Environmental Technology & Innovation 25 (2022) 102207

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Environmental Technology & Innovation

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

Analysis of viable biogas production from anaerobic digestion

of swine manure with the magnetite powder addition
Maxi Estefany Huamán Córdova a , Hellen Luisa de Castro e Silva b ,
∗
Regina Mambeli Barros c , , Electo Eduardo Silva Lora d ,
Ivan Felipe Silva dos Santos e , João Victor Rocha de Freitas f ,
Afonso Henriques Moreira Santos c , Juliano Romanzini Pedreira g ,
Bárbara K. Flauzino h
a
Master of Science in Engineering of Energy, Federal University of Itajubá, (Engenharia de Energia da Universidade Federal de
Itajubá), Excellence Group in Thermal Power and Distributed Generation-NEST, Av. BPS, 1303, Itajubá-MG, CEP: 37500-903, Brazil
b
Student of Master of Science in Environment and Hydric Resources, Natural Resources Institute, Federal University of Itajubá,
(Mestrado em Meio Ambiente e Recursos Hídricos, Instituto de Recursos Naturais da Universidade Federal de Itajubá), Av. BPS,
1303, Itajubá-MG, CEP: 37500-903, Brazil
c
Professor of Natural Resources Institute, Federal University of Itajubá, (Instituto de Recursos Naturais da Universidade Federal de
Itajubá), Av. BPS, 1303, Itajubá-MG, CEP: 37500-903, Brazil
d
Federal University of Itajubá (UNIFEI), Mechanical Engineering Institute – IEM, Excellence Group in Thermal Power and
Distributed Generation (NEST), Minas Gerais, Av. BPS, 1303, Itajubá-MG, CEP: 37500-903, Brazil
e
Doctorate in Mechanical Engineering at UNIFEI, and Master of Science in Engineering of Energy, Federal University of Itajubá,
(Engenharia da Energia da Universidade Federal de Itajubá), Hydric Engineer, UNIFEI, Av. BPS, 1303, Itajubá-MG, CEP:
37500-903, Brazil
f
Graduation in chemistry at UNIFEI, Laboratory Technician at Federal University of Itajubá, (Engenharia da Energia da
Universidade Federal de Itajubá), Av. BPS, 1303, Itajubá-MG, CEP: 37500-903, Brazil
g
Professor at IFSM/Pouso Alegre-MG, Brazil. Master of Science in Engineering of Energy, Federal University of Itajubá, (Engenharia
da Energia da Universidade Federal de Itajubá), Av. BPS, 1303, Itajubá-MG, CEP: 37500-903, Brazil
h
Graduation in Environmental Engineering at UNIFEI (Engenharia Ambiental da Universidade Federal de Itajubá), Av. BPS,
1303, Itajubá-MG, CEP: 37500-903, Brazil

article info a b s t r a c t

Article history: The development of new technologies during the processes of Anaerobic Digestion (AD)
Received 8 February 2021 has occurred through the use of new types of additives, to maximize the CH4 produc-
Received in revised form 19 November 2021 tion. Therefore, this study aimed to technically analyze the effect of magnetite powder
Accepted 9 December 2021
in the AD process of the pigs’ litter in anaerobic reactors under mesophilic conditions. In
Available online 16 December 2021
this sense, the experiments were carried out in triplicate under two sequential processes
Keywords: to analyze the physicochemical characteristics and concentrations of trace elements (Fe,
Anaerobic digestion Zn, Mn, and Cu) before and after AD. The volume of biogas and yields of CH4 were
Magnetite powder analyzed under normal conditions of temperature and pressure, to infer the role of
Methane magnetite in the digestion process. The results showed that the magnetite powder has
Pig slurry
a significant impact on yields of methane during the digestion process of pig slurry. The
Biogas
maximum methane generated were 3.82.10−2 Nm3 CH4 /kg VS with the addition of 8 g
Renewable energy
of magnetite. The minimum methane produced was 2.18.10−1 Nm3 CH4 /kg VS with the
addition of 12 g of magnetite. The concentrations of trace elements were consistent with

∗ Corresponding author.
E-mail addresses: maxiestefanyhc@gmail.com (M.E.H. Córdova), hellen-luisa@hotmail.com (H.L. de Castro e Silva), remambeli@hotmail.com
(R.M. Barros), electo@unifei.edu.br (E.E.S. Lora), ivanfelipedeice@hotmail.com (I.F.S. dos Santos), jvictor_rocha@yahoo.com.br (J.V.R. de Freitas),
afonsohms@gmail.com (A.H.M. Santos), juliano.pedreira@ifsuldeminas.edu.br (J.R. Pedreira), barbara@ixconsult.com.br (B.K. Flauzino).

https://doi.org/10.1016/j.eti.2021.102207
2352-1864/© 2021 The Author(s). Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.
org/licenses/by-nc-nd/4.0/).
M.E.H. Córdova, H.L. de Castro e Silva, R.M. Barros et al. Environmental Technology & Innovation 25 (2022) 102207

the literature data contributing to the smooth progress of the enzymatic activities of the
methanogenic microorganisms.
© 2021 The Author(s). Published by Elsevier B.V. This is an open access article under the CC
BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction

