Journal of Biotechnology 156 (2011) 286–301

Contents lists available at ScienceDirect

Journal of Biotechnology
journal homepage: www.elsevier.com/locate/jbiotec

Review

Lactic acid production from lignocellulose-derived sugars using lactic acid

bacteria: Overview and limits
Mohamed Ali Abdel-Rahman a,b , Yukihiro Tashiro c , Kenji Sonomoto a,d,∗
a
Laboratory of Microbial Technology, Division of Applied Molecular Microbiology and Biomass Chemistry, Department of Bioscience and Biotechnology, Faculty of Agriculture,
Graduate School, Kyushu University, 6-10-1 Hakozaki, Higashi-ku, Fukuoka 812-8581, Japan
b
Botany and Microbiology Department, Faculty of Science (Boys), Al-Azhar University, PN:11884, Naser City, Cairo, Egypt
c
Department of Life Study, Seinan Jo Gakuin University Junior College, 1-3-5 Ibori, Kita-ku, Kokura, Kitakyushu City, Fukuoka 803-0835, Japan
d
Laboratory of Functional Food Design, Department of Functional Metabolic Design, Bio-Architecture Center, Kyushu University, 6-10-1 Hakozaki, Higashi-ku, Fukuoka 812-8581,
Japan

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

Article history: Lactic acid is an industrially important product with a large and rapidly expanding market due to its
Received 2 February 2011 attractive and valuable multi-function properties. The economics of lactic acid production by fermenta-
Received in revised form 31 May 2011 tion is dependent on many factors, of which the cost of the raw materials is very significant. It is very
Accepted 17 June 2011
expensive when sugars, e.g., glucose, sucrose, starch, etc., are used as the feedstock for lactic acid produc-
Available online 23 June 2011
tion. Therefore, lignocellulosic biomass is a promising feedstock for lactic acid production considering
its great availability, sustainability, and low cost compared to refined sugars. Despite these advantages,
Keywords:
the commercial use of lignocellulose for lactic acid production is still problematic. This review describes
Lignocellulose-derived sugar
Lactic acid production
the “conventional” processes for producing lactic acid from lignocellulosic materials with lactic acid bac-
Lactic acid bacteria (LAB) teria. These processes include: pretreatment of the biomass, enzyme hydrolysis to obtain fermentable
Metabolic pathways sugars, fermentation technologies, and separation and purification of lactic acid. In addition, the difficul-
Designed biomass ties associated with using this biomass for lactic acid production are especially introduced and several
key properties that should be targeted for low-cost and advanced fermentation processes are pointed
out. We also discuss the metabolism of lignocellulose-derived sugars by lactic acid bacteria.
© 2011 Elsevier B.V. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 287
2. Overview of lactic acid production from lignocellulosic biomass . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 287
2.1. Composition of lignocellulosic biomass . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 287
2.2. Conventional processes for lactic acid production by LAB from lignocellulosic biomass . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 288
2.2.1. Pretreatment methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 288
2.2.2. Enzymatic hydrolysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 289
2.2.3. Fermentation process with LAB . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 289
2.2.4. Separation and purification of lactic acid . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 290
2.3. Difficulties in using lignocellulosic biomass for efficient lactic acid production by LAB . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 290
2.3.1. Resistant nature of biomass and pretreatment problems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 290
2.3.2. High-cost enzymes and their feedback inhibition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 290
2.3.3. Formation of by-products due to the heterofermentation of pentose sugars . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 290
2.3.4. Carbon catabolite repression caused by the heterogeneity of the hydrolysate-sugar composition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 291

∗ Corresponding author at: Laboratory of Microbial Technology, Division of Applied Molecular Microbiology and Biomass Chemistry, Department of Bioscience and
Biotechnology, Faculty of Agriculture, Kyushu University, 6-10-1 Hakozaki, Higashi-ku, Fukuoka 812-8581, Japan. Tel.: +81 92 642 3019; fax: +81 92 642 3019.
E-mail address: sonomoto@agr.kyushu-u.ac.jp
(K. Sonomoto).

0168-1656/$ – see front matter © 2011 Elsevier B.V. All rights reserved.
doi:10.1016/j.jbiotec.2011.06.017
 M.A. Abdel-Rahman et al. / Journal of Biotechnology 156 (2011) 286–301 287

3. Fermentative lactic acid production by LAB . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 291

3.1. Improvement of lactic acid production by LAB in the field of microbial technology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 291
3.2. Lactic acid production by LAB using lignocellulosic biomass and lignocellulose-derived sugars . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 292
4. Metabolism of lignocellulose-derived sugars by LAB . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 295
5. Designed biomass study and conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 296
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 297

1. Introduction any impact on the human food chain. Nowadays, lignocellulosic

materials from agricultural, agro-industrial, and forestry sources
Lactic acid (2-hydroxypropanoic acid, CH3 –CH(OH)–COOH) is represent a potentially inexpensive and renewable carbohydrate
a natural organic acid with a long history of use in the food and feedstock for the large-scale fermentation of lactic acid due to their
non-food industries, including the cosmetic and pharmaceutical abundance, low price, high polysaccharide content, and renewa-
industries, and for the production of oxygenated chemicals, plant bility (Duff and Murray, 1996; Parajo et al., 1996; Taniguchi et al.,
growth regulators, and special chemical intermediates (Oshiro 2005; Wyman, 1999). However, the cellulose and hemicellulose in
et al., 2009; Singhvi et al., 2010; Tashiro et al., 2011). Currently, lignocellulose are not directly available for bioconversion to lac-
there is an increased demand for lactic acid as a feedstock for the tic acid because of their intimate association with lignin (Schmidt
production of biopolymer poly-lactic acid (PLA), which is a promis- and Thomsen, 1998) and the lack of hydrolytic enzymes in LAB
ing biodegradable, biocompatible, and environmentally friendly (Tokuhiro et al., 2008).
alternative to plastics derived from petrochemicals. PLA has many There have been numerous investigations on the development
uses in surgical sutures, orthopedic implants, drug delivery sys- of biotechnological processes for lactic acid production, with the
tems, and disposable consumer products (Adnan and Tan, 2007), ultimate objective of making the process more effective and eco-
and its use would significantly alleviate waste disposal problems. nomical. In this review, we focus on the “conventional” processes
The physical properties of PLA depend on the isomeric composition for lactic acid fermentation by LAB from lignocellulosic biomass
of lactic acid. Pure isomers, l- and d-lactic acid, are more valuable and lignocellulose-derived sugars. Moreover, we describe the lim-
than the racemic dl form because each isomer has its own spe- itations of lactic acid production using such materials. We also
cific industrial application. l-Lactic acid is used for the synthesis describe fermentative processes and technologies with practical
of poly l-lactic acid (PLLA), a semi-crystalline biodegradable and examples, the metabolism of biomass-derived sugars, and the
thermostable polymer that has a potentially large market in goods promising prospects of lactic acid fermentation.
packaging. PLLA has high tensile strength and low elongation with
a high modulus that makes it suitable for medical products used in 2. Overview of lactic acid production from lignocellulosic
orthopedic fixation (e.g., pins, rods, ligaments, etc.), cardiovascular biomass
applications (e.g., stents, grafts, etc.), dental applications, intestinal
applications, and sutures (John et al., 2006a). d-Lactic acid is used 2.1. Composition of lignocellulosic biomass
for the production of poly d-lactic acid (PDLA) (John et al., 2009).
These pure polymers are relatively heat sensitive, while stereocom- The global production of plant biomass, of which over 90%
plexes of PLLA and PDLA have a melting point ∼50 ◦ C higher than is lignocellulose, amounts to ∼200 × 109 tons per year, where
their respective pure polymers (Ikeda et al., 1987; Tsuji and Fukui, ∼8–20 × 109 tons of the primary biomass remains potentially
2003) and are more biodegradable (de Jong et al., 2001; Tashiro accessible (Lin and Tanaka, 2006). Lignocellulosic biomass is
et al., 2011). The ratio of l- and d-lactic acids influences the prop- organic material derived from a biological origin, and represents
erties and the degradability of PLA (Kharras et al., 1993). the most abundant global source of biomass that has been largely
Lactic acid can be produced either by chemical synthesis or unutilized (Lin and Tanaka, 2006). It is mainly composed of cellu-
by microbial fermentation. Chemical synthesis from petrochemi- lose (insoluble fibers of ␤-1,4-glucan), hemicellulose (noncellulosic
cal resources always results in racemic mixture of dl-lactic acid, polysaccharides including xylans, mannans, and glucans), and
which is a major disadvantage of this approach (Hofvendahl and lignin (a complex polyphenolic structure), which form ∼90% of the
Hahn-Hägerdal, 2000). Conversely, microbial lactic acid fermenta- dry matter, plus lesser amounts of minerals, oils, and other com-
tion offers an advantage in terms of the utilization of renewable ponents (Balat, 2011; Molina-Sabio and Rodríguez-Reinoso, 2004;
carbohydrate biomass, low production temperature, low energy Yang et al., 2009). This biomass includes forest and crop residues
consumption, and the production of optically high pure lactic acid (Chen and Lee, 1997; Melzoch et al., 1997), municipal solid waste
by selecting an appropriate strain (Ilmen et al., 2007; Pandey et al., (John et al., 2007), waste paper (McCaskey et al., 1994), and wood
2001). Presently, almost all lactic acid produced globally is man- (Linko et al., 1984). The structural and chemical composition of lig-
ufactured by fermentation routes. In particular, there have been nocellulosic material has varying amounts of these components
numerous studies of lactic acid production by lactic acid bacteria because of genetic and environmental influences and their inter-
(LAB) in comparison with other microorganisms. actions (Demirbas, 2005). The proportion of biomass constituents
The demand for lactic acid has increased considerably due to its varies between species, and there are distinct differences between
wide range of applications; however, the high cost of the raw mate- hardwoods and softwoods. The total content of cellulose and hemi-
rials, e.g., starch and refined sugars, which accounts for the highest cellulose is higher in hardwoods (78.8%) than in softwoods (70.3%),
portion of the production cost, represents one of the most serious but the total content of lignin is higher in softwoods (29.2%) than in
obstacles for the fermentative production of lactic acid to compete hardwoods (21.7%) (Balat, 2009). As shown in Table 1, the cellulose,
with chemical synthesis (Datta et al., 1995). Cheap raw materials hemicellulose, and lignin content depends on the type of lignocellu-
are essential for the feasibility of the biotechnological production losic biomass, which indicates that an appropriate material should
of lactic acid because polymer producers and other industrial users be selected for the corresponding fermentation.
usually require large quantities of lactic acid at a relatively low Cellulose, the major component of plant biomass (30–60% of
cost. The use of low-cost non-food materials for lactic acid pro- total feedstock dry matter), is a homopolysaccharide composed
duction appears to be more attractive because they do not have of ␤-d-glucopyranose units, linked by ␤-(1 → 4)-glycosidic bonds.
288 M.A. Abdel-Rahman et al. / Journal of Biotechnology 156 (2011) 286–301

