i n t e r n a t i o n a l j o u r n a l o f h y d r o g e n e n e r g y x x x ( 2 0 1 8 ) 1 e1 2

Available online at www.sciencedirect.com

ScienceDirect

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

Nanoparticles augmentation on biogas yield from

microalgal biomass anaerobic digestion

Asad A. Zaidi a, Feng RuiZhe a, Yue Shi a,*, Sohaib Z. Khan b,c,
Kashif Mushtaq d
a
College of Power and Energy Engineering, Harbin Engineering University, Harbin 150001, PR China
b
Department of Mechanical Engineering, Faculty of Engineering, Islamic University of Madinah, Madinah, P. O. Box
170, Saudi Arabia
c
Department of Engineering Sciences, PN Engineering College, National University of Sciences and Technology,
Karachi 75350, Pakistan
d
Massachusetts Institute of Technology Portugal Program, Faculty of Engineering, University of Porto (FEUP),
Portugal

article info abstract

Article history: This study evaluates the influence of metal and metal-oxide nanoparticles (NPs) on biogas
Received 22 March 2018 production from green microalgae Enteromorpha. The concentration of metallic NPs (Ni, Co)
Received in revised form was 1 mg/L and oxides NPs (Fe3O4, MgO) was 10 mg/L. An anaerobic digestion was carried
5 May 2018 out batch-wise with working volume, operating temperature, mixing rate and hydraulic
Accepted 23 May 2018 retention time as 500 ml, 37
C, 150 rpm and 170 h, respectively. The measurements of
Available online xxx chemical oxygen demand (COD), volatile fatty acids (VFAs), reducing sugar and biogas
production were observed to monitor effectivity of nanoparticles. The results showed that
Keywords: NPs has moderate positive influence in biogas production until 60 h of retention time but
Anaerobic digestion significantly improve afterward. The maximum total biogas yield of 624 ml was achieved
Biogas by Fe3O4 NPs whereas highest biohydrogen, 51.42% (v/v) was achieved by Ni NPs. The cu-
Green microalgae mulative increase in biogas production for Fe3O4, Ni, Co and MgO NPs was 28%, 26%, 9% and
Kinetic models 8%, respectively. A modified Gompertz and Logistic function model were used to determine
Nanoparticles (NPs) kinetic constants of the reaction. The logistic model has the better predicting ability for
microalgae anaerobic digestion.
© 2018 Hydrogen Energy Publications LLC. Published by Elsevier Ltd. All rights reserved.

anaerobic digestion [2]. It can also be used to treat animal

Introduction
Anaerobic digestion is the biochemical and microbiological
degradation process of organic substrates which takes place
in the absence of oxygen [1]. Liquid and solid waste such as
high organic content waste water, sewage sludge and organic
fraction of municipal solid waste (MSW) can be treated by
manure, energy crops, food waste, microalgae and agricul-
tural residues [3].
The anaerobic digestion process consists of four main
conversion phases of organic matter into biogas namely; hy-
drolysis, acidogenesis, acetogenesis and methanogenesis [4].
In the first phase large and complex organic matter such as

* Corresponding author. College of Power and Energy Engineering, Harbin Engineering University, Harbin 150001, PR China.
E-mail address: shiyue@hrbeu.edu.cn (Y. Shi).
https://doi.org/10.1016/j.ijhydene.2018.05.132
0360-3199/© 2018 Hydrogen Energy Publications LLC. Published by Elsevier Ltd. All rights reserved.

