Bioresource Technology 178 (2015) 178–186

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Bioresource Technology
journal homepage: www.elsevier.com/locate/biortech

Review

Anaerobic digestion of lignocellulosic biomass: Challenges

and opportunities
Chayanon Sawatdeenarunat a, K.C. Surendra a, Devin Takara a, Hans Oechsner b, Samir Kumar Khanal a,⇑
a
Department of Molecular Biosciences and Bioengineering (MBBE), University of Hawai’i at Mānoa, 1955 East-West Road, Agricultural Science Building 218, Honolulu, HI 96822, USA
b
University of Hohenheim, State Institute of Agricultural Engineering and Bioenergy, Garbenstrasse 9, Stuttgart 70599, Germany

h i g h l i g h t s

 Anaerobic digestion of lignocellulose can sustainably produce renewable energy.

 Anaerobic co-digestion is a promising technology to improve digester performance.
 Solid-state anaerobic digestion could efficiently digest high solid organics.
 Rumen microbes can be an effective inoculum for the digestion of lignocelluloses.
 Anaerobic biorefinery could provide both bioenergy and valuable biochemicals.

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

Article history: Anaerobic digestion (AD) of lignocellulosic biomass provides an excellent opportunity to convert
Received 31 July 2014 abundant bioresources into renewable energy. Rumen microorganisms, in contrast to conventional
Received in revised form 19 September microorganisms, are an effective inoculum for digesting lignocellulosic biomass due to their intrinsic
2014
ability to degrade substrate rich in cellulosic fiber. However, there are still several challenges that must
Accepted 20 September 2014
Available online 6 October 2014
be overcome for the efficient digestion of lignocellulosic biomass. Anaerobic biorefinery is an emerging
concept that not only generates bioenergy, but also high-value biochemical/products from the same feed-
stock. This review paper highlights the current status of lignocellulosic biomass digestion and discusses
Keywords:
Anaerobic digestion
its challenges. The paper also discusses the future research needs of lignocellulosic biomass digestion.
Bioenergy Ó 2014 Elsevier Ltd. All rights reserved.
Lignocellulosic biomass
Rumen microorganism
Anaerobic biorefinery

1. Introduction to several inherent and significant merits (Kaparaju et al., 2009;

In recent years, global energy demand has grown rapidly due to
rising world populations and affluence (Surendra et al., 2014).
Worldwide, energy consumption reached 524 QBtu in 2010, and
is estimated to peak at 800 QBtu by 2040; corresponding to an
average growth of 1.5% per year (EIA, 2013). Significantly, a large
fraction of the world’s total energy demands (more than 84%) is
supported by non-renewable fossil resources such as coal, oil,
and natural gas. These resources are not only limited in supply
but also have adverse effects on the environment due to the emis-
sion of greenhouse gases (GHGs) into the atmosphere (EIA, 2013).
Bioenergy, especially biogas produced through the anaerobic
digestion (AD) of renewable feedstocks, is considered to be one
of the highly promising alternatives to fossil-derived energy due
⇑ Corresponding author. Tel.: +1 808 956 3812; fax: +1 808 956 3542.
E-mail address: khanal@hawaii.edu (S.K. Khanal).
Cheng et al., 2011). Because of its advantages over conventional
fossil-derived resources, AD has been adopted and integrated into
society over the last century, with thousands of full-scale plants
currently in operation worldwide. AD is suitable for converting
non-sterile, diverse, complex feedstocks into energy-rich biogas.
Many biodegradable feedstocks such as industrial wastewater,
food wastes, animal manure, agri-wastes, sewage sludge, organic
fraction of municipal solid waste, among others, have been
employed as substrates for commercial biogas production. Such
facilities illustrate the unique potential for bioremediation and
waste stabilization with concurrent bioenergy production.
More recently, lignocellulosic biomass, namely agri-residues
and energy crops, have been gaining much attention as candidate
feedstocks for producing bioenergy and biobased products. Unlike
conventional biorenewable feedstocks (i.e., sugar- and starch-
based crops), lignocellulosic biomass do not directly compete with
food or feed production. Moreover, high biomass yields even under