Table 1
The contents of cellulose, hemicellulose, and lignin in various types of lignocellulosic Lignocellulosic
biomass (% dry weight).a
biomass
Lignocellulosic materials Cellulose (%) Hemicellulose (%) Lignin (%)

Algae (green) 20–40 20–50 NAb

Aspen hardwood 51 29 16
Birch Hardwood 40 39 21
Chemical pulps 60–80 20–30 2–10
Coastal Bermuda grass 25 35.7 6.4 Chemical/physical
Corn cobs 45 35 15
Cornstalks 39–47 26–31 3–5
Pretreatment
Cotton seed hairs 80–95 5–20 0
Cotton, flax, etc. 80–95 5–20 NAb
Grasses 25–40 25–50 10–30
Hardwood 45 ± 2 30 ± 5 20 ± 4
Hardwood barks 22–40 20–38 30–55
Lignin Hydrolyzed Cellulose
Hardwood stems 40–55 24–40 18–25
Leaves 15–20 80–85 0
Hemicellulose
Newspaper 40–55 25–40 18–30
Nut shells 25–30 25–30 30–40
Paper 85–99 0 0–15 Enzymatic
Pine softwood 44 26 29
hydrolysis
Primary wastewater 8–15 NAb 24–29
solids
Softwood 42 ± 2 27 ± 2 28 ± 3
Softwood barks 18–38 15–33 30–60 Mainly Mainly
Softwood stems 45–50 25–35 25–35
Solid cattle manure 1.6–4.7 1.4–3.3 2.7–5.7
Pentoses Glucose
Sorted refuse 60 20 20
Spruce softwood 43 26 29
Swine waste 6.0 28 NAb
Switch grass 45 31.4 12.0
Waste papers from 60–70 10–20 5–10 Fermentation
chemical pulps
Wheat straw 37–41 27–32 13–15
Willow Hardwood 37 23 21

–, Not determined. Separation

a
Source: Balat (2011), Olsson and Hahn-Hägerdal (1996) and Sun and Cheng
(2002).
b
NA – not available.

Lactic acid
The orientation of the linkages and additional hydrogen bond-
ing make the polymer rigid and difficult to break. Hemicellulose Fig. 1. A general flow chart of the “conventional” process for lactic acid production
(20–40% of total feedstock dry matter) is a short, highly branched from lignocellulosic biomass materials.

heterogeneous polymer consisting of pentose (xylose and arabi-

nose), hexose (galactose, glucose, and mannose), and acid sugars
(Saha, 2000). Mannose is the dominant hemicellulose sugar in soft-
woods, while xylose is dominant in hardwoods and agricultural
residues (Taherzadeh and Karimi, 2008). Hemicellulose is more
readily hydrolyzed compared to cellulose because of its branched
and amorphous nature. Lignin (15–25% of total feedstock dry mat-
ter) is an aromatic polymer synthesized from phenylpropanoid
precursors. The phenylpropane units of lignin (primarily syringyl,
guaiacyl, and phydroxy phenol) are bonded together by a set of
linkages to form a very complex matrix (Demirbas, 2008). This com-
plex matrix consists of a variety of functional groups, e.g., hydroxyl,
methoxyl, and carbonyl groups, which impart a high polarity to
the lignin macromolecule (Feldman et al., 1991). Lignin is consid-
ered to be difficult to use as a fermentation substrate because it
makes the biomass resistant to chemical and biological degradation
(Taherzadeh and Karimi, 2008).
can be fermented to lactic acid by wild-type and breeding strains,
with varying degrees of effectiveness. Once the technologies are
established and commercialized, a wide range of valuable products
could be produced from lignocellulosic biomass. The conventional
processes for producing lactic acid from lignocellulosic biomass
include the following 4 main steps (Fig. 1):
(1) Pretreatment—breaking down the structure of the lignocellu-
losic matrix.
(2) Enzymatic hydrolysis—depolymerizing lignocellulose to fer-
mentative sugars, such as glucose and xylose, by means of
hydrolytic enzymes.
(3) Fermentation—metabolizing the sugars to lactic acid, generally
by LAB.
(4) Separation and purification of lactic acid—purification of lactic
acid to meet the standards of commercial applications.

