Journal of Environmental Management 251 (2019) 109597

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Journal of Environmental Management

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

Research article

A state-of-the-art review on the application of nanomaterials for enhancing T

biogas production
Mona Dehhaghia,b, Tabatabaei Meisamc,d,e,∗, Mortaza Aghbashlof,∗∗,
Hamed Kazemi Shariat Panahia,b, Abdul-Sattar Nizamig
a
Department of Microbial Biotechnology, School of Biology and Centre of Excellence in Phylogeny of Living Organisms, College of Science, University of Tehran, Tehran,
Iran
b
Faculty of Medicine and Health Sciences, Macquarie University, NSW, Australia
c
Faculty of Plantation and Agrotechnology, Universiti Teknologi MARA (UiTM), 40450, Shah Alam, Selangor, Malaysia
d
Microbial Biotechnology, Agricultural Biotechnology Research Institute of Iran (ABRII), Agricultural Research, Education and Extension Organization (AREEO), Karaj,
Iran
e
Biofuel Research Team (BRTeam), Karaj, Iran
f
Department of Mechanical Engineering of Agricultural Machinery, Faculty of Agricultural Engineering and Technology, College of Agriculture and Natural Resources,
University of Tehran, Karaj, Iran
g
Center of Excellence in Environmental Studies, King Abdulaziz University, Saudi Arabia

A R T I C LE I N FO A B S T R A C T

Keywords: Anaerobic digestion (AD) of organic wastes is among the most promising approaches used for the simultaneous
Anaerobic digestion (AD) treatment of various waste streams, environment conservation, and renewable bioenergy generation (bio-
Biogas methane). Among the latest innovations investigated to enhance the overall performance of this process both
Nanoparticle qualitatively and quantitatively, the application of some nanoparticles (NPs) has attracted a great deal of at-
Mechanism of action
tention. Typically, the NPs of potential benefit to the AD process could be divided into three groups: (i) zero-
Zero-valent iron (ZVI)
Techno-economic analysis
valent iron (ZVI) NPs, (ii) metallic and metal oxides NPs, and (iii) carbon-based NPs. The present review focuses
on the latest findings reported on the application of these NPs in AD process and presents their various me-
chanisms of action leading to higher or lower biogas production rates. Among the NPs studies, ZVI NPs could be
regarded as the most promising nanomaterials for enhancing biogas production through stabilizing the AD
process as well as by stimulating the growth of beneficial microorganisms to the AD process and the enzymes
involved. Future research should focus on various attributes of NPs when used as additives in biogas production,
including facilitating mixing and pumping operations, enriching the population and diversity of beneficial mi-
croorganisms for AD, improving biogas release, and inducing the production and activity of AD-related enzymes.
The higher volume of methane-enriched biogas would be translated into higher returns on investment and could
therefore, result in further growth of the biogas production industry. Nevertheless, efforts should be devoted to
decreasing the price of NPs so that the enhanced biogas and methane production (by over 90%, compared to
control) would be more economically justified, facilitating the large-scale application of these compounds. In
addition to economic considerations, environmental issues are also regarded as major constraints which should
be addressed prior to widespread implementation of NP-augmented AD processes. More specifically, the fate of
NPs augmented in AD process should be scrutinized to ensure maximal beneficial impacts while adverse en-
vironmental/health consequences are minimized.

1. Introduction
Anaerobic digestion (AD) is a complex microbial process, in which
various organic compounds such as animal manures, agricultural re-
sidues, food industries waste, and sewage sludge are converted into
biogas (Aghbashlo et al., 2019b). The final product, i.e. biogas, con-
stitutes mainly of 60–70% methane (CH4) and 30–40% carbon dioxide
(CO2) as well as trace amounts of other gasses such as ammonia (NH3),
hydrogen (H2), hydrogen sulfide (H2S), nitrogen (N2), oxygen (O2), and
water (H2O) vapors (Alawi et al., 2009; Ganzoury and Allam, 2015;

∗
Corresponding author. Faculty of Plantation and Agrotechnology, Universiti Teknologi MARA (UiTM), 40450, Shah Alam, Selangor, Malaysia.
∗∗
Corresponding author.
E-mail addresses: meisam_tabatabaei@uitm.edu.my, meisam_tab@yahoo.com (M. Tabatabaei), maghbashlo@ut.ac.ir (M. Aghbashlo).

https://doi.org/10.1016/j.jenvman.2019.109597
Received 17 February 2019; Received in revised form 6 September 2019; Accepted 16 September 2019
0301-4797/ © 2019 Elsevier Ltd. All rights reserved.
M. Dehhaghi, et al.
Rajaeifar et al., 2019; Valijanian et al., 2018). The process consists of
four main steps to decompose organic matters into biogas in an oxygen-
free environment. In the first step, i.e. hydrolysis, large polymers such
as carbohydrate, proteins, and lipids are broken into smaller organic
molecules through the enzymatic action of bacterial communities
(Shirzad et al., 2019). The second step, i.e. acidogenesis, involves the
conversion of monomers generated in the hydrolysis step into organic
acids by acidogenic bacteria. In the third step, i.e. acetogenesis,
acetogenic bacteria produce acetic acid, CO2, and H2 from the products
of the acidogenic step (Tabatabaei et al., 2019b). This step requires low
partial hydrogen pressures to support the growth and metabolism of
acetogenic bacteria. The last step is methanogenesis in which acetic
acid, CO2, and H2 are converted into methane by the aid of acetoclastic
and hydrogenotrophic methanogens, belonging to archaea (Angelidaki
et al., 2018; Ghodrat et al., 2018; Tabatabaei et al., 2019b). Indeed,
acetic acid and H2 are two of the most significant intermediates acting
as substrates for methanogenic archaea during the methanogenic as-
similation of organic matters (Conrad, 1999). It should also be noted
that the simultaneous synthesis of H2 by syntrophic and fermenting
bacteria and its consumption by methanogenic archaea determine H2
concentration. Moreover, a Gibbs free energy of −23 kJ/mol CH4 is
required for coupling the generation of 1/3 ATP to that of CH4. Below
this threshold, the production rate of methane would be decreased or
even inhibited, and hydrogen could be, for instance, channeled into
completing pathways such as sulfate reduction (Conrad, 1999). A flow
diagram of a typical AD process is illustrated in Fig. 1.
AD is, in fact, a sustainable method not only to protect the en-
vironment from wastes but also to produce biogas as renewable energy
(Barati et al., 2017; Tabatabaei et al., 2019c). Moreover, the digestate
produced upon the completion of the AD process, which is mainly a
mixture of solid and liquid substances, can be applied as a high-quality
fertilizer to enrich agricultural lands with low organic matters
(Aghbashlo et al., 2019a; Rajaeifar et al., 2017). Straight biogas re-
quires a simple economically-viable purification (H2S < 500 ppm, no
moisture content, no limitation for CO2) and could be used to generate
power (electricity and heat) in combined heat and power plants for use
in urban and rural areas, as adapted by many countries (Shirzad et al.,
2019; Tabatabaei et al., 2019c). The price of electricity generated
through AD depends on the feedstock, technology and equipment in-
volved, size of plant, by-products, as well as managements and policies
implemented (Gebrezgabher et al., 2010; Oreggioni et al., 2017;
Shirzad et al., 2019). Typically and despite its lower electricity pro-
duction cost vs. some other techniques such as solar, wind, and hy-
drothermal gasification, the current AD process is not an economically
viable process for green energy production unless its other benefits, for
example, mineral fertilizers substitution, bioremediation of inorganic
(to some extent) and organic pollution, wastewater treatment, and
greenhouse gases mitigation are completely exploited as well (Shirzad
et al., 2019; Thi et al., 2016). It should be noted that raw biogas could
also be biologically upgraded into more advanced fuels such as
Fig. 1. Anaerobic digestion process. 1–4: fermentative bacteria, 5: acetogens
(H2 producing), 6: acetogens (H2 consuming), 7: acetoclastic methanogens, and
8: CO2 reducing methanogens.
2
Journal of Environmental Management 251 (2019) 109597
methanol (Kazemi Shariat Panahi et al., 2019c). Through this strategy,
the major step of conventional biogas purification, i.e., H2S removal
would no longer be required leading to saving of approximately USD
0.38/m3 CH4 (Kazemi Shariat Panahi et al., 2019c). Given the various
advantages of waste-oriented biogas production, a great deal of re-
search is focused on further advancing this field by introducing a wide
range of innovative approaches.
Along with different recently-introduced innovations such as biogas
production under integrated biofuels production schemes (i.e., bior-
efinery concept), bioaugmentation, anaerobic co-digestion, etc. (Kazemi
Shariat Panahi et al., 2019b,c,d; Tabatabaei et al., 2019b,c),The ap-
plication of nanoparticles (NPs) is also receiving increasing attention
due to their remarkable properties such as extremely small size, variety
in morphology, high reactivity, and chemical stability (Rahimzadeh
et al., 2018; Sekoai et al., 2019; Tabatabaei et al., 2019c). Additionally,
NPs have high surface area to volume ratios increasing the number of
active sites available, an essential attribute for proceeding reactions of
different types. For instance, NPs can facilitate hydrolysis processes by
providing a large surface area to volume ratio for microorganisms to
attach the active sites of organic molecules (Hsieh et al., 2016). Alter-
natively, NPs could also function as electron donors/acceptors and
cofactor of important enzymes involved in various bioprocesses en-
hancing their yields.
The term nanotechnology first coined by Richard Feynman in his
1959 talk at the American Physical Society meeting (Feynman, 1959).
In the following years, a rolled up sheet of carbon in tubular structure,
called Fullerences/Buckyballs, was discovered. Twenty one years after
the Feynman's famous talk about nanotechnology, Eric Drexler pub-
lished probably the first scientific paper dealing with molecular en-
gineering (Drexler, 1981). In 1986, he published an influential book
introducing fundamentals of nanotechnology (Eric, 1986). Intriguingly,
Drexler was the first teacher presenting a formal course on nano-
technology in 1988 and was the first student who received a PhD in
molecular nanotechnology in 1991 as well. Nanotechnology could be
defined as research and development at the atomic scale of 1–100 nm
for measuring and manipulating matters to obtain fundamentally dif-
ferent chemical, physical, and biological characteristics, compared to
their corresponding bulk materials.
Despite huge efforts devoted to the application of nanoparticles in
different fields including remediation of various pollution from soil and
water (Chowdhury and Yanful, 2010; Jorfi et al., 2016; Vitela-
Rodriguez and Rangel-Mendez, 2013), its potential application in
biogas industry has remained largely unattended. In one of the first
study, Scott (2006) described the general potentials of unmentioned
NPs for enhancing biogas production from animal manures. However, it
was only in 2011 that the impact of particle size of some metal oxide
(CuO, ZnO) on methane and biogas production in AD process was
evaluated for the first time (Luna-delRisco et al., 2011). In the sub-
sequent year, researchers noticed the accumulation of NPs in municipal
wastes due to increasing applications of these compounds in various
industries. This triggered investigations into the potential effects of
various metallic and metal oxide NPs on AD of municipal sludge in the
same year. Preliminary investigations showed that, at certain con-
centrations, some NPs (e.g., Ag and TiO2) exert no harmful effects on AD
process with respect to methane and biogas productions, as well on the
microorganisms population involved in AD and their diversity whereas
others (Au, CeO2) could negatively impact this process (García et al.,
2012; Yang et al., 2012a, 2012b). The study of the impacts of NPs on
AD continued in following years and some other NPs (such as ZVI, CuO,
ZnO, CeO2, Cu0, TiO2) were also investigated (Carpenter et al., 2015;
Eduok, 2015; Gonzalez-Estrella et al., 2015; Nguyen et al., 2015; Otero-
Gonzalez et al., 2014b; Yang et al., 2013a, 2013b; Zheng et al., 2015).
In light of the above, this review presents the state-of-the-art of the
application of various nanomaterials used to enhance/improve biogas
production via AD process with a focus on the studies conducted most
recently. NPs covered in the present review are categorized into three
M. Dehhaghi, et al. Journal of Environmental Management 251 (2019) 109597

