Chemosphere 242 (2020) 125080

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Chemosphere
journal homepage: www.elsevier.com/locate/chemosphere

An overview on bioethanol production from lignocellulosic feedstocks

Manju Toor a, 1, Smita S. Kumar a, 1, Sandeep K. Malyan b, Narsi R. Bishnoi a,
Thangavel Mathimani c, Karthik Rajendran d, Arivalagan Pugazhendhi e, *
a
Department of Environmental Science and Engineering, Guru Jambheshwar University of Science and Technology, Hisar, 125 001, Haryana, India
b
Institute for Soil, Water, and Environmental Sciences, The Volcani Center, Agricultural Research Organization (ARO), Rishon LeZion - 7505101, Israel
c
Department of Energy and Environment, National Institute of Technology, Tiruchirappalli - 620 015, Tamil Nadu, India
d
Department of Environmental Science, SRM University-AP, Amaravati, Andhra Pradesh - 522502, India
e
Innovative Green Product Synthesis and Renewable Environment Development Research Group, Faculty of Environment and Labour Safety, Ton Duc Thang
University, Ho Chi Minh City, Viet Nam

h i g h l i g h t s

 Various ethanol production processes with their advantages and shortcomings.

 Singlepot biorefineries, combined bioprocessing, bioenergy with carbon capture are promising.
 Bioconversion process in bioethanol production.
 This review focused on lucrative bioethanol production and the remedial solutions.

a r t i c l e i n f o a b s t r a c t

Article history: Lignocellulosic ethanol has been proposed as a green alternative to fossil fuels for many decades.
Received 1 April 2019 However, commercialization of lignocellulosic ethanol faces major hurdles including pretreatment,
Received in revised form efficient sugar release and fermentation. Several processes were developed to overcome these challenges
25 September 2019
e.g. simultaneous saccharification and fermentation (SSF). This review highlights the various ethanol
Accepted 5 October 2019
production processes with their advantages and shortcomings. Recent technologies such as singlepot
Available online 9 October 2019
biorefineries, combined bioprocessing, and bioenergy systems with carbon capture are promising.
Handling Editor: Veeriah (Jega) Jegatheesan However, these technologies have a lower technology readiness level (TRL), implying that additional
efforts are necessary before being evaluated for commercial availability. Solving energy needs is not only
Keywords: a technological solution and interlinkage of various factors needs to be assessed beyond technology
Lignocellulosic development.
Bioethanol © 2019 Elsevier Ltd. All rights reserved.
Fermentation
Saccharification
Microorganism

1. Introduction
Depriving fossil fuels are the primary energy sources worldwide.
Fossil fuels are non-renewable resources primarily responsible for
the increased carbon dioxide (CO2) level in the environment and
associated climate changes (Barreto, 2018; Saravanan et al., 2018).
Declining petroleum reservoir and its negative impacts on the
environment have raised interest in exploring alternative resources
for energy (Bhatia et al., 2012; Mussatto, 2016). Various alternative
* Corresponding author.
E-mail address: arivalagan.pugazhendhi@tdtu.edu.vn (A. Pugazhendhi).
1
The authors contributed equally as first author to this work.
resources such as solar, geothermal, hydro and wind are available.
Among the resources, solar energy or solar fuels, a rapidly growing
technology, considered as the prospective technology to avert en-
ergy and environmental issues (Reshma et al., 2017). In addition to
the above mentioned renewable energy sources, biofuels are
perceived as a discrete type of alternative and viable renewable
energy due to their non-toxic, biodegradable, and carbon neutral
features (Koley et al., 2018; Mathimani and Mallick, 2019). Different
kinds of biofuels exist in the market as well as under development,
for example, biogas, biodiesel, biohydrogen and biobutanol (Lee,
2016; Saravanan et al., 2018). Yet, the predominant one is un-
doubtedly ethanol (Naik et al., 2010; Ibrahim et al., 2018).
Bioethanol is being used as a fuel since 1826. S. Morey was the

https://doi.org/10.1016/j.chemosphere.2019.125080
0045-6535/© 2019 Elsevier Ltd. All rights reserved.
2 M. Toor et al. / Chemosphere 242 (2020) 125080

1908
14-Dec-47
1992
17-Nov-85
1876
02-Apr-12
Ford Model T
Ethanol blending (E85) 2015
16-Nov-15
Nikolaus Otto uses 1939 - 45
08-Dec-61 act in US
DuPont largest
ethanol in ICE
31-Dec-99 1896
14-Jan-28
Ethanol demand 1975
30-Oct-75 Cellulosic ethanol facility
increases due to Brazil promotes
Samuel Morey uses Henry Ford builds first world war-II ethanol
alcohol in ICE prototype automobile running on ethanol

1899
1826 1899
01-Jul-32 1920 s
26-Mar-55 1970
14-Dec-70 2019
Germany announces Ethanol blending Peak oil crisis
subsidy for ethanol production with gasoline creates interests
in ethanol
1850
29-Apr-05 1980
31-Oct-80 2005
02-Mar-05
Ethanol was used US imposes on E85 becomes
tariffs on cheaper than gasoline
as a lighting fuel Brazil ethanol

Fig. 1. Timeline of developments in using ethanol for transportation.

