R

Lb

Ma

Gb

c

d

J

a

ARRAA

KLLLMD

C

B

(

0d

Journal of Biotechnology 156 (2011) 286– 301

Contents lists available at ScienceDirect

Journal of Biotechnology

j ourna l ho me pag e: www.elsev ier .com/ locate / jb io tec

eview

actic acid production from lignocellulose-derived sugars using lactic acidacteria: Overview and limits

ohamed Ali Abdel-Rahmana,b, Yukihiro Tashiroc, Kenji Sonomotoa,d,∗

Laboratory of Microbial Technology, Division of Applied Molecular Microbiology and Biomass Chemistry, Department of Bioscience and Biotechnology, Faculty of Agriculture,raduate School, Kyushu University, 6-10-1 Hakozaki, Higashi-ku, Fukuoka 812-8581, JapanBotany and Microbiology Department, Faculty of Science (Boys), Al-Azhar University, PN:11884, Naser City, Cairo, EgyptDepartment of Life Study, Seinan Jo Gakuin University Junior College, 1-3-5 Ibori, Kita-ku, Kokura, Kitakyushu City, Fukuoka 803-0835, JapanLaboratory of Functional Food Design, Department of Functional Metabolic Design, Bio-Architecture Center, Kyushu University, 6-10-1 Hakozaki, Higashi-ku, Fukuoka 812-8581,

apan

r t i c l e i n f o

rticle history:eceived 2 February 2011eceived in revised form 31 May 2011ccepted 17 June 2011vailable online 23 June 2011

eywords:ignocellulose-derived sugar

a b s t r a c t

Lactic acid is an industrially important product with a large and rapidly expanding market due to itsattractive and valuable multi-function properties. The economics of lactic acid production by fermenta-tion is dependent on many factors, of which the cost of the raw materials is very significant. It is veryexpensive when sugars, e.g., glucose, sucrose, starch, etc., are used as the feedstock for lactic acid produc-tion. Therefore, lignocellulosic biomass is a promising feedstock for lactic acid production consideringits great availability, sustainability, and low cost compared to refined sugars. Despite these advantages,the commercial use of lignocellulose for lactic acid production is still problematic. This review describes

actic acid productionactic acid bacteria (LAB)etabolic pathwaysesigned biomass

the “conventional” processes for producing lactic acid from lignocellulosic materials with lactic acid bac-teria. These processes include: pretreatment of the biomass, enzyme hydrolysis to obtain fermentablesugars, fermentation technologies, and separation and purification of lactic acid. In addition, the difficul-ties associated with using this biomass for lactic acid production are especially introduced and severalkey properties that should be targeted for low-cost and advanced fermentation processes are pointedout. We also discuss the metabolism of lignocellulose-derived sugars by lactic acid bacteria.

© 2011 Elsevier B.V. All rights reserved.

ontents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2872. Overview of lactic acid production from lignocellulosic biomass . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 287

2.1. Composition of lignocellulosic biomass . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2872.2. Conventional processes for lactic acid production by LAB from lignocellulosic biomass . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 288

2.2.1. Pretreatment methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2882.2.2. Enzymatic hydrolysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2892.2.3. Fermentation process with LAB . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2892.2.4. 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 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2902.3.2. High-cost enzymes and their feedback inhibition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2902.3.3. Formation of by-products due to the heterofermentation of pentose sugars . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2902.3.4. Carbon catabolite repression caused by the heterogeneity of the hydrolysate-sugar composition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 291

∗ Corresponding author at: Laboratory of Microbial Technology, Division of Applied Moiotechnology, Faculty of Agriculture, Kyushu University, 6-10-1 Hakozaki, Higashi-ku, Fu

E-mail address: sonomoto@agr.kyushu-u.ac.jpK. Sonomoto).

168-1656/$ – see front matter © 2011 Elsevier B.V. All rights reserved.oi:10.1016/j.jbiotec.2011.06.017

lecular Microbiology and Biomass Chemistry, Department of Bioscience andkuoka 812-8581, Japan. Tel.: +81 92 642 3019; fax: +81 92 642 3019.