Fig. 2. Effects of ZVI NPs on biogas production during AD process.

subclasses; (i) zero-valent metal NPs, (ii) metallic and metal oxides NPs, through enriching organic load i.e., disrupting the cell membrane of the
and (iii) carbon-based NPs. Techno-economic and environmental ana- other microorganisms that are comparatively more susceptible. This
lysis of NPs on biogas production along with practical implications of lysis phenomenon leads to the release of a considerable deal of proteins
this study is discussed in detail. and celluloses, further stimulating the growth of hydrolyzing-acidifying
populations (Wang et al., 2018). From the mechanism point of view, the
disruption of the membranes is due to the direct interaction of ZVI NPs
2. Effect of nanoparticles (NPs) on biogas production
with microbial cells rendering reductive decomposition of functional
groups in lipopolysaccharides and proteins of the outer membranes
2.1. Zero-valent iron NPs/nano zero-valent iron
(Wang et al., 2018). However, it should be noted that higher con-
centrations of Fe2+ could also inhibit the methanogenesis probably
Zero-valent Iron (ZVI) NPs have been characterized as a proper low-
through a similar mechanism i.e., disruption of cell integrity. This could
release electron donor (i.e., Fe2+) during the methanogenesis process
justify the conflicting results obtained in some studies (lacking anae-
leading to enhanced biogas production yields (Ma et al., 2015). These
robic granular sludge, AGS) with lower methane production in response
NPs could also participate in the synthesis of microbial key enzymes
to the application of ≥1 mM ZVI NPs (Cerri et al., 2017; Wang et al.,
that are essential for the AD process (Fig. 2). For example, the activity
2016; Yang et al., 2013a).
of coenzyme F420 increases in the presence of ZVI NPs, because Fe2+ is
In addition to the above, the dissolution of ZVI NPs in water releases
an essential part of this coenzyme (Ma et al., 2015). Similarly, in a
H2 (Huang et al., 2016). This phenomenon may exert negative or po-
different study (Wang et al., 2016) the addition of 10 mg ZVI NPs/g
sitive effects on methane production yield by enriching hydro-
total suspended solids enhanced methane production by up to 120%
genotrophic bacteria or acting as an electron donor for hydro-
during a 30-d fermentation process as compared to the control
genotrophic archaea for methane production, respectively (Cerri et al.,
(180.96 mL/g volatile suspended solids, VSS).
2017; Yang et al., 2013a) (Fig. 2). More specifically, rapid H2 release
It has been reported that ZVI NPs were capable of optimizing the
decreases methane production whereas its slow release improves its
microbial population and consequently, enhancing hydrolysis fermen-
production (Cerri et al., 2017; Yang et al., 2013a). Intriguingly, the
tation (Ganzoury and Allam, 2015) (Fig. 2). More specifically, the
presence of extracellular polymeric substances (EPS) in the substrate
strong reductant property of iron could facilitate hydrolysis-acidifica-
could improve methane production through inhibition of H2 generation
tion steps; the rate-limiting steps throughout AD (Ganzoury and Allam,
as well as through protecting microorganisms against toxicity (Cerri
2015). In better words, at certain concentrations, ZVI NPs act in favor of
et al., 2017).
the microorganisms responsible for hydrolysis-acidification processes