http://dx.doi.org/10.1016/j.biortech.2014.09.103
0960-8524/Ó 2014 Elsevier Ltd. All rights reserved.
 C. Sawatdeenarunat et al. / Bioresource Technology 178 (2015) 178–186
low inputs of energy, water, fertilizers, and pesticides, make these
crops ideal for biogas (and bioenergy) production (McKendry,
2002). The composition of lignocellulosic biomass, however,
consists primarily of cellulose, hemicellulose, and lignin, and the
interactions of these components create a highly resistant and
recalcitrant biomass structure. Consequently, the hydrolysis of lig-
nocellulose often becomes the rate-limiting step during traditional
AD (Khanal, 2008).
Several studies have focused on enhancing the digestibility of
lignocellulosic biomass through physical, chemical, biological and
hybrid pretreatments in the production of liquid fuels (primarily
ethanol) via biochemical pathways (FitzPatrick et al., 2010;
Takara and Khanal, 2011). Mechanical milling, steam explosion,
hot water washing, acid and alkali pretreatments and ammonia
fiber expansion, among others, have been employed as upstream
unit operations to disrupt the complex structure of biomass,
thereby increasing its porosity, removing lignin and/or hemicellu-
lose, and reducing the overall crystallinity of the biomass structure
to facilitate the biological conversion of biomass into bioenergy
and biobased products (Monlau et al., 2013; Agbor et al., 2011).
Many of these pretreatments, however, are economically and envi-
ronmentally unfavorable due to the high cost of enzymes and the
production of solid/liquid waste streams (Shrestha et al., 2008;
Monlau et al., 2013; Alvira et al., 2010; Agbor et al., 2011; Kumar
et al., 2009).
AD is the naturally occurring, biological pretreatment of organic
substrates carried out by robust, mixed culture microbial commu-
nities in the absence of oxygen (Khanal, 2008). The consortium of
microbes works synergistically to deconstruct recalcitrant biomass
structures (like lignocellulose) into their respective fundamental
components. In conventional bioprocessing strategies, the whole
lignocellulosic feedstock is ground and fed into an anaerobic biore-
actor to convert complex carbohydrates and organic matter into
energy-rich biogas (Weiland, 2010). Though effective, this
Fig. 1. The schematics of integrated process for producing biogas and biobased products from lignocellulosic biomass.
179
approach is time consuming and energy intensive, consequently
limiting its application for large-scale bioenergy production from
dedicated energy crops. An insightful study conducted by Yue
et al. (2010) suggested that certain microorganisms present in
the AD slurry may prefer specific biomass constituents over others.
In particular, the authors found that the heterogeneous polysac-
charide, hemicellulose, was broken down and metabolized before
other structural components. By carefully adjusting the solids
retention time (SRT), among several other operating conditions,
the AD process may have the ability to promote methane (CH4)
production from hemicellulose exclusively, while leaving behind
cellulose and lignin in the fibrous solid residue. The removal of
hemicellulose effectively destabilizes the recalcitrant biomass
structure, thus allowing for the solubilization (i.e., saccharification)
of cellulose by commercial enzymes in the downstream processes
(Maclellan et al., 2013; Yue et al., 2011). Glucose, derived from the
hydrolysis of cellulose, can serve as a substrate for producing drop-
in biofuels via the carboxylate platform (Agler et al., 2011) or as a
precursor for high-value products such as bioplastics, succinic acid,
fungal protein, etc. (FitzPatrick et al., 2010; Cherubini and
Strømman, 2011). The organic acids produced through fermenta-
tive processes (where applicable) also have potential use in a num-
ber of chemical industries and products (e.g., resins, pesticides,
fertilizers, etc.) (Cherubini and Strømman, 2011). Any lignin
remaining in the solid residue has little commercial value in cur-
rent markets, but can be burned for in-house heat and electricity
generation. Unique to an AD biorefinery approach, in contrast to
conventional biofuel/bioenergy production, is the inherent genera-
tion of digestate (i.e., the nutrient-rich residue) resulting from the
digested slurry. The digestate has important land-use applications
and serves to improve nutrient retention in soil. The idealized AD
biorefinery, as illustrated in Fig. 1, is a rapidly emerging concept
that can significantly improve the commercial viability and appli-
cability of the AD process. The main purpose of this review is to
180 C. Sawatdeenarunat et al. / Bioresource Technology 178 (2015) 178–186

highlight recent advances with respect to AD biorefinery. A partic-
ular emphasis has been placed on leading energy crops, the current
status of energy crop digestion, and opportunities and challenges
that are associated with energy crop digestion. Further research
needs and recommendations are also discussed.
2. Lignocellulosic biomass: composition
Lignocellulosic biomass is an abundantly available bioresource
with an annual (global) yield of over 200 billion dry metric tons
per year (Kumar et al., 2008). For example, U.S. alone produces
about 1.37 billion dry tons of such biomass per year for biofuel
production (Limayem and Ricke, 2012). Common examples of
these renewable resources include agri- and forest residues, and
dedicated energy crops (Cherubini, 2010). The basic structure of
lignocellulose is comprised primarily of cellulose (35–50%), hemi-
cellulose (20–35%), and lignin (10–25%) (Liu et al., 2008), along
with smaller quantities of other organic and non-organic com-
pounds like proteins, lipids, and other extractives (Frigon and
Guiot, 2010). Table 1 summarizes the typical composition of some
commonly used lignocellulosic feedstocks. It is prudent to mention
that the amounts of these constituents not only varies between
species, but can also vary due to growth conditions and matura-
tion. Cellulose is the main constituent of virtually all plant cell
walls, thus making this compound one of the most abundant
(renewable) polymers on the planet. At the molecular level, cellu-
lose (C6H10O5)n is a linear (unbranched) homopolysaccharide con-
sisting of 10,000–15,000 D-glucose units linked by b(1 ? 4)
covalent bonds. The b configuration of the glucose residues creates
a structure with physical properties that are very different from
starch; another homopolysaccharide of glucose with a oriented
bonds. The b(1 ? 4) linkages of cellulose also make the polysac-
charide nearly indigestible for most animals (except ruminants)
since special enzymes, known as cellulases, are required to
hydrolyze the covalent bonds. Hemicellulose, in contrast, is a
highly branched heteropolysaccharide consisting of a wide variety
of sugars (C-5 and C-6). The side groups extending off of the main
hemicellulosic backbone preclude the polymer from forming crys-
talline structures reinforced by hydrogen bonding, unlike cellulose.
The individual sugars of hemicellulose can differ considerably
depending on the plant species, however, in general, the sacchari-
fication of hemicellulose typically produces a mixture of glucose,
galactose, mannose, arabinose, xylose, and rhamnose. The last
main constituent of lignocellulose, namely lignin, is a phenylpro-
pane-based polymer with little value for bioenergy production,
despite being the second most abundant polymer on the earth. Lig-
nin is an essential part of the biomass structure as it provides
mechanical support and water impermeability to the secondary
cell walls of plants, but lignin also serves as both a physical and
biochemical barrier that impedes most biomass-to-bioenergy con-
version processes.
3. Lignocellulosic biomass: methane production potential
The AD of lignocellulosic biomass produces energy-rich CH4 gas.
The yield of CH4 per unit area is often used to determine the energy
productivity of a particular feedstock, and can vary significantly
between species, as well as with maturity, geographical location,
and inputs (water, fertilizer etc.) within the same species (Yang
et al., 2013). The Biochemical Methane Potential (BMP) test is
widely used to examine the anaerobic digestibility of organic sub-
strates. The characteristics of selected energy crops with respect to
BMP are summarized in Table 2.
The economic feasibility of AD is strongly contingent on the CH4
potential of the substrate. Higher CH4 production from a given
feedstock directly corresponds to shorter payback periods (on
investments) for commercial AD facilities. The feedstock composi-
tion is an important factor affecting both the CH4 yield as well as
digester stability; which in turn is governed by the plant species,
geographical location, and biomass maturity as discussed previ-
ously (Amon et al., 2007b). The authors correlated the effects of
harvesting time with biogas production for whole maize (both sto-
ver and ear(s)), and found that the best harvesting age with respect
to CH4 yield per hectare was at the end of wax ripeness (i.e., after
122 days). During this stage, the plant contained between 35–39%
dry matter. At full ripeness (i.e., after 151 days), increases in CH4
production were minimal. This occurrence can likely be attributed
to the carbon-to-nitrogen (C/N) ratio of the maize, reported as 42,