The use of energy sources from fossil fuels is linked to distinct environmental problems such as the contamination
of soil and water resources, caused by atmospheric pollution, from the release of hydrocarbons (HC), sulfur (SOx),
and nitrogen (NOx) oxides, and carbon monoxide (CO) (Drumm et al., 2014). In this context, new types of research on
energy generation from biomass have been developed. In this field, energy from sugar cane and the municipal solid waste
(MSW), forestry, and agricultural sector can be highlighted, which provide approximately 8.2% of the Brazilian domestic
supply of electric energy (EPE, 2017; Fernandes, 2012; Silva and Amaral, 2013).
In the agricultural landscape, the activity of equines contributes to 22% of the Brazilian Gross Domestic Product (GDP),
generating 16 million temporary and permanent jobs (Santos, 2014). This activity is characterized by interconnected com-
ponents, occurring the dynamism of inputs such as water, energy, rations, medicines, and sanitizers, types of production
units, management techniques, and management of effluents and wastes (Fernandes, 2012). Currently, as forms of treat-
ment most often used for waste treatment consists of composting, settling lagoons, biodigesters, overlapping or biological
beds, and Anaerobic Digestion (AD), which provides biogas and organic substrates as byproducts (Perdomo, 1996; Diesel
et al., 2002; Pitz et al., 2009). Several methanogens drive the process of AD as Methanosarcina barkeri; Methanospirillum
hungatii; Methanocorpusculum parvum, Methanobacterium thermoautotrophicum and Methanococcus voltae, Methanococcus
vanielli, and Methanococcoides methylutens (Demirel and Scherer, 2011).
Methane (CH4 ) is the main component that determines the energy content of biogas, present in 50% to 75% of its
composition. The second main constituent is carbon dioxide (CO2 ), estimated at between 25% and 50%, and approxi-
mately 2%–8% of other gases. These gases are nitrogen (N2 ), water (H2 O), oxygen (O2 ), traces of sulfur (S2 ), hydrogen
sulfide (H2 S), and ammonia (NH3 ) (Costa Gomez, 2013). Besides being a fuel for generating electrical energy, biogas is
an ecological fuel because it allows the capture of CH4 and CO2 in the atmosphere. These gases cause the absorption of
electromagnetic energy enhancement, increasing the greenhouse effect (Jean et al., 2019; Pagliuso and Regattieri, 2008).
Currently, the development of new research on the AD process has endorsed the optimization of this process to
facilitate the dissemination of renewable energy sources and contribute to environment preservation (Weib et al., 2010;
Chiew and Shimada, 2013; Liu et al., 2015. Therefore, the development of these technologies aims to evaluate the energy
production potential through the use of new types of additives, to maximize the CH4 production.
As the optimization of this process, the current research suggests modifications of the parameters involved in
the AD process of organic compounds by interference from electromagnetic fields. Therefore, there is evidence that
methane production can be facilitated through the development of the magnetized reactor (Wang et al., 2017). Magnetite
can be inorganic or biologically generated, abundant in igneous, metamorphic, and sedimentary environments (Perez-
Gonzalez et al., 2010). Recent studies have revealed that magnetite acts as a conduit to improve the rates of organic
biodegradation and methane production in anaerobic conditions. This ore application increases the syntropic metabolism
or cooperation among microorganisms that donate electrons and those electrons accepters through direct-interspecies
electronic transfer (Aulenta et al., 2013; Cruz Viggi et al., 2014; Kato et al., 2012). Also, according to Xiao et al. (2017),
the use of nano-minerals strengthens the bond between bacteria and methanogenic microorganisms. In this context,
the tracks of methanogenesis involved (acetoclastic methanogenesis and syntrophic oxidation of acetate coupled to
hydrogenotrophic methanogenesis) are flexible in natural soil. Besides, particles of nano-Fe3 O4 can promote electro-
methanogenesis, engaging syntrophic oxidation of acetate (SAO) and Direct Interspecies Electron Transfer (DIET). Li et al.
(2018) investigated the effect of carbon as representative of conductive materials of carbon, the production of methane
with moist soil incubated. According to the authors, the application of the electrochemical technology indicated that
the carbon material promoted acetoclastic methanogenesis instead of reducing CO2 in a natural environment. Another
study conducted by Xiao et al. (2019a) revealed the formation of a secondary mineral driver to accelerate the transfer
of electrons as an essential factor in methanogenesis. The research conducted by the authors showed the increase of
the abundance of bacteria with the ability to release electrons, as Thermincola, Rombotusia, and Shewanella, as well as a
Methanosarcin archaea known as methanogen electrons accepters. For this study, the horizon of red clay (RHC) enjoys
the syntropy between partners, donors, and recipients of electrons with the assistance of the magnetite biologically
diagenetic. Besides, according to Xiao et al. (2019b), the presence of conductive materials such as magnetite and graphene
significantly accelerates the transfer of electrons based on electrochemical analysis, stimulating even more acetoclastic
methanogenesis.
In this sense, there is an increase in the efficiency of microbial activity in anaerobic biodegradation processes of organic
compounds under a magnetic field (Matos, 2017). Dębowski et al. (2016) determined the impact of applying a constant
magnetic field (CMF) on the AD effectiveness of algal biomass. The authors found a correlation between CMF exposure
time and methane-producing parameters values. Complementarily, Sarvenoei et al. (2018) established a new technique
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M.E.H. Córdova, H.L. de Castro e Silva, R.M. Barros et al. Environmental Technology & Innovation 25 (2022) 102207