3
M. Dehhaghi, et al.
Enhancement of biogas production in the presence of ZVI NPs could
also be attributed to their influence on the physical and chemical
properties of the environment surrounding methanogenic microorgan-
isms by controlling pH, ammonia nitrogen concentration, and volatile
fatty acids content (Fig. 2). The impacts exerted through pH mod-
ification could be ascribed to the oxidation of Fe0 to Fe2+ by water or
some organic compounds as an oxidant during the AD process gen-
erating iron oxide or covering the surface of NPs by oxyhydroxide (Li
et al., 2007; Suanon et al., 2017). It should be noted that iron oxide and
oxyhydroxide could also be produced through reaction of ZVI NPs with
some other compounds present in the AD process including chlorinated
pesticides, H2S, toxic metal ions (such as lead and mercury), and methyl
sulfides (Li et al., 2007). These could donate an additional buffering
capacity to the system against volatile fatty acids produced. ZVI NPs
could also stimulate hydrogen-consuming microorganisms and the
consumption of the produced volatile fatty acids (Suanon et al., 2017).
Moreover, there is an inverse relationship between the amount of am-
monia nitrogen and pH value in AD (Suanon et al., 2017). It is worth
mentioning that ammonia nitrogen could be adsorbed by the oxy-
hydroxide generated in the presence of ZVI NPs (Suanon et al., 2017).
On this basis, Jia et al. (2017) added various concentrations of ZVI NPs
(1–4 g/L) with average diameter sizes of 50–70 nm to biogas production
reactors. Optimum performance parameters such as biogas production
volume (> 600 mL), methane content (68.75%), and ammonia nitrogen
(< 600 mg/L) were associated with 1 g/L ZVI NPs. The authors con-
cluded that cumulative (35 d) biogas production and methane content
were respectively enhanced by 18.11% and 6.93% in the presence of
ZVI NPs in comparison with the control (biogas, ~500 mL; methane
content, ~61%).
ZVI NPs can lower H2S content through the formation of nonvolatile
and stable superficial complexes and could, therefore, improve the
quality and quantity of the biogas produced (Li et al., 2007). The me-
chanism of removal include, for instance, impacts of ZVI NPs on AD of
sewage sludge, methane production, and COD under mesophilic tem-
perature (Suanon et al., 2017). The presence of ZVI NPs (0.1 wt%) re-
spectively enhanced COD removal, methane production, and methane
content by 17.8%, 25.2%, and 3.1%, improving the control values for
the mentioned parameters from 44.6% (2968 mg/L), 8563.9 mL/kg
VSS, and about 70.3%–54.4% (3618.9 mg/L), 9108.2 mL/kg VSS, and
73.4% within 30 d of AD process (Suanon et al., 2017). In their study,
ZVI NPs were also used to treat high-concentration (10,000 ppm) H2S
biogas in a fixed-bed reactor. The H2S removal capacity of ZVI NPs was
recorded at 12.56 and 14.77 mg H2S/g ZVI NPs at room temperature
and 100 °C, respectively. The capacity was significantly increased to
391.02 and 488.95 mg H2S/g ZVI NPs at elevated temperatures of
200 °C and 250 °C, respectively. It is worth mentioning that the removal
of impurities such as CO, H2S, and NH3 from biogas is critical in im-
proving the economic profitability of the process by both increasing the
quality of the biogas generated and by protecting the equipment from
corrosion (Achinas et al., 2017; Sahota et al., 2018).
Compared to floc sludge, AGS plays a critical function in AD systems
(Cerri et al., 2017). These granules have a three-layered structure: (i)
the outer layer that is highly heterogeneous, consisting of hydro-
genotrophic methanogens archaea, as well as syntrophic and fermen-
tative eubacteria; (ii) the middle layer with lower heterogeneity than
the outer layer; and (iii) the internal core consisting of large popula-
tions of Methanothrix-like cells (Cerri et al., 2017). Cerri et al. (2017)
investigated the effect of ZVI NPs on the stability of AGS, fate, and
distribution of Fe2+, and modification of microbial diversity. They
achieved 30% more methane production by enriching the reaction
mixture with 30 mmol/L ZVI NPs. At this concentration, insignificant
increases in chemical oxygen demand (COD) revealed that granular
sludge cells were not completely disrupted when they came into direct
contact with ZVI NPs. Microscopic analysis of iron particles distribution
in sludge also showed that ZVI NPs have mostly attached on the AGS
surface as well as EPS in the form of iron oxides, rather than entering
4
Journal of Environmental Management 251 (2019) 109597
into its inner side. This behavior could protect methanogens against the
toxic effects of ZVI NPs. Interestingly, in the same study, it was found
that ZVI NPs could significantly enrich phylum Thermotogae and genera
Methanobacterium while discouraging the growth of Chloroflexi and
class Methanomicrobia. The increase in Methanobacteria was due to the
availability of higher amounts of H2 triggered by the decreased popu-
lation of Chloroflexi (disruption of the cell membrane) in the presence of
ZVI NPs (Krakat et al., 2011). Increases in the abundance of Actino-
bacteria, Bacteroidetes, Firmicutes, and Proteobacteria in the presence
of ZVI NPs were also observed by Wang et al. (2018).
2.2. Metallic and metal oxide NPs
Some trace metal elements such as Co, Cu, Fe, Mo, and Ni could play
significant roles in stimulation as well as stabilization of AD of waste
organic materials when they are present at low concentrations
(Abdelsalam et al., 2016; Luna-delRisco et al., 2011). In fact, the pre-
sence of these heavy metal ions is essential for enzymes and cofactors
and is fundamental for various reactions taking place during AD. More
specifically, cobalt is essential (as protein cofactor of vitamin B12) for
degradation of methanol by methanogenic bacteria whereas methano-
genic archaea need nickel as their coenzyme F430 (Roussel, 2013). Zinc
plays key roles in enzymes (e.g., as methyl coenzyme M) and as struc-
tural ions in transesterification factor while copper is essential for
coenzyme and biological electron transport (Bartacek et al., 2008;
Fermoso et al., 2008; Metcalf, 2003). Finally, Fe is required for proper
growth and activities of AD microorganisms by acting as oxidation-re-
duction agent, co-enzyme, and terminal electron acceptor (Roussel,
2013). Therefore, given the unique properties of nanomaterials, the
application of these elements in nano range size has attracted a great
deal of attention. For instance, Abdelsalam et al. (2016) studied the
effect of Co and Ni NPs on AD of cattle dung slurry in a batch system.
Compared to the control (biogas, 26.7 L; methane, 13 L), the treatment
of feedstock with Co (1 mg/L), Fe (20 mg/L), Fe3O4 (20 mg/L), and Ni
(2 mg/L) NPs increased both cumulative biogas production (1.7, 1.5,
1.7, and 1.8 times, respectively) and methane production (2, 1.67, 2.16,
and 1.86 and 2.17 times, respectively) through 40 d hydraulic retention
time. Moreover, the addition of these NPs reduced the lag phase time
required to reach the production peak of biogas and methane.
Ali et al. (2017) studied the impact of Fe3O4 NPs on AD of municipal
solid waste under the mesophilic condition for 60 d of reaction time at
different concentrations (50–125 mg/L) and particle sizes (15–22 nm).
The maximum yield of methane (5000 mL) was obtained at 75 mg/L of
NPs whereas any further increases in the concentration of NPs reduced
methane production. In another study, Noonari et al. (2018) reported a
relatively similar concentration of magnetic Fe3O4 NPs (81 mg/L) for
optimum methane production (256.0 mLCH4/gVS) through co-diges-
tion of canola straw and banana waste plant with buffalo dung under
mesophilic conditions for 40 d. Chen et al. (2018) examined the role of
Fe3O4 NPs as iron releasing agent on the growth of methanogen Me-
thanosarcina barkeri. The tubes containing Difco Sporulation Medium
120 medium was supplemented with 0–20 ppm of Fe3O4 NPs (with a
mean size of 8.1 ± 2.4 nm) and degassed using deoxygenized gas
pressure injector before inoculation of M. barkeri. The amount of Fe2+
released from 20 ppm Fe3O4 during the first 6 h was 10 μM and kept
gradually increasing. Methane production in the presence of NPs sig-
nificantly increased (up to 60%) as compared to the control of iron-free
medium. The authors also claimed that the addition of methanol (as a
substrate) had an immediate and synergistic effect on the rate of me-
thane production, compared to the medium supplemented with Fe3O4
NPs alone. This could be ascribed to the increasing number of metha-
nogens in the last step in response to the addition of a readily available
substrate like methanol to an enzymatically active environment caused
by Fe3O4 NPs.
Overall, these improvements in biogas production could be due to
the vital effect of metal ions (such as Fe2+ and Fe3+) on the growth of
M. Dehhaghi, et al.
Fig. 3. Effects of metallic and metal NPs on biogas production during AD process.
anaerobic microbial populations as well as decreasing the lag time in
AD process (Fig. 3). On the other hand, the application of Fe3O4 NPs
could facilitate direct interspecies electron transfer during the syn-
trophic methanogensis (Ali et al., 2017) (Fig. 3). In contrast, it should
be noted that these metal oxides could also inhibit methanogenesis by
mainly acting on acetoclastic methanogens at elevated concentrations
(Otero-Gonzalez et al., 2014a). For example, CuO and Fe2O3 NPs re-
portedly led to decreased methane production by suppressing acet-
oclastic methanogenes and H2-consuming methanogens, respectively.
High concentrations of both CeO2 and Mn2O3 NPs have been associated
with the inhibition of both groups of methanogens (Otero-Gonzalez
et al., 2014a).
Contrary to the above-mentioned metallic and metal oxide NPs that
have been shown to exert positive impacts at certain concentrations,
NPs containing Cr, Cd, and Zn have been associated with interference
with biogas production (Fig. 3). These metal species could inhibit or kill
microorganisms involved in AD and could, therefore, suppress the
whole process. The cellular mechanisms may be through adverse
modification of membrane properties of microorganisms and/or sti-
mulation of oxidative stress (Hamedi et al., 2015; Yang et al., 2013b).
The latter route is less common in AD as metal oxides need either
oxygen or illumination to produce reactive oxygen species. Temizel
et al. (2017) investigated the long-term effect of nano-ZnO (100 mg/kg
of dry waste) on the digestion of municipal solid waste in both con-
ventional and bioreactor manners. Up to 15% reduction in biogas
production in the presence of ZnO in both conventional and bioreactor
modes were observed probably due to the inhibitory effect of ZnO on
methanogenic microorganisms. Moreover, approximately 99% of the
ZnO could persist in the waste matrix for a long-term period with still
unclear fate and impact on the environment. In another study by Mu
et al. (2011), it was concluded that the inhibitory effect of ZnO NPs on
biogas production was concentration dependent with 6 mg/g-total
suspended solids not influence methane production. The activity of
