residue firmness (ºBrix) acid (g/kg) acidity (%) life residue (%)
(Conc.) (Newton) (days) (Conc.)
Before After Before After Before After
Control 6.8 ± 0.5a 3.8 22.6 0.57 11.9 AD AD AD AD AD AD
± 0.2a ± 0.2a ± 0.01a ± 0.3a
Control 0.03 0.03 0.13 0.13 0.14 0.12
RSR (10%) 10.5 ± 0.7b 4.2 25.2 0.61 15.6
± 0.01a ± 0.01a ± 0.03a ± 0.0a ± 0.03a ± 0.02a
± 0.2abc ± 0.2b ± 0.02b ± 0.3b
RSR 0.04 0.05 0.32 0.33 0.17 0.18
RSR (20%) 11.4 4.1 25.8 0.62 16.3
(10%) ± 0.01a ± 0.0b ± 0.02b ± 0.04b ± 0.04a ± 0.0b
± 0.2bc ± 0.0b ± 0.3c ± 0.00b ± 0.3c
RSR 0.06 0.07 0.75 0.81 0.28 0.29
RSR (25%) 11.8 4.2 25.8 0.63 18.0
(20%) ± 0.02ac ± 0.01c ± 0.04c ± 0.04c ± 0.03b ± 0.04c
± 0.6bc ± 0.2abc ± 0.2c ± 0.01bc ± 0.4d
RSR 0.11 0.13 0.95 1.02 0.71 0.77
CSR (10%) 10.9 4.1 25.5 0.63 16.6
(25%) ± 0.01b ± 0.02d ± 0.05d ± 0.02d ± 0.05c ± 0.07d
± 0.7bc ± 0.0b ± 0.3bc ± 0.02bc ± 0.4c
CSR 0.07 0.07 0.30 0.32 0.16 0.17
CSR (20%) 12.0 ± 0.4c 4.1 26.7 0.64 19.5
(10%) ± 0.01c ± 0.0c ± 0.05b ± 0.02b ± 0.02a ± 0.02b
± 0.1ab ± 0.0d ± 0.01bc ± 0.5e
CSR 0.13 0.14 0.67 0.72 0.26 0.28
CSR (25%) 12.5 4.5 27.2 0.65 20.2
(20%) ± 0.02bd ± 0.02d ± 0.07c ± 0.05c ± 0.04b ± 0.04c
± 0.6cd ± 0.2c ± 0.2e ± 0.01cd ± 0.2e
CSR 0.14 0.15 0.87 0.94 0.85 0.91
GSR (10%) 13.4 ± 0.3d 4.7 28.4 ± 0.4f 0.64 22.4
(25%) ± 0.01d ± 0.02d ± 0.07d ± 0.04d ± 0.05d ± 0.09d
± 0.1cd ± 0.01bc ± 0.4f
GSR 0.09 0.10 0.50 0.54 0.48 0.51
GSR (20%) 14.6 ± 0.5e 4.9 29.9 0.67 24.5
(10%) ± 0.01c ± 0.01d ± 0.05e ± 0.04e ± 0.04e ± 0.03e
± 0.1d ± 0.1g ± 0.01d ± 0.5g
d GSR 0.12 0.13 0.98 1.05 0.80 0.85
GSR (25%) 13.0 ± 0.2 4.6 28.2 ± 0.2f 0.66 20.6
(20%) ± 0.0b ± 0.01d ± 0.08d ± 0.05d ± 0.01cd ± 0.05d
± 0.1c ± 0.02 cd ± 0.3f
GSR 0.31 0.34 1.19 1.27 1.13 1.20
P-value 0.974 0.969 0.994 0.958 0.995
(25%) ± 0.01e ± 0.03e ± 0.19d ± 0.06 f ± 0.03f ± 0.0f
RSR = Rice straw residue, CSR = Corn stalk residue, GSR = Grape stem residue, P-value 0.9931 0.9942 0.9373 0.9984 0.9968 0.9887
TSS = Total soluble solids. RSR = Rice straw residue, CSR = Corn stalk residue, GSR = Grape stem residue,
Values are the mean of three replicates ± SD. AD = Anaerobic digestion.
Different letters in the same column indicate statistically significant differences Values are the mean of three replicates ± SD.
(P < 0.05). Different letters in the same column indicate statistically significant differences
(P < 0.05).
In order to boost the nutritional value of tomatoes, the yield was
increased relative to conventional fertilizer treatments (Zheng et al., nitrous oxide and nitrate leaching emissions while also providing an
2020). In addition, the treatment improved soil environmental vari­ extra source of energy in the form of biogas (Möller, 2009). Organic
ables, which could serve as a model for replacing fertilizer with biogas fertilizers have the ability to enhance crops’ healthy growth and
slurry (Ali et al., 2019c). improve crops’ productivity and quality by enhancing soil structure
All concentrations of RSR, CSR, and GSR significantly reduced the (Rong et al., 2018). Therefore, the replacement of inorganic fertilizers
colony diameters of F. oxysporum compared to the control. A significant with organic ones may help in constructing a safer food production
decrease in colony diameter was observed at 20% and 25% of GSR system with adequate environmental and ecological safety achieve­
(1.00 cm) with approximately 88.9% growth inhibition, followed by ments on cultivated lands. In addition, AD can be considered a central
25% of RSR (1.50 cm) with 83.3% growth inhibition (Fig. S4). The in­ unit of holistic farming enhancement by providing energy, recycling
crease in bioreactor residue concentration in the soil led to a significant wastewater, and producing organic fertilizer to improve crop yield and
improvement in tomato growth and metrics (Table 6). These findings soil physicochemical properties.
reveal that exceeding the GSR increases the physical and chemical
qualities of tomato fruits in comparison to the control, RSR, and CSR. 4. Conclusion
These findings are in accordance with Mupambwa et al. (2019), who
found that the treatments with biogas residues significantly reduced wilt The increased production of livestock results in a significant rise in
disease infections caused by F. oxysporum in tomato seedlings under field the amount of lignocellulosic biomass and animal waste that must be
conditions. Using the residue of AD from agricultural wastes reduced managed. Among the wide range of waste valorization methods

9
O.A. Awadalla et al. Industrial Crops & Products 195 (2023) 116420

Table 6 Ali, S.S., Sun, J., 2015. Physico-chemical pretreatment and fungal biotreatment for park
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10.1186/s40064-015-1466-9.
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Biomass residue (Conc.) Colony diameter (cm) Growth inhibition (%) crassipes) for the enhancement of biomethanation: VIT® gene probe technology for
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Ali, S.S., Kornaros, M., Manni, A., Al-Tohamy, R., El-Shanshoury, A.E.-R.R., Matter, I.M.,
Omayma Awadalla: Conceptualization, Writing – review & editing. Elsamahy, T., Sobhy, M., Sun, J., 2021e. Advances in microorganisms-based
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Ali, S.S., Sun, J., Koutra, E., El-Zawawy, N., Elsamahy, T., El-Shetehy, M., 2021h.
The authors declare that they have no known competing financial Construction of a novel cold-adapted oleaginous yeast consortium valued for textile
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Sun, J., Azab, M., 2022. Exploring the potential of anaerobic co-digestion of water
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