Please cite this article in press as: Zaidi AA, et al., Nanoparticles augmentation on biogas yield from microalgal biomass anaerobic
digestion, International Journal of Hydrogen Energy (2018), https://doi.org/10.1016/j.ijhydene.2018.05.132
2 i n t e r n a t i o n a l j o u r n a l o f h y d r o g e n e n e r g y x x x ( 2 0 1 8 ) 1 e1 2
carbohydrates, fats and proteins react with water to form
monomers by the assistance of hydrolytic bacteria. During the
second phase conversion of monomers into volatile fatty acids
(VFAs) is carried out by the aid of fermentative bacteria. The
third phase involves the transformation of VFA into acetic
acid, carbon dioxide (CO2) and hydrogen under the action of
acetogenic bacteria. During the final phase, methanogenic
bacteria convert acetic acid and hydrogen into methane (CH4)
and CO2 [5]. Biogas is produced by anaerobic digestion and
typically has a calorific value of 21e24 MJ/m3 [6]. The pro-
duction of biogas has increased rapidly since 2000 [7]. Conti-
nent wise global biogas production contribution from Global
Bioenergy Statistics 2017 by World Bioenergy Association
(WBA) is shown in Fig. 1.
The concerns about expansion in bioenergy sector during
past decade have driven a number of scientists and re-
searchers to pursue innovative solutions for its production.
Nanotechnology is one of the emerging branches of science.
From a materials point of view, it deals with materials having
one of the dimensions less than 100 nm. Nanotechnology can
be applied in bioenergy field for the purpose of feedstock
modification and catalysis that is more efficient. Nano-
materials include nanoparticles (NPs), nanofibers, nanotubes;
nanosheets and others have been employed for bioenergy
production [8].
NPs have a high surface to volume ratio, which increases
the chemical reaction sites. It is generally hypothesized that
trace metals improve the digestion process by exciting the
bacterial action causing an increase in biogas production
during anaerobic digestion [6]. Trace metals worked as an
electron donor in an anaerobic digestion process. They in-
crease the total consumption of hydrogen methanogens and
activity. They release ions and contribute to the production
of key enzymes [9]. They can also optimize the microbial
population, change the hydrolysis fermentation types and
stimulate the acetic acid content [10]. It has been reported
that iron, cobalt and nickel were successfully exciting the
Fig. 1 e Global biogas production contribution [7].
Please cite this article in press as: Zaidi AA, et al., Nanoparticles augmentation on biogas yield from microalgal biomass anaerobic
digestion, International Journal of Hydrogen Energy (2018), https://doi.org/10.1016/j.ijhydene.2018.05.132
production of methanogens in digester sludge [11]. In
another study, Qiang et al. [9] stated that the development of
anaerobic bacteria during enzyme synthesis is reliant on the
presence of iron, nickel, and cobalt. Comparison of the ef-
fects of micronutrients of NiCl2, Fe2O3, CoCl2, (NH4)6Mo7O24
along with their NPs with cattle manure slurry on biogas
production is carried out by Juntupally et al. [12]. They
concluded that all NPs have an increasing effect on biogas as
compared to their micronutrients. NiCl2 micronutrient and
Ni NPs produced the highest biogas production. In another
study conducted by Abdelsalam et al. [13], comparison of Ni,
Co and Fe3O4 NPs on biogas production was obtained with
anaerobic digestion of livestock manure. This study also
showed an increase in biogas production by NPs of these
trace metals during anaerobic digestion. Ambuchi et al. [14]
studied the response of Fe2O3 NPs on anaerobic granular
sludge during beet sugar industrial wastewater treatment.
He reported that due to the utilization Fe2O3 NPs as conduits
for electron transfer toward methanogens improves biogas
production.
An intriguing raw biomass, other than conventional
organic wastes used for the production of bioenergy, is
Aquatic Algal [15]. It can be sourced from natural algal bloom
or mass cultivation, is considered a promising substrate for
hydrogen fermentation [16]. Hydrogen has high energy con-
tent on a mass basis as compared to hydrocarbon fuels [17].
The main benefit of hydrogen as a fuel is the absence of CO2,
CO and hydrocarbon emissions. Photo-fermentation is
commonly applied process to treat microalgae for bio-
hydrogen production. However, hydrogen production through
this process remained less effective as the oxygen production
during photo-fermentation impede the activity of hydroge-
nase enzymes and eventually stop the hydrogen production
[18]. In recent years, dark fermentation of microalgae biomass
for biohydrogen production has received increasing consid-
eration [19]. Low biohydrogen potential were obtained
through the dark fermentation method, therefore, a
 i n t e r n a t i o n a l j o u r n a l o f h y d r o g e n e n e r g y x x x ( 2 0 1 8 ) 1 e1 2
pretreatment step is frequently needed to convert organic
matter to sugars which increase biohydrogen production [16].
An alternative process for collective bioenergy production and
depollution is linking an anaerobic digester to a microalgal
culture [20]. Studies have shown that anaerobic sludge and
microalgae were co-cultured to enhance the energy conver-
sion for hydrogen production as well as nutrients removal
from starch wastewater [21]. Biohydrogen production, in
particular, is aided by hydrogenase enzymes which can be
categorized into two types, [NieFe] hydrogenases and [FeeFe]
hydrogenases, in accordance with the metal content present
at their active site. The [NieFe] hydrogenases are widely
disseminated among bacteria, and on the other hand, the
[FeeFe] hydrogenases are confined to a few bacteria [22]. Since
nickel is the key component of the [NieFe] hydrogenases, it
plays an imperative role in fermentative hydrogen production
[23].
Taherdanak et al. [24] have investigated the effects of Fe
and Ni NPs versus Fe2þ and Ni2þ ions at concentrations
ranging from 0 to 50 mg/L on hydrogen production from
anaerobic sludge from glucose as feed. The results showed
that both Fe NPs and Fe2þ ion increase hydrogen production
15% and 37% at dosages of 10 mg/L and 25 mg/L in comparison
with control. The Ni2þ ions showed 55% enhancement in
hydrogen yield at 25 mg/L concentration, whereas Ni NPs did
not show any significant improvement. In another study, Li
et al. [25] examined the effect of Fe2O3 NPs using Enterobacter
aerogenes on hydrogen production from dark fermentation of
glucose. An increase of 17% in biohydrogen production was
observed at a concentration of 200 mg/L Fe2O3 NPs from
glucose. The authors reported that hydrogenase activity was
enhanced by ferric oxide NPs. Liu et al. [26] examined the ef-
fect of TiO2, ZnO and SiC NPs on photo-fermentative hydrogen
production form photo-fermentative bacteria (Rhodop-
seudomonas sp. nov. strain A7). The outcomes revealed that all
NPs improved the hydrogen production. The authors
mentioned that combining NPs with photo-fermentative
bacteria is one promising method to improve hydrogen
yield. Recently, Keskin et al. [27] investigated the influence of
trace metals on biohydrogen yield from the dark fermentation
of fruit and vegetable waste. The authors inspected eleven
diverse trace metals micro particles such as Fe, Ni, Zn, Co, Cu,
Mn, Al, B, Se, Mo and W. The results showed that biohydrogen
production was enhanced by 1.1e2.8 times in comparison
with control. The study concluded that out of all trace metal
micro particles Fe, Ni, Cu and Zn produced more biohydrogen.
A number research works that have been conducted using
different NPs on various kinds of waste and resources; how-
ever, to the best of the authors' knowledge, NPs interaction
with microalgal biomass for biogas and biohydrogen produc-
tion has not been studied yet.
The present study aims to explore the influence of trace
metal and metal-oxide NPs such as Ni, Co, Fe3O4 and MgO on
biogas and hydrogen production from green microalgae
Enteromorpha. To understand the effectiveness of the NPs,
measurements of soluble indexes including chemical oxygen
demand (COD), volatile fatty acids (VFAs), reducing sugar was
carried out. Established prediction models have been studied
from the experimental results for the estimation of the biogas
production with the NPs.
Please cite this article in press as: Zaidi AA, et al., Nanoparticles augmentation on biogas yield from microalgal biomass anaerobic
digestion, International Journal of Hydrogen Energy (2018), https://doi.org/10.1016/j.ijhydene.2018.05.132
3
Materials and methods
Raw material
An anaerobic sludge acquired from an Anaerobic-Anoxic-Oxic
(AAO) reactor at Harbin Wenchang Sewage Treatment Plant,
Harbin, China. It had been aeration cultured for two weeks,
according to the ratio of 300:5:1 plus glucose, NH4Cl, KH2PO4
[28]. Total suspension solids (TSS) and Volatile Suspension
Solids (VSS) of sludge were 6420 mg/L, 2530 mg/L, respectively.
The Enteromorpha was from the freshwater algae and acquired
from the Institute of Hydrobiology of The Chinese Academy of
Science, Wuhan, China. I had been air-dried in the drying
oven, and sealed with a breathable film in the bottle. Each
biodigester inoculated with 60 ml of sludge and 20 g of
Enteromorpha powder. The amounts were selected based on
the previous study conducted by us using response surface
methodology (RSM) for optimization of Enteromorpha and
anaerobic sludge digestion [29].
Four different types of NPs were used in this study. Two
were metal NPs (Ni, Co) while other two were metallic-oxide
NPs (Fe3O4, MgO). NPs were purchased from China Metallur-
gical Research Institute, Beijing. The average size of the NPs
was less than 100 nm with a spherical shape. Most of the
studies in literature reported spherical shape NPs; smaller
nano-sizes with minor dosages are better for anaerobic
digestion of organic matter. However, no study reported NPs
with other morphology. The concentration of NPs in the
biomass was 1 mg/L for Ni and Co NPs whereas the concen-
tration of NPs for Fe3O4 NPs and MgO NPs was 10 mg/L. Similar
concentrations have been used in other studies for these NPs
by Qiang et al. [9] and Abdelsalam et al. [30]. The suspensions
of NPs for above mentioned concentrations were prepared by
adding distilled water containing sodium dodecylbenzene
sulfonate (SDS) 0.1 mM to reduce the agglomeration of NPs
[31].
Experimental procedure
The experiments were carried out via anaerobic batch system.
Anaerobic glass lab-scale bottles with a working volume of
500 ml were used as biodigesters and operated for 170 h. The
digesters were sealed with rubber stoppers, purged with ni-
trogen gas for 5 min to create anaerobic condition inside
digester [32]. The digestion environment has been maintained
at 37
C [13] and 150 rpm mixing speed. Each experiment was
repeated three times to minimize possible errors, and the
average values are reported here. One-way ANOVA was done
by using Origin Pro 8 software, p < 0.05 was considered to be
statistically significant.
Analytical methods
The measurements of soluble indexes, including chemical
oxygen demand (COD), pH, volatile fatty acids (VFAs) and
reducing sugar were determined according to standard
methods [33]. Biomass concentration like glucose concentra-
tion was estimated by 3,5-dinitrosalicylic acid (DNS) method
using spectrophotometer (DR 3900, HACH, USA) at a
4 i n t e r n a t i o n a l j o u r n a l o f h y d r o g e n e n e r g y x x x ( 2 0 1 8 ) 1 e1 2