coenzymes F420 dropped to 66.2%, 89.8%, and 99.3% of the control in
the presence 150, 30, and 1 mg ZnO NPs/g total suspended solids, re-
spectively (Mu et al., 2011). It has also been shown that ZnO had no
considerable improving effect on solubilization and acidification steps
5
Journal of Environmental Management 251 (2019) 109597
(Mu et al., 2012).
The long-term effect of CuO NPs (37 nm, 1.4 mg/L, 43 d) on AD of
AGS was studied by Otero-Gonzalez et al. (2014b). Based on the results
obtained, methane production was reduced to 85% of the control in the
presence of CuO NPs mainly due to the inhibition of acetoclastic me-
thanogens rather than H2-consuming methanogens, a similar me-
chanism observed during biogas reduction by ZnO NPs (Otero-Gonzalez
et al., 2014a, b). The negative impacts of both of NPs mentioned above
(i.e., CuO, ZnO) on methane production were also reported by Luna-
delRisco et al. (2011), highlighting their toxic effects on anaerobic
microbes involved in the AD process. In their study, the application of
120 mg/L of CuO or ZnO significantly reduced biogas production in a
14-d AD process at 36 °C. Although the study emphasized that the
adaptation of microorganisms to these NPs and/or removal of the NPs
from the medium, for example, by microbial bioremediation/bioad-
sorption led to some improvements over the last days of the experiment.
The impact of NPs on AD highly depends on their size as well. More
specifically, smaller-sized NPs are reportedly more favorable (Nel et al.,
2006). The existing literature has proved enhancement of biogas pro-
duction and methane content in the presence of metallic and metal
oxides NPs such as Ni, Co, Fe, Fe3O4, Fe2O3, MgO, and Al2O3, however,
there are reports highlighting the inhibitory effect of NPs such as ZnO
and TiO2 on the biogas production process when used at higher con-
centrations.
2.3. Carbon-based nanomaterials
All nanocompounds with carbon atoms in their structures are con-
sidered as carbon-based nanomaterials. These compounds are classified
mainly based on their geometrical structure. Carbon nanotubes (CNTs),
graphene, and fullerenes are the most significant carbon nanomaterials
of various industrial applications (Zaytseva and Neumann, 2016).
Among the carbon-based nanomaterials, CNTs have been introduced
into a wide range of applications due to their remarkable thermal,
mechanical, electronic, and adsorption features (Rahimzadeh et al.,
2018; Shojaei et al., 2019; Zaytseva and Neumann, 2016). Similarly,
their potential applications in renewable energy and biogas production
M. Dehhaghi, et al.
have also been investigated recently (Ambuchi et al., 2016;
Rahimzadeh et al., 2018; Wang et al., 2018). Nevertheless, there are
still no accurate information on the risks associated with their release
into the environment and their interactions with the living organisms.
Single-wall carbon nanotubes (SWCNTs) could facilitate direct in-
terspecies electron transfer (DIET) during the AD process. Compared to
the control, the rates of feedstock consumption and methane produc-
tion were speeded up in response to the addition of SWCNTs but me-
thane production yield remained unchanged (~14 mL after 180 h) (Li
et al., 2015). In fact, DIET allows microorganisms to directly exchange
electrons apart from formate or hydrogen transfer (Ambuchi et al.,
2017; Yan et al., 2017). In light of that, materials with electrical con-
duction (such as SWCNTs) could serve as conduits between electron-
accepting and electron-donating microbes (i.e., exoelectrogenic bacteria
and methanogenic archaea) during the DIET process (Li et al., 2015;
Park et al., 2018). Intriguingly, methane production is more efficiently
promoted in the presence of conductive materials allowing DIET than
H2 or other electron carriers consumed as interspecies electron transfer
(Park et al., 2018).
Another electrically conductive material is multi-wall carbon na-
notube (MWCNT) that could enhance biogas and methane production
rates by transferring electrons toward methanogens (Ambuchi et al.,
2017). Generally, CNTs could noticeably enrich electroactive bacteria
such as Caloramator sp. or Geobacter sp. along with other bacteria or
methanogenic archaea (Methanosarcina, Methanosaeta, etc.) (Ambuchi
et al., 2017; Yan et al., 2017). For example, MWCNTs could enrich
bacterial community and growth with the two of the top largest phyla
affected the most, i.e., Bacteroidetes (11.2%) and Firmicutes (8.4%)
(Ambuchi et al., 2017). Ambuchi et al. (2016) studied the effect of
MWCNTs on the AD of granular sludge obtained from the beer industry
under the mesophilic condition for 96 h. The results showed that after
the termination of the experimental period, the cumulative CH4 pro-
duction was higher in the presence of 1500 mg/L of MWCNTs as
compared to the control (151.8 vs. 106 mL/g volatile-suspended solids).
Scanning electron microscopy (SEM) revealed that the sludge granules
sampled from the bioreactor treated with MWCNTs had a denser ag-
gregation of microorganisms due to a probable interaction between
MWCNTs, microbes, and microbial EPS. In a more recent study, Wang
et al. (2018) studied the long-term effect of MWCNTs on the activity
and structure of the microbial community in AGS for 110 d. Although
MWCNTs did not show a significant influence on biogas production and
COD reduction, it increased the removal of total phosphorus by
29.34%. 16 S rRNA gene sequencing indicated that MWCNTs had no
effect on microbial diversity but changed the composition and structure
of microorganisms. For example, in the presence of MWCNTs, Sac-
charibacteria replaced Proteobacteria suggesting the probable adverse
effect of MWCNTs on specific microbial populations.
The ash-based nanomaterial is another choice of carbon-based ad-
ditives for enhancing biogas production. Lo et al. (2012) obtained
micro/nano fly ash and micro/nano bottom ash from a municipal solid
waste incinerator and applied them for enhancing biogas production. A
considerable increase in biogas production was observed in the pre-
sence of different concentrations of these ashes during a 90-d AD at
35 °C. This observation could be attributed to the expanding habitats of
anaerobic microorganisms caused by the agglomeration nature of these
nano-compounds (Lo et al., 2012). The long-term application of full-
erene (C60) NPs was shown to have no improving effects on biogas
production (Nyberg et al., 2008).
A summary of the effects of different NPs on the biogas production
process is presented in Table 1.
6
Journal of Environmental Management 251 (2019) 109597
3. Techno-economic and environmental analysis of NPs on biogas
production
3.1. Techno-economic analysis of NPs on biogas production
The application of NPs is generally beneficial in terms of accurate
dosing of ions capable of enhancing AD process leading to higher biogas
production. However, the large-scale application of NPs could trigger
some concerns (Gottschalk et al., 2013). More specifically, apart from
the cost involved, such large-scale applications could raise environ-
mental and health-related complications. Unfortunately, these compli-
cations of NPs such as ZVI NPs in the AD process and biogas production
have not been yet considered in detail. In fact, there are currently no
universal and effective guidelines available in the field of NPs-enhanced
AD processes at an industrial scale (see Section 3.3). The establishment
of such guidelines could facilitate the application of these beneficial
additives to enhance the conversion of various organic materials in-
cluding waste streams into biogas via AD process. These guidelines
should also encompass environmental, economic, and technical (e.g.,
preventing inhibitory effects) aspects of NPs applications.
If the constraints mentioned above were overcome, among the NPs
investigated so far, the most promising NPs for enhancing biogas pro-
duction would be ZVI NPs. In fact, they could directly or indirectly
render positive effects on biogas-producing microorganisms during the
AD process when applied at appropriate concentrations. In summary,
their mechanisms of action may be through (i) low release of Fe ions,
(ii) direct interaction with membranes of susceptible non-biogas pro-
ducing microorganisms, (iii) release of H2, and (iv) improving the
physicochemical characteristics of the AD environment. As mentioned
earlier, Fe2+ is an essential trace element for both microorganisms
growth involved in the AD as well as for their enzymes activity. In fact,
AD-related microorganisms are capable of tolerating somewhat higher
concentrations of Fe2+ and ZVI NPs than the AD-contaminating mi-
croorganisms. As a result of the degradation of non-favorable micro-
organisms, more nutrients (proteins, cellulose) are provided for biogas
formation, and the microbial population is also regulated. Moreover,
this process leads to optimization of microbial diversity as well as
modification of hydrolysis fermentation. Slow release of H2 could po-
sitively contribute to methane production by acting as an electron
donor for hydrogenotrophic methanogens. As elaborated earlier, com-
pounds such as ammonia nitrogen, H2S, heavy metals, volatile fatty
acids on the one hand and pH, on the other hand, exert direct effects on
biogas production. At specific concentrations, ZVI NPs is capable of
adsorbing and remediating some of these compounds, decrease their
production, and/or increase their degradation. It can also act as a good
buffering agent maintaining pH within a suitable range for AD-related
microorganisms.
From the techno-economic point of view, NPs can be synthesized
from readily available chemicals with minimum infrastructure (Faisal
et al., 2019). The technology involved in NPs production is also well-
known but their impacts on biogas production during AD process still
need further assessments. The concentration, time of addition, and
particle size determine the effects of NPs, i.e., inhibition, enhancement,
etc. on this process (Faisal et al., 2019). Generally, smaller particle size
and higher surface area to volume increase the effects of NPs. AD
process coupled with appropriate NPs dosing, type, and addition time
could assist with achieving an enhanced biogas production process.
Case study. In order to understand the potential economic impacts
of NPs augmentation during the AD process, a case study was designed
according to the data available in the literature. More specifically, the
techno-economic analysis of two mesophilic (20–40 °C, optimum at
35 °C) farm-scale (i.e., 3670 m3) AD scenarios for combined heat and
power energy (CHP) generation was considered. One scenario included
conventional biogas production from biomass (agricultural residues),
manure, glycerol defined as BMG scenario without no NPs addition,
whereas the other scenario involved NPs (ZVI) augmentation under
 Table 1
A summary of the effects of NPs on the biogas production process.
Nanoparticle type Concentration of NP Feedstock Reaction time Biogas/Methane yield (compared to control) Reference(s)
M. Dehhaghi, et al.