first to use ethanol as fuel in the American prototype of the internal
combustion engine. Ethanol-driven car and engine were built by
Henry Ford, Nicholas Otto and others in the last years of the 18th
century (Demirbas and Karslioglu, 2007). In order to enhance the
use of ethanol and to decrease the difference in price between
ethanol and gasoline price, the German government provided
subsidies for ethanol during 1899. In 1908, Ford formed a Model T
vehicle with carburettors having flexible fuel capacity, which can
utilize gasoline, alcohol or a ‘‘gasohol’’ mixture (Azhar et al., 2017)
(Fig. 1). The world’s bioethanol production has augmented from 90
billion L in 2012 to approximately 117 billion L in 2014. The United
States, Brazil and China are the largest producers and among them,
USA and Brazil fulfill about 80% of the world’s requirement, mainly
using food crop substrates (corn or sugarcane) (Kang et al., 2010;
Zhao, 2015). China has also spent a large amount of money for
bioethanol production using food crops (Ivanova et al., 2011; Bhatia
et al., 2012). In 2012, there was a sharp decline in ethanol pro-
duction and then, global ethanol production raised in 2013, sur-
passing the production levels of 2011 due to lower costs of grains
and sugar. This increasing trend implied to succeed during the
outlook period and the world ethanol supply should reach
approximately 158 billion L by 2023. Worldwide, both the expen-
diture and production of bioethanol have been estimated to in-
crease from 45 billion liters to 71 billion liters in 2023 and the
volume of ethanol as a fuel would increase up to 5% i.e. to a level of
87.2 billion liters (Outlook, 2014) (Fig. 2) (https://ethanolrfa.org/
resources/industry/statistics/#1549569130196-da23898a-53d8).
Considering the significance of bioethanol being produced
across the world to satiate the energy demand, it is imperative to
comprehend the overall process design of bioethanol production.
Therefore, this comprehensive review aims to describe the overall
process of bioethanol production viz., properties of bioethanol,
various feedstocks used and their structures, phases of production,
different pretreatment techniques adopted for biomass, merits, and
demerits thereof, cellulolytic indigenous microbes and mechanism
of cellulose enzyme. Eventually, the article has attempted to
address the various concerns that impede the lucrative bioethanol
production and the remedial solutions thereof.
2. Physiochemical properties of bioethanol
The octane number of bioethanol is superior with more flame
speed, broad flammability and high heat of vaporization in com-
parison with gasoline. Bioethanol has a high compression ratio,
reduced burning time and lean burn engine, which has made it
superior over gasoline (Balat, 2007; Balat et al., 2008; Splitter et al.,
2016; Carrillo-Nieves et al., 2019). Octane number measures the
engine performance, wherein, a higher number indicates better
combustion. After combustion, ethanol emits less quantity of par-
ticulate matters, hydrocarbons and NOx because of the oxygen
content of ethanol i.e. 35% oxygen. Moreover, the octane number
and combustion efficiency of bioethanol are higher than gasoline.
Properties of ethanol and diesel are given in Table 1. As per MacLean
and Lave, “Despite advantages, bioethanol has some shortcomings
such as lesser energy density (66% of the energy that gasoline),

Fig. 2. Global ethanol production in a heat map as of 2017 (units: million gallons). Rest of the world accounts for 2% ethanol production (Data from: https://ethanolrfa.org/).
 M. Toor et al. / Chemosphere 242 (2020) 125080 3

Table 1 hydrolysis of cellulose (Sun and Cheng, 2002).

Typical physiochemical properties of diesel and ethanol.

Unit Diesel Ethanol

4. Feedstocks for bioethanol production
Density kg/L 0.84e0.86 0.789
Energy content MJ/L 35.6e38.4 23 Based on the feedstock used, the biofuels have been categorized

Cloud point C 9 >8
 as shown in Fig. 3. First generation: fermentation of sugar-based
Flash point C 76 13.5
Viscosity cSt@40C 3 1.2 raw substrates or edible substrates is known as “first generation”
Sulphur Ppm 1e10 e biofuels. First generation fuels are usually made from grains, sugars
Cetane number 48 5e8 or seeds of which, one uses only a specific (usually edible) part and
air/fuel ratio 14.95 9
quite simple processing steps are required to produce a refined fuel
Avg. Molecular weight kg/mol 190 46
Boiling Point 
C 124e330 78 (Azhar et al., 2017; Derman et al., 2018). Second generation:
Heat of Vaporization kcal/kg 232 204 lignocellulosic biomass as the raw substrate is called “second
generation” bio-ethanol. The second generation bioethanol pro-
cesses use sugars released from cellulose, which requires the
small flame luminosity, corrosive nature, lesser vapor pressure additional cost of enzymes to hydrolyze cellulose (Carrillo-Nieves
(making cold starts difficult), water miscibility and toxicity to et al., 2019; Rocha-Meneses et al., 2019). Under second genera-
ecosystems” (MacLean and Lave, 2003). tion, various agricultural byproducts eg. corn stalks or rice husks,
The lower cetane number of ethanol makes it difficult to mix wheat straw, rice straw etc., and non-edible plants eg. trees or
with diesel and possesses less burning efficiency on compression. grasses grown specifically for energy, wood trimmings, sawdust,
Certain emulsifiers such as ethylhexyl nitrate or diterbutyl peroxide bamboo, cotton stocks and other cellulose-containing biomass, can
can enhance the miscibility and cetane number of bioethanol for be used for bioethanol production (Derman et al., 2018; Carrillo-
improving compression ignition (CI) of the engine (Kang et al., Nieves et al., 2019). Third generation: algae can be used as “third
2014; Elfasakhany, 2015). generation” feedstocks for bioethanol production, however, still it
is in early stages (Jambo et al., 2019). Fourth generation: fourth
generation biofuels include metabolic engineering or systems
3. Steps involved in bioethanol production
biology strategies in feedstock modification by using E. coli gene
altercations, which have a high efficiency over yeasts (Azhar et al.,
Bioethanol can be made from diverse cellulosic biomass and
2017; Jambo et al., 2019). In addition, the fourth generation fuels
these feedstocks are classified into the following three types: (i)
include solar fuels or the ones that include carbon capture from the
sucrose containing feedstocks (e.g. sugarcane, sugar beet and sweet
process (Rastogi and Shrivastava, 2017)
sorghum) (ii) starchy compounds (e.g. rice, wheat, corn and barley),
Although bioethanol from algae is a potential technology, still
and (iii) cellulosic biomass (e.g. wood, forestry residue, straw and
there are some limitations and challenges that need to be overcome
grasses). In India, sugarcane molasses is mainly used as the feed-
so as to achieve the commercialization and large-scale production
stock for ethanol production and cane juice is not utilized for this
process at present (Sukumaran et al., 2010; Marvin et al., 2012). The
conversion of cellulosic biomass into simple sugars is an important
process. Cellulosic biomass undergoes the subsequent processes
(Kumar et al., 2016a; Rastogi and Shrivastava, 2017).

 Pretreatment: breaks the rigidity of lignocellulosic structure in

order to access the lignin, hemicellulose and cellulose
molecules.
 Hydrolysis: splits cellulose and hemicellulose molecules into
glucose units.
 Fermentation: sugars fermented using microbes (yeast or bac-
teria) in order to produce ethanol.
 Distillation: separates the products of fermentation.