M.A. Abdel-Rahman et al. / Journal of Biotechnology 156 (2011) 286– 301 287

3. Fermentative lactic acid production by LAB . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2913.1. Improvement of lactic acid production by LAB in the field of microbial technology. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2913.2. Lactic acid production by LAB using lignocellulosic biomass and lignocellulose-derived sugars . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 292

4. Metabolism of lignocellulose-derived sugars by LAB . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2955. Designed biomass study and conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 296

. . . . . .

1

anigetpiautaTotcotpaoaafTpt2ee

bcwHtccb2un(

wrpowaoucd

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

. Introduction

Lactic acid (2-hydroxypropanoic acid, CH3–CH(OH)–COOH) is natural organic acid with a long history of use in the food andon-food industries, including the cosmetic and pharmaceutical

ndustries, and for the production of oxygenated chemicals, plantrowth regulators, and special chemical intermediates (Oshirot al., 2009; Singhvi et al., 2010; Tashiro et al., 2011). Currently,here is an increased demand for lactic acid as a feedstock for theroduction of biopolymer poly-lactic acid (PLA), which is a promis-

ng biodegradable, biocompatible, and environmentally friendlylternative to plastics derived from petrochemicals. PLA has manyses in surgical sutures, orthopedic implants, drug delivery sys-ems, and disposable consumer products (Adnan and Tan, 2007),nd its use would significantly alleviate waste disposal problems.he physical properties of PLA depend on the isomeric compositionf lactic acid. Pure isomers, l- and d-lactic acid, are more valuablehan the racemic dl form because each isomer has its own spe-ific industrial application. l-Lactic acid is used for the synthesisf poly l-lactic acid (PLLA), a semi-crystalline biodegradable andhermostable polymer that has a potentially large market in goodsackaging. PLLA has high tensile strength and low elongation with

high modulus that makes it suitable for medical products used inrthopedic fixation (e.g., pins, rods, ligaments, etc.), cardiovascularpplications (e.g., stents, grafts, etc.), dental applications, intestinalpplications, and sutures (John et al., 2006a). d-Lactic acid is usedor the production of poly d-lactic acid (PDLA) (John et al., 2009).hese pure polymers are relatively heat sensitive, while stereocom-lexes of PLLA and PDLA have a melting point ∼50 ◦C higher thanheir respective pure polymers (Ikeda et al., 1987; Tsuji and Fukui,003) and are more biodegradable (de Jong et al., 2001; Tashirot al., 2011). The ratio of l- and d-lactic acids influences the prop-rties and the degradability of PLA (Kharras et al., 1993).

Lactic acid can be produced either by chemical synthesis ory microbial fermentation. Chemical synthesis from petrochemi-al resources always results in racemic mixture of dl-lactic acid,hich is a major disadvantage of this approach (Hofvendahl andahn-Hägerdal, 2000). Conversely, microbial lactic acid fermenta-

ion offers an advantage in terms of the utilization of renewablearbohydrate biomass, low production temperature, low energyonsumption, and the production of optically high pure lactic acidy selecting an appropriate strain (Ilmen et al., 2007; Pandey et al.,001). Presently, almost all lactic acid produced globally is man-factured by fermentation routes. In particular, there have beenumerous studies of lactic acid production by lactic acid bacteriaLAB) in comparison with other microorganisms.

The demand for lactic acid has increased considerably due to itside range of applications; however, the high cost of the raw mate-

ials, e.g., starch and refined sugars, which accounts for the highestortion of the production cost, represents one of the most seriousbstacles for the fermentative production of lactic acid to competeith chemical synthesis (Datta et al., 1995). Cheap raw materials

re essential for the feasibility of the biotechnological production

f lactic acid because polymer producers and other industrial userssually require large quantities of lactic acid at a relatively lowost. The use of low-cost non-food materials for lactic acid pro-uction appears to be more attractive because they do not have

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 297

any impact on the human food chain. Nowadays, lignocellulosicmaterials from agricultural, agro-industrial, and forestry sourcesrepresent a potentially inexpensive and renewable carbohydratefeedstock for the large-scale fermentation of lactic acid due to theirabundance, low price, high polysaccharide content, and renewa-bility (Duff and Murray, 1996; Parajo et al., 1996; Taniguchi et al.,2005; Wyman, 1999). However, the cellulose and hemicellulose inlignocellulose are not directly available for bioconversion to lac-tic acid because of their intimate association with lignin (Schmidtand Thomsen, 1998) and the lack of hydrolytic enzymes in LAB(Tokuhiro et al., 2008).