Table 1
The composition of selected lignocellulosic biomass and animal manure.

Biomass Cellulose (%) Hemicellulose (%) Lignin (%) C/N ratio References
Corn stover 37.5 22.4 17.6 63 Karthikeyan and Visvanathan (2012) and Li et al. (2014)
Wheat straw 38.2 21.2 23.4 60 Karthikeyan and Visvanathan (2012) and Brown et al. (2012)
Switch grass 31.0–45.0 20.0–31.0 12.0–18.0 90 Karthikeyan and Visvanathan (2012) and Brown et al. (2012)
Bagasse 38.2 27.1 20.2 118 Karthikeyan and Visvanathan (2012) and Brown (2003)
Sugarcane 25.0 17.0 12.0 NA Karthikeyan and Visvanathan (2012)
Rice straw 32.0 24.0 13.0 47 Karthikeyan and Visvanathan (2012) and Ye et al. (2013)
Eucalyptus 38.0–45.0 12.0–13.0 25.0–37.0 NA Karthikeyan and Visvanathan (2012)
Giant reed stalk 33.1 18.5 24.5 NA Monlau et al. (2012a)
Giant reed leaves 20.9 17.7 25.4 NA Monlau et al. (2012a)
Sunflower stalk 31.0 15.6 29.2 NA Monlau et al. (2012a)
Biomass sorghum 22.2 19.4 21.4 NA Monlau et al. (2012a)
Barley straw 37.5 25.3 26.1 NA Monlau et al. (2013)
Rye straw 38.0 36.9 17.6 20 Monlau et al. (2013) and Nizami et al. (2009)
Napier grass 45.7 33.7 20.6 26 Reddy et al. (2012) and Janejadkarn and Chavalparit (2013)
Cornstalk NA NA NA 27 Wu et al. (2010)
Oat straw NA NA NA 46 Wu et al. (2010)
Cocksfoot grass NA NA NA 12 Nizami et al. (2009)
Meadow foxtail grass NA NA NA 14 Nizami et al. (2009)
Sorghum stalk NA NA NA 29 Brown (2003)
Alfalfa straw NA NA NA 47 Brown (2003)
Sudan grass NA NA NA 37 Brown (2003)
Chicken manure NA NA NA 10 Li et al. (2013)
Swine manure NA NA NA 17 Ye et al. (2013)
Cattle manure NA NA NA 24 Chandra et al. (2012a)

NA = not available.
 C. Sawatdeenarunat et al. / Bioresource Technology 178 (2015) 178–186 181

Table 2 that the lignin fraction alone could be used to predict BMP,
The biomass yield and methane (CH4) production potential of selected lignocellulosic however, the model produced slightly better predictions when
biomass.
the effects of cellulose were also accounted for. Importantly, there
Biomass Biomass yield CH4 potential are still limitations in the modelling approach, particularly for
(metric ton wet weight/ha) (Nm3 CH4/metric ton VS) inaccuracies observed with lipid-rich substrates. The model is also
Sugar beet 40–70 387–408 unable to incorporate different physical and chemical attributes of
Fodder beet 80–120 398–424 the feedstocks such as pH, particle size, moisture content and
Maize 40–60 291–338
Wheat 30–50 351–378
porosity among others (Monlau et al., 2012b).
Triticale 28–33 319–335
Sorghum 40–80 286–319
Grass 22–31 286–324 4. Challenges in digesting lignocellulosic biomass
Red clover 17–25 297–347
Sunflower 31–42 231–297
Wheat grain 6–10 371–398 The low yield of quality biomass (i.e., biomass high in energy
content and easy to convert into end product, CH4) is still one of
(Source: Adapted from Weiland (2010)).
the major challenges. Thus, one of the approaches of increasing
the CH4 yield per unit cropping area is to improve the biomass
yield. Selection of appropriate biomass species for a particular geo-
which was much higher than the recommended C/N ratio (i.e., 20– graphic location with improved photosynthetic efficiency, better
30) for AD (Chandra et al., 2012b). Additionally, the lignin content efficiency for input utilization (e.g., fertilizer, and irrigation) and
of the maize may have increased as the crop matured in the field. resistant to diseases and pests would improve the biomass yield
In general, CH4 production is known to be less from lignocellulosic (Sims et al., 2006). Further, conversion of lignocellulosic biomass
crops which are high in lignin content (Agbor et al., 2011; Alvira into end product (i.e., CH4), is another major hurdle due to the
et al., 2010). Despite the lower conversion efficiency of the complexity of lignocellulosic biomass structure. Thus, biomass
matured crop, however, the highest CH4 yield per unit area was should be harvested at the appropriate stage of maturity which
observed for maize at full ripeness due to the significantly high vol- would not only provide the good yield of biomass but also provide
atile solids (VS) yield per cropping area. The increased VS content the biomass which could be converted into CH4 without intense
for older maize compensated for a lower CH4 yield per unit VS biomass pretreatment. Additionally, lack of good digester for han-
added (Schittenhelm, 2008). With respect to other candidate feed- dling high solids feedstocks such as lignocellulosic biomass is
stocks, like cereal crops, for example, (e.g., wheat, triticale, and rye) another limitation in digesting lignocellulosic biomass. Significant
harvesting should be conducted between the grain-in-the-milk part of knowledge in the current anaerobic digester designs came
stage and grain-in-the-dough stage to obtain the highest CH4 yield from the wastewater treatment plant and was mainly developed
per unit area (Amon et al., 2007a). Similarly, for perennial grasses, for handling low solids feedstocks. Operating such a digester for
the first cut should be conducted after the ear-emergence stage to digesting lignocellulosic biomass is energy intensive, especially in
optimize the CH4 yield (Amon et al., 2007a). mixing biomass and ultimately results in lower net energy yield.
As mentioned previously, the lignin content of the feedstock Thus, an appropriate digester design capable of efficient handling
also affects the CH4 production potential. Triolo et al. (2012) of high solids feedstocks could enhance the energy balance of lig-
reported that lignin contents greater than 100 g/kg VS was a criti- nocellulosic biomass digestion to CH4. Finally, the comprehensive
cal point for AD, resulting in notably low CH4 potentials. A statisti- system for efficient utilization of both digested residue (i.e., solid
cal model to predict CH4 yield based on the composition and residue after AD) and effluent is yet to be developed. The digested
structure of lignocellulosic biomass was developed by several residue, usually rich in cellulose, can be broken down into simple
researchers as shown in Table 3. These equations were primarily sugar via enzymatic hydrolysis and utilized for producing high
proposed to estimate the CH4 yield without conducting the time- value products (as discussed in the later section). The effluent, on
consuming BMP test. Compared to other biomass characteristics, the other hand, is usually rich in nitrogen and other trace elements
the lignin content was reported to be the most important factor and needs to be treated before discharging into an environment.
affecting CH4 production (Gunaseelan, 2007); more than cellulose The combined AD and microalgae production has recently been
crystallinity (Monlau et al., 2012b). Triolo et al. (2011) concluded developed to utilize the nutrients in the effluent by algae. Lipids