In concern with pretreatment of lignocellulosic feedstocks for

bioethanol, various physical, catalytic, solvent, biological mode of
pretreatments are being used to decompose lignin in the feedstock
as lignin is a complex polymer to decompose. Further, lignin re-
inforces the strength of crystalline cellulose in the cell wall, middle
lamellae and represents 10e20% in the biomass of grasses and
agricultural residue (Li et al., 2016). The pretreatment methods
were used to decompose lignocellulosic residues into cellulose,
hemicellulose, and lignin for the production of high-value products
(Li et al., 2016). Recent past, hydrothermal based pretreatment of
biomass assisted by AlCl3 provided a more effective approach for
biomass pretreatment (Wu et al., 2015).
Pyrolysis is also used as a pretreatment technique for lignocel-
lulose and it is reported that, at 573 K, cellulosic biomass is
decomposed into gases and char (Sun and Cheng, 2002). Further,
dilute sulfuric acid pretreatment of lignocellulose material are be-
ing studied for hydrolysis of hemicellulose and enzymatic Fig. 3. Various generations of feedstocks for ethanol production.
4 M. Toor et al. / Chemosphere 242 (2020) 125080
of biofuel. Some of the most crucial challenges include the pro-
duction of algal biomass in the required quantity, harvesting of
biomass, efficient low-cost pretreatment of the algal biomass, and
optimization of fermentation. Moreover, microalgae may not pro-
duce important metabolites under normal conditions (Khan et al.,
2018; Zhang et al., 2019).
Lignocellulose includes such diverse sources as switch grass,
cornstalks, wood, herbaceous crops, waste paper and paper prod-
ucts, agricultural and forestry residues, pulp and paper mill waste,
municipal solid waste and food industry waste. Unlike starch-based
biomass, lignocellulosic materials are structurally complex. Native
lignocellulosic biomass, a heterogeneous, is composed of cellulose,
hemicellulose, lignin, protein, ash, and minor extractives. Even
though ethanol production depends on the feedstock used, it can be
generally categorized into three chief steps: pre-treatment of raw
materials to obtain fermentable sugars, conversion of sugars to
ethanol via fermentation, and finally distillation and purification of
ethanol produced (Khan et al., 2018). Fig. 4 illustrates the produc-
tion of bioethanol from lignocellulose biomass.
4.1. Cellulosic biomass and composition
Cellulosic material degradation has gained popularity in
research because of the global availability of those materials and
huge possibilities of their conversion into simple sugars and as
substitutes to fossil fuel (Arnoult et al., 2015; Carrillo-Nieves et al.,
2019). Various countries are in the track of bioethanol production in
an demonstration scale. Bioethanol is produced at about 700,000 L
from lignocellulosic sources in Canada per year and in North
America, numerous lignocellulosic bioethanol plants have been
planned (Sirajunnisa and Surendhiran, 2016).
Available cellulosic biomass can be categorized into primary
sources (sugarcanes, short rotation energy crop plantations),
Enzym e production H ydrolysis
SH F
SSF
SSCF
CBP
Fig. 4. Key fermentation strategies for ethanol production.
secondary sources (residues from processing) and tertiary sources
(a residue left during and after the process ends) (Arnoult et al.,
2015; Datta and Mandal, 2016). Cellulosic biomass, usually, has
50e80% complex carbohydrates containing C6 and C5 sugar units.
Therefore, this complex robust structure requires a multistep pro-
cedure such as e pretreatment, enzymatic hydrolysis and fermen-
tation (which increases the cost of biofuel manufacturing) in order
to be converted into biofuels (Klein-Marcuschamer et al., 2012;
Kumagai et al., 2014; Salehi Jouzani and Taherzadeh, 2015). There
are three main components of vast indigenous cellulosic biomass
i.e. cellulose, hemicelluloses and lignin. Cellulose and hemi-
celluloses (naturally comprising approximately two third of the dry
biomass) components can be easily fermented to ethanol whereas
lignin cannot. These three components form microfibrils that are
further organized into macrofibrils, which provide structural
strength to plant cell walls (Rubin, 2008).
Cellulose is the most abundant organic component on earth
(Glazer and Nikaido, 2007). It has a flat ribbonlike structure made
up of thousands of glucose molecules, which are linked together.
Cellulose has to be converted into glucose before the fermentation
process (Glazer and Nikaido, 2007; Qin et al., 2016; Dos Santos
et al., 2018). The hemicelluloses are complex polysaccharides
with lower molecular weights than cellulose and structurally ho-
mologous to cellulose. Hemicelluloses contain small profusely
branched chains of different sugars: namely, xylose and arabinose
(pentose), glucose, galactose and mannose (hexose), deoxyhexoses
(L-rhamnose) and uronic acids (D-glucoronic acid) (Glazer and
Nikaido, 2007; Dos Santos et al., 2018). Hemicelluloses also
contain some fraction of non-sugars i.e. acetyl groups (Hamelinck
et al., 2005). In comparison to cellulose, the hydrolysis of hemi-
celluloses is somewhat simple and easy because of the branched
structure and amorphous nature. They do not form aggregates
(Pe
rez et al., 2002; Wu et al., 2016) even when they are co-
C6 Fermentation C5 Fermentation
 M. Toor et al. / Chemosphere 242 (2020) 125080
crystallized with cellulose chains. Lignin is the component of the
cell walls of plants, ferns and club mosses. It is heteropolymeric,
amorphous in nature and insoluble in water. Lignin, a composite
aromatic macromolecule, is shaped by polymerization of phenyl-
propane alcohols (p-coumarilic, coniferilic and synapilic alcohols)
(Milagres et al., 2011). As the molecular weight of lignin is high
(Demirbas, 2009), it smears into the cell walls of the plant and
binds the cells mutually. It is not easily degradable, only a few
microbes can degrade it into highvalue products i.e. organic acids,
phenols and vanillin (Pe €