ZVI NPs
ZVI NPs 15 and 30 mmol/L Granular sludge 250 h 7.45 mmol CH4 at 30 mmol/L ZVI NPS (Control: 5.74 mmol CH4) Cerri et al. (2017)
1.1 g VSS/L
ZVI NPs 10 and 30 mM Municipal sludge 14 d 98 mL methane volume at 10 mM NPs (−20.3%) Yang et al. (2013b)
38 mL methane volume at 30 mM NPs (−69%)
(Control methane volume of 123 mL)
ZVI NPs 0.10 wt% Municipal sludge 17 d 5.1–13.2% methane content improvement Su et al. (2013)
22.2 L cumulative biogas volume (+30.4%)
13.7 L cumulative methane volume (+40.4%)
(Respective control cumulative biogas and methane volumes of
15.46 L and 8.16 L)
cZVI NPs 2.5 and 5 g/L Brewery wastewater 10 d 182 mL methane production (+28%) Carpenter et al. (2015)
(Control methane production of 142.19 mL)
ZVI NPs 10 mg/g total suspended solids Municipal sludge 30 d 217.16 mL/VSS methane production (+120%) Wang et al. (2016)
(Control methane production of 180.97 mL/VSS)
ZVI NPs 1000 mg/L Municipal sludge 35 d 6.93% methane content improvement Jia et al. (2017)
> 600 mL of biogas volume (+18.11%)
(Control: 500 mL of biogas; 61% methane content)
ZVI NPs 0.1 wt% Municipal sludge 30 d +3.1% methane content improvement Suanon et al. (2017)
9108.2 mL/kg VSS methane production
(Control methane production of 8563.9 mL/kg VSS)
ZVI NPs, IMZ, ICZ 500 and 1000 mg/L Domestic sludge 14 d > 800 mL of biogas at ICZ 1000 mg/L Amen et al. (2017)
TS: 1.64%; VS: 74.9%; COD: > 700 mL of biogas at ZVI NPS 1000 mg/L
3873 mg/L > 600 mL of biogas at IMZ 500 mg/L
(Control biogas volume of < 150 mL)