There have been numerous investigations on the developmentof biotechnological processes for lactic acid production, with theultimate objective of making the process more effective and eco-nomical. In this review, we focus on the “conventional” processesfor lactic acid fermentation by LAB from lignocellulosic biomassand lignocellulose-derived sugars. Moreover, we describe the lim-itations of lactic acid production using such materials. We alsodescribe fermentative processes and technologies with practicalexamples, the metabolism of biomass-derived sugars, and thepromising prospects of lactic acid fermentation.

2. Overview of lactic acid production from lignocellulosicbiomass

2.1. Composition of lignocellulosic biomass

The global production of plant biomass, of which over 90%is lignocellulose, amounts to ∼200 × 109 tons per year, where∼8–20 × 109 tons of the primary biomass remains potentiallyaccessible (Lin and Tanaka, 2006). Lignocellulosic biomass isorganic material derived from a biological origin, and representsthe most abundant global source of biomass that has been largelyunutilized (Lin and Tanaka, 2006). It is mainly composed of cellu-lose (insoluble fibers of �-1,4-glucan), hemicellulose (noncellulosicpolysaccharides including xylans, mannans, and glucans), andlignin (a complex polyphenolic structure), which form ∼90% of thedry matter, plus lesser amounts of minerals, oils, and other com-ponents (Balat, 2011; Molina-Sabio and Rodríguez-Reinoso, 2004;Yang et al., 2009). This biomass includes forest and crop residues(Chen and Lee, 1997; Melzoch et al., 1997), municipal solid waste(John et al., 2007), waste paper (McCaskey et al., 1994), and wood(Linko et al., 1984). The structural and chemical composition of lig-nocellulosic material has varying amounts of these componentsbecause of genetic and environmental influences and their inter-actions (Demirbas, 2005). The proportion of biomass constituentsvaries between species, and there are distinct differences betweenhardwoods and softwoods. The total content of cellulose and hemi-cellulose is higher in hardwoods (78.8%) than in softwoods (70.3%),but the total content of lignin is higher in softwoods (29.2%) than inhardwoods (21.7%) (Balat, 2009). As shown in Table 1, the cellulose,hemicellulose, and lignin content depends on the type of lignocellu-losic biomass, which indicates that an appropriate material should

be selected for the corresponding fermentation.

Cellulose, the major component of plant biomass (30–60% oftotal feedstock dry matter), is a homopolysaccharide composedof �-d-glucopyranose units, linked by �-(1 → 4)-glycosidic bonds.

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

Table 1The contents of cellulose, hemicellulose, and lignin in various types of lignocellulosicbiomass (% dry weight).a

Lignocellulosic materials Cellulose (%) Hemicellulose (%) Lignin (%)

Algae (green) 20–40 20–50 NAb

Aspen hardwood 51 29 16Birch Hardwood 40 39 21Chemical pulps 60–80 20–30 2–10Coastal Bermuda grass 25 35.7 6.4Corn cobs 45 35 15Cornstalks 39–47 26–31 3–5Cotton seed hairs 80–95 5–20 0Cotton, flax, etc. 80–95 5–20 NAb

Grasses 25–40 25–50 10–30Hardwood 45 ± 2 30 ± 5 20 ± 4Hardwood barks 22–40 20–38 30–55Hardwood stems 40–55 24–40 18–25Leaves 15–20 80–85 0Newspaper 40–55 25–40 18–30Nut shells 25–30 25–30 30–40Paper 85–99 0 0–15Pine softwood 44 26 29Primary wastewater

solids8–15 NAb 24–29

Softwood 42 ± 2 27 ± 2 28 ± 3Softwood barks 18–38 15–33 30–60Softwood stems 45–50 25–35 25–35Solid cattle manure 1.6–4.7 1.4–3.3 2.7–5.7Sorted refuse 60 20 20Spruce softwood 43 26 29Swine waste 6.0 28 NAb