2.2. Conventional processes for lactic acid production by LAB
from lignocellulosic biomass
Despite the advantages in its sustainability and availability,
the commercial use of lignocellulose in lactic acid production is
still problematic due to its complexity. The biochemical conver-
sion of lignocellulosic biomass requires several processing steps
designed to convert structural carbohydrates to monomeric sug-
ars, e.g., glucose, xylose, arabinose, and mannose. These sugars
2.2.1. Pretreatment methods
The enzymatic susceptibility of native lignocellulose is difficult
and slow due to the association of cellulose and hemicellulose
with lignin (Schmidt and Thomsen, 1998). The main goals of
pretreatment are to remove lignin, separate cellulose and hemicel-
lulose, increase the accessible surface area, partially depolymerize
cellulose, and increase the porosity of the materials to aid in
the subsequent access of the hydrolytic enzymes (Chandel et al.,
2007; Hendriks and Zeeman, 2009; Kumar et al., 2009; Sun and
 M.A. Abdel-Rahman et al. / Journal of Biotechnology 156 (2011) 286–301
Cheng, 2002; Taherzadeh and Karimi, 2007; Zhang et al., 2009).
The hemicellulose should be removed or altered without degra-
dation for a high ultimate yield of sugars (Mosier et al., 2005).
Pretreatment includes physical (milling and grinding), chemical
(alkali, dilute acid, oxidizing agents, and organic solvents), physico-
chemical (steam explosion/autohydrolysis, hydrothermolysis, and
wet oxidation), and biological methods. Some methods disrupt
the lignin–carbohydrate complex, and other disrupts the highly
ordered crystalline cellulose structure (Sun et al., 1995).
Different pretreatment methods have been extensively devel-
oped, including ammonia fiber explosion and ammonia recycle
percolation (Jorgensen et al., 2007), lime (Kaar and Holtzaple,
2000), organosolv (Pan et al., 2006), liquid hot water (Antal, 1996),
ionic liquid (Dadi et al., 2006), alkaline pretreatment (Lau et al.,
2008), dilute acid and steam explosion (Laser et al., 2002; Mosier
et al., 2005; Parisi, 1989; Yang and Wyman, 2008), and enzymatic
treatment (Anderson et al., 2005; Converse, 1993; Hayn et al.,
1993; Ladisch et al., 1983). Among these methods, dilute acid pre-
treatment is still the method of choice in several model processes
(Wyman et al., 2005). The initial pretreatment reaction involves a
mild acid-catalyzing hydrolysis of the glycosidic bonds of hemi-
cellulose and the ether linkages in lignin (Fengel and Wegener,
1989), in which the organic acids, formed by the cleavage of labile
ester groups, catalyze the hydrolysis of hemicellulose. Fractiona-
tion is achieved by the enlargement of the inner surface. The effects
of different pretreatment methods upon different lignocellulosic
materials, e.g., corn stover (Chen et al., 2009), wheat straw (Sun
and Chen, 2008), switchgrass (Esteghlalian et al., 1997), rice straw
(Zhang and Cai, 2008), and sugarcane bagasse (Rabelo et al., 2009),
have been investigated.
The pretreatment process is a very critical stage in lignocellu-
lose bioconversion. If pretreatment is not sufficiently efficient, the
resultant residue is not easily saccharified by hydrolytic enzymes
and, if it is too severe, toxic compounds can be produced that
inhibit microbial metabolism and growth (Kodali and Pogaku,
2006). Therefore, pretreatment has a great potential to influence
the downstream costs by determining fermentation toxicity, enzy-
matic hydrolysis rates, enzyme loading, mixing power, product
concentrations, product purification, waste treatment demands,
power generation, and other process variables. An effective pre-
treatment process should meet the following requirements: (1)
highly digestible pretreated solid; (2) no significant degradation
of sugars; (3) good recovery of high sugar concentrations; (4) sugar
formation by subsequent enzymatic hydrolysis; (5) effective at low
moisture contents; (6) form minimal or no microbial inhibitory
by-products; (7) require minimal energy input; (8) high degree of
simplicity; (9) not require biomass size reduction; (10) low cost
materials for the construction of pretreatment reactors and to be
easily managed at large volumes; (11) produce less residues; (12)
consume few and cheap chemicals; and (13) have environmentally
acceptable features (Galbe and Zacchi, 2007; Lynd, 1996; Sun and
Cheng, 2002; Wu et al., 2011; Yang and Wyman, 2008).
2.2.2. Enzymatic hydrolysis
Enzymatic hydrolysis is the most promising means to yield fer-
mentable sugars from pretreated lignocellulosic biomass, and is
necessary to allow LAB to utilize polysaccharides as a carbon source
(Hinman et al., 1992; Lin and Tanaka, 2006; Lynd et al., 1996; Ogier
et al., 1999; Taniguchi et al., 2005; Yu and Zhang, 2004). The goal
of enzymatic hydrolysis is to depolymerize the polysaccharides in
the water-insoluble solid fraction that remains after pretreatment.
There are 2 general categories of enzymes necessary to convert
cellulose and hemicellulose into soluble sugars: cellulases and
hemicellulases, respectively. To maximize enzymatic hydrolysis,
mixtures of these enzymes are needed to increase hemicellulose
hydrolysis and thus increase the access of cellulase, leading to a
289
decreased hydrolysis time and process cost (Öhgren et al., 2007; Tu
and Saddler, 2010; Zhang et al., 2010a).
The rate of the enzymatic hydrolysis of cellulose is greatly
affected by its degree of polymerization (Chang and Holtzapple,
2000; Cohen et al., 2005; Kumar et al., 2008). Efficient degradation
and saccharification of cellulose require a synergistic reaction of
the following 3 classes of cellulolytic enzymes:
(a) Endo-␤-1,4-glucanases (EG; EC 3.2.1.3): randomly hydrolyze
accessible intramolecular ␤-1,4-glucosidic bonds of cellulose
chains and insert a water molecule in the ␤-(1,4) bond, creating
a new reducing and non-reducing chain end pair.
(b) Exo-␤-1,4-glucanases or cellobiohydrolases (CBH; EC 3.2.1.91):
cleave cellulose chains at the ends of the polymer, releasing
soluble cellobiose or glucose.
(c) ␤-Glucosidases (␤-G; EC 3.2.1.21) (cellobiases): complete the
hydrolysis by cleaving cellobiose into 2 glucose molecules (Lynd
et al., 2002) and thus relieve the system from end-product
inhibition (Fujii et al., 1995). They are also active on cello-
oligosaccharides (Kumar et al., 2008).
Individual cellulases have very limited hydrolytic activity, while
a mixture of cellulases can exhibit a synergistic effect (Nidetzky
et al., 1994; Zhang et al., 2007). Extensive research has been per-
formed to improve the hydrolytic efficiency of such enzymes (Baker
et al., 1998; Mais et al., 2002; Selig et al., 2008). In addition to these
3 major groups of cellulases, accessory or “helper” enzymes that
attack hemicellulose (Berlin et al., 2005) and lignin (Palonen and
Viikari, 2004) may also play a role in hydrolysis by clearing the
access of the main enzymes to cellulose.
Unlike cellulose, xylans are chemically quite complex, and
their degradation requires multiple enzymes. Enzymatic hydrolysis
of hemicellulose requires endo-1,4-␤-xylanase, ␤-xylosidase, ␤-
glucuronidase, ␣-l-arabinofuranosidase, and acetylxylan esterase,
which act on xylan degradation and saccharification (Carvalheiro
et al., 2008; Saha, 2004), and ␤-mannanase and ␣-mannosidase,
which cleave the glucomannan polymer backbone (Kumar et al.,
2008). Although more enzymes are required for xylan hydrolysis
than for cellulose hydrolysis, the substrate is more easily accessible
because xylan does not form tight crystalline structures (Keshwani
and Cheng, 2009).
The hydrolytic efficiency of a multi-enzyme mixture in the
process of lignocellulose hydrolysis depends on the properties of
the individual enzymes and their ratio in the multi-enzyme cock-
tail (Irwin et al., 1993; Zhou et al., 2009). Recently, Lin et al.
(2011) constructed a cellulase cocktail for a more efficient enzy-
matic hydrolysis of lignocellulose and a more rational utilization of
enzymes by using combinations of the 3 enzymes, 2 cellulases, and
1 xylanase.
2.2.3. Fermentation process with LAB
The hydrolysate of a lignocellulosic biomass is a mixture of
hexoses (e.g., glucose) and pentoses (e.g., xylose and arabinose).
Lignin cannot be used for lactic acid fermentation. The effective uti-
lization of cellulose- and hemicellulose-derived sugars can reduce
the production cost of biomaterials by as much as 25% (Hinman
et al., 1989). Fermentation technologies must be cost competitive
with chemical synthesis to validate the use of biotechnological pro-
cesses on an industrial scale (Bustos et al., 2007). The key economic
drivers in the fermentation process are high product yields, produc-
tivity, and the concentration of products formed, which strongly
influences the product recovery costs. In order to achieve maxi-
mum lactic acid yield and productivity, a large number of studies
have investigated lactic acid fermentation by LAB from lignocel-
lulosic biomass in the field of microbial technology, as described
290 M.A. Abdel-Rahman et al. / Journal of Biotechnology 156 (2011) 286–301
in detail in Section 3.2. Biomass materials have been used as
substrates for lactic acid production by LAB, including lignocel-
lulose/hemicellulose hydrolysates (Karel et al., 1997), cottonseed
hulls (Vickroy, 1985), corncob (Guo et al., 2010; Moldes et al., 2006;
Shen and Xia, 2006; Wang et al., 2010), corn fiber hydrolysates and
stalks (Saha and Nakamura, 2003; Vickroy, 1985), apple pomace
(Gullon et al., 2008), wood hydrolysate (Wee et al., 2004), beet
molasses (Göksungur and Güvenç, 1999; Kotzamanidis et al., 2002),
sugar cane press mud and bagasse (Xavier and Lonsane, 1994;
Laopaiboon et al., 2010), cassava bagasse (John et al., 2006a,b; Rojan
et al., 2005), cellulose (Venkatesh, 1997; Singhvi et al., 2010), paper
sludge (Marques et al., 2008), carrot processing waste (Pandey et al.,
2001), molasses spent wash (Sharma et al., 2003), and wheat bran
(John et al., 2006c; Naveena et al., 2005a,b).
2.2.4. Separation and purification of lactic acid
In the traditional chemical separation process, the fermentation
broth is first neutralized by calcium carbonate. The calcium lactate-
containing broth is then filtered to remove cells, carbon treated,
decolored, evaporated, and acidified with sulfuric acid to produce
lactic acid and insoluble calcium sulfate (Datta and Henry, 2006).
Pure lactic acid is further obtained by hydrolysis, esterification, and
distillation. The disadvantages of this process include the produc-
tion of a large amount of calcium sulfate (gypsum) as a by-product
and high sulfuric acid consumption (Qin et al., 2010). Other alter-
native lactic acid separation technologies such as adsorption (Chen
and Ju, 1998), reactive distillation (Kumar et al., 2006), ultrafiltra-
tion and electrodialysis (Choi et al., 2002; Datta and Henry, 2006;
Hábová et al., 2004; Kim and Moon, 2001; Madzingaidzo et al.,
2002), and nanofiltration (Gonzalez et al., 2008; Li and Shahbazi,
2006) have also been studied as lactic acid separation and purifi-
cation processes that do not yield salt waste. These separation
processes are more cost and energy efficient when compared with
traditional chemical separation processes. In addition, they have
several advantages including the lack of energy-intensive phase
changes or potentially expensive solvents or adsorbents as well as
the potential for the simultaneous separation and concentration of
lactic acid (Li et al., 2008).
2.3. Difficulties in using lignocellulosic biomass for efficient lactic
acid production by LAB
The effective utilization of lignocellulosic biomass has some
inherent limitations due to its seasonal availability, scattered dis-
tributions, and the high costs of storage and transportation (Lin
and Tanaka, 2006; Polman, 1994). In addition, the main problems
encountered in the efficient conversion of lignocellulosic biomass
to lactic acid are: (a) the resistant nature of biomass and pre-
treatment problems; (b) high cost enzymes and their feedback
inhibition; (c) formation of by-products due to the heterofermen-
tation of pentose sugars; and (d) carbon catabolite repression
caused by the heterogeneity of hydrolysate-sugar composition.
These obstacles are briefly discussed as follows:
2.3.1. Resistant nature of biomass and pretreatment problems
Crystalline nonreactivity and, in particular, resistance to hydrol-
ysis are the major problems for efficient lignocellulose utilization
(Kumar et al., 2008). Although various pretreatment procedures
have been evaluated, its utilization is a major drawback and affects
the total economy of the bioconversion of lignocellulosic biomass
(Zhang et al., 2009). Pretreatment is an expensive step and has a
major influence on the cost of the enzymatic hydrolysis and fer-
mentation processes (Lynd et al., 1996; Wooley et al., 1999). Also,
lignin limits the rate of cellulose hydrolysis by acting as a physi-
cal barrier that prevents the digestible parts of the substrate from
being hydrolyzed (Chang and Holtzapple, 2000; Esteghlalian et al.,
2001). Different strategies have been examined to overcome the
nonproductive adsorption of lignin to cellulase by alkali extraction
and the addition of proteins or other additives, e.g., polyethylene
glycol and Tween (Börjesson et al., 2007; Pan et al., 2005).
Another obstacle is the release of inhibitory compounds dur-
ing the pretreatment process. Although the composition of the
released compounds depends not only on the type of lignocellu-
losic material and the chemistry but also on the characteristics of
the pretreatment process. These inhibitory compounds interfere
with the hydrolysis of cellulosic substrates by cellulase (Mes-
Hartree et al., 1987). In addition, many potentially inhibitory
compounds released by pretreatment processes have been iden-
tified for the microorganisms used for fermentation (Mussatto
and Roberto, 2004; Palmqvist and Hahn-Hägerdal, 2000). Although
detoxification methods such as bioabatement (Lopez et al., 2004;
Nichols et al., 2005) and overliming (Nilvebrant et al., 2003) have
been proposed, the efficiency of fermentation is still in need of
improvement. The isolation of superior LAB strains or genetically
engineered strains that are resistant to inhibitors, and advances
and improvements in the pretreatment of lignocellulose are still
needed to reduce the overall cost. Recently, wild-type Lactobacillus
brevis S3F4 was shown to have strong resistance to fermentation
inhibitors such as ferulic acid and furfural (Guo et al., 2010). Biolog-
ical delignification with white rot fungi, which selectively degrade
lignin and leave cellulosic materials, also has potential advantages
such as low-capital cost, low-energy input, no chemical require-
ments, mild environmental conditions, and high yields without
generating polluting by-products (Chaudhary et al., 1994; Kuhad
and Johri, 1992; Kumar et al., 2009). However, drawbacks of this
process include its long treatment period and low hydrolysis rate
(Kumar et al., 2008; Sun and Cheng, 2002).
2.3.2. High-cost enzymes and their feedback inhibition
The high costs of enzyme production, feedback inhibition, and
the excessive enzymatic dosages necessary to hydrolyze pre-
treated biomass are some of the drawbacks limiting the commercial
application of lignocellulose hydrolysis as a lignocellulosic-lactate
industry (Himmel et al., 1999; Wooley et al., 1999). During cellu-
lose saccharification, the sugar end products of hydrolysis do not
accumulate quickly because the saccharified glucose and cellobiose
inhibit the EG and CBH activities by feedback inhibition (Adsul et al.,
2007b; Ghosh and Das, 1971; Holtzapple et al., 1990; Lee and Fan,
1983). Several methods have been developed to reduce this inhi-
bition, including the improvement of ␤-G activity in the cellulase
system (Shen and Xia, 2004), removing the released sugars dur-
ing hydrolysis by ultrafiltration or simultaneous saccharification
and fermentation (SSF) (Rezaei et al., 2008), optimizing cellulase
enzyme conditions (i.e., temperature, pH, and enzyme loading
amounts) (Sun and Cheng, 2002; Ou et al., 2009), or supplying ␤-G
during hydrolysis to avoid cellobiose accumulation (Caminal et al.,
1985; Moldes et al., 2001; Ramos and Saddler, 1994). Studies to
remove such forms of inhibition are still in progress.
2.3.3. Formation of by-products due to the heterofermentation of
pentose sugars
Lignocellulosic hydrolysates contain not only hexoses but also
pentoses. Hexoses can easily be fermented by LAB, while pen-
tose sugars cannot be fermented by most LAB (Hofvendahl and
Hahn-Hägerdal, 2000; Tanaka et al., 2002). In general, a few LAB
metabolize pentose sugars via the phosphoketolase (PK) pathway,
which exhibits heterofermentation with equimolar amounts of lac-
tic acid and acetic acid produced and reaches only 0.60 C-mol/C-mol
in terms of the theoretical yield of lactic acid to pentose sugars