for solubilization of residual sludge using a combined magnetic field and CO2 injection as a pretreatment before applying
the AD process.
Concerning the optimization of CH4 generation from swine’s slurry AD, Liu et al. (2015) analyzed biogas production
optimization using magnetite and zeolite. According to the authors, the maximum increments of the production of CH4
were 52.01% and 51.01% for the addition of 3 g of magnetite and 1 g of natural zeolite. Wang et al. (2017) analyzed the
magnetite powder using swine manure and wheat straw co-digestion. Using the Gompertz model, the authors found
the optimum efficiency of the AD process to add 3 g of powdered magnetite, with the highest potential for methane
production (206 mL/gTS ) in their experiments. The anaerobic co-digestion of wheat straw with the addition of magnetite
ore contributed to the improvement of the C:N ratio of the process, resulting in a higher yield of biogas. In terms of the
use of nanoparticles, Zhang et al. (2019a) analyzed the response and mechanisms of the performance and fate of antibiotic
resistance genes (ARGs) to nano-magnetite during the anaerobic effect of swine manure in sequential batch processes.
The authors concluded that magnetite has no significant influence on microbial activity. At the same time, the nano-
magnetite can increase methanogenesis instead of acetogenesis, reflected by the analysis of functional genes. Besides,
the authors showed that the improvement in methane production is closely correlated with the reduction of ARGs, and
the enhancement of its reduction occurs as the improvement of the production of methane during AD of the pig manure.
Another similar study conducted by Zhang et al. (2019b) exposes the effects of magnetite in the AD of pig manure and
focuses on the production of methane and the fate of genes conferring resistance to antibiotics. According to the authors,
the increase in the production of CH4 was 16.1% through the use of the additive. The improvement of production can be
attributed to improving the DIET of propionate degradation and SAO track. According to the authors, the functional genes
and the analysis of the microbial community indicated the increase of the acetoclastic methanogenesis and not of the
hydrogenotrophic methanogenesis by the use of magnetite.
The improvement of the production of CH4 by these studies is supported by the work of Abdelsalam et al. (2017),
in which the addition of nanoparticles of 20 mg/L Fe and 20 mg/L Fe3 O4 increased, respectively, the volume of biogas
in 1.45 and 1.66 times and CH4 in 1.59 and 1.96 times concerning the control. According to the authors, the largest
production of biogas and CH4 were obtained by adding 20 mg/L Fe3 O4 , which were obtained from 584 ml of biogas/
gvs and 351.8 ml of CH4 /gvs . The reproduction of this result for chicken substrate showed a higher rate of production
of CH4 (2.55 mL CH4 /gvsf .d) and cumulative yield (137.23 mL CH4 /gvsf .d), the latter with 73.9% compared to the
control (Aguilar-Moreno et al., 2020).
Another advantage is related to the bioavailability of heavy metals in the process. Liang et al. (2017) analyzed the effect
of microscale ZVI/magnetite on methane production and bioavailability of heavy metals during the anaerobic effect of
diluted pig manure. According to the authors, the addition of ZVI decreased the bioavailability of Cu and Zn in the solid
waste digested, coupled with a better performance in the combined action of the microscale ZVI and magnetite, in which
the end product of anaerobic corrosion ZVI and magnetite can contribute to the improvement of the production of methane
through direct transfer of electrons interspecies in ZVI-anaerobic digestion process.
The more human activities increase, the more solid waste is generated. Furthermore, mining in the state of Minas Gerais
(in Brazil) is the most expressive economic activity. According to Xiao et al. (2020b), nanomagnetite has been found to
accelerate methane generation by dismuting acetate in pure culture. Conducting minerals increases acetate dismutation
and, consequently, increases methanogenesis (Xiao et al., 2020a,b). According to Xiao et al. (2020a), the reduction
of DIET-CO2 may not be the only mechanism that explains electromethanogenesis. Nevertheless, Xiao et al. (2020b)
preconized that it remains unclear how conductive nanomaterials function to accelerate acetoclastic methanogenesis in
multi-community environments, and therefore, more studies are needed to verify the benefits of conductivity. Therefore,
considering the significant Brazilian agricultural and mining activity in the state of Minas Gerais, we studied the
improvement of biogas generation from the anaerobic digestion of swine slurry by magnetite adding for energy use
purposes.
The present study technically studied the effect of magnetite powder in the AD process of pig slurry in a sequential
batch reactor (SBR) under mesophilic conditions. The SBR reactors have been used in swine wastewater treatment since
they efficiently promote the biological removal of organic matter, nutrients, and pathogens. Besides, SRB benefits the
flexibility of phases of the AD process at a low cost on a pilot scale (Oliveira et al., 2013a,b). Experiments were carried
out in triplicate under two sequential processes to find the optimal dosage of magnetite ore. The physicochemical
characteristics and concentration of trace elements were analyzed before and after the AD experiments procedure.
The biogas volume and CH4 yields were quantified under standard temperature and pressure conditions (STPC) to
investigate the role of magnetite in the AD process.

2. Methodology

2.1. Site from the sample collection and additive characterization

The company chosen to perform the collections of samples acts as a follow-up to the agribusiness and in the
industrialization of its production of cattle and pigs, located in the city of Cachoeira de Minas, south of the state of Minas
Gerais, Brazil. The municipality, located on the geographic coordinates 22◦ 21′ 18′′ S 45◦ 46′ 44′′ W, has 849 m of altitude
(see Fig. 1) .
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M.E.H. Córdova, H.L. de Castro e Silva, R.M. Barros et al. Environmental Technology & Innovation 25 (2022) 102207

Fig. 1. Location of the region under study.

Source: Adapted from IBGE (2018).

According to Reboita et al. (2015), the site fits in the subtropical climate of dry winter (Cwa) by the Köppen classification
with minimum and maximum average temperatures with very close values, respectively to 18 ◦ C to 28 ◦ C. The enterprise
has an area of 300 hectares and approximately 1300 heads of pigs. The production unit worked is a full-cycle type,
encompassing all stages of the pig’s life cycle on the same farm, from birth to slaughter (Souza et al., 2013).
Gross magnetite powder was used as an additive and was obtained from a company municipality of Timóteo, Minas
Gerais. It was prepared by crushing and was sifted until it became powder with particle sizes between 0.5 mm and 1.0 mm.
The powders were washed with deionized water and then dried at 105 ◦ C for 12 h in the oven.

2.2. Fitting and operation of biodigesters

The construction of the digesters was performed according to the model proposed by Cañote et al. (2021) and Ribeiro
et al. (2016). In this way, six SBRs units were built using returnable bottles of polyethylene terephthalate (PET) of the
volume of 2.16 liters each. The usable area of the reactors was reserved for 1.62 liters of the substrate and 0.54 liters of
gasometer for biogas-generated storage.
A copper male-pin fixed adapter of 1/4′′ × 1/4′′ was attached to the cover of each reactor to exhaust outlet system
assembling, allocating the crystal level hose of 1/4′′ close to a control valve of the same diameter and female-pin fixed
adapter, using clamps 5/16′′ × 1/2′′ to extremes. Silicone and insulating tape between the connections to prevent biogas
leakage. Fig. 2 shows the dimensions the reactor used for the application of the process on a pilot scale.
Digesters were coupled to an electrical thermostat with a power of 75 W and voltage of 110 V, and in the water-
bath to maintain a constant temperature of the system at 35 ◦ C under mesophilic conditions. This procedure aimed to
contribute to increasing efficiency in biogas production (Chen and Neibling, 2014; EPA, 2018).
The volume of each biogas digester was recorded per day and was measured using the water displacement method in a
manometer, with the gasometer and the hose volume from each reactor. The period for which the biogas generated from
reaching a methane content between 50–80% in its composition was considered to determine hydraulic retention time
(HRT). In other words, time to reach the apex of its production, followed by its decay. In this sense, it was established
an HRT of 70 days for two sequential cycles, comprising the steps of filling, reaction, sedimentation and draining of the
effluent in the reactors. Also, the digesters were manually agitated daily, aiming to stimulate the microbial activity of the
environment and optimize the biogas production in the reactors.
®
The gas GEM™ 5000 (serial no. 501,944) device, manufactured by LandTec , was employed for gas monitoring. The
measurements were performed using simultaneous and continuous detection of methane (%), carbon dioxide (%), oxygen
(%), carbon monoxide (ppm), and hydrogen sulfide (ppm) gases.
According to Gacitúa et al. (2014), the electrically conductive nanoparticles of magnetite accelerate the syntrophic
or cooperative metabolism promoting processes of extracellular electron transfers. This fact favors the electrosynthesis
microbial and increases certain microorganisms’ capacity to reduce inorganic compounds (CO2 or protons) in stable
more-energetic molecules (CH3 COOH, H2 , and CH4 ). According to the study conducted by the authors, the addition of
small amounts (10 mg L−1 ) of electrically conductive nanoparticles of magnetite ore contributes to the enhancement
of catalytic activity, resulting in greater efficiency in the process of digestion. In this sense, for the present study, we
considered doses of 8.0 g and 12.0 g, which were added, respectively, in bioreactors labeled as M.1 and M.2.
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M.E.H. Córdova, H.L. de Castro e Silva, R.M. Barros et al. Environmental Technology & Innovation 25 (2022) 102207