Table 3
The statistical models to predict Biochemical Methane Potential (BMP) of selected lignocellulosic biomass.

Substrate Number of sample Compositional parameter Model equation R2 References

BMP (L CH4/kg VS)
Animal manure 10 Lignin (Lig) 1.649Lig 0.035Cell + 430.0 0.89 Triolo et al. (2011)
Energy crops 10 Cellulose (Cell)
Raw and thermo-chemical-pretreated 8 Lignin (Lig) 0.65Lig + 379.8 0.92 Monlau et al. (2012b)
sunflower stalk
Lignocellulosic residues, biomass crops 18 Soluble sugar (SolSu) 303.14–4.53Lig + 0.77SolSu + 0.88 Monlau et al. (2012b)
and carbohydrate rich substrates Uronic acids (Ua) 1.28Pro 1.59Cri+0.61Am + 1.33Ua
Proteins (Pro)
Crystalline cellulose (Cri)
Amorphous cellulose (Am)
Lignin (Lig)
Sweet sorghum 5 Soluble carbohydrate (SCarb) 0.18 + 0.48SCarb + 0.2ADF 0.99 Gunaseelan (2007)
Napier grass 2 Acid Detergent Fiber (ADF) 0.003Lig/ADF + 2.8Pro 0.83A
Protein (Pro)
Lignin (Lig)
Ash (A)

(Source: Adapted from Monlau et al. (2012b)).