(Abdel-Rahman et al., 2011b; Oshiro et al., 2009; Patel et al., 2006;
Tanaka et al., 2002). This co-production of acetic acid and lactic acid
also results in an increase of the lactic acid purification cost (Garde
 M.A. Abdel-Rahman et al. / Journal of Biotechnology 156 (2011) 286–301
et al., 2002; Patel et al., 2006); therefore, this approach is not con-
ducive for the industrial fermentation of pentoses to lactic acid. To
overcome this obstacle, we previously isolated a LAB strain, Lac-
tococcus lactis IO-l, which could utilize xylose with a high lactate
yield and low acetate production (Tanaka et al., 2002). Okano et al.
(2009a,b) engineered the LAB Lb. plantarum strain to produce lac-
tic acid from xylose and arabinose via the pentose phosphate (PP)
pathway, leading to homolactate production. Recently, we reported
that a novel LAB, Enterococcus mundtii QU 25, consumed xylose
homofermenatively without acetate production (Abdel-Rahman
et al., 2010a, 2011b); therefore, the purification cost will be sig-
nificantly decreased with this strain.
2.3.4. Carbon catabolite repression caused by the heterogeneity
of the hydrolysate-sugar composition
One of the major obstacles in using lignocellulosic biomass as
a feedstock is the inherent heterogeneity of its sugar composition
(Kim et al., 2010a). To achieve maximum product yield and pro-
ductivity, the complete utilization of these sugars is essential (Kim
et al., 2010b; Saha, 2003). In many LAB, fermentation of mixed
carbohydrates is achieved sequentially, whereby the utilization of
glucose represses the consumption of alternative sugars due to car-
bon catabolite repression (Saier, 1998; Stulke and Hillen, 1999;
Titgemeyer and Hillen, 2002). This sequential utilization of mixed
sugars makes the fermentation process complex and often reduces
the yield and productivity (Bothast et al., 1999). Carbon catabolite
repression by LAB has been reported in many strains, e.g., Lb. casei
(Gosalbes et al., 1999; Veyrat et al., 1994; Viana et al., 2000), Lb.
pentosus (Chaillou et al., 1999, 2001; Mahr et al., 2000), Lb. plan-
tarum (Marasco et al., 1998), Lb. sakei (Zuniga et al., 1998), and Lb.
delbrueckii (Morel et al., 1999; Schick et al., 1999). A few LAB strains
have been reported to simultaneously consume lignocellulose-
derived sugars, e.g., Lb. brevis (Guo et al., 2010; Kim et al., 2009),
Lb. plantrum (Guo et al., 2010), and our newly isolated strain E.
mundtii QU 25 (Abdel-Rahman et al., 2010a,b, 2011a). Mixed LAB
cultures have also been used to maximize the yield and productivity
from mixed sugars (Cui et al., 2011; Taniguchi et al., 2004). There-
fore, it is essential to isolate LAB strains or to establish genetically
engineered strains for efficient lignocellulose utilization.
3. Fermentative lactic acid production by LAB
3.1. Improvement of lactic acid production by LAB in the field of
microbial technology
It has generally been observed that pH, nutrient concentration,
substrate concentration, end products concentration, and tem-
perature significantly affect the growth of LAB and lactic acid
production. These factors may decrease cell density and the lac-
tic acid titer, yield, and productivity in some cases. Researchers in
the field of microbial technology have conducted numerous studies
to establish an efficient method of lactic acid production by LAB.
In lactic acid fermentation, low pH has an inhibitory effect on
cellular metabolism and lactic acid production. The majority of LAB
cannot grow below pH 4, although the pKa of lactic acid is 3.78
(Adachi et al., 1998); therefore, neutralizing agents such as cal-
cium carbonate, sodium hydroxide, or ammonium hydroxide must
be added to keep the pH at a constant value in order to reduce
the inhibitory effects of low pH. pH-controlled batch fermentation
significantly improves lactic acid production, yield, and produc-
tivity by different LAB strains, e.g., Lb. delbrueckii (Tashiro et al.,
2011), E. mundtii QU 25 (Abdel-Rahman et al., 2011a,b), and E. fae-
cium (Shibata et al., 2007). Batch fermentation is a simple closed
culture system that contains an initial and limited amount of nutri-
ent, and nothing is added during fermentation except possibly acid
291
or alkali for pH control. The low levels of nutrient limit the cell
concentration, final lactic acid concentration, and productivity. It
was reported that the addition of nutrients to a culture broth of E.
mundtii QU 25 during batch fermentation increased the cell mass
and lactic acid production and productivity (Abdel-Rahman et al.,
2011a). In addition, batch fermentation was superior to contin-
uous fermentation in some respects, particularly lactic acid titer
(Buyukgungor and Bueschelberger, 1986; Hofvendahl and Hahn-
Hägerdal, 2000; Nomura et al., 1987). High lactic acid production
has been obtained with batch fermentation of LAB with the pro-
duction of 150 g/L l-lactate from glucose (Bai et al., 2004), 87.2 g/L
d-lactate from glucose (Tashiro et al., 2011), and 119 g/L l-lactate
(Abdel-Rahman et al., 2011a) and 80 g/L d-lactate (Joshi et al., 2010)
from cellobiose.
Substrate inhibition always occurs at high sugar concentra-
tions (Ding and Tan, 2006; Gatje and Gottschalk, 1991; Oshiro
et al., 2009). To overcome or reduce substrate inhibition, fed-batch
cultures were a better fermentation system than batch and contin-
uous cultures because they allow for an increased maximum viable
cell concentration and prolonged culture lifetime, which result in
product accumulation to a higher concentration. Bai et al. (2004)
developed a process for the production of ammonium lactate with
Lb. lactis in pH-controlled fed-batch fermentation with 161.2 g/L
of lactic acid. Ding and Tan (2006) developed a high lactic acid
concentration process using 4 different fed-batch feeding strate-
gies with Lb. casei: pulse fed-batch, constant feed rate fed-batch,
constant residual glucose concentration fed-batch, and exponential
feed rate fed-batch fermentations. They generated up to 210 g/L of
lactic acid and a 97% yield with an exponential rate of feeding glu-
cose solution and yeast extract (Ding and Tan, 2006). However, in
all fed-batch technologies, the substrate concentration in the fer-
mentation broth is unstable, thereby generating more stress on the
producing strain. Recently, a method was developed to control the
concentration of the substrate through the automatic adjustment
of pH. Using this method, 96.3 g/L and 170 g/L of lactic acid were
obtained with Lb. lactis-11 (Zhang et al., 2010b) and Lb. rhamnosus
LA-04-1 (Li et al., 2010), respectively. Chang et al. (2011) suggested
multi-stage continuous high cell density culture as a new produc-
tion platform for obtaining high lactic acid titers (212.9 g/L) and
productivity (10.6 g L−1 h−1 ) with Lb. rhamnosus. In addition to fed-
batch fermentation, continuous and semi-continuous fermentation
processes have been used for lactic acid production by reducing
substrate inhibition (Amrane and Prigent, 1996; Nolasco-Hipolito
et al., 2002; Tashiro et al., 2011). The choice of the most suitable fer-
mentation process will depend upon the kinetic properties of the
LAB species used, the type of substrates, and the economic aspects
of the process.
High productivity was achieved with a high LAB cell density
without reducing the yield (Ohleyer et al., 1985). Many reports
showed that high cell density by cell recycling through filtration
drastically increased lactic acid productivity with Lb. helveticus
(Kulozik and Wilde, 1999), E. faecium (Shibata et al., 2007), and Lb.
delbrueckii (Tashiro et al., 2011). The cell recycling system, along
with repeated batch and continuous processes, generated a high
cell concentration and productivity in these processes (Kwon et al.,
2001; Oh et al., 2003). The immobilization of cells has been one
of the means used for high cell retention in bioreactors; however,
many studies were not very successful in terms of yield and produc-
tivity (Cotton et al., 2001; Göksungur and Güvenç, 1999; Senthuran
et al., 1999; Zhang et al., 2011).
One of the major problems associated with lactic acid pro-
duction by fermentation is end-product inhibition; therefore, to
decrease the inhibitory effect of lactic acid during fermentation, it
must be selectively removed from the fermentation broth. Many
attempts have been directed to develop processes that remove
lactic acid from the fermentation broth, e.g., extraction from the
292 M.A. Abdel-Rahman et al. / Journal of Biotechnology 156 (2011) 286–301
fermentation broth (Hano et al., 1993; Honda et al., 1995; Iyer and
Lee, 1999a,b; Yabannavar and Wang, 1991; Ye et al., 1996), elec-
trodialysis (Boyaval et al., 1987; Hongo et al., 1986; Kim and Moon,
2001; Min-Tian et al., 2005; Nomura et al., 1998; van Nispen and
Jonker, 1991; Vonktaveesuk et al., 1994), and nanofiltration mem-
branes and ion exchange resins (Jeantet et al., 1996; Monteagudo
and Aldavero, 1999; Srivastava et al., 1992; Vaccari et al., 1993). The
continuous removal of lactic acid with extraction or electrodialysis
results in even higher lactic acid concentrations and yields com-
pared to conventional batch fermentation processes. Li et al. (2004)
developed a bioreactor combining conventional electrodialysis and
bipolar membrane electrodialysis for product removal and pH con-
trol in lactic acid fermentation. Min-Tian et al. (2005) achieved high
lactic acid productivity and yields with a continuous electrodial-
ysis fermentation system. Even though these methods lower the
purification cost, the price of the membranes and decreases in the
permeate flow rate make the process less cost efficient and are still
considerable drawbacks. Other methods, e.g., two phase systems,
have been developed; however, the extracting material must be
biocompatible and not harm the organism in order to be efficient
(Planes, 1998).
The influence of temperature on lactic acid fermentation is
related to the growth kinetic parameters of LAB, lactic acid pro-
duction, and substrate consumption. Among LAB, most lactic acid
productivity studies have been conducted at temperatures of
30–43 ◦ C. We recently isolated a new LAB strain, Lb. delbrueckii QU
41, that exhibits a high thermotolerance and produces d-lactic acid
at temperatures ≥50 ◦ C (Tashiro et al., 2011).
3.2. Lactic acid production by LAB using lignocellulosic biomass
and lignocellulose-derived sugars
Separate hydrolysis and fermentation (SHF) is a process with
separate enzymatic hydrolysis and fermentation steps. The main
advantage of SHF is the ability to carry out each step under opti-
mal conditions for each process. However, the main disadvantage
of this method is the feedback inhibition of saccharified sugars,
e.g., glucose, xylose, cellobiose, and other oligosaccharides, on the
activity of hydrolytic enzyme during the hydrolysis process, which
demands lower loadings of the lignocellulosic biomass and higher
loadings of the hydrolytic enzymes to achieve reasonable yields
(Jeffries and Jin, 2000; Philippidis, 1996). In addition, this 2-step
process increases the total processing time. To overcome these
problems, SSF for lactic acid production by LAB has been devel-
oped as described in detail below. In comparison with SHF, SSF
offers many advantages, including: (1) reduced reactor volume due
to the usage of only a single reactor; (2) rapid processing time;
(3) reduced feedback inhibition; (4) increased productivity; (5)
enhanced rate of hydrolysis; (6) lower enzyme loading; and (7)
higher lactic acid yields (Ehrman and Himmel, 1994; Hofvendahl
and Hahn-Hägerdal, 2000; Iyer and Lee, 1999a,b; John et al., 2006c;
Linko and Javanainen, 1996; Moritz and Duff, 1996; Sun and Cheng,
2002; Tsai and Moon, 1998; Zheng et al., 1998).
SSF technology is a good strategy for lactic acid production by
LAB from renewable bioresources such as lignocellulosic mate-
rials. In SSF, cellulases and xylanases convert the lignocellulosic
materials to fermentable sugars. These enzymes are notoriously
susceptible to feedback inhibition by the saccharified sugars, e.g.,
glucose, xylose, cellobiose, and other oligosaccharides (Jeffries and
Jin, 2000). As described above, one of the advantages of SSF is that
the immediate consumption of sugars by microorganism maintains
the sugar concentration at a low level in the bioreactor, thereby sig-
nificantly reducing feedback inhibition (Balat et al., 2008; Mosier
et al., 2005). In SSF, hydrolysis is usually the rate-limiting process
(Philippidis and Smith, 1995). SSF with cellulose has been stud-
ied with Lb. delbrueckii (Abe and Takagi, 1991) and Lb. rhamnosus
(Parajo et al., 1997; Schmidt and Padukone, 1997). Other studies
have reported lactic acid production by SSF from lignocellulosic
biomasses such as corncob, waste wood, wheat straw, and alfalfa
fiber (Adenis et al., 1999; Cui et al., 2011; Garde et al., 2002; Jun et al.,
1998; Lee et al., 2004; Miura et al., 2004; Moldes et al., 1999; Romani
et al., 2008; Sreenath et al., 2001; Yanez et al., 2003). SSF technol-
ogy with lignocellulosic materials needs to be further improved,
including the co-fermentation of multiple sugar substrates, i.e., the
saccharification of cellulose to glucose and hemicellulose to xylose,
and the fermentation of saccharified glucose and xylose.
Compared to SHF, the disadvantages of SSF lie in the differ-
ent temperatures and pH optima required for saccharification and
fermentation (Krishna et al., 2001; Huang et al., 2005), and the inhi-
bition of enzyme function by lactic acid. In general, the optimal
conditions for enzymatic hydrolysis and lactic acid fermentation
are 50 ◦ C and 37–43 ◦ C, and a pH < 5.0 and 5.0–7.0, respectively
(Hofvendahl and Hahn-Hägerdal, 2000). To perform SSF more effi-
ciently, thermotolerant LAB are expected to raise the temperature
close to the optimal hydrolysis temperature, as have succeeded
in high lactic acid production with SSF technology by thermotol-
erant Bacillus coagulans (Ou et al., 2009, 2011). In addition, Iyer
and Lee (1999a) studied the effect of lactic acid on the enzy-
matic hydrolysis of cellulose in SSF. They found that the enzymatic
digestibility decreased from 79% to 56% as the lactic acid concen-
tration increased from 0 to 90 g/L. At levels higher than 90 g/L lactic
acid, they observed a 50% inhibition of the digestibility. However,
the inhibition of enzymatic hydrolysis by lactic acid is much lower
than the feedback inhibition caused by glucose buildup (Takagi,
1984).
Depending on the source of lignocellulosic biomass (Table 1),
hemicellulose forms a substantial fraction of the lignocellulosic
biomass as well as cellulose, which yields pentose sugars such
as xylose and arabinose by saccharification. The majority of LAB
strains, e.g., Lb. delbrueckii (Monteagudo et al., 1997), Lb. helveti-
cus (Tango and Ghaly, 2002), and Lb. acidophilus (Portilla et al.,
2008), can convert cellulose-derived glucose to lactic acid, but not
hemicellulose-derived sugars. Others are capable of utilizing pen-
tose sugars for lactic acid production, including Lb. pentosus ATCC
8041 (Bustos et al., 2005; Zhu et al., 2007), Lb. bifermentans DSM
20003 (Givry et al., 2008), Lb. brevis (Chaillou et al., 1998), Lb. plan-
tarum (Helanto et al., 2007), Leuconostoc lactis (Ohara et al., 2006),
Lc. lactis (Tanaka et al., 2002), and E. mundtii QU 25 (Abdel-Rahman
et al., 2010a, 2011b). Recently, Okano et al. (2009a,b) succeeded
in replacing the PK pathway with the PP pathway in Lb. plan-
tarum ldhL1 in order to obtain a higher yield and production of
d-lactic acid from xylose and arabinose with very low amounts of
by-products. Among the LAB reported so far, only the wild-type E.
mundtii QU 25 (Abdel-Rahman et al., 2011a,b) and the genetically
modified Lb. plantarum ldhL1 (Okano et al., 2009a,b) can perform
homo-lactate fermentation of pentose sugars, which is expected to
generate significant levels of lactic acid production from lignocel-
lulosic biomass.
To date, direct lactic acid fermentation from xylan or cel-
lulose has not been demonstrated, and very few studies have
examined lactic acid production from xylooligosaccharides and cel-
looligosaccharides. Leu. lactis SHO-47 and SHO-54 were reported to
assimilate xylooligosaccharides from disaccharides to hexasaccha-
rides to produce d-lactic acid (Ohara et al., 2006). Recently, lactic
acid production from cellobiose with LAB has been established,
including Lb. delbrueckii mutant Uc-3 (Adsul et al., 2007b), Lb. plan-
tarum (Okano et al., 2010a), Lb. lactis mutant RM2-24 (Joshi et al.,
2010; Singhvi et al., 2010), and E. mundtii QU 25 (Abdel-Rahman
et al., 2011a). To our knowledge, only 2 reports have examined lac-
tic acid production from cellooligosaccharides. Adsul et al. (2007b)
used the Lb. delbrueckii mutant Uc-3 strain for the utilization of
cellotriose, while Okano et al. (2010a) developed genetically mod-
 M.A. Abdel-Rahman et al. / Journal of Biotechnology 156 (2011) 286–301 293