Fig. 2. Dimensions of the biodigester.

Table 1
Parameters analyzed in the chemical characterization of the effluent.
Parameter Method
Total solids 2540 method B
Fixed solids
2540 method and
Volatile solids
pH Method 4500-H+-B
Biochemical oxygen demand 5210 method B
Chemical oxygen demand 5220 method D
Total nitrogen The Kjeldahl method

2.3. Analysis of chemical characterization of the effluent

This step aimed to quantify the organic matter reductions and the presence of trace elements before and after the
AD. Consequently, it was possible to evaluate its efficiency and the supply of nutrients absorbed by the biomass. Table 1
shows the analysis performed under the methodology of effluent characterization according to the Standard Methods for
Examination of Water and Wastewater (APHA, 2017).
The technique spectrometry of x-rays absorption by dispersion of energy, with the SpectrAA Software, was used to
determine the trace element concentration.

2.4. Biogas production

The STPC values were calculated to standardize the volume of biogas production, according to the laws of Boyle and
Gay-Lussac (Eq. (1)). The pressure and temperature values from the city of Itajubá-MG as an average of 935 mmbar
(equivalent to 93.500 BP) were considered, according to the local meteorological station, the average annual temperature
5
M.E.H. Córdova, H.L. de Castro e Silva, R.M. Barros et al. Environmental Technology & Innovation 25 (2022) 102207

Fig. 3. Average of the chemical parameters before and after the biodigestion during the sequential process: (a) I (left); and (b) II (right).

in Itajubá was estimated as 20.1 ◦ C.

P0 V0 /T0 = P1 V1 /T1 (1)

By isolating the volume to be standardized (V0 ), get Eq. (2):

VN = Pabs × VG × TC /TR × PC (2)

3 ◦
where: V0 = normalized Volume (m ); TC = temperature corrected biogas to 20,1 C expressed at 293.25 K; PC = cor-
rected pressure of the biogas from 101,325 Pa for 1 atm; VG = volume of biogas in the gasometer moved on gauge
(m3 ); Pabs = biogas pressure is provided by the gas analyzer considering the pressure of the city of Itajubá (Pa); TR =
Temperature of the biogas under mesophilic conditions = 308.5 K.
After completing laboratory tests concerning the volume of gas generated in the STPC and its composition, the
generation of biogas from the substrate analyzed (2.16 liters of sludge) was determined. A sludge density of 1.020 kg/m3
for the realization of calculations was considered (Dartora et al., 1998).

3. Results and discussion

3.1. Analysis of reduction of organic constituents

The analysis of the chemical characterization of the reactors substrates are presented in Fig. 3. The average concen-
trations of substrate digesters units M.1 and M.2, before and after the period of anaerobic digestion, for both sequential
batch processes (I and II), were considered.
As with Chernicharo (1997, 2005), the pH values situated in the range of 6.0 to 8.0, are favorable for the growth of
methanogenic microorganisms. Before and after the AD for M.1 and M.2 dosages, the pH values results were in the range
of 6.19 to 6.65 and 6.15 to 6.90, respectively, for the sequential processes I and II. These results provided the framework
of this variable under optimal operational conditions to anaerobic reactors.
The reduction of the organic fraction was found using analysis of parameters such as chemical oxygen demand (COD),
biochemical oxygen demand (BOD), fixed solids (FS), volatile solids (VS), and total solids (TS), which were evaluated before
and after the anaerobic biodigestion process. During the sequential process I, the variable COD presented an average
reduction of 62.51% and 68.67% for the reactors M.1 and M.2, respectively. Similarly, the average reduction percentage
was also higher in the M.2 reactor during the sequential process II, ranging from 82.20% to 86.36% for M.1 and M.2 in
that order. Also, the concentration of output to the experimental unit M.2 was close to the 2,076 ± 560 mg/L value for
the variable analyzed after anaerobic treatment in UASB reactor carried out by Kunz et al. (2009).
The BOD variable represents the concentration of biodegradable matter present in organic matter. In the sequential
process I, this variable presented an average reduction of 54.11% and 62.38% for the experimental units M.1 and M.2,
respectively. Regarding the sequential process II, the percentage of reduction was more significant, reaching 86.18% and
69.12% for both reactors. Besides, the concentration of output to reactor M.2 during the sequential process II was 2088
mg/L, whose value was a little above 1203 ± 411 mg/L, after application of anaerobic treatment by Kunz et al. (2009).
When considering the percentage of variation of SF for the reactors M.1, there is an average reduction of 72% for
sequential process I and 42% for sequential process II. The percentages reached by the reactors M.2 were more significant
than M.1 because average reductions of respectively, 87% and 52% for both processes were observed. An average decrease
of TS for the reactors M.1 and M.2, respectively, ranged between 83% and 93% in the sequential process I. These values
ranged from 40% to 48%, respectively, in the sequential process II. The percentages of VS reduction were similar for both
types of dosages applied during the procedures. Because the average reduction achieved was 85% for M.1 and 94% for M.2
for the sequential process I. these values were 30% for M.1 and 39% for M.2 for the sequential process II.
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M.E.H. Córdova, H.L. de Castro e Silva, R.M. Barros et al. Environmental Technology & Innovation 25 (2022) 102207