Switch grass 45 31.4 12.0Waste papers from

chemical pulps60–70 10–20 5–10

Wheat straw 37–41 27–32 13–15Willow Hardwood 37 23 21

–, Not determined.a

(

Ti(hn(wrratpglpmtem(

2f

tssda

Lignocellulosic biomass

Chemical/physical Pretreatment

CelluloseHydrolyzed Hemicellulose

Enzymatic hydrolysis

Lignin

Mainly Glucose

Mainly Pentoses

Fermentation

Lactic acid

Separation

Source: Balat (2011), Olsson and Hahn-Hägerdal (1996) and Sun and Cheng

2002).b NA – not available.

he orientation of the linkages and additional hydrogen bond-ng make the polymer rigid and difficult to break. Hemicellulose20–40% of total feedstock dry matter) is a short, highly branchedeterogeneous polymer consisting of pentose (xylose and arabi-ose), hexose (galactose, glucose, and mannose), and acid sugarsSaha, 2000). Mannose is the dominant hemicellulose sugar in soft-oods, while xylose is dominant in hardwoods and agricultural

esidues (Taherzadeh and Karimi, 2008). Hemicellulose is moreeadily hydrolyzed compared to cellulose because of its branchednd amorphous nature. Lignin (15–25% of total feedstock dry mat-er) is an aromatic polymer synthesized from phenylpropanoidrecursors. The phenylpropane units of lignin (primarily syringyl,uaiacyl, and phydroxy phenol) are bonded together by a set ofinkages to form a very complex matrix (Demirbas, 2008). This com-lex matrix consists of a variety of functional groups, e.g., hydroxyl,ethoxyl, and carbonyl groups, which impart a high polarity to

he lignin macromolecule (Feldman et al., 1991). Lignin is consid-red to be difficult to use as a fermentation substrate because itakes the biomass resistant to chemical and biological degradation

Taherzadeh and Karimi, 2008).

.2. Conventional processes for lactic acid production by LABrom lignocellulosic biomass

Despite the advantages in its sustainability and availability,he commercial use of lignocellulose in lactic acid production is

till problematic due to its complexity. The biochemical conver-ion of lignocellulosic biomass requires several processing stepsesigned to convert structural carbohydrates to monomeric sug-rs, e.g., glucose, xylose, arabinose, and mannose. These sugars

Fig. 1. A general flow chart of the “conventional” process for lactic acid productionfrom lignocellulosic biomass materials.

can be fermented to lactic acid by wild-type and breeding strains,with varying degrees of effectiveness. Once the technologies areestablished and commercialized, a wide range of valuable productscould be produced from lignocellulosic biomass. The conventionalprocesses for producing lactic acid from lignocellulosic biomassinclude 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 ofhydrolytic enzymes.

(3) Fermentation—metabolizing the sugars to lactic acid, generallyby LAB.

(4) Separation and purification of lactic acid—purification of lacticacid to meet the standards of commercial applications.

2.2.1. Pretreatment methodsThe enzymatic susceptibility of native lignocellulose is difficult

and slow due to the association of cellulose and hemicellulosewith lignin (Schmidt and Thomsen, 1998). The main goals ofpretreatment are to remove lignin, separate cellulose and hemicel-

lulose, increase the accessible surface area, partially depolymerizecellulose, and increase the porosity of the materials to aid inthe subsequent access of the hydrolytic enzymes (Chandel et al.,2007; Hendriks and Zeeman, 2009; Kumar et al., 2009; Sun and

l of Bi

CTdP(cwto

op2i2et1t(mc1etoma(h

lrai2tmcpthofmbsmecaC

2

mn(eotTchmh

(

(

M.A. Abdel-Rahman et al. / Journa

heng, 2002; Taherzadeh and Karimi, 2007; Zhang et al., 2009).he hemicellulose should be removed or altered without degra-ation for a high ultimate yield of sugars (Mosier et al., 2005).retreatment includes physical (milling and grinding), chemicalalkali, dilute acid, oxidizing agents, and organic solvents), physico-hemical (steam explosion/autohydrolysis, hydrothermolysis, andet oxidation), and biological methods. Some methods disrupt

he lignin–carbohydrate complex, and other disrupts the highlyrdered crystalline cellulose structure (Sun et al., 1995).