Fig. 2. Pathways for lactic acid production from lignocellulose-derived sugars (glucose, xylose, and arabinose) by lactic acid bacteria. Enzymes: (1) hexokinase; (2) glucose-6-
phosphate isomerase; (3) glucose-6-phosphate dehydrogenase; (4) 6-phosphogluconate dehydrogenase; (5) arabinose isomerase; (6) ribulokinase; (7) ribulose-5-phosphate
3-epimerase; (8) xylose isomerase; (9) xylulokinase; (10) phosphoketolase; (11) acetate kinase; (12) phosphotransacetylase; (13) aldehyde dehydrogenase; (14) alcohol dehy-
drogenase; (15) lactate dehydrogenase; (16) transketolase; (17) transaldolase; (18) 6-phosphofructokinase; (19) fructose-bisphosphate aldolase; and (20) triosephosphate
isomerase. Solid lines indicate the homofermentative pathway. Thick-solid lines and dashed lines indicate PP/glycolytic pathway and PK pathway, respectively.

ified Lb. plantarum for cellotriose and cellopentaose fermentation xylose, and xylooligosaccharides; therefore, the mixed sugars in
to produce lactic acid. lignocellulose hydrolysates need to be utilized simultaneously for
As mentioned above, lignocellulosic biomass yields several effective fermentation. Lb. buchneri NRRL B-30929 simultaneously
types of sugars by hydrolysis, e.g., glucose, cellooligosaccharides, and completely ferments lignocellulosic hydrolysates (glucose
 294
Table 2
Lactic acid production from lignocellulosic biomass materials and lignocellulose-derived sugars by lactic acid bacteria.