Table 2
Results of volume, pressure, and volume by the STPC for the sequential process I and II.
EU (VG) (BAPS) TC T1 PC VN
(m3 ) (Pa) (◦ K) (◦ K) (Pa) (m3 )
M.1 6.00.10−4 100,142.80 293.25 308.15 101.32 5.64.10−4
I
M.2 6.20.10−4 100,143.56 293.25 308.15 101.32 5.83.10−4
M.1 5.80.10−4 100,140.60 293.25 308.15 101.32 5.46.10−4
II
M.2 6.10.10−4 100,160.40 293.25 308.15 101.32 5.74.10−4

The efficiency of the anaerobic biodigestion is affected by factors ranging from environmental conditions, such
as temperature, pressure, and management of the system to the chemical composition of the substrate. Substrate
composition characteristics include the pH of the medium, COD/BOD rate, and species of microorganisms present in the
digester. Braile and Cavalcanti (1993) considered a residue readily biodegradable when their chemical and biochemical
oxygen demands reach a COD/BOD less than 2. This ratio value ranged from 2.32 to 1.90 for the reactors M.1 and 2.32 to
1.93 for the reactors M.2 during the sequential process I. In the sequential process II, these values ranged from 1.2 to 1.6
(M.1 reactors) and 1.2 to 1.39 (M.2 reactors) , considering affluent and effluent analyses for both procedures.
Castro e Silva (2018) and Castro e Silva et al. (2021a) conducted the AD of swine manure in sequential batch reactors
and the study exposed for the same substrate and HRT. According to these authors, the COD/BOD ratio presented higher
values than the results obtained here, ranging from 2.32 to 2.43 and 1.20 to 1.44 for both sequential processes. These
results denote the influence of magnetite ore on the biodegradability of the substrate. When comparing the reduction of
organic constituents to the sequential process I, the average values of reduction to the reactors M.2 were superior to the
results obtained in the process of anaerobic digestion without the presence of additives as those obtained by Castro e
Silva (2018) and Castro e Silva et al. (2021a).

3.2. Biogas production in laboratory scale

The average biogas production during the sequential processes I and II for the reactors M.1 and M.2 are shown in
Table 2. The STPC were applied for all reactor’s results.
To analyze the variables for the sequential process I, the experimental unit M.2 showed a higher displacement of the
hose, showing a higher result of 100,143.56 pressure (Pa) and volume of biogas production (6.20 × 10−4 m3 ) normalized
volume. These values represented an increase of biogas production of 3.26% concerning the experimental unit M.1. At
the same time, this fact can also be observed in the sequential process II, in which the production volume normalized
was 6.10 × 10−4 m3 and pressure equal to 100,160.40 Pa, indicating an increase in the volume generated from 4.88%
concerning reactor M.1.
In addition to the increased production of biogas, it is observed that the dosage of the additive applied in reactor
M.2 resulted in higher percentages of reduction of organic constituents and the largest fractions of biodegradation. These
facts denoted the higher efficiency in a pilot-scale of the process of anaerobic digestion for this experimental unit. Despite
this fact, it is necessary to emphasize that, although the generated volumes are small, these figures represent an
experiment on a laboratory scale with only 2.16 liters of substrate. In this sense, it should be emphasized that, on a large
scale, this difference would be considerably more significant. The scaling of technology is one of the great difficulties in
the innovation process, i.e., going from the milligram or gram scale, which is performed in a research laboratory, to the
kilogram (or hundreds of kilograms) scale (Vasconcellos et al., 2021). The authors preconized that this scaling process is
essential to take a product from the research laboratories to the market because necessary information is obtained about
the technical, economic and marketing viability of the new product. Scaling is a broad concept with different names, such
as ‘‘scale up’’, described as reproducing the results technicians obtained on smaller scales (laboratory) through physical
and/or chemical operations for larger scales to obtain a new commercial product (Vasconcellos et al., 2021). Besides,
scaling may be defined as a process used in the expansion, replication and adaptation of successful results on an industrial
scale, based on previous experiments, which should be framed in the innovation–learning–expansion cycle (Vasconcellos
et al., 2021; Cooley and Linn, 2014). In this sense, innovation, learning, and scaling up should be treated as separate, linked
processes, the innovation–learning–scaling up process is not linear but an iterative and interactive cycle, and scaling up
involves two types of possible errors: i. type 1 error: no or too little scaling up; and ii. type 2 error: wrong scaling up,
among other lessons (Cooley and Linn, 2014). All these project-related uncertainties, whether technical or financial, are
directly related to the immaturity of the biogas market in Brazil and tend to be overcome with the installation of reference
plants on commercial and replicable scales, which contribute to dynamize the sector from the creation of demand for
components and services, promoting greater attractiveness in the sales prices of materials and equipment, encouraging
training and investment in after-sales services and also encouraging the regulation of markets for by-products (Brazil,
2016a).
In Asia, especially in China and India, initiatives to valorize MSW using methanization are recurrent, but on smaller
scales and using simpler, low-cost and less efficient technologies (Brazil, 2016a). It is worth noting that, during project
preparation, the most appropriate division must be determined according to the project’s needs. More modules can better
7
M.E.H. Córdova, H.L. de Castro e Silva, R.M. Barros et al. Environmental Technology & Innovation 25 (2022) 102207

Table 3
Volume of methane generated by the reactors per kg of substrate, COD, BOD, TS, and VS in the sequential process I and II.
Sample Pilot scale Nm3 CH4 per kg of substrate, COD, BOD, ST, and SV
Q biogas LCH4 /L m3 CH4 .m3 Nm3 CH4 /kg Nm3 CH4 / Nm3 CH4 / Nm3 CH4 / Nm3 CH4 /
(L/day) Silt Silt substrate kg COD kg BOD kg ST kg SV
M.1 8.06.10−3 1.81.10−1 1.81.10−4 1.77.10−4 1.16.10−2 3.12.10−2 4.44.10−3 5.18.10−3
I
M.2 8.33.10−3 1.38.10−1 1.38.10−4 1.35.10−4 8.10.10−3 2.07.10−2 3.02.10−2 3.57.10−3
M.1 7.80.10−3 2.02.10−1 2.02.10−4 1.97.10−4 1.15.10−2 1.33.10−2 2.13.10−2 3.82.10−2
II
M.2 8.30.10−3 1.47.10−1 1.47.10−4 1.44.10−4 8.00.10−3 9.51.10−3 1.35.10−2 2.18.10−2