Different pretreatment methods have been extensively devel-ped, including ammonia fiber explosion and ammonia recycleercolation (Jorgensen et al., 2007), lime (Kaar and Holtzaple,000), organosolv (Pan et al., 2006), liquid hot water (Antal, 1996),

onic liquid (Dadi et al., 2006), alkaline pretreatment (Lau et al.,008), dilute acid and steam explosion (Laser et al., 2002; Mosiert al., 2005; Parisi, 1989; Yang and Wyman, 2008), and enzymaticreatment (Anderson et al., 2005; Converse, 1993; Hayn et al.,993; Ladisch et al., 1983). Among these methods, dilute acid pre-reatment is still the method of choice in several model processesWyman et al., 2005). The initial pretreatment reaction involves a

ild acid-catalyzing hydrolysis of the glycosidic bonds of hemi-ellulose and the ether linkages in lignin (Fengel and Wegener,989), in which the organic acids, formed by the cleavage of labilester groups, catalyze the hydrolysis of hemicellulose. Fractiona-ion is achieved by the enlargement of the inner surface. The effectsf different pretreatment methods upon different lignocellulosicaterials, e.g., corn stover (Chen et al., 2009), wheat straw (Sun

nd Chen, 2008), switchgrass (Esteghlalian et al., 1997), rice strawZhang and Cai, 2008), and sugarcane bagasse (Rabelo et al., 2009),ave been investigated.

The pretreatment process is a very critical stage in lignocellu-ose bioconversion. If pretreatment is not sufficiently efficient, theesultant residue is not easily saccharified by hydrolytic enzymesnd, if it is too severe, toxic compounds can be produced thatnhibit microbial metabolism and growth (Kodali and Pogaku,006). Therefore, pretreatment has a great potential to influencehe downstream costs by determining fermentation toxicity, enzy-

atic hydrolysis rates, enzyme loading, mixing power, productoncentrations, product purification, waste treatment demands,ower generation, and other process variables. An effective pre-reatment process should meet the following requirements: (1)ighly digestible pretreated solid; (2) no significant degradationf sugars; (3) good recovery of high sugar concentrations; (4) sugarormation by subsequent enzymatic hydrolysis; (5) effective at low

oisture contents; (6) form minimal or no microbial inhibitoryy-products; (7) require minimal energy input; (8) high degree ofimplicity; (9) not require biomass size reduction; (10) low costaterials for the construction of pretreatment reactors and to be

asily managed at large volumes; (11) produce less residues; (12)onsume few and cheap chemicals; and (13) have environmentallycceptable features (Galbe and Zacchi, 2007; Lynd, 1996; Sun andheng, 2002; Wu et al., 2011; Yang and Wyman, 2008).

.2.2. Enzymatic hydrolysisEnzymatic hydrolysis is the most promising means to yield fer-

entable sugars from pretreated lignocellulosic biomass, and isecessary to allow LAB to utilize polysaccharides as a carbon sourceHinman et al., 1992; Lin and Tanaka, 2006; Lynd et al., 1996; Ogiert al., 1999; Taniguchi et al., 2005; Yu and Zhang, 2004). The goalf enzymatic hydrolysis is to depolymerize the polysaccharides inhe water-insoluble solid fraction that remains after pretreatment.here are 2 general categories of enzymes necessary to convert

ellulose and hemicellulose into soluble sugars: cellulases andemicellulases, respectively. To maximize enzymatic hydrolysis,ixtures of these enzymes are needed to increase hemicellulose

ydrolysis and thus increase the access of cellulase, leading to a

otechnology 156 (2011) 286– 301 289

decreased hydrolysis time and process cost (Öhgren et al., 2007; Tuand Saddler, 2010; Zhang et al., 2010a).

The rate of the enzymatic hydrolysis of cellulose is greatlyaffected by its degree of polymerization (Chang and Holtzapple,2000; Cohen et al., 2005; Kumar et al., 2008). Efficient degradationand saccharification of cellulose require a synergistic reaction ofthe following 3 classes of cellulolytic enzymes:

a) Endo-�-1,4-glucanases (EG; EC 3.2.1.3): randomly hydrolyzeaccessible intramolecular �-1,4-glucosidic bonds of cellulosechains and insert a water molecule in the �-(1,4) bond, creatinga 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, releasingsoluble cellobiose or glucose.

(c) �-Glucosidases (�-G; EC 3.2.1.21) (cellobiases): complete thehydrolysis by cleaving cellobiose into 2 glucose molecules (Lyndet al., 2002) and thus relieve the system from end-productinhibition (Fujii et al., 1995). They are also active on cello-oligosaccharides (Kumar et al., 2008).