maximum wavelength (lmax) of 550 nm. Proteins were Levenberg-Marquardt (L-M) algorithm. The algorithm com-
measured by the Bradford method [34] whereas carbohydrates bines the Gauss-Newton method and the steepest descent
were measured by sulfuric acid e UV method [35]. The pH was method.
recorded using a pH analyzer (PHS-3C, INESA, China). Volatile To find out which model is closely matching with the
fatty acids (VFA) were analyzed using gas chromatography (GC experimental data a second order Akaike Information Crite-
7820A, Agilent Technologies, USA) with Flame Ionization De- rion (AIC) test was carried out [45]. The lower value of the AIC
tector (FID). The hydrogen content of the biogas was analyzed suggests a better fit and predicting capability of the model. For
by gas chromatography (SP-2100A, BFRL, USA) with Thermal each model, the AIC value and Akaike's weight value was
Conductivity Detector-Flame Ionization Detector (TCD-FID). calculated by using Eqs (3) and Eq (4) [46]:
Gas samples were taken using a 50 ml syringe to measure the 8
> RSS þ 2K N
gas composition. A volume of 0.5 ml of biogas was injected >
< Nln ; when  40
N K
into a gas chromatography (SP-2100A, BFRL, USA) to measure AIC ¼ (3)
>
> RSS 2KðK þ 1Þ N
biogas composition. The biogas production was observed : Nln þ 2K þ ; when < 40
N NK1 K
twice a day and its composition was measured once during
the experiment. The samples were taken using typical medi-
Þ
ð0:5DAICÞ
cal type syringe with a long needle; 4 ml of sample was Akaike's weight ¼ eð0:5DAICÞ=ð1þe (4)
collected from each digester by injecting the needle through where:
sealed rubber caps and immediately transferred to the small
tubes sealed with rubber stoppers to avoid gas losses. The N ¼ Number of points
sample tubes were then stored in a refrigerator at a temper-
RSS ¼ Residual sum of square
ature of 80
C and used for analysis.
K ¼ Number of model parameters
DAIC ¼ The relative difference between two AIC values.
Mathematical kinetic models

Multiple models are available for anaerobic digestion of

Results and discussion
various biomasses. The forerunners of these models were
Graef and Andrews [36,37] in the late 1960's. In the year 2002,
Influence of nanoparticles on biogas and hydrogen
the Anaerobic Digestion Model No.1 (ADM1) [38] was devel-
production
oped by the International Water Association (IWA) group.
The plus point of ADM1 model was its capability of simu-
All NPs showed a positive effect on biodegradability of
lating the anaerobic digestion of different biomasses. The
microalgal biomass (Enteromorpha), which is certain by the
disadvantage, however, is that it is aided through many
enhanced biogas production compared with the control
input parameters. This is not only time-consuming but also
experiment as shown in Fig. 2. It can be observed that during
takes a toll on expense from an experimental point of view.
the initial 60 h, biogas production had a low significant posi-
For such inconveniences to be eliminated, statistical linear
tive influence of NPs in comparison with the control sample.
and nonlinear regression models (modified Gompertz model,
The production of biogas then significantly increased, with
Logistic function, Transference function e Reaction curve
the passage of time, for all the samples containing NPs in
type model, etc.) were established so that the anaerobe
comparison to the control sample. The initial duration of the
digestion performances can be both described and predicted
[39e42].
The calculation and comparison of biogas production ki-
netic during digestion of algal biomass with different NPs
were modeled via modified Gompertz model Eq. 1 [43] and
Logistic Function model Eq. 2 [44].


 
B ¼ Bp :exp exp MBPR:2:7183 Bp :ðBPDT  tÞ þ 1 (1)


  
B ¼ Bp 1 þ exp 4MBPRðBPDT  tÞ Bp þ 2 (2)

where:

B ¼ Cumulative biogas volume at digestion time t (ml)

BP ¼ Biogas production potential (ml)
MBPR ¼ Maximum biogas production rate (ml/h)
BPDT ¼ Biogas production delay time (hrs)
t ¼ Total digestion time (hrs).

The parameters for both the models were determined by

using Origin Pro 8 software. The software calculates and ad- Fig. 2 e Biogas production influenced by nanoparticles,
justs the parameter values in the iterative procedure based on standard deviations are represented by error bars.