182 C. Sawatdeenarunat et al. / Bioresource Technology 178 (2015) 178–186
from such produced algae could be utilized for biodiesel produc-
tion and the residue after lipid harvest could be further fed into
the digester for CH4 production. The effluent after the algae pro-
duction can be recycled for operating anaerobic digester.
5. Current technology in lignocellulosic biomass digestion
5.1. Anaerobic co-digestion
As alluded to earlier, the C/N ratio of feedstocks is critically
important to facilitate the conversion of lignocellulosic biomass
to CH4 (Wu et al., 2010). Dedicated energy crops are often rich in
carbohydrates, but are low in nitrogen (Giuliano et al., 2013; Ye
et al., 2013). Thus, the mono-digestion of energy crops alone may
result significantly low CH4 yield (i.e., biogas high in carbon diox-
ide (CO2) but low in CH4 content) if an optimal C/N ratio of 20–
30 is not properly maintained. Another significant demerit of
mono-digestion of energy crops is the lack of essential trace ele-
ments such as iron, cobalt, nickel, molybdenum, selenium, and
tungsten. These metals, though present in miniscule quantities,
are considered vital for sustaining methanogens. Thus, the supple-
mentation of nutrients and trace elements enhances CH4 yields in
addition to improving digester stability. For example, CH4 yield
from Napier grass reportedly increased by 40% when nickel, cobalt,
molybdenum and selenium were added to the reactor (Demirel
and Scherer, 2011).
The mono-digestion of conventional AD substrates, such as ani-
mal waste, is also not recommended as it can result in digester
instability caused by ammonia toxicity from the rapid degradation
of organic nitrogen such as urea and protein (Abouelenien et al.,
2014). Thus, the co-digestion of carbohydrate-rich lignocellulosic
biomass with nitrogen-rich animal waste has significant
implications in maintaining an optimal C/N ratio for commercial
CH4 production with renewable feedstocks (Giuliano et al., 2013).
Several studies to date have demonstrated the successful anaerobic
co-digestion of livestock wastes and lignocelluloses as illustrated
in Table 4. The establishment and maintenance of an appropriate
C/N ratio was one of the key factors surrounding a successful co-
digestion. Ye et al. (2013) reported the co-digestion of rice straw
and swine manure in a series of batch experiments. The CH4 yield
increased by an impressive 71% compared to the mono-digestion
of rice straw when the quantity of swine manure-to-rice straw
was adjusted to 2:1 (on a VS basis). The C/N ratios of the
co-substrates (i.e., mixture of swine manure and rice straw) and
mono-substrate (i.e., rice straw) were 21.7 and 47, respectively.
In an earlier study, a C/N ratio of 20 resulted in the highest biogas
yields during the co-digestion of swine manure and three
lignocellulosic substrates; namely, wheat straw, corn stalk and
oat straw (Wu et al., 2010). The volume of biogas produced
Table 4
The anaerobic co-digestion of selected lignocellulosic biomass and animal manure.
Co-substrate Reactor operating Co-substrate mixing ratio
mode
Swine manure and rice straw Batch 2/1 VS basis
Chicken manure and corn stover Batch 1/3 VS basis
Chicken manure and corn stover Semi-continuous CSTR 1/1.4 VS basis
Chicken manure and agricultural waste Batch 7.0/0.5/1.3/0.3 wet weight basis
(chicken manure/coconut/coffee grounds/
cassava)
Chicken manure, dairy manure and Batch 2.7/2.7/1 VS basis (chicken manure/
wheat straw dairy manure/wheat straw)
Cattle slurry and raw cheese whey Semi-continuous CSTR 1/1 wet weight basis
Cow manure and crop silage Semi-continuous CSTR 4/1 wet weight basis
CSTR = continuous stirred tank reactor; NA = not available.
reportedly increased by 11, 8, and 6-folds when compared with
AD of swine manure as the control, respectively.
Chicken manure is rich in organic nitrogen, compared to most
other animal wastes. Consequently, during mono-digestion, AD
systems are often prone to suffer from ammonia toxicity. Li et al.
(2014) investigated the co-digestion of chicken manure and corn
stover using batch and continuously-stirred tank reactors (CSTR),
where C/N ratio was adjusted to 20. The authors found that the
CH4 yield obtained from their batch experiment achieved 62% of
the calculated theoretical yield. The CSTR reactor was operated at
an organic loading rate of 4 kg VS/m3/day with stable performance
without VFAs accumulation. This enhancement in biogas produc-
tion strongly supports the importance of an optimal C/N ratio for
better CH4 yields.
5.2. Solid-state anaerobic digestion (SS-AD)
In general, AD is classified into three important groups based on
their operating total solids (TS) contents namely; liquid (L-AD),
semi-solid (S-AD), and solid-state (SS-AD) with respective TS con-
centrations of less than 10%, 10–20% and more than 20%
(Karthikeyan and Visvanathan, 2012; Cui et al., 2011). The criteria
is rather loosely defined, however, as Brown et al. (2012) refers to
AD with TS contents less than 15% and more than 15% as L-AD and
SS-AD, respectively. The L-AD is typically suitable for substrates
which are high in moisture content, such as domestic and indus-
trial wastewater (Xu and Li, 2012). For dilute waste streams (e.g.,
wastewater with TS content <1%), the term digestion should not
be used. For such streams, the focus is on wastewater treatment
coupled with biogas production. The SS-AD, on the other hand, is
ideal for high solids organic feedstocks like energy crops, food
wastes, livestock manures, agri-residues etc. which typically have
TS content between 10% and 50% (Lehtomäki et al., 2008). In recent
years, there have been growing interests in SS-AD with agricultural
and forest residues, and dedicated energy crops. The advantages of
SS-AD in comparison to L-AD are lower reactor volumes, higher
organic loading rates (OLRs), less water for dilution, less mixing
requirement, no floating substrates (in the bioreactor), lower costs
for managing the digestate, and overall, lower energy input for
operation (Liew et al., 2012; Karthikeyan and Visvanathan, 2012).
SS-AD using energy crops as primary substrates and/or co-sub-
strates is presented in Table 5.
Brown et al. (2012) compared the CH4 yield between L-AD and
SS-AD using three lignocellulosic feedstocks (namely, corn stover,
switchgrass, and wheat straw) and reported no significant
difference in overall yields. Interestingly, however, when the CH4
volumetric productivity (L CH4/Lworking volume of reactor) was com-
pared between the two systems, SS-AD yielded 6–7 folds higher
than L-AD for all three feedstocks tested. This result suggested that
SS-AD required less reactor volume for similar solid loading rates.
C/N ratio CH4 yield References
(L/kg VS added)
21.7 350 Ye et al. (2013)
27.3 298 Li et al., (2013)
20.0 223 Li et al. (2014)
17.1 506 Abouelenien et al. (2014)
25.0 235 Wang et al. (2012)
NA 343 Comino et al. (2012)
NA 249 Comino et al. (2010)
 C. Sawatdeenarunat et al. / Bioresource Technology 178 (2015) 178–186 183

Table 5
The solid state anaerobic digestion (SS-AD) of lignocellulosic biomass and animal manure.

Substrate Total solids (%) Reactor operating mode Temperature Retention time CH4 yield References
(°C) (day) (L/kg VSadded)
Rice straw and piggery 20 Batch with leachate 30–40 189 231 Mussoline et al. (2012)
wastewater recirculation
Wheat straw from horse bed 22 Batch 37 30 55–60 Cui et al. (2011)
Spent wheat straw 22 Batch 37 ± 1 30 150 Cui et al. (2011)
Horse dung and straw 15–30 Batch 35 42 170 Kusch et al., 2008
Corn stover 18–19 Batch 37 ± 1 30 132 Brown et al. (2012)
Switchgrass 18–19 Batch 37 ± 1 30 117 Brown et al. (2012)
Wheat straw 18–19 Batch 37 ± 1 30 124 Brown et al. (2012)
Leaves 22 Batch 37 ± 1 30 55 Liew et al. (2012)
Yard waste 22 Batch 37 ± 1 30 41 Liew et al. (2012)
Dog food waste and corn stover 22 Batch 37 ± 1 30 304 Xu and Li (2012)
Grass silage 26a Single-stage (LB reactor 35 ± 1 55 60 Lehtomäki et al. (2008)
with-leachate recirculation)
Grass silage 26a Two-stage (LB + UASB reactors) 35 ± 1 55 197 Lehtomäki et al. (2008)

LB = leach bed, UASB = upflow anaerobic sludge blanket.

a
Total solids content of substrate in the leach-bed reactor.