rez et al., 2002; Ohgren et al., 2006a;
Kobayashi and Fukuoka, 2013).
4.2. Water hyacinth as a substrate
Water hyacinth (Eichhornia crassipes) is a freshwater mono-
cotyledonous aquatic weed, a native of Amazon River, Brazil, South
America (Parsons et al., 2001; Mukaratirwa-Muchanyereyi et al.,
2016). In 1884, water hyacinth plant was introduced into USA
(Penfound and Earle, 1948) and in the 1930s it entered Europe
(Portugal) (EPPO (European and Mediterranean Plant Protection
Organization), 2008) and later, introduced as an ornamental plant
in the Asian countries. It is well known for its ecological, environ-
mental and socioeconomic impacts (Villamagna and Murphy,
2010). Water hyacinth trims down dissolved oxygen (DO) concen-
trations, which is one of the most vital water quality parameters for
aquatic life (Perna and Burrows, 2005), by arresting the mixing of
oxygen from the air into the water body. It favors nutrient enriched
water and can easily be adapted to great deviations in nutrients,
temperature, pH and toxic substances if present. It can survive at a
varied ranges of pH and temperature (DiTomaso and Healy, 2003;
Wilson et al., 2005). Water hyacinth spreads extremely fast lead-
ing to huge biomass (about two tons of biomass per acre) within
5e15 days (Craft et al., 2003; Mukaratirwa-Muchanyereyi et al.,
2016). According to Ubate
(2005) Water hyacinth increases biomass
up to 12% per day and biomass accumulation rate can range from
7.7 to 60 g/m2/day. Because of these, it is troublesome to human
population and recognized as ‘Blue Devil’ or ‘Bengal terror’ in our
country (India), ‘German weed’ in Bangladesh, ‘Florida devil’ in
South Africa and ‘Water terror’ in the South West of Nigeria. Water
hyacinth is normally detached by three methods i.e. manually by
hand pulling/cutting, biological control (eg., introduction of insects
to destroy water hyacinth) and mechanical removal.
The enormous growth rate and favorable chemical composition
(18e35% cellulose, 18e49% hemicelluloses and 3.5e9% lignin) of
water hyacinth makes it a superior substrate for bioethanol pro-
duction (Mishima et al., 2008; Ganguly et al., 2012; Singh and
Bishnoi, 2013). As it is aquatic, no matter of competition arises
with the food crops from the arable land resources. Water hyacinth
for ethanol production will also serve the purpose of weed reduc-
tion (Aswathy et al., 2010; Singh et al., 2013) and can provide
employment and source of earning in rural areas. Water hyacinth
can also be converted into biogas as well as biofuel (ethanol) and
this opportunity is presently realized by various developing coun-
tries, especially in India.
5. Fermentation process and mechanism
Fermentation is the process of converting cellulosic biomass
(containing glucose and other sugars) to bioethanol using microbes
such as yeast (Liu et al., 2019a; Xia et al., 2019). For this biological
path, microorganism selection depends upon the conditions and
types of substrates to be fermented into alcohol, lactic acid and/or
other products. S. cerevisiae has been extensively used in fer-
menting industry i.e. brewery and wine industries for many years.
5
Typically, in the batch process, S. cerevisiae has fermented hexose
sugars, chiefly glucose, into ethanol in the big tank by way of
Embden Meyerhof Pathway (EMP) under optimized temperatures
and anaerobic environments. S. cerevisiae can yield high ethanol
(90% of the theoretical) using hexose sugars. Yeast-based fermen-
tation is supplemented with nitrogen in order to augment the re-
action and CO2 is produced as the byproduct, usually (Gombert and
van Maris, 2015; Sulieman et al., 2016; Liu et al., 2019a; Xia et al.,
2019).
5.1. Role of microorganisms in fermentation
Microorganisms of different generaproduce diverse range for
fermentation products. S. cerevisiae is the mainly accepted yeast for
fermentation because of its high ethanol yields and high tolerance
limits (Ishola et al., 2013; Surendhiran and Sirajunnisa, 2019; Xia
et al., 2019). S. cerevisiae has fermented only the hexose sugars
present in the hydrolyzate but not the pentose sugars (Talebnia,
2008; Kumar et al., 2016b). The effective yeasts having the capa-
bility of fermenting both C5 and C6 sugars include Pichia stipitis,
Candida shehatae and Pachysolan tannophilus but their yields of
ethanol were approximately five-fold less than S. cerevisiae using
glucose (Solomon and Johnson, 2009; Singh and Bishnoi, 2012a,
2012b, 2013). High intracellular ethanol was accumulated while
using S. cerevisiae, which showed an inhibitory effect on the growth
and fermentation capacity of S. cerevisiae, thus, making it a subject
of huge controversy. Other microorganisms used in the fermenta-
tion process include Escherichia coli, Candida brassicae, Pachysolen
tannophilus, Candida shehatae, Pichia stipitis, Zymomonas mobilis
and Mucor indicus (Talebnia, 2008; Sarkar et al., 2012; Adnan et al.,
2014; Xia et al., 2019). Scientists have also found Brettanomyces
clausenii yeast to act on cellobiose and it can be used in simulta-
neous saccharification and fermentation (SSF) of cellulose to
ethanol (Bhatia et al., 2012).
6. Types of fermentation in bioethanol production
The traditional design engaged for fermentation of hydrolysate
of biomass has a definite procedure in which the fermentation is
performed in different types after cellulose hydrolysis. The con-
ventional batch fermentation, fed-batch, continuous fermentation,
and also solid state fermentation, separate hydrolysis and
fermentation, simultaneous saccharification and fermentation,
Nonisothermal simultaneous saccharification and fermentation,
simultaneous saccharification and co-fermentation, simultaneous
saccharification, filtration and fermentation were practiced for
bioethanol production.
6.1. Separate hydrolysis and fermentation
In separate hydrolysis and fermentation process, lignocellulosic
material is decomposed into monomeric sugars through enzymatic
saccharification, which will be further converted into ethanol
(Rastogi and Shrivastava, 2018). It’s a kind of conventional bio-
ethanol production method where saccharification and fermenta-
tion processes are performed separately, which is time-consuming
and expensive. The key advantage of this process is hydrolysis and
fermentation can operate at their specific standardized reaction
conditions. The major limitation of the separate hydrolysis and
fermentation (SHF) process is cellulase activity inhibition by the
sugars released in the hydrolysis phase (So €derstro
€ m et al., 2005;
Salehi Jouzani and Taherzadeh, 2015; Tavva et al., 2016). Recent
past, various integrated techniques of hydrolysis and fermentation
were established in the case of hydrolysis.
6 M. Toor et al. / Chemosphere 242 (2020) 125080
6.2. Simultaneous saccharification and fermentation (SSF)
Recently, simultaneous saccharification and fermentation
method is used wherein biomass saccharification is coupled with
simultaneous fermentation of sugars in single reactor (Rastogi and
Shrivastava, 2018). On a simpler note, in SSF process, lignocellulosic
biomass undergoes decomposition and fermentation simulta-
neously. In this strategy, the enzymes are used up to maximum
levels such that the soluble sugar concentration does not reach the
level of inhibition of the fermentating microorganisms (Da Costa
Nogueira et al., 2019; Siriwong et al., 2019). The overall ethanol
production in SSF is usually better than SHF. The merits of SSF
include that the hydrolysis goods i.e. glucose and cellobiose units