Please cite this article in press as: Zaidi AA, et al., Nanoparticles augmentation on biogas yield from microalgal biomass anaerobic
digestion, International Journal of Hydrogen Energy (2018), https://doi.org/10.1016/j.ijhydene.2018.05.132
 i n t e r n a t i o n a l j o u r n a l o f h y d r o g e n e n e r g y x x x ( 2 0 1 8 ) 1 e1 2
experiments can be categorized as less-effective domain and
later part as a high-effective domain. The less effective
domain is attributed to the presence of a highly resistant cell
wall of microalgae biomass [47]. This cell wall comprises two
layers. The external layer is electron dense polymeric matrix
composed of protein and carbohydrates. The internal layer
composed of cellulose and hemicellulose [48]. In the high
effective domain, the mechanism behind the increase in
biogas is credited to NPs stimulating effect responsible for the
dissolution of proteins, carbohydrates and cellulose. NPs
dissolve the microalgae organics and increase the lysis rate
which is attributed to the increasing effect on biogas pro-
duction. These dissolvable organics released intracellular
components into the liquid phase due to microalgae disinte-
gration by NPs. Initially, NPs thrashes the external layer
(protein and carbohydrates) and then solubilize the internal
layer (cellulose and hemicellulose) [49]. The glycosidic bond in
carbohydrates and polysaccharides hydrolyze by NPs which
turn into simple sugars. This effect resulted in increased
permeability of external layer. Later, NPs attacks the internal
layer and hydrolyze cellulose into oligosaccharides such as
cellobiose and cellodextrin [50]. The release of biopolymers
(Carbohydrates and proteins) is shown in Fig. 3. The carbo-
hydrates and proteins released by dissolution of the cell
structure of microalgae are then converted into amino acids,
simple sugars, peptides and volatile fatty acids [51]. The
maximum cumulative biogas and the amount of hydrogen
produced during the experiment are presented in Fig. 4. Ni NPs
produced highest biohydrogen i.e, 51.42% (v/v) followed by
Fe3O4 NPs, 44.61% (v/v).
The results show that Fe3O4 and Ni NPs have a high biogas
and biohydrogen yield as compared to other two and control
samples. Our results obtained by microalgae interaction with
NPs are in agreement with multiple studies available in liter-
ature with the different feedstock. Similar trends were ob-
tained by the study conducted by Abdelsalam et al. [13], it
showed that Ni, Fe3O4 and Co NPs produced 1.8, 1.7 and 1.7
times enhancement in biogas yield from anaerobic digestion
of cattle manure slurry, respectively. Another study
Fig. 3 e Proteins and carbohydrates production influenced
by nanoparticles, standard deviations are represented by
error bars.
Please cite this article in press as: Zaidi AA, et al., Nanoparticles augmentation on biogas yield from microalgal biomass anaerobic
digestion, International Journal of Hydrogen Energy (2018), https://doi.org/10.1016/j.ijhydene.2018.05.132
5
conducted by Elreedy et al. [52] showed 23% increase in biogas
production by 60 mg/L Ni NPs on anaerobic digestion of in-
dustrial wastewater containing mono-ethylene glycol. The
ability of iron to gain or lose electrons makes it a potential
candidate to be used as an additive in anaerobic digestion
process [6]. An increase of 1.25 times in biogas production by
Fe3O4 NPs on anaerobic digestion of waste water sludge
identified by Suanon et al. [53]. Casals et al. [54] reported that
100 ppm of 7 nm Fe3O4 NPs showed a considerable increase in
biogas production in an anaerobic waste treatment reactor.
The authors showed that iron oxide NPs act as a source to
produce Fe2þ ions and increase biogas production. This
observation accords with Feng et al. [55], who reported an
improved digestion performance due to the presence of Fe2þ/
Fe3þ ions present in the reactor in the form of NPs. Fe2þ ions
are essential for power generation and DNA replication. The
effortlessness with which iron ions gain or lose electrons
makes them a perfect and adaptable cofactor for various
proteins. The surplus iron can easily produce very reactive
and toxic free radicals that are harmful to different bio-
molecules (nucleic acids and lipids, amongst others) [54]. Our
results are also in agreement with Ambuchi et al. [14], the
authors reported an increase of 1.25 times in biogas produc-
tion by Fe3O4 NPs as compared to control experiment. The
effect of nZVI (nanozero-valent iron), Ag, Fe2O3 and MgO NPs
on waste activated sludge was conducted by Wang et al. [56].
The average concentrations of Fe2þ, Agþ and Mg2þ released
were 1.3, 3.3 and 9.8 mg/L, respectively. They reported that
lower concentrations of Fe2þ facilitate the anaerobic digestion
of sludge whereas high concentrations of Agþ and Mg2þ ions
inhibit the anaerobic digestion. The concentration of MgO NPs
used was 500 mg/g of the total suspended solids. Our result
shows 8% increase in biogas production by MgO NPs as low
concentration used in present study released the lower
amount of Mg2þ ions in the digester and improves gas pro-
duction. Our results also agrees with Guo et al. [57], the au-
thors considered Fe2þ and Mg2þ as the most critical nutrient
salts for hydrogen fermentation. They studied the effect of
these nutrition components on Hydrogen producing strain E.
harbinense B49 and found a positive effect of these nutritions
on hydrogen production. The optimal condition (glucose
14,500 mg/L, Fe2þ 180 mg/L and Mg2þ 690 mg/L) provided -
production of 0.024H2 g/g - glucose. In another study, Liu et al.
[58] investigated the effect of Ni2þ, Fe2þ and Mg2þ concentra-
tions on hydrogen production from Rhodopseudomonas faecalis
RLD-53. The results showed that Ni2þ (236 mg/L) and Fe2þ
(4480 mg/L) produced maximum hydrogen production of 
0.032 and 0.031 g H2/g glucose -, respectively. However, Mg2þ
did not affect hydrogen production yield. The study indicated
that the presence of metal ions (Ni2þ and Fe2þ) stimulated the
bioactivity of hydrogen producing bacteria. The hydrogen
production could be affected by supplementation of Ni2þ and
Fe2þ ions into the active sites of [Ni-Fe] hydrogenase by
prompting the [Ni-Fe]- hydrogenase activity. Ni2þ and Fe2þ are
the essential components of [Ni-Fe] hydrogenase and have an
integral role in the production of hydrogen. Mg2þ ion, how-
ever, does not in any way contribute to hydrogen production
[58]. The authors also mentioned that higher concentrations
of these metal ions decrease hydrogen yield; our results agree
with these findings.
6 i n t e r n a t i o n a l j o u r n a l o f h y d r o g e n e n e r g y x x x ( 2 0 1 8 ) 1 e1 2

Fig. 4 e (A) Cumulative Biogas Production, (B) Hydrogen content % (v/v) from green microalgae Enteromorpha with the
presence of NPs, standard deviations are represented by error bars.

COD, reducing sugar and pH change
The influence of NPs on biogas production during anaerobic
digestion is noticeable by the evolution of COD. It is shown in
Fig. 5 (A) that concentration of COD increases for the first
60 h of digestion. COD becomes stable for the next 48 h. COD
concentration decreased for control, Co NPs and MgO NPs
during the last 72 h, however it increases for Ni NPs and
Fe3O4 NPs. The highest amount of COD is provided by Fe3O4
and Ni NPs which are 14,760 mg/L and 14,745 mg/L,
respectively.
The rising trend indicated the cell lysis and production of
inter-cellular segments (glycoproteins, carbohydrates and
cellulose) due to disruption of cell walls of microalgal biomass
by the addition of metal and metal oxide NPs. The peaks show
the higher COD level which indicates that more substantial
oxidizable organic matter is present in the digesters which
reduce the dissolved oxygen level and promotes anaerobic
conditions. The results presented in Figs. 2 and 5 (A) shows
that digesters inoculated with Fe3O4 NPs and Ni NPs had better
performance than other digesters which shows that additive
amounts of these NPs promoted the dissolution of COD.