Moreover, the addition of water, which was used for adjusting the
operating TS content, was significantly less in SS-AD. Conse-
quently, SS-AD may have applications in geographically isolated
regions where water supply is limited. Many other researchers
have reported successful operation of the SS-AD technology in
the digestion of various lignocellulosic feedstocks as discussed
below.
When digestion tests were conducted at a TS content of 22% and
substrate-to-inoculum ratio of 2, corn stover and wheat straw,
which contain higher quantities of cellulose and hemicellulose
and less lignin, showed greater CH4 yields compared to leaves
and yard waste. The majority of CH4 generated from corn stover
and wheat straw originated from cellulose and hemicellulose
(34–41%) unlike in the case of leaves and yard waste (6–21%).
CH4 from the latter lignin-rich substrates were likely from the
digestion of free sugars, oligomers, and organic acids (Liew et al.,
2012).
Spent wheat straw, which is often used as bedding in horse
barns, was also among the feedstocks examined in a batch SS-AD
digester, and was compared with the SS-AD of raw wheat straw.
The initial cellulose and hemicellulose content of the spent wheat
straw was significantly lower than in the raw material, however,
the concentrations of nitrogen and VFAs were much higher due
to bacterial and fungal degradation of lignocellulose in the barn
(Cui et al., 2011). The highest CH4 yield was observed at a sub-
strate-to-inoculum ratio of 4. The reported value was approxi-
mately 56% higher than that obtained for raw wheat straw,
which was evident from higher conversion efficiencies of cellulose
(37.8%) and hemicellulose (44.7%) into CH4. The cellulose and
hemicellulose conversion efficiencies for raw wheat straw were
only 30.4% and 29.0%, respectively. When the authors increased
the substrate-to-inoculum ratio to 6, however, SS-AD failed for
both substrates. High concentrations of VFAs and low pH indicated
that there may have been an accumulation of acid in the system;
but the underlying cause of reactor instability was not identified
due to contradicting data and observations (Cui et al., 2011). More
research is required to elucidate a better understanding of how SS-
AD systems operate, and how to best avoid system failure.
In 2012, Xu and Li, applied SS-AD to co-digest expired dog food,
a highly digestible substrate rich in nitrogen, and corn stover in
mesophilic batch reactors. The highest CH4 yield was obtained
when dog food waste and corn stover was mixed at a 1:1 ratio
on a VS basis. The CH4 yield during co-digestion was 229% and
109% higher than the mono-digestion of corn stover and dog food
waste, respectively, and strongly suggests the potential for co-
digesting carbon- and nitrogen-rich substrates.
In many cases, a leach-bed reactor, a well-known SS-AD system,
is used in the digestion of lignocellulosic energy crops. Lehtomäki
et al. (2008) examined grass silage as a potential feedstock for a
single-stage and two-stage system (leach-bed + Upflow Anaerobic
Sludge Blanket (UASB)). The aim was to separate and improve
the hydrolysis and methanogenesis of the complex feedstock. (As
mentioned previously, hydrolysis is often the rate limiting step
during AD of lignocellulosic biomass.) The two-stage reactor
resulted in a CH4 yield about 3-folds higher than the leach-bed
reactor alone; which produced only 20% of the substrate’s CH4
potential. In the two-stage system, 98% of the CH4 production
was obtained from the second stage UASB reactor. This result sug-
gests that there are significant advantages when installing a meth-
anogenic reactor following hydrolysis and the acidogenic leach-
bed reactor.
As in conventional AD, buffering intensity is another important
parameter essential for maintaining proper pH and preventing fail-
ure in SS-AD systems as a result of acid accumulation (Ward et al.,
2008). Mussoline et al. (2012) studied the co-digestion of rice
straw and pig wastewater in a farm-scale single-stage leach-bed
reactor with leachate recirculation. The authors concluded that
the piggery wastewater could provide sufficient buffering capacity
for the AD process and could serve as a source of macronutrient to
adjust the C/N ratio of the feedstock in addition to providing some
of the trace elements required for microflora. In the study, the
researchers presented the following scenario: a 100-ha rice farm
has the ability to produce 100,000 m3 CH4 annually, which could
be converted to 328 MWh of electricity. The generation of CH4
could be increased by raising the operating TS in SS-AD, but the
high solids concentration (greater than 28–30%) could cause VFAs
accumulation and a pH drop due to the inhibition of methanogens
and physical limitations surrounding liquid/gas transfer. This phe-
nomenon would ultimately lead to the unavoidable failure of SS-
AD (Abbassi-Guendouz et al., 2012).
5.2.1. Challenges and future research needs for SS-AD
Although SS-AD has several advantages over L-AD, there are
some challenges that impede the application of this technology
at the commercial scale. Typically, because of the higher OLR dur-
ing SS-AD, VFAs and ammonia accumulation may likely to occur
and the entire system is prone to fail, especially when energy crops
are used as a mono-substrate. Thus, as mentioned previously,
anaerobic co-digestion with feedstock rich in nitrogen such as
livestock manure would serve to enhance the process stability.
Moreover, some reactor configurations, such as leach-bed, may
not receive proper mixing and is also likely to suffer from an
184 C. Sawatdeenarunat et al. / Bioresource Technology 178 (2015) 178–186
accumulation of organic acids and ammonia (Li et al., 2011). The
high solids content in SS-AD, which is regarded as an advantage,
can also produce dead zones in the reactor, and may lead to reduc-
tions in CH4 yield in addition to causing reactor overloading.
Understanding the microbial community is another important
research area in lignocellulosic biomass digestion.
To address some of these drawbacks, significant research efforts
are needed with respect to reactor configurations to eliminate the
accumulation of toxic and/or inhibitory compounds in SS-AD
systems. Innovations such as novel mixing or improved water
distribution in leach bed reactors may be among the topics consid-