do not inhibit cellulase activities because of the immediate action of
simultaneous fermentation (Sakimoto et al., 2017). For the first
time, South et al. (1993) reported the simultaneous/continuous
conversion of pretreated hardwood floor to ethanol using
S. cerevisiae along with the cellulase enzymes and C. thermocellum
strain. Fan et al. (2003) evaluated a semicontinuous, simultaneous
saccharification and fermentation system for proficient paper
sludge conversion to ethanol and achieved an average conversion
of 92% and 42 g/L ethanol when cellulose loading was 82 g/L and
the enzymes were 20 FPU g/L/d. Kumagai et al. (2014) also reported
that the development of a SSF process was perfect for the pro-
duction of ethanol from Hinoki cypress and Eucalyptus after
fibrillation by steam-pretreatment and subsequent wet-disk mill-
ing. Pothiraj et al. (2014) worked on simultaneous saccharification
and fermentation of cassava waste. They found that a mixture of
amylase and amyloglucosidase (AMG) has resulted in a high rate of
saccharification (79.6%) than the amylase alone (68.7%) in simul-
taneous saccharification and fermentation (SSF). The main limita-
tion of SSF is that the optimal temperature required for cellulase
activity is generally higher than the appropriate temperature
required for yeast activity and numerous bacterial biofuel
fermentation strains (Bhalla et al., 2013; Kumagai et al., 2014; Wang
et al., 2015).
6.3. Batch fermentation
In batch fermentation, the microorganisms have to function at
high substrate concentrations in the starting phase of the experi-
ments but in the end, they have to work at high product concen-
trations. The batch process requires a number of vessels and in this
mode; the process is easily controlled but provides lower yields
after exhaustive operations. Before batch fermentation, the com-
plex preliminary task is required and high labour costs are incurred
with this process because of irregular starting and close down
operations. Due to these innate drawbacks and lower yields, the
commercial market believes in shifting towards other fermentation
techniques (Puligundla et al., 2018; De Araujo Guilherme et al.,
2019; Liu et al., 2019a).
6.4. Fedbatch fermentation
In fedbatch fermentation, microbes provide improved yields of
metabolites frequently in comparison to the batch mode. As cell
mass density rises in the mixture, specific ethanol productivity
declines. However, in fed-batch fermentation, the feed rate is
limited and therefore, the cell mass density is not increased in
excess. Hence, the cell mass concentration has to be maintained at a
specific level, which provides the highest ethanol productivity
(Ariyanti et al., 2014; Moshi et al., 2014; Phukoetphim et al., 2018).
Moshi et al. (2014) proposed a fed-batch simultaneous saccharifi-
cation and fermentation approach to overcome the inhibition of
S. cerevisiae due to high sugar concentrations, which resulted from
the enzymatic hydrolysis of starch-rich wild cassava.
6.5. Continuous fermentation
Continuous fermentation is performed in bioreactors such as
single or series stirred tank reactors, plug flow reactors etc.
Continuous fermentation results in high ethanol output compared
to the batch mode (Phwan et al., 2018). It works at a lower dilution
rate but provides maximum productivity. Continuous operations
are generally easy to control and are not as much laborious as the
batch one but there is a serious issue of contamination with this
operating method (Mahboubi et al., 2017; Carrillo-Nieves et al.,
2019). When an interruption occurs within the process, the whole
equipment set up has to be cleaned and the process has to be
started again with the new inoculum. The continuous method
eliminates expenditure of time on cleaning, recharging, media
adjustment and sterilization. In the exponential phase, a high cell
concentration of microbes is achieved within the continuous
fermenter, which gives higher production and short processing
time, nearly 4e6 h less in comparison to the batch fermentation i.e.
24e60 h. As a result, it saves extensive labour and trims down ex-
penses as it achieves a specific production with a smaller plant
(Chan et al., 2007).
6.6. Solid state fermentation
Solid state fermentation (SSF) is the process of microorganisms
nurturing insufficient moisture so as to support microbial growth
within the solid insoluble substrate. SSF conditions are mainly
appropriate for the growth of microbes i.e. bacteria, yeasts and
filamentous fungi on solid substrates as SSF raises the chances of
using them in bioprocess (Ortiz et al., 2016; Marín et al., 2019;
Salom~ ao et al., 2019). The solid matrix of the substrate is either
used by the microorganisms or it serves as an inert support for their
growth (Singh et al., 2011). Major factors for the success of SSF are
the suitability of the selected substrates and their suitable particle
sizes. Small size particles have better exposed surface areas and
thus, the accessibility of the microorganisms for their nutrition is
improved. On the basis of the type of substrate and moisture level,
the material gets compacted, which results in impairing of aeration,
heat dissipation and limits the microbial growth, but large size
particles make aeration possible. Microbial growth is hindered
because of restrictive substrate contact area and difficulty in heat
transfer (Pandey et al., 2000; Ortiz et al., 2016). Pandey (2003) also
evaluated and optimized some other factors such as initial mois-
ture, aeration, pH, temperature, nutrient supplementation, inoc-
ulum size, final product extraction and purification for high process
efficiencies.
The most adapted microorganism for solid state fermentation is
the filamentous fungi because with their hyphae, they can easily
grow and cover the particle surfaces and simultaneously, penetrate
within the intraparticle channels and, make their colonies over the
solid residues (Koyani and Rajput, 2015; Saloma ~o et al., 2019). The
use of SSF for filamentous fungal growth is advantageous because it
provides natural habitat and thus, makes it easy for the fungi to
grow and adapt in the environment. As a result, the production of
enzymes is also better. Other advantages of this process are
decreased risks of bacterial contamination as free water is absent;
more concentrated enzymes are produced, which can be extracted
with a small amount of water (Kapilan, 2015). When compared
with submerged fermentation, SSF uses less water and thus, results
in a reduction in the effluent generation, lesser space and minimum
energy requirement, stable product formation and minute protein
deprivation (Pandey et al., 2000; Pandey, 2003).
 M. Toor et al. / Chemosphere 242 (2020) 125080
6.7. Non-isothermal simultaneous saccharification and
fermentation
In simultaneous saccharification and fermentation, glucose
formed as a result of hydrolysis, is instantaneously taken up by the
microorganisms for fermentation; hence, the inhibition effects of
cellobiose and glucose are declined to a minimum. As mentioned
earlier, the main problem linked with the SSF method is the
different optimal temperatures for the hydrolytic enzymes and the
fermenting microorganisms (Romaní et al., 2012; Goshadrou et al.,
2013; Siriwong et al., 2019). In this method of SSF, the operating
temperature of enzymatic hydrolysis is lower than the optimum,
which affects enzyme activity, significantly and consequently, can
cause increased enzyme consumption (Ka
d