Please cite this article in press as: Zaidi AA, et al., Nanoparticles augmentation on biogas yield from microalgal biomass anaerobic
digestion, International Journal of Hydrogen Energy (2018), https://doi.org/10.1016/j.ijhydene.2018.05.132
 i n t e r n a t i o n a l j o u r n a l o f h y d r o g e n e n e r g y x x x ( 2 0 1 8 ) 1 e1 2
Fig. 5 e Measurement of soluble indexes (A) COD change (B)
Reducing sugar change (C) pH change affected by
nanoparticles, standard deviations are represented by
error bars.
The evolution of reducing sugar during the digestion pro-
cess is presented in Fig. 5 (B). The reducing sugar concentra-
tions at 24 h in the digestion medium with NPs was about
0.35 g/L whereas for control it had a higher value of about
0.47 g/L. Reducing sugar value increased for all groups during
the next 24 h. It decreased for all NPs afterwards, however,
kept on increasing for control. Low reducing sugar value with
Please cite this article in press as: Zaidi AA, et al., Nanoparticles augmentation on biogas yield from microalgal biomass anaerobic
digestion, International Journal of Hydrogen Energy (2018), https://doi.org/10.1016/j.ijhydene.2018.05.132
7
a high gas production meant most reducing sugar had been
used to produce the biogas in this period. The reducing sugar
consumption was slower for control after 72 h whereas the
consumption of sugar by anaerobic bacteria was faster for
groups with NPs.
The pH value continuously decreases during the digestion
period for all groups as shown in Fig. 5 (C). The pH value
maintained at the level at 5.6e6.6. The decline in the pH value
attributes to the production of organic acids during the
anaerobic digestion process.
VFA production during fermentation
Volatile fatty acids (VFAs) contents revealed the influence of
NPs on biogas production. VFA production was measured at
the beginning and the end of digestion. At the start, after in-
cubation of NPs and before anaerobic digestion, VFA produc-
tion values were relatively low and almost the same among
each group except for oxide NPs. Both oxide NPs had greater
amount butyric acid at the start. It is clear from Fig. 6 that after
a hydraulic retention time of 170 h, the digestion process
significantly increased VFA production content for all groups,
indicating that the digestion was surely hydrolyzing some
insoluble components of algae biomass. This tendency was in
accordance with the gas production profile during the diges-
tion shown in Fig. 2. The amount of increase can reach
1988 mg/L and 1865 mg/L in a group of Ni NPS, and Fe3O4 NPs,
respectively. The amount of butyric acid had the most sig-
nificant effect on algal biomass digestion. High amounts of
acetic acid and butyric acid caused more biogas yield [29].
According to Dareioti et al. [59] higher biogas and biohydrogen
production depend on the final amount of acetic acid and
butyric acid production. The high COD peaks for Fe3O4 and Ni
NPs and more biogas production along with the VFAs gener-
ation attributes to more cell wall disruption and dissolution of
glycoproteins, carbohydrates and cellulose as compared to
other groups and control. This observation is in agreement
with Greden et al. [60] who stated that rising of COD value in
anaerobic digestion is accompanied by cell membranes
disruption and VFAs generation.
Mathematical kinetic models
Modified Gompertz and Logistic models were used to conduct
the kinetic study for the cumulative biogas produced [43,44].
The kinetic study results obtained from modified Gompertz
and Logistic model are given in Tables 1 and 2, respectively.
The comparison of experimental and predicted cumulative
biogas production by all groups is shown in Figs. 7 and 8.
While using modified Gompertz model, maximum biogas
production rate (MBPR) for the control was 4.21 ml/hr. For Ni,
Co, Fe3O4 and MgO NPs, the MBPR increased to 5.40, 4.67, 5.18
and 4.32 ml/hr, respectively. Similarly, for the Logistic model,
the maximum biogas production rate (MBPR) for the control,
Ni, Fe3O4, Co and MgO NPs were 4.71, 6.00, 5.19, 5.75 and 4.77
ml/hr respectively. It is identified by both the kinetic models
that Ni NPs and Fe3O4 NPs had enhanced the biogas produc-
tion rate and shorten the lag phase period compared to other
groups. The reason for reduction in lag was due to cell walls
disruption occurred during more effective domain of biogas
8 i n t e r n a t i o n a l j o u r n a l o f h y d r o g e n e n e r g y x x x ( 2 0 1 8 ) 1 e1 2

Fig. 6 e VFA production affected by NPs at Start and End of the experiment, standard deviations are represented by error
bars.

Table 1 e Parameters of modified Gompertz model.

Parameter Treatments
Control Ni NPs Co NPs Fe3O4NPs MgO NPs
BP (ml) 608.45 772.18 656.44 802.55 664.08
MBPR (ml/hr) 4.21 5.40 4.67 5.18 4.32
BPDT (Hrs) 1.14 1.40 1.25 1.23 1.05
R2 0.99246 0.99719 0.99493 0.99739 0.99716
Predicted Biogas Yield (ml) 505.50 629.73 547.50 636.68 540.62
Measured Biogas Yield (ml) 488 618 535 624 529
Difference between measured and predicted biogas yield (%) 3.58 1.89 2.33 2.03 2.19

Remarks: BP, Biogas production potential; MBPR, Maximum biogas production rate; BPDT, Biogas production delay time; R2, Correlation
Coefficient.

Table 2 e Parameters of Logistic Function model.

Parameter Treatments
Control Ni NPs Co NPs Fe3O4NPs MgO NPs
BP (ml) 517.42 651.76 560.14 667.89 561.38
MBPR (ml/hr) 4.71 6.00 5.19 5.75 4.77
BPDT (Hrs) 1.45 1.69 1.58 1.53 1.30
R2 0.99766 0.99796 0.99742 0.99764 0.99824
Predicted Biogas Yield (ml) 491.04 612.95 531.76 620.95 526.74
Measured Biogas Yield (ml) 488 618 535 624 529
Difference between measured and predicted biogas yield (%) 0.62 0.82 0.60 0.49 0.42

Remarks: BP, Biogas production potential; MBPR, Maximum biogas production rate; BPDT, Biogas production delay time; R2, Correlation
Coefficient.

production, high COD and faster consumption of sugar by The results for Akaike Information Criterion (AIC) test
anaerobic bacteria. The correlation coefficient for modified performed for two models are shown in Table 3. In this study,
Gompertz model and Logistic Function model was above Logistic function model has lower AIC value which is sug-
99.58% and 99.77% respectively. gesting to be a better model to use in this case.