Microorganism Substrate Ferment. process CLA a (g/L) YLA b (g/g) PLA c (g L−1 h−1 ) Reference

E. mundtii QU 25 Cellobiose Batch 119 0.83 1.12 Abdel-Rahman et al. (2011a)

Xylose Batch 86.7 0.84 0.90 Abdel-Rahman et al. (2010a, 2011b)
Glucose/cellobiose Batch 35.1 0.91 2.99 Abdel-Rahman et al. (2010b, 2011a)
Glucose/xylose Batch – 0.83 3.6d Abdel-Rahman et al. (2010b)
Glucose/xylose/cellobiose Batch – 0.79 2.6d Abdel-Rahman et al. (2010b)
E. faecalis RKY1 Wood hydrolysate Batch 93.0 0.93 1.7 Wee et al. (2004)

E. casseliflavus and Lb. casei Xylose and glucose Batch 95.0 – – Taniguchi et al., 2004
Lb. bifermentans DSM 20003 Wheat bran hydrolysate Batch with cell 62.8 0.83 1.17 Givry et al. (2008)
immobilization
Lb. brevis Corncob Batch 39.1 0.70 0.81 Guo et al. (2010)
Lb. brevis and Lb. pentosus Wheat straw hemicellulose Batch 7.1 0.95 – Garde et al. (2002)
Lb. casei NCIMB 3254 Cassava bagasse Batch SSF 83.8 0.96 1.40 John et al. (2006a)
Lb. casei subsp rhamnosus Soft wood Batch 21.1–23.75 0.74–0.83 0.15–0.23 Iyer et al. (2000)