contribute to the possibility of performing a staged deployment or greater technical availability (Brazil, 2016b). On the
other hand, the ‘‘scale effect’’ significantly impacts price, whereby purchasing two or more smaller modules rather than
a single module can lead to economic non-viability (Brazil, 2016b).
Table 3 presents the volume (in liters) of biogas daily generated, liters of methane produced by each liter of substrate
used, and the volume of methane (in m3 ) per volume of substrate (in m3 ) for sequential processes I and II. Besides, the
methane (Nm3 CH4 ) yields under other essential parameters (kg of the substrate, COD, BOD, TS, and VS) are also presented.
The calculations were performed based on the measurements of volumes of biogas generated and variations of organic
constituents observed in experiments during both sequential processes. According to the obtained results, reactors M.2
showed a higher production volume of biogas, but reactors M.1 provided the highest increments of the standardized
volume of methane (1.77 × 10−4 and 1.97 × 10−4 Nm3 CH4 /kg substrate ). These results revealed an average yield of 52%
and 59.80% in processes I and II, respectively. In contrast to the average of 25.63% and 41.60% obtained for the methane
production in both cases, these results were obtained.
Aguilar-Moreno et al. (2020) performed treatments for chicken litter AD by adding different concentrations of
magnetite nanoparticles Fe3 O4 (20, 40, and 60 mg/L). According to the results from these authors, the treatment with
the lowest concentration, 20 mg/L of magnetite nanoparticles, presented the highest rate of methane production (2.55
mL CH4 /gvsf ·d) and the highest cumulative yield of methane (137.23 mL CH4 /gvsf). The last one increased 73.9% of methane
production compared to the control, while the concentration of volatile fatty acids was similar in all treatments. According
to Aguilar-Moreno et al. (2020), the control presented the lowest value (73.29 mL CH4 /gvsf) and the treatment with 20
mg/L the highest (126.42 mL CH4 /gvsf).
The ratio of methane yield (Nm3 CH4 ) with organic matter (in kg of COD and BOD) was high for the reactors M.1 during
the sequential process I, once the smaller variations of reduction of organic constituents occurred in the mixture (62.51%
to 54.11% for COD and BOD). The methane generated in sequential process II, in which the most significant volumes
of standard CH4 with organic matter in the reactors M.1 were produced at the expense of the smallest percentage of
variability of removal of constituents (82.20% and 86.18%).
Similarly, reactors M.1 had the highest methane yield during both sequential processes, and the most significant
production was during process II as 3.82 × 10−2 Nm3 CH4/kg VS (38.2 Nm3 CH4 /tVS ). This value corresponded to
the lowest percentage of reduction of volatile solids on the pilot scale. In the case of the reactors M.2, this value
was 2.18 × 10−2 Nm3 CH4 /kg VS (21.8 Nm3 CH4 /tVS ), resulting in a second production of significantly more methane
to this process. The results obtained indicate that the magnetite mineral significantly accelerated the increase in the
transfer of electrons that is not the reduction of DIET-CO2 . According to Xiao et al. (2020a), a classic process that describes
methane production comprises the reduction of CO2 by DIET. Xiao et al. (2020a) hypothesized that methane could
also be generated by direct acetate dismutation by syntrophy between electron donor Shewanella oneidensis MR-1 and
electron acceptor methanogens. Besides, Xiao et al. (2020b) advocated the hypothesis that conductive carbon nanotubes
(CNTs) stimulate, independently of eletrigens, the acetoclastic methanogenesis in pure cultures of Methanosarcina spp. and
anaerobic swamp soil. The authors found a substantial rise in the rate of methane production through the growth phase.
They advocated that CNTs would not increase the abundance of electromicrobes or the electron transfer rate in anaerobic
soils via microbial diversity and electrochemical analysis. Besides, CNTs closely linked to the cell surface were observed
by Xiao et al. (2020b) by transmission electron microscopy. Proteome analysis carried out by Xiao et al. (2020b) exposed
a stimulation of protein synthesis with about twice the enhancement involved in –COOH oxidation and electron transfer.
Xiao et al. (2020b) also demonstrated that the conduction of CNTs benefits methane generation and that the mechanism
involved is acetoclastic methanogenesis via acetate dismutation, at least partially, instead of the classic reduction of CO2 .
In this sense, exoelectrogenic activity improves acetate dismutation, signifying that electrons from S. oneidensis MR-1
convert methyl groups to methane (Xiao et al., 2020a). The results from the authors reveal DIET-acetate dismutation as
an alternative mechanism for generating biomethane, which is vastly stimulated by conductive carbon-based materials.
From this assumption, the magnetite can acquire a significant role in future platforms of renewable energy by process of
AD of pig manure due to the improvement of electromethanogenesis in complex systems, as exposed in recent studies of
the literature (Xiao et al., 2017; Li et al., 2018; Xiao et al., 2019a,b).
It is possible to observe, then, that the dosage of 8 g of iron ore magnetite used in this study contributed to greater
success in the process of methanogenesis, corroborating the findings reported by Wang et al. (2017) and Liu et al. (2015).
According to these authors, concentrations close to 3 g contributed to further generations of methane in the process of
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M.E.H. Córdova, H.L. de Castro e Silva, R.M. Barros et al. Environmental Technology & Innovation 25 (2022) 102207

Fig. 4. Composition of the biogas generated by experimental unit: (a) M.1 for the sequential process I (superior left); (b) I M.2 for the sequential
process I (superior right); (c) M.1 for the sequential process II (inferior left); and (d) M.2 for the sequential process II.

co-digestion. However, further studies must be conducted to analyze the behavior of percentages generated employing
the addition of iron ores in studies of anaerobic digestion.
Besides, the technical studies involving these additives should be tied to the costs of implementing and maintaining
biogas plants, since there is the cost of acquiring iron ore. In this sense, new raw materials should be investigated that
are conducive to the dissemination and optimization of the process at a low cost.