Please cite this article in press as: Zaidi AA, et al., Nanoparticles augmentation on biogas yield from microalgal biomass anaerobic
digestion, International Journal of Hydrogen Energy (2018), https://doi.org/10.1016/j.ijhydene.2018.05.132
 i n t e r n a t i o n a l j o u r n a l o f h y d r o g e n e n e r g y x x x ( 2 0 1 8 ) 1 e1 2 9

Fig. 7 e Non-linear Fit of cumulative biogas production for Gompertz model.

Fig. 8 e Non-Linear Fit of cumulative biogas production for Logistic Function model.

Table 3 e Results for Akaike's information criterion (AIC) test.

Model RSS N AIC Akaike Weight
Modified Gompertz Model 2408.60702 14 84.5129 2.79964E-4
Logistic Function Model 748.55971 14 68.15176 0.99972

Remarks: RSS, the Residual sum of the square; N, Number of Points; AIC, Akaike's Information Criterion.

Please cite this article in press as: Zaidi AA, et al., Nanoparticles augmentation on biogas yield from microalgal biomass anaerobic
digestion, International Journal of Hydrogen Energy (2018), https://doi.org/10.1016/j.ijhydene.2018.05.132
10 i n t e r n a t i o n a l j o u r n a l o f h y d r o g e n e n e r g y x x x ( 2 0 1 8 ) 1 e1 2
Conclusions
The cumulative increase in biogas yield from Fe3O4, Ni, Co and
MgO NPs were 28%, 26%, 9% and 8%, respectively. Fe3O4 and Ni
NPs attained the highest amount of COD of 14,760 mg/L and
14,745 mg/L, respectively. Both these NPs showed low
reducing sugar value as compared to other groups and control.
The increase in VFA produced by Ni and Fe3O4 NPs was
1988 mg/L and 1865 mg/L, respectively. The experimental data
obtained was modeled by using Modified Gompertz and Lo-
gistic function model. Pre-treatment methods can be used
along with NPs in microalgae anaerobic digestion for disrup-
tion of its resilient cell wall to achieve an overall high energy
gain and further process improvement. The presented results
show robustness of metal and metal oxide NPs with anaerobic
digestion of microalgae (Enteromorpha) for enhancement in
biogas and hydrogen yield.
Acknowledgment
This research was financially supported by the National Key
R&D Plan of China (2017YFC1404605), the Natural Science
Foundation of China (Grant No. 51579049 and 51509044) and
the High Tech Ship Program.
references
[1] Seadi TA, Rutz D, Prassl H, Ko € ttner M, Finsterwalder T,
Volk S, et al. Biogas handbook. 2008. https://doi.org/10.1533/
9780857097415.1.85.
[2] Vasco-Correa J, Khanal S, Manandhar A, Shah A. Anaerobic
digestion for bioenergy production: global status,
environmental and techno-economic implications, and
government policies. Bioresour Technol 2018;247:1015e26.
https://doi.org/10.1016/j.biortech.2017.09.004.
[3] Mushtaq K, Zaidi AA, Askari SJ. Design and performance
analysis of floating dome type portable biogas plant for
domestic use in Pakistan. Sustain Energy Technol Assess
2016;14:21e5. https://doi.org/10.1016/j.seta.2016.01.001.
[4] Hagos K, Zong J, Li D, Liu C, Lu X. Anaerobic co-digestion
process for biogas production: progress, challenges and
perspectives. Renew Sustain Energy Rev 2017;76:1485e96.
https://doi.org/10.1016/j.rser.2016.11.184.
[5] Mao C, Feng Y, Wang X, Ren G. Review on research
achievements of biogas from anaerobic digestion. Renew
Sustain Energy Rev 2015;45:540e55. https://doi.org/10.1016/
j.rser.2015.02.032.
[6] Ganzoury MA, Allam NK. Impact of nanotechnology on
biogas production: a mini-review. Renew Sustain Energy Rev
2015;50:1392e404. https://doi.org/10.1016/j.rser.2015.05.073.
[7] Kummamuru Bharadwaj. Wba global bioenergy Statistics
2017. 2017. https://doi.org/10.1016/0165-232X(80)90063-4.
[8] Antonio F, Antunes F, Gaikwad S, Ingle AP. Nanotechnology
for bioenergy and biofuel production. Green Chem. Sustain:
Technol., Springer International Publishing; 2017. p. 3e18.
https://doi.org/10.1007/978-3-319-45459-7.
[9] Qiang H, Niu Q, Chi Y, Li Y. Trace metals requirements for
continuous thermophilic methane fermentation of high-
solid food waste. Chem Eng J 2013;222:330e6. https://doi.org/
10.1016/j.cej.2013.02.076.
Please cite this article in press as: Zaidi AA, et al., Nanoparticles augmentation on biogas yield from microalgal biomass anaerobic
digestion, International Journal of Hydrogen Energy (2018), https://doi.org/10.1016/j.ijhydene.2018.05.132
[10] Liu C, Yuan H, Zou D, Liu Y, Zhu B, Li X. Improving
biomethane production and mass bioconversion of corn
stover anaerobic digestion by adding NaOH pretreatment
and trace elements. BioMed Res Int 2015;2015. https://
doi.org/10.1155/2015/125241.
[11] Krongthamchat K, Riffat R, Dararat S. Effect of trace metals
on halophilic and mixed cultures in anaerobic treatment. Int
J Environ Sci Technol 2006;3:103e12.
[12] Juntupally S, Begum S, Allu SK, Nakkasunchi S, Madugula M,
Anupoju GR. Relative evaluation of micronutrients (MN) and
its respective nanoparticles (NPs) as additives for the
enhanced methane generation. Bioresour Technol 2017.
https://doi.org/10.1016/j.biortech.2017.04.049.
[13] Abdelsalam E, Samer M, Attia YA, Abdel-hadi MA,
Hassan HE, Badr Y. Comparison of nanoparticles effects on
biogas and methane production from anaerobic digestion of
cattle dung slurry. Renew Energy 2016;87:592e8. https://
doi.org/10.1016/j.renene.2015.10.053.
[14] Ambuchi JJ, Zhang Z, Shan L, Liang D, Zhang P, Feng Y.
Response of anaerobic granular sludge to iron oxide
nanoparticles and multi-wall carbon nanotubes during beet
sugar industrial wastewater treatment. Water Res
2017;117:87e94. https://doi.org/10.1016/j.watres.2017.03.050.
[15] Rahman KM, Melville L, Huq SMI, Khoda SK. Understanding
bioenergy production and optimisation at the nanoscale e a
review. J Exp Nanosci 2016;11:762e75. https://doi.org/
10.1080/17458080.2016.1157905.
[16] Xia A, Cheng J, Song W, Su H, Ding L, Lin R, et al.
Fermentative hydrogen production using algal biomass as
feedstock. Renew Sustain Energy Rev 2015;51:209e30.
https://doi.org/10.1016/j.rser.2015.05.076.
[17] Wieczorek N, Kucuker MA, Kuchta K. Fermentative hydrogen
and methane production from microalgal biomass (Chlorella
vulgaris) in a two-stage combined process. Appl Energy
2014;132:108e17. https://doi.org/10.1016/j.apenergy.2014.
07.003.
[18] Wang J, Yin Y. Fermentative hydrogen production using
pretreated microalgal biomass as feedstock. Microb Cell Fact
2018;17:22. https://doi.org/10.1186/s12934-018-0871-5.
[19] Rajhi H, Puyol D, Martinez MC, Diaz EE, Sanz JL. Vacuum
promotes metabolic shifts and increases biogenic
hydrogen production in dark fermentation systems. Front
Environ Sci Eng 2016;10:513e21. https://doi.org/10.1007/
s11783-015-0777-y.
[20] Mairet F, Bernard O, Ras M, Lardon L, Steyer JP. A dynamic
model for anaerobic digestion of microalgae. IFAC Proc Vol
2011;18:5034e9. https://doi.org/10.3182/20110828-6-IT-
1002.02636.
[21] Ren H-Y, Liu B-F, Kong F, Zhao L, Ren N. Hydrogen and lipid
production from starch wastewater by co-culture of
anaerobic sludge and oleaginous microalgae with
simultaneous COD, nitrogen and phosphorus removal.
Water Res 2015;85:404e12. https://doi.org/10.1016/
j.watres.2015.08.057.
[22] Wang J, Wan W. Influence of Ni2þ concentration on
biohydrogen production. Bioresour Technol 2008;99:8864e8.
https://doi.org/10.1016/j.biortech.2008.04.052.
[23] Kothari R, Singh DP, Tyagi VV, Tyagi SK. Fermentative
hydrogen production e an alternative clean energy source.
Renew Sustain Energy Rev 2012;16:2337e46. https://doi.org/
10.1016/j.rser.2012.01.002.
[24] Taherdanak M, Zilouei H, Karimi K. The effects of Fe0 and Ni0
nanoparticles versus Fe2þ and Ni2þ ions on dark hydrogen