M.A. Abdel-Rahman et al. / Journal of Biotechnology 156 (2011) 286–301

Lb. coryniformis ATCC 25600 Cellulose SSF 54.0 0.89 0.5 Yanez et al. (2003)
Lb. coryniformis spp. torquens ATCC 25600 Pretreated cardboard Batch SSF 23.4 0.56 0.48 Yanez et al. (2005)
Lb. delbreuckii Alfalfa fibers SSF 35.4 0.35 0.75 Sreenath et al. (2001)
Lb. delbreuckii NRRL-B445 Cellulose SSF 65.0 0.18 – Iyer and Lee (1999a,b)
Lb. delbrueckii IFO 3202 Defatted rice bran SSF 28.0 0.28 0.77 Tanaka et al. (2006)
Lb. delbrueckii mutant Uc-3 Cellobiose Batch 90.0 0.90 2.25 Adsul et al. (2007b)
Molasses Batch 166 0.95 4.15 Dumbrepatil et al. (2008)
Lb. delbrueckii NCIM 2025 Cassava bagasse Batch SSF 81.9 0.94 1.36 John et al. (2006a)
Lb. delbrueckii subsp. delbrueckii Mutant Uc-3 Sugar cane bagasse Batch SSF 67.0 0.83 0.93 Adsul et al. (2007a)
Lb. delbrueckii UFV H2B20 Brewer’s spent grain Batch 35.5 0.99 0.59 Mussatto et al. (2008)
Lb. delbrueckii ZU-S2 Corn cob residue Batch/continuous 48.7/44.2 0.95/0.92 1.01/5.7 Shen and Xia (2006)
Lb. casei and Lb. lactis Date juice Batch 60.3 – 3.2d Nancib et al., 2009
Lb. lactis RM 2-24 Cellobiose Batch 80.0 0.8 1.66 Singhvi et al. (2010)
␣-Cellulose SSF 73.0 0.73 1.52 Singhvi et al. (2010)
Lb. pentosus Vine shoots Batch 24.0 0.76 0.51 Moldes et al. (2006)
Barley bran husks hydrolysates Batch 33.0 0.57 0.60 Moldes et al. (2006)
Corncob Batch 26.0 0.53 0.34 Moldes et al. (2006)
Lb. pentosus ATCC 8041 Vine-trimming wastes Batch 0.77 0.84 Bustos et al. (2004)
Corn stover Fed-batch SSF 74.8 0.65 – Zhu et al. (2007)
Lb. planlarum Alfalfa fibers SSF 46.4 0.46 0.64 Sreenath et al. (2001)
Lb. plantarum (Recombinant) ␤-Glucan/cellopentaose/cellohexaose Batch 1.47/ – – Okano et al. (2010a)
1.27/ – –
1.27 – –
Lb. plantarum (Recombinant) Arabinose Batch 38.6 0.82 3.78d Okano et al. (2009a)
Lb. plantarum (Recombinant) Xylose Batch 41.2 0.89 1.6d Okano et al. (2009b)
Lb. rhamnosus and Lb. brevis Corn stover SSF 20.95 0.70 0.58 Cui et al. (2011)
Lb. rhamnosus ATCC 7469 Paper sludge Batch SSF 73.0 0.97 2.9 Marques et al. (2008)
Lb. rhamnosus ATCC 9595 (CECT288) Apple pomace Batch 32.5 0.88 5.41 Gullon et al. (2008)
Cellulosic biosludge SSF 39.4 0.36 0.82 Romani et al. (2008)
Lactobacillus sp. RKY2 Rice and wheat bran Batch 129 0.95 2.9 Yun et al. (2004)
Lignocellulosic hydrolysates Continuous with 27.0 0.9 6.7 Wee and Ryu (2009)
cell-recycle
Lc. lactis IO-1 Xylose Batch 33.26 0.68 – Tanaka et al. (2002)
Sugar cane baggase Batch 10.9 0.36 0.17 Laopaiboon et al. (2010)
Leuconostoc lactis SHO-47 and SHO-54 Hydrolyzed xylan Batch 2.3 – – Ohara et al. (2006)
(Xylooligosaccharides)