ar et al., 2004;
Taherzadeh and Karimi, 2007). To overcome this problem, non-
isothermal simultaneous saccharification and fermentation has
been recommended. In this method, enzymatic hydrolysis is car-
ried out fairly at optimum temperature and after media inocula-
tion; temperature is set at an optimum value for the
microorganisms (Goshadrou et al., 2013). In this type of fermen-
tation, both saccharification and fermentation are carried out in
two separate reactors simultaneously at different temperatures.
Pretreated cellulosic biomass is moved to a hydrolysis reactor
where hydrolysis with the help of enzymes is carried out at opti-
mum temperature (50  C), then, the hydrolyzed effluent is fer-
mented in a fermenter, which is set at the optimum temperature for
alcohol-producing microorganisms (30  C). It has been found that
the cellulase activity would increase up to two to three times when
the hydrolysis temperature is 50  C instead of 30  C and the need of
total enzymes is also reduced to 30e40% compared to the condi-
tions employed in SSF (Taherzadeh and Karimi, 2007).
6.8. Simultaneous saccharification and co-fermentation (SSCF)
During alcohol production process from cellulosic materials,
alcohol concentration is an important factor in addition to yield.
The distillation cost affects the process; as the final alcohol con-
centration increases, there is a decrease in the distillation cost (Jin
et al., 2012; Romaní et al., 2012; Liu et al., 2019b). Disadvantage
coupled with SSF is the use of only hexose sugars except for pen-
toses. In this method, the viscosity of the medium is maintained
low by slowly feeding new substrates into the reactor. In addition,
the effects of hydrolysate toxicity are decreased because of yeast
adaptation and gradual biological detoxification. This scheme may
also have encouraging effects on xylose uptake due to significant
changes in the xylose to glucose concentration ratio in the reaction
mixture (Hodge et al., 2009; Zhang et al., 2009; Olofsson et al.,
2010a). Generally, glucose concentration affects xylose uptake
negatively in S. cerevisiae and therefore, must be kept low for
attaining a proficient xylose uptake. While keeping glucose con-
centration as low as possible, there is an increase in xylose/glucose
ratio, which is required for the co-fermentation process of hexose
and pentose (Ko €tter and Ciriacy, 1993; Meinander et al., 1999;
Moyse
s et al., 2016). Clearly, in cellulosic ethanol production, in
addition to hexose sugar fermentation, pentoses fermentation is
also an inevitable course of action because of the high xylan content
of the cellulosic materials. However, ethanol concentration using
pentose sugars fermentation is usually too squat (<10 g/L) and
therefore, it is not economic to be distilled (Jin et al., 2012; Ullah
et al., 2014; Yasuda et al., 2014). As a result, co-fermentation of
hexose and pentose sugars is performed using different wild and
recombinant microorganisms using diverse cellulosic biomass.
SSCF process is analogous to SSF except for the fermentation of
hexose and pentose sugars covered in a single step.
7
SSCF, a cascade process, involving microbial assimilation of
sugars released from the pretreatment process and concurrent
hydrolysis of lignocellulosic material (Koppram et al., 2013). SSCF
technology has a potential to trim down the total cost of alcohol
production as pentose sugars are also used during the process and
the inhibitory effects of xylose are also reduced (Zhang and Lynd,
2010). The main advantage of SSCF in contrast with the separate
hydrolysis and co-fermentation is the simultaneous fermentation
of the released glucose which maintains the glucose concentration
within the medium. It minimizes the inhibition caused by the end
product during enzymatic hydrolysis step and also increases xylose
to glucose concentration ratio and thus, diverts the fermenting
microorganism to consume xylose (Olofsson et al., 2010a, 2010b).
Previously, this technology was used for both ethanol and lactic
acid (Patel et al., 2005; Zhu et al., 2007; Zhang et al., 2009; Kang
et al., 2010).
6.9. Simultaneous saccharification, filtration and fermentation
The enzyme cocktail and fermenting microbe work best at their
optimum conditions. In a SSF process, both of these parameters will
be traded-off. Furthermore, the fermenting microbes cannot be
reused in a SSF process as they are mixed in the slurry with
biomass. One of the solutions to this problem is the simultaneous
saccharification, filtration and fermentation (SSFF) process. In SSFF,
enzymes are recycled back to hydrolysis step via a filtration
membrane while fermenting microbes are retained via flocculation
and internal settling mechanisms. This process, thus, provides op-
timum conditions yet avoids enzyme inhibitions (Ishola et al., 2013;
So
ti et al., 2018).
6.10. Direct microbial conversion/consolidated bioprocessing
Depolymerizing cellulosic biomass to simple sugars is a multi-
step complex route, which includes the loosening of structural
complexity present in lignocelluloses, pectin hydrolysis, lignin
decomposition, hemicellulose depolymerization and cellulose hy-
drolysis (Mazzoli et al., 2012; Salehi Jouzani and Taherzadeh, 2015;
Kumar et al., 2016b). The substrate, enzymes and pretreatment cost
would account for roughly two-thirds of the total production cost
of which the enzyme cost is primary (Himmel et al., 2007). This cost
restraint can be overcome by designing and constructing strong
cellulolytic and fermenting microbes and using them in a direct
microbial conversion/consolidated bioprocessing (CBP) system
(Parisutham et al., 2014). CBP has been known as the most hopeful
fermentation approach for bioethanol production using cellulosic
materials and studies have been increased for this purpose in
recent years. However, CBP is yet in its premature stage of estab-
lishment and hence, more research work is required on this. In CBP,
different actions including enzyme production, enzymatic
saccharification/hydrolysis and then, fermentation of the resultant
sugars to bioethanol or any other valuable products are carried out
simultaneously (Daniel et al., 2012; Kumagai et al., 2014;
Parisutham et al., 2014). During the last decade, a number of
wildtypes and genetically-engineered bacteria, fungi and yeasts
have been employed in CBP (Schuster and Chinn, 2013).
Recent advancement in bioethanol production was taken place
in order to increase the bioethanol yield both at processing and