7
Copper iron-based bimetallic (ZVI 100, 250, 500, 1500 and 3000 mg/L Municipal sludge 14 d 693 mL of biogas at 1500 mg/L NPs (+202.62%) Amen et al. (2018)
NPs/Cu°) TS: 4.22%; OC: 72.8%; COD: (Control biogas volume of 229 mL)
5453 mg/L
ZVI NPs 100, 250, 500, 1500 and 3000 mg/L Municipal sludge 14 d 477 mL of biogas at 3000 mg/L (+208.29) Amen et al. (2018)
TS: 4.22%; OC: 72.8%; COD: (Control biogas volume of 229 mL)
5453 mg/L
Metal and metal oxide NPs
Ag Up to 40 mg/L Municipal sludge 20–30 d No significant effect (184 mL of methane and ~400 mL of biogas) Yang et al. (2012a)
(Control biogas and methane volumes of ~400 mL and < 190 mL,
respectively)
Ag 10 mg/kg Municipal solid waste 200 d 27.2 L of methane volume (−80%) Yang et al. (2013a)
(Control methane volume of ~120.2 L)
Ag NM Cellulose 50 d No significant effect (~380 mL/g VSS of biogas) García et al. (2012)
(Control biogas volume of ~390 mL/g VSS)
CeO2 10 mg/L Municipal sludge 40 d ~1800 mL of biogas volume (11%) Nguyen et al. (2015)
(Control biogas volume of ~1600 mL)
CeO2 NM Cellulose 50 d ~40 mL/g VSS of biogas volume (−90%) García et al. (2012)
(Control biogas volume of ~390 mL/g VSS)
TiO2 NM Cellulose 50 d ~430 mL/g VSS of biogas volume (+10%) García et al. (2012)
(Control biogas volume of ~390 mL/g VSS)
CuO 1.4 mg Cu/L Municipal wastewater 107 d > -50% in methane (Otero-Gonzalez et al., 2014b)
CuO 10.7 mg Cattle manure 14 d −50% in methane Luna-delRisco et al. (2011)
Co, Ni, Fe, Fe3O4 Co: 1 mg/L; Ni: 2 mg/L; Fe and Fe3O4: Livestock manure 45 d Ni: 658 mL of biogas (Abdelsalam et al., 2016; Cerri
20 mg/L TS: 14.8%; VS: 11.67%; OC: Co: 596 mL of biogas et al., 2017)
47.7% Fe: 580 mL of biogas
Fe3O4: 633.3 mL of biogas
Control: 159.3 mL of biogas
Fe2O3 100 mg/g TSS Waste sludge 36 d 212.43 mL/g VSS of CH4 (117%) (Amen et al., 2017; Wang et al.,
2016)
(continued on next page)
Journal of Environmental Management 251 (2019) 109597
 Table 1 (continued)

Nanoparticle type Concentration of NP Feedstock Reaction time Biogas/Methane yield (compared to control) Reference(s)

Fe3O4 50, 75, 100, and 125 mg/L Municipal solid waste 60 d > 5000 mL of CH4 at 75 mg/L NPs (Ali et al., 2017; Amen et al., 2018)
M. Dehhaghi, et al.

TS: 31%; VS: 29.3%; OC: 54.7%

Fe3O4 0.4, 0.5, 0.81, 1.22 and 1.63 mg Canola straw: 40 d 256 mL/g VSS of CH4 at 0.81 mg of NP from canola straw (Control: Noonari et al. (2018)
155 mL of CH4)
TS: 93%; VS: 83.1%; OC: 44% 202.3 mL/g VSS of CH4 at 0.5 mg NP from banana plant wastes
Banana plant wastes: (Control: 135.5 mL of CH4)
TS: 92.1%; VS: 84%; OC: 39.9%
Fe2O3 750 mg/L Granular sludge 74 d 25.1 L/g VSS of biogas (control: 20.1 L/g VSS) (Ambuchi et al., 2017; Amen et al.,
0.879 g VSS/L 8.4 L/g VSS of CH4(control: 6.5 L/g VSS) 2018)
Fe3O4, NiO, Co3O4, MoO3 – Cattle manure slurry 20 d Fe3O4: 731 mL of biogas; NiO: 752 mL of biogas; Co3O4: 672 mL of Juntupally et al. (2017)
biogas; MoO3: 662 mL of biogas
TS: 19%; VS: 80%; OC: 14% (Control: 492 mL of biogas)
ZnO 500 and 1000 mg/L Municipal sludge 40 d ~1500 mL of biogas volume at 500 mg/L NPs (−8.4%) Nguyen et al. (2015)
~560 mL of biogas volume at 1000 mg/L NPs (−65.3%)
(Control biogas volume of ~1600 mL)
ZnO 15–60 mg/kg Municipal solid waste and cow 60 d −110-(−)430% lower biogas Eduok (2015)
dung
ZnO 100 mg/kg dry waste Municipal solid waste 300 d Bioreactor: 1392 L of biogas (control: 1665 L of biogas) Temizel et al. (2017)
OW: 52% Conventional reactor: 1765 L of biogas (control: 1970 L of biogas)
Al2O3 5, 50, 150, 250, 500, 750 and 1000 Waste sludge 48 d 14.8% increase in CH4 at 250 mg/gTS of NP Unsar and Perendeci (2018)
mg/gTS TS: 182.6 g/kg
VS: 124.8 g/kg
TiO2 30–150 mg/g TSS Municipal sludge 105 d No significant effect Zheng et al. (2015)
Carbon-based nanomaterials
MWCNTs 1500 mg/L Granular sludge 96 h 151.8 mL/g VSS of CH4 (control: 106 mL/g VSS of CH4) Ambuchi et al. (2016)