fermentation. Int J Hydrogen Energy 2016;41:167e73. https://
doi.org/10.1016/j.ijhydene.2015.11.110.
[25] Lin R, Cheng J, Ding L, Song W, Liu M, Zhou J, et al. Enhanced
dark hydrogen fermentation by addition of ferric oxide
nanoparticles using Enterobacter aerogenes. Bioresour
 i n t e r n a t i o n a l j o u r n a l o f h y d r o g e n e n e r g y x x x ( 2 0 1 8 ) 1 e1 2
Technol 2016;207:213e9. https://doi.org/10.1016/j.biortech.
2016.02.009.
[26] Liu B, Jin Y, Wang Z, Xing D, Ma C, Ding J, et al. Enhanced
photo-fermentative hydrogen production of
Rhodopseudomonas sp. nov. strain A7 by the addition of
TiO2, ZnO and SiC nanoparticles. Int J Hydrogen Energy
2017;42:18279e87. https://doi.org/10.1016/j.ijhydene.2017.
04.147.
[27] Keskin T, Arslan K, Nalakth Abubackar H, Vural C, Eroglu D,
Karaalp D, et al. Determining the effect of trace elements on
biohydrogen production from fruit and vegetable wastes. Int
J Hydrogen Energy 2018. https://doi.org/10.1016/j.ijhydene.
2018.01.028.
[28] Waligo  rska M. Fermentative hydrogen production -process
design and bioreactors. Chem Process Eng 2012;33:585e94.
https://doi.org/10.2478/v10176-012-0048-4.
[29] Feng R, Shi Y, Zhang K. Optimisation and enhancement of
microwave pre-treatment on algae biomass fermentation.
In: 16th Int. Conf. Sustain. Bologna, Italy: Energy Technol.;
2017.
[30] Abdelsalam E, Samer M, Attia YA, Abdel-Hadi MA,
Hassan HE, Badr Y. Influence of zero valent iron
nanoparticles and magnetic iron oxide nanoparticles on
biogas and methane production from anaerobic digestion of
manure. Energy 2017;120:842e53. https://doi.org/10.1016/
j.energy.2016.11.137.
[31] Khan SZ, Yuan Y, Abdolvand A, Schmidt M, Crouse P, Li L,
et al. Generation and characterization of NiO nanoparticles
by continuous wave fiber laser ablation in liquid. J
Nanoparticle Res 2009;11:1421e7. https://doi.org/10.1007/
s11051-008-9530-9.
[32] Xia A, Jacob A, Tabassum MR, Herrmann C, Murphy JD.
Production of hydrogen, ethanol and volatile fatty acids
through co-fermentation of macro- and micro-algae.
Bioresour Technol 2016;205:118e25. https://doi.org/10.1016/
j.biortech.2016.01.025.
[33] China M of EP. Standard methods for the examination of
water and waste water. fourth ed. Beijing: Environmental
Press; 2002.
[34] Kavitha S, Jayashree C, Adish Kumar S, Kaliappan S, Rajesh
Banu J. Enhancing the functional and economical efficiency
of a novel combined thermo chemical disperser
disintegration of waste activated sludge for biogas
production. Bioresour Technol 2014;173:32e41. https://
doi.org/10.1016/j.biortech.2014.09.078.
[35] Albalasmeh AA, Berhe AA, Ghezzehei TA. A new method for
rapid determination of carbohydrate and total carbon
concentrations using UV spectrophotometry. Carbohydr
Polym 2013;97:253e61. https://doi.org/10.1016/j.carbpol.
2013.04.072.
[36] Andrews JF. A mathematical model for the continuous
culture of microorganisms utilizing inhibitory substrates.
Biotechnol Bioeng 1968;10:707e23. https://doi.org/10.1002/
bit.260100602.
[37] Graef S P AJF. Mathematical modeling and control of
anaerobic digestion. AIChE Symp Ser 1974;136:101e31.
[38] Batstone DJ, Keller J, Angelidaki I, Kalyuzhnyi SV,
Pavlostathis SG, Rozzi A, et al. The IWA anaerobic digestion
model No 1 (ADM1). Water Sci Technol 2002;45. 65 LP-73.
[39] Donoso-Bravo A, Pe rez-Elvira SI, Fdz-Polanco F. Application
of simplified models for anaerobic biodegradability tests.
Evaluation of pre-treatment processes. Chem Eng J
2010;160:607e14. https://doi.org/10.1016/j.cej.2010.03.082.
[40] Kafle GK, Kim SH. Anaerobic treatment of apple waste with
swine manure for biogas production: batch and continuous
operation. Appl Energy 2013;103:61e72. https://doi.org/
10.1016/j.apenergy.2012.10.018.
Please cite this article in press as: Zaidi AA, et al., Nanoparticles augmentation on biogas yield from microalgal biomass anaerobic
digestion, International Journal of Hydrogen Energy (2018), https://doi.org/10.1016/j.ijhydene.2018.05.132
11
[41] Wu X, Zhu J, Miller C. Kinetics study of fermentative hydrogen
production from liquid swine manure supplemented with
glucose under controlled pH. J Environ Sci Heal Part B
2013;48:477e85. https://doi.org/10.1080/03601234.2013.761907.
[42] Li C, Champagne P, Anderson BC. Evaluating and modeling
biogas production from municipal fat, oil, and grease and
synthetic kitchen waste in anaerobic co-digestions.
Bioresour Technol 2011;102:9471e80. https://doi.org/10.1016/
j.biortech.2011.07.103.
[43] Syaichurrozi I, Budiyono, Sumardiono S. Predicting kinetic
model of biogas production and biodegradability organic
materials: biogas production from vinasse at variation of
COD/N ratio. Bioresour Technol 2013;149:390e7. https://
doi.org/10.1016/j.biortech.2013.09.088.
[44] Deepanraj B, Sivasubramanian V, Jayaraj S. Effect of
substrate pretreatment on biogas production through
anaerobic digestion of food waste. Int J Hydrogen Energy
2017;42:26522e8. https://doi.org/10.1016/j.ijhydene.2017.
06.178.
[45] Rawlings JO, Pantula SG, Dickey Da. Applied regression
analysis: a research tool. 2nd ed. Springer-Verlag New York,
Inc.; 1998. https://doi.org/10.1007/b98890.
[46] Wong CS, Li WK. A note on the corrected Akaike information
criterion for threshold autoregressive models. J Time Ser
Anal 1998;19:113e24. https://doi.org/10.1111/1467-
9892.00080.
[47] Kavitha S, Yukesh Kannah R, Rajesh Banu J, Kaliappan S,
Johnson M. Biological disintegration of microalgae for
biomethane recovery-prediction of biodegradability and
computation of energy balance. Bioresour Technol
2017;244:1367e75. https://doi.org/10.1016/j.biortech.2017.
05.007.
[48] Demuez M, Mahdy A, Toma  s-Pejo
 E, Gonza lez-Ferna ndez C,
Ballesteros M. Enzymatic cell disruption of microalgae
biomass in biorefinery processes. Biotechnol Bioeng
2015;112:1955e66. https://doi.org/10.1002/bit.25644.
[49] Mahdy A, Mendez L, Ballesteros M, Gonza  lez-Ferna ndez C.
Enhanced methane production of Chlorella vulgaris and
Chlamydomonas reinhardtii by hydrolytic enzymes
addition. Energy Convers Manag 2014;85:551e7. https://
doi.org/10.1016/j.enconman.2014.04.097.
[50] Ehimen EA, Holm-Nielsen J-B, Poulsen M, Boelsmand JE.
Influence of different pre-treatment routes on the anaerobic
digestion of a filamentous algae. Renew Energy
2013;50:476e80. https://doi.org/10.1016/j.renene.2012.06.064.
[51] Kavitha S, Yukesh Kannah R, Yeom IT, Do K-U, Banu JR.
Combined thermo-chemo-sonic disintegration of waste
activated sludge for biogas production. Bioresour Technol
2015;197:383e92. https://doi.org/10.1016/j.biortech.
2015.08.131.
[52] Elreedy A, Ibrahim E, Hassan N, El-Dissouky A, Fujii M,
Yoshimura C, et al. Nickel-graphene nanocomposite as a
novel supplement for enhancement of biohydrogen
production from industrial wastewater containing mono-
ethylene glycol. Energy Convers Manag 2017;140:133e44.
https://doi.org/10.1016/j.enconman.2017.02.080.
[53] Suanon F, Sun Q, Li M, Cai X, Zhang Y, Yan Y, et al.
Application of nanoscale zero valent iron and iron powder
during sludge anaerobic digestion: impact on methane yield
and pharmaceutical and personal care products degradation.
J Hazard Mater 2017;321:47e53. https://doi.org/10.1016/
j.jhazmat.2016.08.076.
[54] Casals E, Barrena R, Garcia A, Gonzalez E, Delgado L,
Busquets-Fite M, et al. Programmed iron oxide nanoparticles
disintegration in anaerobic digesters boosts biogas
production. Small 2014;10:2801e8. https://doi.org/10.1002/
smll.201303703.
12 i n t e r n a t i o n a l j o u r n a l o f h y d r o g e n e n e r g y x x x ( 2 0 1 8 ) 1 e1 2