feedstock improvement. Lignocellulosic biomass is hydrolyzed to
fermentable sugars with the help of many strategies. Therefore, an
efficient and economical viable technique is of interest in ethanol
production. Among the methods, enzymatic method is preferred
and has been reported to be environmentally benign. Still this
technology is rather immature and there are challenges that need
8 M. Toor et al. / Chemosphere 242 (2020) 125080
to be addressed so as to make it commercially viable. A couple of
the main obstacles hindering the practical application of enzymatic
biotransformation technology for lignocellulosic biomass are the
higher enzyme production cost and low production efficiency. Be-
sides, owing to the heterogeneity and compositional variability of
lignocellulosic biomass, the same enzyme may not be efficient for
all and hence a cocktail of multifunctional enzymes can prove to be
more efficient. Various approaches that can be employed for
improvement of enzymes include but are not limited to the
development of novel enzymes having the capability to hydrolyze a
wide range of feedstocks, identification, isolation and purification
of such enzymes in high titers, improvement of efficient enzymes
with the help of genetic/molecular approaches, and reducing the
cost of production (Binod et al., 2019). Hence, all these factors
should be taken into consideration before selecting a particular
enzyme-based strategy. Further, major research works have been
undertaken recently on improving the tolerance capability of yeast
towards ethanol, withstanding high substrate concentration, to
avoid bacterial contamination risk for increasing bioethanol pro-
duction efficiency.
6.10.1. Advantages of CBP
It is recommended that CBP is a capable approach, which will
check the cost and limitations of conventional biofuel production
from cellulosic biomass. CBP technology uses single microbe or
consortium for the enzyme production, cellulosic saccharification
and fermentation process in a single step. This is an alternative
approach with outstanding prospects. This may improve the effi-
ciency of the whole process, elimination of external hydrolytic
enzyme addition and minimize the inhibition caused by sugars on
cellulases (Daniel et al., 2012; Rastogi and Shrivastava, 2017). CBP is
an alternative technology, which decreases the total capital cost by
cutting down various operations of the conventional method
(Daniel et al., 2012; Parisutham et al., 2014). Normally, the final
production of simple sugars inhibited saccharification capacity in
the conventional systems while in CBP, fermentation converts
sugars to bioalcohol, simultaneously before they become inhibitory
to hydrolysis (Dashtban et al., 2009; Salehi Jouzani and Taherzadeh,
2015). CBP microbes do not require external saccharifying enzymes
as the same (i.e. cellulolytic and hemicellulolytic enzymes) can be
produced by them for cellulose decomposition, which results in
large cost savings (Lu et al., 2006; Rastogi and Shrivastava, 2017).
CBP systems appreciably cut down the number of unit operations
(i.e., fewer reactor vessels) and as a result, maintenance and capital
costs are decreased (Xu et al., 2009; Den Haan et al., 2015). Adding
to this, if the efficient microorganisms are found, the pretreatment
step could be avoided partially or completely (Daniel et al., 2012;
Schuster and Chinn, 2013).
As stated above, the fermentation process is especially impor-
tant for the preparation of bioethanol. Fermentation can be carried
Table 2
A representative yield using different methods of fermentation with different feedstocks.
Fermentation method Conditions
SSF (Continuous) 33  C, 56 h, 25% WIS
SSF (Batch) 38  C, 150 rpm, 96 h, 36.1% WIS
SSF (Batch) 30  C, 150 rpm, 96 h, 1% WIS
SSF (Semi fed-batch) 36  C, 60 h, 10% WIS
SSF (Fed-batch) 30  C, 700 rpm, 72 h, 10% WIS
SSF 30  C, 96 h, 10% WSF
SSF 37  C, 348 rpm, 72 h, 7.5% WIS
SHCF (Fed-batch) 32  C, 300 rpm, 120 h, 7.5% WIS
SSCF (Batch) 3  C, 96 h, 8% WIS
SHF (Batch) 32  C, 500 rpm, 96 h, 10% WIS
out in solid state fermentation i.e. without any free water or in
stirred tank reactor in liquid state fermentation (Yadav, 2017). A
special low-cost medium containing only inorganic salts, or
manure in certain quantity is used. Researchers have also studied
the comparative assessment of different techniques of fermenta-
tion using the same feedstock. Aspergillus niger isolated from coir
was used for cellulase production through solid state and sub-
merged fermentation (Mrudula and Murugammal, 2011). As
compared to submerged, cellulase production was found to be
better in solid state fermentation in less time. In case of solid-state
fermentation cellulase production maximized in 76 h whereas it
took 96 h to produce maximum cellulase in case of submerged
fermentation. Generally, simultaneous saccharification and
fermentation and simultaneous saccharification and co-
fermentation are preferred over separate hydrolysis and fermen-
tation due to the involvement of single reactor in the former (Azhar
et al., 2017). Moreover, both these processes are cost-efficient, and
give high ethanol yield in a shorter time as compared to separate
hydrolysis and fermentation (Chandel et al., 2007). A strategic
method for cost-efficient bioethanol production in less time is cell
recycle batch fermentation. In addition to easy cell collection, a few
other advantages of this process include stable and long-term
productivity. Simultaneous saccharification and fermentation in
integration cell recycle batch fermentation was successfully used to
ferment cassava starch with the help of flocculating yeast (Matano
et al., 2013). On the other hand, its application was found to be
extremely difficult in simultaneous saccharification and fermen-
tation of lignocellulosic materials due to the presence of residual
lignocelluloses in the fermentation medium along with yeast cells
(Choi et al., 2009). A representative yield using different methods of
fermentation with different feedstocks is illustrated in Table 2.
SSF has been reported to be more economic and sustainable as
compared to SHF due to prevention of sugar loss, lesser cost
involvement and biomass doesn’t need to be separated from the
hydrolysate (Di Donato et al., 2019; Hans et al., 2019). Kang et al.
reported 69.2% of bioethanol concentration during continuous SSF
of Miscanthus sacchariflorus (Kang et al., 2015). Li et al. reported a