ered. Better reactor operating strategies, including but not limited
to appropriate OLR and retention time, along with maintaining
healthy and right microbial communities may also further enhance
the efficiency of SS-AD systems. One likely avenue to pursue for
future SS-AD is the two-stage co-digestion of energy crops and ani-
mal manure. This approach could enhance microbial hydrolysis of
the substrates, prevent the accumulation of VFAs, and provide the
required nutrients and trace elements. Research efforts are also
needed to identify and quantify the efficient lignocellulosic bio-
mass digesting microbes using advanced molecular techniques.
More fundamental studies are needed to understand how feed-
stock maturity and composition affect biomass digestibility. More-
over, a rigorous life cycle assessment (LCA) must also be conducted
before the technology is deployed at a commercial scale.
5.3. Alternative biological pretreatment of feedstock: rumen
microorganisms (RM)
RM are a complex anaerobic microbial consortium which are
mainly found in a specific stomach of ruminant animals (Barnes
and Keller, 2003). In many cases, RM are present in livestock (i.e.,
cattle) excreta used in AD, but often in modest quantities. Mem-
bers of this synergistic community include bacteria, fungi, proto-
zoa and archaea (Yue et al., 2013). The microflora found in
ruminant stomachs in situ create a cellulolytic ecosystem which
has a high potential to degrade the complex carbohydrate struc-
tures of lignocellulosic biomass (Hu and Yu, 2005). Although RM
have been studied previously as an anaerobic pretreatment
(Barnes and Keller, 2003), a deficiency of appropriate molecular
technology to evaluate diversity and classify these microorganisms
has limited the broader application of this method. Recent devel-
opments of molecular techniques, however, have resulted in a bet-
ter understanding of the diversity and metabolism of such
microbial communities. The enhancement of many bioreactor pat-
terns, which were inoculated with RM, was recognized as artificial
rumen reactors. These innovations included continuous- and dual-
flow reactor, two-phase AD reactor, anaerobic sequencing batch
reactor and UASB (Yue et al., 2013; Barnes and Keller, 2003). Due
to their higher cellulolytic activities, RM promote higher rates of
lignocellulose degradation than conventional inoculums such as
anaerobic sewage sludge (Gijzen et al., 1990; Yue et al., 2013).
The higher VFA yield during digestion is the key indicator to assert
an advantage of using RM against the other inocula for lignocellu-
lose digestion. The maximum VFAs yield during the semi-continu-
ous digestion study of corn stover, using RM as an inoculum, was
28% higher than those produced when conventional acidogenic
bacteria from sewage sludge was used as an inoculum (Hu and
Yu, 2005). Anaerobic degradation using RM as a specific seed is a
pH dependent process. The highest efficiency in terms of substrate
digestion was found at a pH between 6.8 and 7.3. Acetic acid dom-
inated at low pH (i.e., less than 5.5) and the concentration gradu-
ally decreased with increasing pH. On the contrary, propionic
acid production was favored at high pH (i.e., more than 6.0) (Hu
et al., 2004). The operating temperature is also an important factor
in the digestion process. Yue et al. (2013) reported that compared
to microbes from other inoculum sources, RM exhibited a much
faster attack to the cellulose during lignocellulose digestion. In
addition, the cellulolytic biofilm formed by RM was more stable
than that generated by the conventional anaerobic microorganism
derived from the leachate of the anaerobic leach-bed reactor treat-
ing organic fraction of municipal solid waste (O’Sullivan et al.,
2009). Interestingly, the main products generated by RM were
low-molecular weight carboxylic acids (namely, acetic, propionic
and butyric acids along with a small amount of iso-butyric and
valeric acids) (Hu and Yu, 2005). The production of such organic
acids opens up an avenue for the application of RM in an AD-based
biorefinery. The produced organic acids are important precursors
for producing bio-based products inherent in the biorefinery con-
cept. For example, mixed VFAs generated by RM would serve as
substrate for microorganisms to produce energy-rich gases such
as CH4 and H2 under anaerobic condition. Also these VFAs could
be used as precursors for biochemical synthesis of different types
of alcohols (Agler et al., 2011). Bioplastic is another example of a
biobased product which could be generated by using the com-
pounds (i.e., VFAs) generated from RM as the initial substrate
(Yue et al., 2013). Although RM have a high potential as an effective
inoculum for hydrolyzing lignocellulosic feedstocks during AD,
there are some barriers in the application of these microflora in
full-scale plants. Firstly, the direct withdrawal of RM in a large vol-
ume from the stomach of the ruminant host animal is not possible,
particularly at a commercial scale. Secondly, due to the lack of in-
depth understanding of microbial community diversity and the
inherent interactions among the different colonies, the mass pro-
duction of these microorganisms to inoculate a full scale AD plant
remains unanswered. The recent development of advanced molec-
ular techniques, however, have facilitated the study of the rumen
microbial communities, their interaction, and network between
the species (Sauer et al., 2012). A clear understanding of the com-
plexity governing rumen systems possesses the potential of mass
production of RM to test and inoculate commercial anaerobic
digesters for the most efficient utilization of lignocellulosic
feedstocks.
6. Anaerobic digestion-based biorefinery
AD is among the promising bioconversion technologies for pro-
ducing renewable bioenergy, however, the production of CH4 alone
may not sufficiently justify the capital and operational costs
investment associated with building a commercial biogas facility.
More likely, AD can be integrated into a biorefinery as an effective
biological pretreatment that facilitates the subsequent breakdown
of lignocellulosic biomass into its constituent sugars (i.e., glucose,
galactose, xylose, arabinose and mannose) and/or short chain fatty