8
TS: total solids; VS: volatile solids; OC: organic carbon content; TSS: total suspension solids; VSS: volatile-suspended solids; OW: organic waste; IMZ: ZVI NPS and zeolite mixture; ICZ: ZVI NPS coated zeolite.
Journal of Environmental Management 251 (2019) 109597
M. Dehhaghi, et al.
Fig. 4. Schematic block diagram of AD of BMG and NPA scenarios for CHP
generation.
similar conditions, defined as NPA scenario, leading to enhanced biogas
production. The AD plants were assumed to be co-located with a cattle
feedlot with a target digester input of 90 MT. The process model of the
system is illustrated inFig. 4.
The data for this model process were adapted from Aui et al. (2019)
with some modifications and included a feedlot with 2400 beef cattle
and two AD plants with 3670 m3 capacities. The AD process is com-
pleted in six technical areas including feedstock pre-processing, feed-
stock pretreatment, feedstocks mixing, AD, by-products (liquid diges-
tate, 2 wt% organic matter; solid digestate, 28 wt% organic matter)
separation, and steam and power generation (Aui et al., 2019). The
feedstocks (9 wt% total suspended solids) used in this wet digestion
process consisted of biomass (such as rye, wheat, corn stover, etc.) and
cattle manure, supplemented with glycerol to obtain a final ratio of
10.15:79.85:10 wt%, respectively. This cheap supplement (i.e., crude
glycerol), which is infinitely available as by-product of biodiesel in-
dustry, could enhance both biogas yield and methane content due to its
high amount of easily degradable COD for anaerobic microorganisms
(Kazemi Shariat Panahi et al., 2019d; Robra et al., 2010; Tabatabaei
et al., 2019b). Regardless of the type of feedstock, the addition of ZVI
NPs (typically, 0.1 wt%) has been proven to enhance biogas yield
(18.11–366.7%, typical average of 50.3%) and methane content
(3.1–120%, typical average of 40.1%) (Table 1) (Carpenter et al., 2015;
Cerri et al., 2017; Jia et al., 2017; Su et al., 2013; Suanon et al., 2017;
Wang et al., 2016), through the mechanisms discussed in Section 2. The
selection of mesophilic process was due to its higher stability (over
thermophilic processes) as well as its common application for large-
scale AD plants (Abbasi et al., 2012; Aui et al., 2019; Baldwin et al.,
2009). The results were fortified by incorporation of a conservative
generation potential value (power efficiency) of 42% and operating
capacity of 85%, corresponding to the traditional low-efficient farm-
scale AD plants (Aui et al., 2019; Klavon et al., 2013).
The data related to BMG scenario was obtained from the techno-
economic analysis (including capital and operating costs) conducted by
Aui et al. (2019). They used a modified analysis version originally de-
veloped by the National Renewable Energy Laboratory, i.e., the multi-
year discounted cash flow rate of return. Mixers, reactors, anaerobic
digesters, storages tanks, pumps, heat exchangers, and CHP units were
the considered equipment. The costs of these equipment, together with
installation costs, land expenses, and indirect costs (e.g legal fees, en-
gineering design) constituted the capital cost (estimated at 3.12 million
USD) (Aui et al., 2019). For the NPA scenario, it was assumed that no
step was involved for separation of unreacted NPs from the distillate.
Therefore, both scenarios shared the same capital costs. However, the
main (operating) cost difference between these scenarios was the NPs
cost in the NAP scenario. NPs transportation cost was excluded due to
low concentration of ZVI NPs required (0.1 wt%). The feedstock cost
(i.e., manure, biomass, and glycerol) for both scenarios was estimated at
25 USD/MT with 5 USD/MT solids handling costs (Aui et al., 2019).
Plant life time of 30 yrs; construction period of 2.5 yrs; equity of 40%;
depreciation period of 7 yrs; start-up time of 6 months; working capital
of 15% of Fixed Capital Cost; interest rate for financing of 7.5%/yr;
9
Journal of Environmental Management 251 (2019) 109597
income tax rate of 39%; and electricity price of 0.064 USD/kWh were
some key financial assumptions considered through the design of this
case study (Humbird et al., 2011). Upon the completion of AD process,
0.015 USD/kWhe (Renewable Electricity Production Tax Credit), 35.25
USD/MT solid digestate, and 2.64 USD/MT liquid digestate could be
gained (Aui et al., 2019).
According to the calculations performed by Aui et al. (2019), about
8335 m3/d of biogas could be generated from a 90 MT of digester input
in the BMG scenario, leaving 80 MT of digestate. The electricity power
of 950 kW could be assumed with a gas turbine power efficiency of
42%. While the NPA scenario could provide about 1809 kWe (about
90.4% more electricity) if enhanced biogas and methane content of
50.3% and 40.1% were assumed in the presence of 0.1 wt% ZVI NPs.
Unfortunately, there is no data available on the ratio of digester input to
digestate (DItD) as well as digestate quality when ZVI NPs are aug-
mented into AD process. Therefore, to simplify the calculations, we
assumed the same ratio of DItD (i.e., 1.125) in both scenarios and
consequently, a similar amount of digestate (i.e., 80 MT) was taken into
account. It should also be noted that the quality of the digestate from
these two scenarios should also be different and must be analyzed and
compared in future studies.
In the BMG scenario, 137 kW of parasitic electricity consumption
was considered while another 152 kW was taken into account for
heating feedstock to 35 °C prior to AD process and to maintain the AD
process at mesophilic temperatures through the heat exchanged be-
tween the recycled process water and feedstock (Aui et al., 2019). Si-
milarly, the NPA scenario requires similar operating energy (289 kW).
Both scenarios have also similar estimated capital costs of about 3.12
million USD (Aui et al., 2019). This capital cost is translated into
electricity production costs of 0.44 and 0.23 USD/kWhe for the BMG
and NPA scenarios, respectively. For the BMG scenario, the translation
of operating costs into electricity cost results in an additional expense of
about 0.07 USD/kWe totalling 0.51 USD/kWhe (Aui et al., 2019). It can
be assumed that the NPA scenario has the same operating costs and
credits including capital depreciation, labour and maintenance, bio-
mass, solid and liquid digestate credit, and solid handling costs for
electricity generation up to 950 kWh. Then, we can estimate whether
the 859 kWh more electricity generated under the NPA scenario would
be worth the higher feedstock cost (i.e., ZVI NPs) or not. In this esti-
mation, income tax was not included.
Overall, under the conditions of the NPA scenario, the gain related
to renewable tax credit for the additional electricity generated (i.e., 859
kWhe) would be about 12.88 USD/h. The revenue obtained through
selling the excess electricity of 859 kW would be 54.98 USD/h. The
higher operating cost attributed to the NPs cost could be compensated,
to some extent, by the lower capital cost of the NPA scenario (i.e., up to
377.96 USD/h less expense), compared to that of BMG scenario.
Therefore, it could be concluded that the price of NPs for feasible NPA
scenario (consuming 90 kg/d ZVI NPs) must be ≤ 118.88 USD/kg.
More specifically, if the price of ZVI NPs would be ~118.88 USD/kg, an
equal profit vs. the BMG scenario would be expected and any further
improvements in cost-effective production of ZVI NPs (< 118.88 USD/
kg) would translate into corresponding profits.
3.2. Environmental analysis of NPs on biogas production
The commercial application of NPs in various industries has posed
great risks to the environment. The toxic effects of NPs on micro-
organisms, plants, and animals have been reported by several studies
requesting for more precautions and further investigations prior to their
extensive utilization in biological processes such as AD. For instance,
NPs could have various physical hazards owing to their considerable
lower phase transition temperature or melting point, as well as different
magnetic properties, electrical conductivity, and chemical reactivity,
compared to their bulk-sized counterparts (European Commmission,
2014). Moreover, metallic or carbon-based NPs may require special
M. Dehhaghi, et al.
storage precautions due to potential increase in self-heating properties,
flammability, and even dust explosivity. In addition to the above, NPs
could cause health complications due to their altered absorption rates
into human (and animal) body via skin contact, ingestion, and inhala-
tion (European Commmission, 2014). Following absorption, NPs may
reach the body parts, for example, by crossing blood-brain barrier or
cell boundaries while their corresponding bulk sized counterparts are
unable to do so. Consequently, the chance for toxicity (in susceptible
organs) would be enhanced. It is worth to mention that oxidative stress
(which could also be rendered by NPs) in brain could induce cell
apoptosis, neuroinflammation, and neurodegeneration as well as neu-
ronal cell loss developing various neurodegeneration diseases such as
Huntington's disease, Alzheimer's disease, multiple sclerosis, amyo-
trophic lateral sclerosis, and Parkinson's disease (Dehhaghi et al., 2018,
2019). Therefore, the impacts of NPs on brain function and health must
be carefully assessed as well (Teleanu et al., 2018). Adhesion, en-
docytosis, semi-endocytosis, and penetration are the four main inter-
action methods of NPs with cells (Moore et al., 2016). Additionally,
greater surface area of NPs evokes higher toxic dose-response, for a
given mass, than bulk forms (European Commmission, 2014). It should
also be noted that the existence of surface coatings could influence the
level of NPs toxicity. It is believed that poor miscibility of fiber-like NPs
with biological fluids have potential inhalation consequences such as
direct entering into bloodstream from lungs, and ultimately, affecting
all body organs (Amoabediny et al., 2009). In the case of the release of
NPs into the environment, these compounds may exert biocidal or
biostatic effects on microbial communities through the mechanisms
already mentioned in Section 2. Additionally, some fungal species (such
as wood-decay fungi) may degrade NPs into some antimicrobial meta-
bolites, affecting microbial ecology. A key release pathway of NPs into
the environmental is through wastewaters generated by different in-
dustry.
The toxicity of NPs depends on their type, exposure time, and
concentration in a given reaction (Wang and Chen, 2016). Cell mem-
brane disruption and generation of reactive oxygen species have been
proposed as the main toxicity mechanisms of some NPs such as ZVI NPs.
Therefore, it is worth mentioning that even NPs capable of enhancing
biogas production via AD process could exhibit inhibitory effects if used
at beyond-optimal concentrations. In light of that, optimizing the con-
centration of the NPs of interest must be conducted.
The potential human health and environmental impacts of any
products or services could be analyzed through life cycle assessment
(LCA) (Salieri et al., 2018). However, to the best of our knowledge, no
study has been published on the LCA of NPs application in AD pro-
cesses, highlighting the need for future research in this domain. It
should be noted that increasing the environmental burdens associated
with NPs application (regardless of their biogas enhancement char-
acteristics) through the addition of fresh NPs into AD process is not
recommended until appropriate environmental safety assessments are
conducted and proper guidelines are generated. The application of NPs-
contaminated digestate as organic fertilizer would be another important
risk that must be thoroughly evaluated. An alternative to application of
fresh NPs into AD process is the usage of waste streams containing NPs
generated by other industries. This would not only result in partial/
complete bioremediation of these NPs streams but also would lead to
enhanced AD process. It should be mentioned that the AD process itself
holds great promises in remediating environmental pollution con-
taining NPs through their adsorption and accumulation by the sludge
(Wang et al., 2016). Since these waste streams are already disposed of
in the environment, therefore, they raise less concerns in comparison
with the first approach discussed above, i.e., usage of fresh NPs.
In general, the treatment of NPs-contaminated sewage sludge and
post-processing of biosolids by AD and some processes such as those
mimicking composting/stockpiling could be appreciable in remediating
some NPs, such as Zn, Cu, and probably Ag NPs (Lombi et al., 2012). In
the case of ZnO NPs, the AD process could remediate them into ZnS and
10
Journal of Environmental Management 251 (2019) 109597
Zn complexes with cysteine or phosphate. The prescribed composting/
stockpiling procedure could further oxidize ZnS or any other sulfides
prior to the application of the digestate as agricultural fertilizer (Lombi
et al., 2012). More specifically, many microorganisms could consume
different NPs through mechanisms discussed in Section 2, out of which
the main two mechanisms are interaction with microorganisms’ mem-
branes and participation in enzymatic activities of microorganisms.
Apart from these mechanisms, NPs could be aggregated by bacterially-
synthesized proteins, affecting the chemical reactivity of the NPs
(Aruguete and Hochella, 2010; Moreau et al., 2007). For example, the
extracellular mineralization of NPs (such as ZnS) has been observed in
sulfate-reducing bacteria (Moreau et al., 2007).
The degradation of some NPs by bacteria has also been documented.
For example, Streptococcus agalactiae made the up-taken ZnO NPs less
crystalline and more amorphous (Huang et al., 2008). Similarly, Sta-
phylococcus aureus could break cadmium selenide NPs inside its cell
(Kloepfer et al., 2003). In addition to concentration, the rate of mi-
crobial bioremediation of NPs is determined by physiochemical prop-
erties of NPs, such as core chemical composition, NP size and shape,
and coating or surface functionalization that influence microorganisms-
NP interactions. Another key determinant is the type and physiological
state of microorganisms and NPs (Aruguete and Hochella, 2010).
Quantitative techniques are important for safety environmental as-
sessment of NPs. In contrast to qualitative techniques, only few tech-
niques are available for quantitative analysis of NPs in environmental
samples (Farre et al., 2011). For instance, Ag NPs in the environmental
samples could be analyzed by inductively coupled plasma mass spec-
trometry, cloud-point extraction coupled to scanning electron micro-
scopy, transmission electron microscopy, ultraviolet detection, or ca-
pillary electrophoresis (Chang et al., 2008; Farre et al., 2011; Geranio
et al., 2009). Chemical mechanical planarization, anodic stripping
voltammetry, atomic absorption spectroscopy, ultra-violet-vis spectro-
scopy, and liquid chromatography have also been applied for NPs de-
termination in the environmental samples (Deye et al., 2008; Farre
et al., 2011; Huang et al., 2006). Liquid chromatography is a versatile
analytical technique and can be coupled with other analytical techni-
ques such as ultra violet and mass spectroscopy to increase its accuracy
(Mohammadipanah et al., 2016). Nevertheless, most of these techni-
ques are ineffective for NPs quantification by showing high limits of
detections (Farre et al., 2011). Another challenge is the presence of
natural NPs in the environment. Sampling and sample preparation steps