3.3. Analysis of the composition of biogas

The averages of gases present in the of biogas compositions for reactors, M.1 and M.2, during the sequential
processes I and II, are exposed in Fig. 4a, b, c, and d, respectively, regarding the hydraulic retention time (HRT).
For analysis, the averages of the values of concentrations of CH4 (%), CO2 (%), O2 (%), CO (ppm), and H2 S (ppm) were
obtained using the experimental studies conducted in triplicate were considered. The analysis of gas generation was
carried out in this way once the anaerobic reactors were susceptible to high variations in the behavior of soil organic
matter.
The importance of the gas CO2 is based on the fact that their presence reduces the calorific power of biogas and the
stoichiometric air demand (Porpatham et al., 2008), while the highest percentages of CH4 gas contribute to greater capacity
for energy production (Jiang et al., 2013; Deng et al., 2014). To the sequential process I, the average concentrations of
CH4 recorded a maximum percentage of 52% and 25.63% for the reactors M.1 and M.2, respectively. In terms of the
average levels of CO2 , the reading values provided average concentrations of 41.60% and 26.60% for both reactors mutually
exclusive.
When considering these parameters to the sequential process II, were obtained mean values for percentages of gas
CH4 , which oscillated in concentrations of 60% and 41.60% for the reactors M.1 and M.2, respectively. The average values
of CO2 analyses obtained were 37% and 31.40% for both reactors in the same order.
It is necessary to emphasize that the highest average production of CH4 gas, for the reactors M.1 and M.2, corresponded
to lower oxygen concentrations (%) and H2 S (ppm) for both sequential processes. This result has favored the present study,
once that the lower levels of oxygen, the higher activity of methanogenic microorganisms. Also, the strict control of the
generation of H2 S is essential because it contributes to the inhibition of acetogenic bacteria (Oelgeschläger and Rother,
2008; Wresta and Saepudin, 2013).
According to the results achieved by Castro e Silva et al. (2021a), the production of methane from anaerobic digestion
of swine manure considering the same HRT reached maximum concentrations of 33.40% and 45.25% for the sequential
processes I and II. The volume of the gases was significantly better stabilized in the reactors M.1 and M.2 because the
magnetite dust effect.

3.4. Analysis of variation of concentration of trace elements

The concentrations of trace elements present in the reactors M.1 and M.2, in mg/l, during the sequential processes I
and II are presented in Table 4. The average concentrations of biodigesters, before and after the AD, for both processes
were considered.
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M.E.H. Córdova, H.L. de Castro e Silva, R.M. Barros et al. Environmental Technology & Innovation 25 (2022) 102207

Table 4
The state of the trace elements for the reactors M.1 and M.2 before and after the
sequential process I and II.
I Metals M.1 M.2
Beforea Aftera Aftera
Iron 8.21 8.05 5.51
Zinc 0.62 1.19 0.70
Manganese 15.31 3.33 8.88
Covers 0 0.13 0.02
II Metals M.1 M,2
Beforea Aftera Aftera
Iron 8.21 7.35 7.60
Zinc 0.62 3.95 4.89
Manganese 15.31 0.76 0.78
Covers 0 0.54 0.80

Note:
a
Before and after the process of anaerobic digestion.

According to Demirel and Scherer (2011), the analysis of the metals iron (Fe), zinc (Zn), Manganese (Mn), and copper
(Cu) is important for the study of the process of anaerobic biodigestion since these factors influence the enzymatic
activities of the methanogenic microorganisms, ensuring the availability of the ideal supply of nutrients. This fact occurs
by stimulating cell growth and ensuring an optimal production of methane gas (Karlsson et al., 2014).
According to Demirel and Scherer (2011), the need for iron (Fe), nickel (Ni), cobalt (Co), molybdenum (Mo), selenium
(Se), and tungsten (W) by various methanogens have already been reported and included by: Methanosarcina bark-
eri; Methanospirillum hungatii; Methanocorpusculum parvum; Methanobacterium thermoautotrophicum, Methanobacterium
wolfei; Methanococcus voltae, Methanococcus vanielli, Methanococcoides methylutens.
In case of malfunction of anaerobic reactors, magnetite supplementation and adapted microbial consortia can be used
as a remedy (Ziganshina et al., 2021). This fact can be affirmed, according to the authors, especially during disturbances
of methanogenesis because inhibitory intermediates accumulation, as volatile fatty acids. Ziganshina et al. (2021) used
iron (II, III) oxide nanopowder (50−100 nm particle size, 97% trace metals basis) in anaerobic digestion of distillers grains
with solubles and sugar beet pulp in mesophilic batch experiments.
However, some authors establish some ranges of concentrations for these elements because despite the benefits
reported, high dosages of trace elements may inhibit the enzyme action of microorganisms active in the AD process.
Besides, the size of trace metal particles can biostimulate or inhibit AD depending on the concentration (Abdelsalam
et al., 2017; Aguilar-Moreno et al., 2020).
The analysis of variation of the concentration of the element iron, present mainly in the food additive of magnetite,
which is composed of the oxides of iron II and III (FeO and Fe2 O3 ), is important in the process since it must be provided
during the fermentation of methane (Ortiz, 2000; Takashima and Speece, 1990).
Concentrations of the iron in the effluent, after anaerobic digestion for both reactors, are in the range of 1 to 10 mg/l,
in accordance with studies envisioned by Weiland (2010). Results from Takashima and Speece (1990) presented a broader
range of concentration for this element, establishing the range from 0.28 to 50.4 mg/L as ideal concentrations for the AD
process.
Castro e Silva (2018) and Castro e Silva et al. (2021a) observed the final concentrations of 3.89 mg/l and 45.45 mg/l for
the element iron for AD of swine, considering the HRT of 70 days for sequential processes I and II. The final concentrations
for this element in the present study are significantly higher when comparing the data obtained by these authors. This fact
is due to the presence of the magnetite dust (Fe2 O3 ) during the processes of digestion of the sample, which composition
is concentrated in 70% of the mass of iron and contributes to the transformation of microorganic enzyme and the AD
process (Parawira, 2012; Chai et al., 2013; Oliveira et al., 2013a,b). The results of Fu et al. (2019) by culturing M. barkeri
with acetate as a carbon source, revelated that the nanoFe3 O4 existed in extracellular and intercellular spaces, cell surfaces,
cell membranes, and cytoplasms. The results obtained in both reactors related to the manganese are within the ranges of
concentrations of 0,005 to 50 mg/L and 0,005 to 55 mg/L. This range was preconized by Bischofsberger et al. (2005) and
Sahm (1981), respectively.
According to Sahm (1981), the ideal concentration range for the copper element is between 0.06 mg/L and 64 mg/L.
The effluent results obtained in the present study fit within the range
The Resolution of the Brazilian Environment National Council (CONAMA, in Portuguese) no. 375/2006 (Brazil, 2006)
determines the criteria for the sewage sludge use generated in Wastewater Treatment Plant (WWTP) as a fertilizer in
the soil for agriculture. This Resolution preconizes the maximum requirements for Zn and Cu as 2.8 mg/g and 1.5 mg/g,
respectively.
The Zinc concentrations are within the parameters established by this resolution considering the density of 1020 kg/m3
for the sample to 3.91% m/v in both reactors (M.1 and M.2). The average concentrations values ranged from 1.17 ×
10
M.E.H. Córdova, H.L. de Castro e Silva, R.M. Barros et al. Environmental Technology & Innovation 25 (2022) 102207