[55] Feng Y, Zhang Y, Quan X, Chen S. Enhanced anaerobic
digestion of waste activated sludge digestion by the addition
of zero valent iron. Water Res 2014;52:242e50. https://
doi.org/10.1016/j.watres.2013.10.072.
[56] Wang T, Zhang D, Dai L, Chen Y, Dai X. Effects of metal
nanoparticles on methane production from waste-activated
sludge and microorganism community shift in anaerobic
granular sludge. Sci Rep 2016;6:25857. https://doi.org/
10.1038/srep25857.
[57] Guo W-Q, Ren N-Q, Wang X-J, Xiang W-S, Ding J, You Y, et al.
Optimization of culture conditions for hydrogen production
by Ethanoligenens harbinense B49 using response surface
methodology. Bioresour Technol 2009;100:1192e6. https://
doi.org/10.1016/j.biortech.2008.07.070.
[58] Liu B-F, Ren N-Q, Ding J, Xie G-J, Guo W-Q. The effect of Ni2þ,
Fe2þ and Mg2þ concentration on photo-hydrogen
production by Rhodopseudomonas faecalis RLD-53. Int J
Hydrogen Energy 2009;34:721e6. https://doi.org/10.1016/
j.ijhydene.2008.11.033.
[59] Dareioti MA, Vavouraki AI, Kornaros M. Effect of pH on the
anaerobic acidogenesis of agroindustrial wastewaters for
maximization of bio-hydrogen production: a lab-scale
evaluation using batch tests. Bioresour Technol 2014;162:
218e27. https://doi.org/10.1016/j.biortech.2014.03.149.
[60] Li Z, Greden K, Alvarez PJJ, Gregory KB, Lowry GV. Adsorbed
polymer and NOM limits adhesion and toxicity of nano scale
zerovalent iron to E. coli. Environ Sci Technol
2010;44:3462e7. https://doi.org/10.1021/es9031198.

Please cite this article in press as: Zaidi AA, et al., Nanoparticles augmentation on biogas yield from microalgal biomass anaerobic
digestion, International Journal of Hydrogen Energy (2018), https://doi.org/10.1016/j.ijhydene.2018.05.132