must be also optimized as they can erroneously lead to a lower con-
centration of NP in question, for example, because of absorption of
organic or inorganic NPs by sample bottles (Farre et al., 2011). Soni-
cation or dispersants must be applied for releasing NPs prior to quan-
tification in the case of soil and sediments samples but these pretreat-
ment methods may interfere with analytical procedures by modifying
physicochemical characteristics of the NPs. Hence, the recommended
pretreatment is centrifugation, despite the induction of some aggrega-
tion (Gimbert et al., 2005).
3.3. Policy and regulations for application of NPs for AD process
The European Commission considers nanotechnology a key en-
abling technology which is relevant for many sectors, including health,
chemicals, the environment, consumer products, and energy (Rauscher
et al., 2017). Consequently, nanomaterials implicitly or explicitly have
been dealt with in the European Union's regulatory framework. This
framework consists of several pieces of sector-specific and horizontal
legislations (European Commission, 2012a, b). In general, the existing
legislations particularly cover the potential risks associated with na-
nomaterials and may explicitly or implicitly mention nanomaterials
(Rauscher et al., 2017). In the case of the EU legislation explicitly ad-
dressing nanomaterials, authorisation of nanomaterials for specific
application, safety assessment with nano-specific characteristics in-
cluded, and nanomaterial specific information are required (Rauscher
M. Dehhaghi, et al.
et al., 2017). European Commission (2012a) has concluded that similar
to normal substances or chemical species, nanomaterials could be
classified as toxic or safe compounds. However, no general classifica-
tions could be defined as the toxicity of nanomaterials depends not only
on the nature of nanomaterials but also on the type of application.
Therefore, a case-by-case risk assessment of nanomaterials should be
conducted using all the relevant information.
Currently, each piece of the EU legislation has established binding
rules only within its subject matter and scope (Rauscher et al., 2017).
For example, a pre-market notification including the presence and
specification of nanomaterials must be conducted under the nanoma-
terial regulations on cosmetic products (European Commission, 2009).
The specification data of a given nanomaterial used must present che-
mical and physical characteristics, estimation of its amount in product,
its particles size, pertinent safety data, the toxicological profile, and
appropriate predicted exposure conditions. As already mentioned, other
legislative provisions have specific definitions of their purpose and each
legislation cover nanomaterials within that purpose and scope only
(Rauscher et al., 2017).
The implicitly of nanomaterials has been covered in certain legis-
lative provisions, for example, in the most comprehensive EU legislative
provisions for chemicals, i.e., Registration, Evaluation, Authorisation,
and Restriction of Chemicals (REACH) regardless of their physical state,
shape, or size (European Commission, 2006). The substances produced
or imported in quantities ≥1 MT/yr must be registered while those
marketed in volumes ≥10 MT/yr also need a chemical safety assess-
ment (Rauscher et al., 2017). All forms of a substance must be ad-
dressed in the safety assessment of registration dossier. Substances only
exist in nanoform(s) require REACH's regulation based on the annual
quantity. In contrast, for substances that exist in two forms (i.e., bulk or
non-nanoform, and nanoform), applicants can either submit a dossier,
explicitly covering nanoform or prepare and submit two dossiers se-
parately covering nanoform and bulk size. European Chemicals Agency
(ECHA) is responsible for safety issues of nanomaterials under the
REACH legislation. Some recommendations on the registration of na-
nomaterials have been covered by the agency in periodically updated
guidance on Information Requirements and Chemical Safety Assess-
ment (IR & CSA) appendices (Rauscher et al., 2017). This agency also
consists of experts from accredited stake-holder's organizations, ECHA,
the European Commission, and EU member states in a group named
nanomaterials working group (NMWG) providing informal re-
commendations on technical and scientific challenges relevant to the
implementation of Classification, Labelling and Packaging (CLP), and
REACH regulations for nanomaterials. The registered nanomaterials are
also investigated by another group organized by ECHA, i.e., group as-
sessing already registered nanomaterials (GAARN), working on finding
the best practices for assessing and managing the nanomaterials safety
under the REACH legislation (Rauscher et al., 2017). The results ob-
tained by GAARN are reflected in guidelines revised or developed by
ECHA.
Similarly, the European Commission relies on Scientific Committee
on Health, Environmental and Emerging Risks (SCHEER), an in-
dependent scientific committee, for preparing proposals and policy
relevant to health and environment safety. SCHEER provides the
European Commission with scientific recommendations on emerging
health and environmental issues/risks developed by new technologies
including nanotechnology (Rauscher et al., 2017). Manufactured na-
nomaterials could be globally discussed in a forum, called Working
Party on Manufactured Nanomaterials (WPMN), launched by Organi-
sation for Economic Co-operation and Development (OECD) in 2006
(Rauscher et al., 2017). A responsible development of nanotechnology
is promoted by this forum through debates on safety evaluation and risk
assessment of produced nanomaterials. Therefore, WPMN seeks inter-
national cooperation on environmental safety and human health as-
pects of produced nanomaterials with an emphasis on endpoints per-
tinent to toxicology and environmental fate, material safety,
11
Journal of Environmental Management 251 (2019) 109597
mammalian toxicology, and physicochemical characteristics. The aim
of OECD's WPMN is, therefore, the generation of proper methodologies
to assure safe application of nanotechnology (Rasmussen et al., 2016;
Rauscher et al., 2017).
Overall, despite some developments, there is no specific regulation
at EU level for many of the nanomaterials, in particular, related to their
application in the AD process. However, nanomaterials may have been
implicitly or explicitly covered in different legislations for specific
groups of products such as biocidal (Regulation 528/2012), cosmetic
(Regulation 1223/2009), novel food (Regulation, 2015/2283), food
additives (Regulation 1333/2008), active and intelligent food contact
(Regulation 450/2009), and plastic food contact products (Regulation
10/2011). More specifically, definition, approval procedure, safety as-
sessment, labelling, and guidelines relevant to nanomaterials have been
already covered to some extent for biocidal, cosmetic, and novel food
products by mentioned regulations. The lack of rigid guidelines and
regulations for application of NPs in the AD process demotivates private
economic operators by not clearing their compliance (legal obligations)
leading to legal uncertainty (Busquets-Fité et al., 2017) and should be
addressed in the near future.
3.4. Patents in the field of NPs-augmented AD process
Probably the first patent exploring the application of NPs in the AD
process was built upon the findings of a US patent No. 4,981,593A
(Priestley and Woods, 1991), which was granted for using the magne-
tite particles (i.e., Fe3O4) in millimeter size (50–100 mm) for H2S re-
moval. Interestingly, despite satisfactory results, the bulk size Fe3O4 led
to decreases in biogas production by up to an order of magnitude vs. the
control (Priestley and Woods, 1991). The authors concluded that biogas
production was proportional with the size of magnetite used. In light of
that, Applied Nanoparticles S.L. (AppNPs) was granted a patent (US
9,416,373 B2 Biogas production, 2016 and EP2683662, 2017), invol-
ving the application of iron oxide NPs for enhancing biogas production
(Puntes et al., 2016). The method named BioGAS+ is the drop-in ad-
ditive derived from NPs aiming at enhancing the AD process with re-
spect to biogas production. The enhancement mechanisms are those
already explained in Section 2. The main advantage of these NPs over
conventional iron oxide NPs are their engineered nature allowing
controlled release/dosing of Fe ions to prevent iron toxicity and excess
reactivity (Busquets-Fité et al., 2017). The NPs introduced formed a
colloidal solution preventing its aggregation while they are miscible in
feedstock, allowing homogeneous distribution of iron ions in feedstock.
This allows a sustained and continuous (long time) supply of iron ions
to AD plant till the depletion of organic materials while avoiding con-
centration fluctuations following inoculation and assimilation of iron
oxide. The Fe3O4 NPs sized 3–100 nm in diameter was decorated with
serum proteins (Puntes et al., 2016). The ideal concentration of Fe3O4
NPs in the solution was determined at 0.5–1 mg/mL of solvents (such as
inorganic salts, deoxygenated tetramethylammonium hydroxide, etc.).
Under optimum conditions (21 d, pH 8), up to 74.84% (232 mL/g) in-
crease in biogas could be obtained in the presence of Fe3O4 NPs,
compared to control (310 mL/g) (Puntes et al., 2016). According to a
report by Busquets-Fité et al. (2017), BioGAS + has a Technology
Readiness Level of nine. However, despite good biogas enhancement
capabilities, the application of iron oxide NPs in AD suffers from a
number of shortcomings, including requirement for very high dose
(0.5–1 mg/mL) and a 10-d lag phase (Pérez Martínez, 2017).
In another patent, Fe3O4 NPs were continuously added into a con-
tinuous-flow anaerobic reactor to enhance the methane production rate
(马文成 et al., 2015). Under optimum conditions (circulation flow of
100 L/d; sludge concentration of 10 g/L, 34–36 °C, pH 6.8–7.2, hy-
draulic retention time of 20 h; water effluent flow of 10 L/d; and water
effluent COD of 5 g/L), the yield of biogas and methane were respec-
tively improved by up to 90.8% and 112.6%, compared with controls.
The NPs size and dose were 40–60 nm in diameter and 0.02–0.04 g/g
M. Dehhaghi, et al.
VSS, respectively (马文成 et al., 2015).
3.5. Practical applications of this study
Among the above-mentioned NPs studied, the most promising na-
nomaterials for enhancing biogas production are ZVI NPs. The growth
of the microorganisms beneficial to the AD process and the enzymes
involved are stimulated in the presence of this type of NPs. Moreover,
ZVI NPs could stabilize the AD process and therefore, enhance biogas
production. Overall, the future commercial application of nano-ad-
ditives for enhancing the AD of waste organic materials seems techno-
economically feasible. However, environmental aspects of NPs appli-
cation for biogas production are yet to be further assessed. More spe-
cifically, the exact compositional analysis of digestates containing NPs
must be conducted in order to assess their environmental benefits (as
fertilizer) and/or hazards (soil pollution, biolcidal, biostatic, etc.). The
analysis of these digestates could also allow determining the fate of
augmented NPs in AD process. In another word, the rate of NPs es-
caping in intact and/or converted forms should be quantified. Overall,
efforts must be devoted to greatly reduce the price of NPs as well as to
reduce the rate of their escape from the AD process. The latter could be
achieved by appropriately dosing the NPs and/or increasing hydraulic
retention time among other methods allowing complete consumption of
the augmented NPs.
It should be stressed that biofuels production could only have en-
vironmental, societal, and economic sustainability when all their trade-
offs/weak-points are determined and appropriately addressed (Kazemi
Shariat Panahi et al., 2019a,d; Tabatabaei et al., 2019a). On the other
hand, the strong-points of innovative procedures in biofuels production
such as the application of NPs to enhance biogas production must also
be improved and fully exploited. In this context, introduction and
commercialization of such innovative processes should be preceded by
thorough assessments to ensure maximal beneficial impacts while ad-
verse environmental/health consequences are minimized.
4. Conclusions
According to the investigations reviewed herein, both positive and
negative effects of NPs on AD (biogas production) and methane content
have been reported. Therefore, it is important to obtain more in-depth
insights into the impacts of NPs on the microbial community and waste
digestion process with an aim to improve biogas production yield
during the AD process. In fact, NPs present a high surface to volume
ratio with high reactivity potential that makes them suitable for various
reactions. It should be noted that the complex microbial community
involved in the AD makes extrapolation of the results of lab-scale NPs
study to commercial-scale ones complicated. Therefore, types of NPs
and their concentrations must be tailored based on the results obtained
at large scale operations. Future research should also focus on various
attributes of NPs when used as additives in biogas production. Those
attributes include but not limited to facilitating mixing and pumping
operations (e.g., through reducing substrate viscosity and decreasing
energy consumption), improving biogas release, enriching the popula-
tion and diversity of beneficial microorganisms for AD, and inducing
the production and activity of AD-related enzymes. Moreover, in-
vestigation of different NPs-augmented AD processes with respect to
changes in Gibbs free energy remains a fascinating field to explore by
future studies.
Overall, the economic viability of large-scale NPs-augmented AD
process is mainly dependent on the price of NPs. Moreover, regardless
of the economic feasibility issue, the application of NPs in any in-
dustries (including biogas industry) raises some environmental risks
that must be appropriately addressed. Therefore, to stay on the safe
side, it is recommended to consider AD as a bioremediating process for
treating sludge contaminated with NPs. In this context, future research
should be directed toward investigating the impacts of various NPs on
12
Journal of Environmental Management 251 (2019) 109597
AD process. For example, simultaneous application of two or more
types of NPs and the potential interactions and beneficial effects should
also be scrutinized. Moreover, NPs speciation during AD process and
the existence of remnant of NPs or NP-derived compounds must be
analyzed and traced in the digestate to avoid contamination of agri-
cultural soil.
Another future research interest would be the application of diges-
tate from NPs-augmented AD (including specific NPs) to enhance
growth of specific agriculture crops. Additionally, it would also be
fascinating to assess the adsorption rate of different NPs from con-
taminated soil or water by plants and their deposition sites (e.g. stalk,
root, fruit, leaves) in the form of intact NPs or their derivatives. In this
context, the NPs-contaminated parts of plants could be employed as
biogas enhancing additives in AD process while assessing their proper
doses.
Acknowledgments
The authors would like to thank the Universiti Teknologi MARA
(UITM), Iranian Biofuel Society (IBS), Agricultural Biotechnology
Research Institute of Iran (ABRII), University of Tehran, and Biofuel
Research Team (BRTeam) for supporting this work.
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