10−3 mg/g and 3.87 × 10−3 mg/g for reactors of the type M.1 and 6.86 × 10−4 mg/g and 4.80 × 10−3 mg/g for the
reactors of the type M.2 during the sequential processes I and II, respectively.
The Copper concentrations values are also within the parameters established by this resolution considering the density
of 1,020 kg/m3 for the sample to 3.91% m/v in both reactors (M.1 and M.2). The average concentrations ranged from 1.27
× 10−4 mg/g and 5.29 × 10−4 mg/g for the reactors of the type M.1 and 1.96 × 10−5 mg/g and 7.84 × 10−4 mg/g for the
reactors of the type M.2, during the sequential processes I and II, respectively.
The oscillations in the concentrations values of trace elements likely occur due to the configuration of the reactor, pH
values, HRT of the AD process, and temperature. In this sense, it is necessary to control the process so that the results
obtained do not exceed the limit established by the literature patterns and this CONAMA resolution established values
(Thanh et al., 2016; Bozym et al., 2015; Castro e Silva, 2018; Castro e Silva et al., 2021b).

4. Conclusions

The present study showed a significant effect of magnetite dust in the anaerobic digestion of pig dung. The higher
methane production was achieved in the reactors M.1 during the sequential process II, which resulted in an average
income of 60% of CH4 and a maximum generation of 3.82.10−2 Nm3 CH4 /kg VS .
The rates of removal of organic constituents and the volumes of biogas produced were significantly higher in the
reactors M.2, whose dosages of magnetite were higher, maybe because magnetite addition reduced the accumulation
of volatile fatty acids and accelerated the release of methane during swine slurry AD. Besides, as advocated by Xiao
et al. (2020a), DIET-acetate dismutation may be acted as an alternative mechanism for generating biomethane, broadly
stimulated by conductive carbon-based materials. In addition, the COD/BOD ratio values (which denotes a residue readily
biodegradable) less than two were achieved in the reactors M.2-process I (between 2.32 to 1.93) and reactors M.2-process
II (between 1.2 to 1.39), considering affluent and effluent analyses for both procedures. Although M.1 (process I and II)
reactors also have demonstrated good COD/BOD values, therefore, reasonable biodegradable rates, the treatment with the
lowest concentration of magnetite nanoparticles presented the highest rate of methane production because high dosages
of trace elements may inhibit the enzyme action of microorganisms active in the AD process. The optimum concentration
was achieved in our study as being 8 g. However, the highest yield of methane (Nm3 CH4 ) under the parameters kg of
the substrate, COD, BOD, ST, and VS, was obtained by applying the lowest dosage of iron ore. An increase in production
of 27% of Nm3 CH4 /kg substrate of the reactors M.1 about the average produced by M.2 was achieved.
This result is corroborated by recent studies exposed in literature but carried out in works of codigestion, in which
measurements were applied on a smaller scale. In this sense, the future studies must perform further projects involving the
application of this type of ore to optimize processes of anaerobic digestion and expand the technical and economic
feasibility of biogas plants.
Also, as a recommendation for future work, the authors endorse performing an electrochemical analysis and the
determination of divalent iron, ferric iron, and total iron to obtain a better understanding of the behavior of electrons
in the process of anaerobic digestion when using the additive of magnetite in SBRs reactors. It is also suggested that
the analysis of the production and behavior of volatile fatty acids to analyze the influence of the addition of magnetite
in anaerobic digestion for the type of reactor of low cost proposed. Finally, it is suggested that a control group without
magnetite powder should be a better choice, and this aspect should be studied in future research.

CRediT authorship contribution statement

Maxi Estefany Huamán Córdova: Data curation, Writing - original draft, Investigation. Hellen Luisa de Castro e
Silva: Data curation, Investigation. Regina Mambeli Barros: Conceptualization, Methodology, Writing - review & editing,
Formal analysis, Supervision. Electo Eduardo Silva Lora: Formal analysis, Visualization. Ivan Felipe Silva dos Santos:
Formal analysis, Investigation. João Victor Rocha de Freitas: Data curation, Investigation. Afonso Henriques Moreira
Santos: Formal analysis, Visualization. Juliano Romanzini Pedreira: Data curation, Investigation. Bárbara K. Flauzino:
Data curation, Investigation.

Declaration of competing interest

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

Funding and acknowledgments

We thank the Coordinator of the Improvement of Higher Education Personnel (Coordenaç ão de Aperfeiçoamento de
Pessoal de Nível Superior, CAPES; in Portuguese) is the given support, evidenced by Doctor of Science scholarship granted
to Ivan Felipe Silva dos Santos and Master Science Scholarships awards to Hellen Luisa de Castro e Silva and Maxi
Estefany huamán Córdoba. The authors would like to thank the Brazilian National Council for Scientific and Technological
Development (Conselho Nacional de Desenvolvimento Científico e Tecnológico, CNPq; in Portuguese), is granting productivity
11
M.E.H. Córdova, H.L. de Castro e Silva, R.M. Barros et al. Environmental Technology & Innovation 25 (2022) 102207

in research scholarship to Prof. Regina Mambeli Barros (FP2, Process number: 303805/2018-8) and to Prof. Electo Eduardo
Silva Lora. We would like to thank the Minas Gerais State Agency for Research and Development (Fundação de Amparo
à Pesquisa do Estado de Minas Gerais, FAPEMIG, in Portuguese) for granting financial support (project PROCESS N.: TEC
- APQ-03080-18, ‘‘Study of the potential of Greenhouse Gases mitigation prognostic in the state of Minas Gerais by the
electric energy generation by biogas from anaerobic digestion of organic fraction of urban solid waste and wastewater
treatment plant sludge’’).

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