acids (namely, acetic, propionic and butyric acids). The solubilized
components can then be used as precursors in the production of
diverse products ranging from bioenergy/biofuel (i.e., CH4, H2, eth-
anol and butanol) (Agler et al., 2011; Rabelo et al., 2011; Kaparaju
et al., 2009) to organic acids (e.g., succinic acid) and biopolymers
(e.g., bioplastic) (FitzPatrick et al., 2010; Cherubini and
Strømman, 2011). The digestate (which usually consists of partially
digested feedstock and microbial cells) (Alburquerque et al., 2012)
can be applied to agricultural land as an organic fertilizer to pro-
mote nutrient retention (Fuchs and Drosg, 2013; Tambone et al.,
2010). The digestate itself is also capable of producing CH4, which
represents both an opportunity, as well as an environmental con-
cern. The composition of digestate, however, strongly depends on
the feedstock type as well as the operating conditions of the plants
(Menardo et al., 2011; Alburquerque et al., 2012). More specifically,
the digestates from the digesters operated at higher OLR usually
contain the higher amount of biodegradable organic compounds
 C. Sawatdeenarunat et al. / Bioresource Technology 178 (2015) 178–186
and ultimately generates higher volume of CH4 during post-diges-
tion storage. For example, the volume of CH4 produced from the
digestate resulting from the co-digestion of animal manure and a
lignocellulosic energy crop at an organic loading rate (OLR) of
2.25 kg VS/m3/d was significantly higher compared to the volume
of CH4 produced from the digestate of a biogas plant operated at
OLR of 0.85 kg VS/m3/d (Menardo et al., 2011). If the CH4 produced
during digestate storage is not properly recovered, thus the
released CH4 may worsen GHG emissions since CH4 has a global
warming potential 20 times greater than CO2. Gioelli et al. (2011)
studied a full-scale biogas plant fed with cattle slurry, farm yard
manure, poultry manure, maize silage, drying maize residue and
rice chaffs with a capacity of 1 MWel. The AD was operated at an
OLR of 1.40 kg VS/m3/day using two digesters with a total volume
of 12,000 m3 and 6000 m3, and an uncovered digestate storage
tank. The average CH4 produced from the storage tank was mea-
sured to be 262 NL/m2 surface/day. If the CH4 was captured with
a cover, the facility would have been able to prevent the GHG emis-
sion of 85–205 kg CO2eq per MWhel produced.
Despite its advantages as an organic fertilizer, in some cases, the
digestate from animal manure may contain high concentrations of
elements such as copper and zinc (micro-and micro-nutrients
supplemented in animal feed), and direct application of the dige-
state to agricultural land may result in phytotoxicity. Under such
conditions, the digestate must be diluted with irrigation water
before being applied to the field. In addition, direct contact of sal-
ine digestates with young plants should be avoided (Alburquerque
et al., 2012).
A significant opportunity exists to prevent negative
environmental impacts caused by commercial AD facilities
(namely, GHGs emission and phytotoxicity) while simultaneously
improving the use of lignocellulose biomass. Specifically, the con-
trolled co-digestion of lignocellulose with animal manure (or other
nitrogen-rich organic wastes) can be used to biologically pretreat
energy crops and remove the amorphous hemicellulose fraction
of the biomass structure. The consortium of microorganisms pres-
ent during AD can convert the sugar constituents of hemicellulose
into CH4, while effectively exposing lignin and cellulosic fibers in
the digestate. The residence time of the substrates must be shorter
than conventional AD so as to prevent the digestion of cellulose. In
later downstream processes, the commercial enzymes (i.e., cellu-
lases) can be added to saccharify cellulose into soluble glucose.
The free monosaccharide can then serve as a precursor for biofuel,
such as bioethanol and biobutanol, or a number of biochemical
products as shown in Fig. 1.
One distinct and important advantage of using the digestate
from AD as a substrate for producing bioproducts is the inherent
size reduction of the biomass following the AD process. The smaller
particle size of lignocellulose after AD could reduce grinding costs
while improving saccharification and fermentation (Yue et al.,
2011). Maclellan et al. (2013) have supported the concept of
coupling biogas production with biorefining to optimize the
production of biofuel from energy crops. The authors applied
anaerobic co-digestion of swine manure and corn stover at differ-
ent stover-to-manure ratios. The digestate obtained from the bio-
reactor was pretreated with 2% NaOH at 130 °C for 2 h and
enzymatically hydrolyzed to produce simple sugars for bioethanol
production. The authors found that a stover-to-manure ratio of
40:60 (by raw weight) exhibited the highest net energy balance,
and could produce 152 g CH4 and 50 g ethanol per kg dry mixed
feed. Rabelo et al. (2011) reported an integrated process for bioeth-
anol and biogas production from sugarcane bagasse in Brazil. The
authors also reported that 63–65% of the potential energy in
bagasse was recovered in the form of CH4 and ethanol, which is
approximately 50% greater than the usable energy captured when
bagasse is used only for producing bioethanol.
185
7. Conclusion
Lignocellulosic biomass has a great potential to serve as a
feedstock for CH4 production. The complexity of the biomass
structure and lack of appropriate digester designed for efficient
handling of the high solids biomass are major challenges in digest-
ing lignocellulosic biomass. However, harvesting biomass at appro-
priate stage of maturity and co-digesting with other feedstocks by
using RM in SS-AD could significantly enhance the CH4 yield. An
anaerobic biorefinery may be one promising avenue to enhance
the economic feasibility of commercial ventures; where a variety
of commodity and high-value products can be generated concur-
rently from co-digested feedstocks in the same facility.
Acknowledgements
This project is being supported by funding from the Sun Grant
Western Regional Center at Oregon State University through a
grant provided by the United States Department of Agriculture
National Institute of Food and Agriculture under proposal number
2012-03373.
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