E, Enterococcus; Lb, Lactobacillus; Lc, Lactococcus; SSF, simultaneous saccharification and fermentation.
a
Lactic acid concentration (g/L).
b
Yield of lactic acid produced (g) to substrate consumed (g).
c
Lactic acid productivity.
d
Maximum volumetric productivity.
 M.A. Abdel-Rahman et al. / Journal of Biotechnology 156 (2011) 286–301
Fig. 3. A flow chart of the approaches used for useful substance production from renewable resources in a recent study and a designed biomass study.
and xylose) with the production of lactate, acetate, and ethanol
(Liu et al., 2009). Lc. lactis IO-1 has been used to convert glu-
cose, xylose, and arabinose in sugarcane bagasse hydrolysates
to a mixture of lactic acid, acetic acid, formic acid, and ethanol
(Laopaiboon et al., 2010). Marques et al. (2008) used Lb. rham-
nosus ATCC 7469 to produce lactic acid from short fiber cellulose
of paper sludge by SSF without any pretreatment, and obtained
a lactic acid yield of 0.97 g/g carbohydrates and a productiv-
ity of 2.9 g L−1 h−1 (Marques et al., 2008). SSF of Lb. rhamnosus
ATCC 9595 with kraft pulp mill biosludge also produced lac-
tic acid with a yield of 0.38 g/g biosludge and a productivity of
0.87 g L−1 h−1 (Romani et al., 2008). Several authors have reported
biotechnological lactic acid production from lignocellulosic mate-
rials, agricultural waste, and forestry, industrial, or municipal solid
materials, e.g., unpolished rice (Lu et al., 2009), defatted rice bran
(Tanaka et al., 2006), and waste cardboard (Yanez et al., 2005).
Recently, in order to increase the conversion efficiency of sub-
strates, co-cultures of LAB (e.g., E. casseliflavus and Lb. casei or Lb.
casei and Lc. lactis) have been reported from lignocellulose-derived
mixed sugars (Cui et al., 2011; Nancib et al., 2009; Taniguchi et al.,
2004). Lactic acid fermentation from various types of lignocellulosic
biomass materials and lignocellulose-derived sugars by LAB strains
were achieved with different fermentation modes, as summarized
in Table 2.
As a result of these kinds of fermentation, cellulose- and
hemicellulose-derived sugars from lignocellulosic biomass can be
utilized with higher efficiency and productivity; however mixed
sugar cultures have not been used on an industrial scale because of
their many limitations. In mixed sugar cultures, the strains used do
not always have similar optimum culture conditions for pH, tem-
perature, nutrients, oxygen demand, etc.; therefore, it is not easy to
define the optimum condition or to maintain stable conditions for
such cultures during fermentation, and corresponding studies are
scarce. The discovery of LAB that have the capability to homofer-
mentatively utilize a wide range of sugars, including C5 and C6
sugars, and can resist the inhibitory compounds generated during
the pretreatment process is still a major challenge in fermenta-
295
tion technology for the production of lactic acid from lignocellulosic
biomass.
4. Metabolism of lignocellulose-derived sugars by LAB
LAB can be classified into 2 groups on the basis of the end product
of their fermentation: homofermentative and heterofermentative.
Homofermentative LAB virtually produce only lactic acid, whereas
other products are generated by heterofermentative LAB along with
lactic acid (Axelsson, 1993; Hofvendahl and Hahn-Hägerdal, 2000).
Fig. 2 shows the metabolic pathways of hexose and pen-
tose in LAB. When hexose sugars such as glucose are used, they
are consumed by the Streptococcus, Lactococcus, Enterococcus, and
Pediococcus genera and some Lactobacillus species to produce lactic
acid homofermentatively (Naveena, 2004), while additional prod-
ucts, e.g., carbon dioxide, ethanol, and acetic acid, are produced by
heterofermentative LAB, the Leuconostoc genera, and certain Lacto-
bacillus species (Carr et al., 2002; Cowan and Steel, 1965; Schillinger
and Lücke, 1987; Singleton and Sainsbury, 1987; Stamer, 1976).
In the metabolism of homofermentative LAB, glucose is metabo-
lized to lactic acid via the Embden–Meyerhof pathway, whereby the
theoretical yield of lactic acid to glucose is 1.0 g/g or 2.0 mol/mol.
On the other hand, heterofermentative LAB possess the pentose
monophosphate pathway, in which glucose 6-phosphate (6 car-
bons) is initially converted to ribulose 5-phosphate (5 carbons) and
carbon dioxide (1 carbon) catalyzed by several enzymes (Reddy
et al., 2008). The resulting ribulose 5-phosphate is cleaved to 1 mol
of glyceraldehyde 3-phosphate (GAP) and acetyl phosphate (acetyl-
P). GAP is further metabolized to lactic acid (3 carbons), while
the acetyl-P is reduced to ethanol (2 carbons) via acetyl-CoA and
acetaldehyde intermediates (Zaunmuller et al., 2006) and/or con-
verted to acetate via acetate kinase. Therefore, the theoretical yield
of lactic acid to glucose reaches only 0.5 g/g or 1.0 mol/mol with
heterofermentative LAB.
There are very few reports describing lactic acid fermentation
from pentose sugars by LAB (Fred et al., 1919; Patel et al., 2006).
Some species of LAB can metabolize pentose sugars as a substrate to
296 M.A. Abdel-Rahman et al. / Journal of Biotechnology 156 (2011) 286–301
lactic acid, e.g., Lc. lactis IO-1 (Oshiro et al., 2009; Tanaka et al., 2002),
Streptococcus sp. (Enterococcus sp.) and Lb. thermophilus T1 (Fukui
et al., 1957), Lactobacillus strain MONT4 (Barre, 1978), E. mundtii QU
25 (Abdel-Rahman et al., 2011b), Lb. pentosus (Bustos et al., 2005),
Lb. brevis (Chaillou et al., 1998), Lb. plantarum (Helanto et al., 2007),
and Leu. lactis (Ohara et al., 2006). Two different pathways, the PK
and PP/glycolic pathways, are proposed as the metabolic pathways
of pentoses in LAB (Fig. 2) (Tanaka et al., 2002). In the PK pathway,
which is used by the majority of pentose-utilizing LAB, xylulose
5-P (5 carbons) is cleaved to GAP and acetyl-P. The resulting GAP
is converted to pyruvic acid and then to lactic acid (3 carbons) as
a final product, while acetyl-P is metabolized to synthesize acetic
acid or ethanol (both 2 carbons). As a result, the theoretical yield
of pentose sugars to lactic acid is 0.6 g/g or 1.0 mol/mol via the PK
pathway (Patel et al., 2006). On the other hand, a few species of
LAB possess the PP/glycolic pathway for the metabolism of pen-
tose sugars. The PP/glycolic pathway produces 5 mol of lactic acid
from 3 mol of pentose without carbon loss, thereby providing a the-
oretical yield of lactic acid to pentose of 1.0 g/g or 1.67 mol/mol
(i.e., homo-lactate fermentation) (Oshiro et al., 2009; Tanaka et al.,
2002). Therefore, to improve the lactate yield, the PP/glycolic path-
way is more useful and valuable than the PK pathway (Oshiro et al.,
2009). Among wild-type LAB, E. mundtii QU 25 (Abdel-Rahman
et al., 2011b), Streptococcus sp. (Enterococcus sp.), Lb. thermophilus
T1 (Fukui et al., 1957), and Lactobacillus strain MONT4 (Barre, 1978)
were reported to only show homo-lactate fermentation of pentose
sugars. In addition, Okano et al. (2009a,b) recently demonstrated
homo-lactate fermentation with arabinose and xylose using genet-
ically modified Lb. plantarum by replacing the PK pathway with the
PP pathway.
The conversion of pyruvic acid to lactate can be affected by
stereospecific NAD-dependent enzymes of l- or d-lactate dehy-
drogenase. Both enzymes have been found to be active in most
lactobacilli, for example, Lb. plantarum (Ferain et al., 1996) and Lb.
casei (Viana et al., 2005). The stereospecificity and optical purity of
the lactic acid produced depends on the type of LAB, whose enzyme
used in its production. In addition, when xylose was used as the
sole carbon source, substrate concentration has been shown to be
a factor for the metabolic flux of lactic acid production in the batch
culture of E. mundtii QU 25 (Abdel-Rahman et al., 2011b) and the
continuous culture of Lc. lactis IO-1 (Tanaka et al., 2002); a higher
concentration of xylose and a higher yield of lactic acid to xylose
was obtained. Thus, further investigations of culture conditions
with LAB are suggested to be necessary for the efficient conversion
of lignocellulosic biomass to lactic acid.
5. Designed biomass study and conclusions
Currently, the fermentative production of useful substances,
e.g., biomaterials and biofuels, from various renewable resources
by microorganisms has become more attractive. For this purpose,
it is essential that the used strain should consume the renew-
able resources as substrates to produce the useful substances. In
a number of recent studies, a targeted substrate is initially decided
upon, e.g., several types of biomass and by-products from industrial
factories. Two main approaches are then applied to achieve effi-
cient bioconversion (Fig. 3). One approach is a screening method to
isolate wild-type strains from natural sources. The isolated strain
should show a great potential in terms of its degrading enzyme
for the targeted substrate, broad substrate specificity for compo-
nents derived from renewable resources, high product yield, low
by-product yield, capacity for high product concentration and pro-
ductivity, and so on. An efficient process can then be investigated
using the isolated strain, e.g., batch, fed-batch, or continuous fer-
mentation, SHF, or SSF. The second approach is breeding a strain
to improve its ability to produce or degrade renewable resources,
to modify metabolic pathways and their flux, including their incre-
ment or decrement, and to provide de novo degradation enzymes.
To date, many breeding strains have been created using mutagene-
sis with physical or chemical mutagens and genetic manipulation.
On the other hand, the active selection of substrates is also
significant for the highly efficient bioconversion of renewable
resources to useful substances. Recently, we proposed a “designed
biomass study” for this purpose. “Designed biomass” refers to
competent substances that can be designed for the corresponding
fermentation, conversion processes, etc. In this type of study, all the
technologies and engineering methods developed to date can be
used, i.e., excellent strains or highly efficient processes; thereafter,
substrates could be modified or identified for the existing technolo-
gies (Fig. 3). The targeted renewable resources should include not
only several types of components (mono-, oligo-, or polysaccha-
rides) derived from various non-edible biomass sources but also
organic acids or glycerol that are readily available and inexpen-
sive as ready-made waste. On the basis of this concept, lactic acid
(Oshiro et al., 2010) and butyric acid (Tashiro et al., 2004; Tashiro
et al., 2007), both are produced fermentatively, were indicated as
designed biomass material for acetone–butanol–ethanol fermen-
tation by using the Clostridium saccharoperbutylacetonicum N1-4
strain. In terms of lactic acid fermentation, we assessed sago starch
as a designed biomass for E. faecium from among several starches
derived from different plants (Shibata et al., 2007). Of course, our
concept also involves investigations on pretreatments and enzy-
matic hydrolysis of renewable resources, as mentioned in Section
2.2.
In this review, we mainly described fermentative lactic acid pro-
duction processes by LAB. Other microorganisms can be considered
as genetically modified hosts for industrial lactic acid production
such as yeasts and Escherichia coli, which generally produce little
lactic acid (Okano et al., 2010b). Yeasts can grow in simpler syn-
thetic media and are more tolerant to low pHs than LAB, which
can eliminate a generation of the precipitated lactate by neutraliz-
ing agents for pH control during fermentation (Abbott et al., 2009;
Skory, 2003). Lactic acid production using several recombinant
yeasts has been reported in Saccharomyces cerevisiae (Tokuhiro
et al., 2008; van Rooyen et al., 2005), Kluyveromyces lactis (Bianchi
et al., 1996; Porro et al., 1999), Candida boidinii (Ikushima et al.,
2009; Osawa et al., 2009). On the other hand, E. coli can grow in a
simple mineral salt medium, and the easy and reproducible meth-
ods of genetic manipulation have been established in E. coli (Zhou
et al., 2006). Very recently, there have been a few interesting reports
on the direct productions of PLA and its copolymers from glucose
using recombinant E. coli strains equipped with several genes for
the polymerization (Jung and Lee, 2011; Jung et al., 2010; Yang et al.,
2010). Conventionally, PLA is industrially produced by two steps:
lactic acid fermentation for lactic acid production and followed
by chemical process for PLA synthesis. Therefore, the constructed
E. coli can develop a novel strategy for PLA production by one-step
process. Although recombinant yeasts and E. coli as described above
could not utilize lignocellulose-derived sugars efficiently, further
researches should have potential and application for lactic acid
production from lignocellulosic materials.
In conclusion, we described many studies and the findings of
lactic acid fermentation by LAB from lignocellulosic materials and
also compared the features of LAB with other microorganisms.
Nevertheless, industrial lactic acid production from lignocellulosic
materials has not been sufficiently profitable. One of the reasons
for this is the high cost of hydrolytic enzymes for the sacchari-
fication of cellulose and hemicellulose. To address this problem,
attempts to isolate LAB that can ferment cellulose or xylan directly
to lactic acid, and the development of genetically modified LAB
that have hydrolytic enzymes with high activity should be con-
 M.A. Abdel-Rahman et al. / Journal of Biotechnology 156 (2011) 286–301
tinued. Designed biomass studies using those LAB would facilitate
the industrial production of lactic acid.
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