concentration of 55.5% using Reed as a feedstock in batch mode (Li
et al., 2009). While, in semi fed-batch mode, using the same feed-
stock, bioethanol concentration declined to 39.4 (Lu et al., 2013). In
€
case of Corn stover, it was found to be 25.7% (Ohgren et al., 2006a,
2006b). Whereas, in case of Miscanthus giganteus, the concentra-
tion was found to be 12.1% (Scordia et al., 2013). The concentration
obtained during fed-batch SHCF of wheat meal and wheat straw
was 53.3% (Erdei et al., 2012). On the other hand, CBP is more
suitable in terms of simplicity, energy needs, yield efficiency and
cost of production as compared to SHF and SSF. In SSCF, both hexose
and pentose sugars are saccharified simultaneously by the co-
fermenting microbes. SSCF of wood chips in batch mode yielded a
concentration of 32.9% (Olofsson et al., 2010a, 2010b). It can be
Feedstock Bioethanol Bioethanol References
concentration productivity
Miscanthus sacchariflorus 69.2 1.24 Kang et al. (2015)
Reed 55.5 0.57 Li et al. (2009)
Liriodendron tulipifera 29.9 0.42 Koo et al. (2011)
Reed 39.4 0.66 Lu et al. (2013)
Corn stover 25.7 0.36 €
Ohgren et al. (2006b)
Miscanthus giganteus 12.1 0.13 Scordia et al. (2013)
Industrial hemp 21.3 0.30 Sipos et al. (2010)
Wheat meal and wheat straw 53.3 0.44 Erdei et al. (2012)
Wood chips 32.9 0.34 Olofsson et al. (2010b)
Arundo donax 20.6 0.21 Ask et al. (2012)
 M. Toor et al. / Chemosphere 242 (2020) 125080
stated that the concentration and productivity of bioethanol pro-
duction depends both on the feedstock as well as fermentation
technique and also same fermentation technique is not equally
suitable for all the feedstocks. Hence, the process needs to be
optimized for key factors governing the process.
7. Conclusion and future perspectives
Ethanol is the most adaptable and promising alternative biofuel
to gasoline. Even though the energy equivalence of ethanol is lower
than petroleum fuel, ethanol have cleaner combustion. There are
certain demerits still associated with the production of bioethanol
but considering the developing technologies employed in bio-
ethanol production, these drawbacks can be corrected easily. In
spite of all the advantages associated with the production of bio-
ethanol from lignocellulosic feedstocks, it also suffers from some
crucial bottlenecks. First of all, owing to the complexity of ligno-
cellulosic materials, i.e. crystallinity of celluloses, hemicellulose
sheathing, and issues related to lignin make these substrates
difficult for enzymatic attack so that production of bioethanol from
these substrates is complex and challenging. Suitable methods of
pretreatment need to be developed to enhance the efficiency of
enzyme activity that make the substrates available for the action of
cellulolytic enzymes. Thus, the main issue is development and
commercialization of cost-effective pretreatment technology to
deal with recalcitrant nature of lignocellulosic materials. Efficiency
of pretreatment also determines the enzyme dose needed in the
next step of hydrolysis. Moreover, the cost of enzymes also needs to
be reduced and efficiency needs to be increased. Thus, the limita-
tions of this process are basically related to feedstock pretreatment,
enzymatic degradation of pretreated feedstock, and then finally
fermentation of both pentose and hexose sugars released during
hydrolysis as well as saccharification. Each of these steps necessi-
tates considerable research and development to improve the effi-
ciency and economics of these processes. In addition to the
pretreatment issues, inhibitors formed cellulosic biomass pre-
treatment may reduce the ethanol yield. It can be overcome by
overliming treatment and simultaneous extraction of inhibitors
with any adsorbent resin preferably nonionic polymer. These
methods need to be demonstrated at largescale to enhance the
ethanol productivity. Novel techniques such as cell-surface tech-
nology can be employed for the production of bio-ethanol in a
single reactor while using single host cell. For instance, yeast cells
have been modified using the same technique to mimic xylanase
activity. Similarly, they can be modified to co-display other en-
zymes involved in the conversion of cellulose to glucose and then
subsequently to bio-ethanol. Moreover, foremost initiatives are
required in comprehensive process incorporation of process sce-
nario, cost and possible advances weighted against it. Even though
lignocellulosic bioethanol is not cost-efficient as compared to gas-
oline or starch-crop based ethanol, supplementary progress in this
field in addition to ample quantities of low-cost substrates, could
take it to a commercially viable option in future.
Therefore, this review has provided a detailed idea on different
technologies, feedstocks and the steps necessary for making bio-
ethanol as the cost-effective, reliable and easily available biofuel for
the growing human race. However, the major challenge for bio-
ethanol production is the availability of feedstock or substrate,
contamination during fermentation, laborious and costlier
methods for the conversion of cellulosic biomass substrate into
bioethanol. Replacement of substrates with cellulose, lignocellulose
and algal biomass will reduce the threat to food crops available for
human consumption, which could also meet the current demands.
Use of renewable sources such as sugar cane, corn, wheat (first
generation), cellulose biomass (second generation) and algal
9
biomass (third generation) will reduce the costs. However,
encouraging algae cultivated in wastewater will provide a syner-
gistic benefit to the fermentation industries and environment. In-
clusion of condenser and reboilers in the ethanol distillation train,
application of very high gravity fermentation, integration of per-
vaporation membranes for developing hybrid process, replacement
of ethanol dewatering process with membrane technology and use
of microfiltration of the growth media to prevent heat exchange
and microbial contamination during fermentation are some im-
provements needed in the ethanol production process. To conclude,
including these improvisations will promote effective and cheaper
bioethanol production strategies for the future generation.
Acknowledgement
The authors would like to thank IGPRED (www.igpred.com) for
providing insight and expertise on the research topic and for the
assistance that greatly improved the manuscript.
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