Individual cellulases have very limited hydrolytic activity, whilea mixture of cellulases can exhibit a synergistic effect (Nidetzkyet al., 1994; Zhang et al., 2007). Extensive research has been per-formed to improve the hydrolytic efficiency of such enzymes (Bakeret al., 1998; Mais et al., 2002; Selig et al., 2008). In addition to these3 major groups of cellulases, accessory or “helper” enzymes thatattack hemicellulose (Berlin et al., 2005) and lignin (Palonen andViikari, 2004) may also play a role in hydrolysis by clearing theaccess of the main enzymes to cellulose.

Unlike cellulose, xylans are chemically quite complex, andtheir degradation requires multiple enzymes. Enzymatic hydrolysisof hemicellulose requires endo-1,4-�-xylanase, �-xylosidase, �-glucuronidase, �-l-arabinofuranosidase, and acetylxylan esterase,which act on xylan degradation and saccharification (Carvalheiroet 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 hydrolysisthan for cellulose hydrolysis, the substrate is more easily accessiblebecause xylan does not form tight crystalline structures (Keshwaniand Cheng, 2009).

The hydrolytic efficiency of a multi-enzyme mixture in theprocess of lignocellulose hydrolysis depends on the properties ofthe 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 ofenzymes by using combinations of the 3 enzymes, 2 cellulases, and1 xylanase.

2.2.3. Fermentation process with LABThe 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 reducethe production cost of biomaterials by as much as 25% (Hinmanet al., 1989). Fermentation technologies must be cost competitivewith chemical synthesis to validate the use of biotechnological pro-cesses on an industrial scale (Bustos et al., 2007). The key economicdrivers 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 studieshave investigated lactic acid fermentation by LAB from lignocel-lulosic biomass in the field of microbial technology, as described

2 l of Bi

islhSs(msLes2(

2

bcdlPdtanatH22cptsctl

2a

itaettitcT

2

y(ht(mmlcb

90 M.A. Abdel-Rahman et al. / Journa

n detail in Section 3.2. Biomass materials have been used asubstrates for lactic acid production by LAB, including lignocel-ulose/hemicellulose hydrolysates (Karel et al., 1997), cottonseedulls (Vickroy, 1985), corncob (Guo et al., 2010; Moldes et al., 2006;hen and Xia, 2006; Wang et al., 2010), corn fiber hydrolysates andtalks (Saha and Nakamura, 2003; Vickroy, 1985), apple pomaceGullon et al., 2008), wood hydrolysate (Wee et al., 2004), beet

olasses (Göksungur and Güvenc , 1999; Kotzamanidis et al., 2002),ugar cane press mud and bagasse (Xavier and Lonsane, 1994;aopaiboon et al., 2010), cassava bagasse (John et al., 2006a,b; Rojant al., 2005), cellulose (Venkatesh, 1997; Singhvi et al., 2010), paperludge (Marques et al., 2008), carrot processing waste (Pandey et al.,001), molasses spent wash (Sharma et al., 2003), and wheat branJohn et al., 2006c; Naveena et al., 2005a,b).

.2.4. Separation and purification of lactic acidIn the traditional chemical separation process, the fermentation

roth is first neutralized by calcium carbonate. The calcium lactate-ontaining broth is then filtered to remove cells, carbon treated,ecolored, evaporated, and acidified with sulfuric acid to produce

actic acid and insoluble calcium sulfate (Datta and Henry, 2006).ure lactic acid is further obtained by hydrolysis, esterification, andistillation. The disadvantages of this process include the produc-ion of a large amount of calcium sulfate (gypsum) as a by-productnd high sulfuric acid consumption (Qin et al., 2010). Other alter-ative lactic acid separation technologies such as adsorption (Chennd Ju, 1998), reactive distillation (Kumar et al., 2006), ultrafiltra-ion and electrodialysis (Choi et al., 2002; Datta and Henry, 2006;ábová et al., 2004; Kim and Moon, 2001; Madzingaidzo et al.,002), and nanofiltration (Gonzalez et al., 2008; Li and Shahbazi,006) have also been studied as lactic acid separation and purifi-ation processes that do not yield salt waste. These separationrocesses are more cost and energy efficient when compared withraditional chemical separation processes. In addition, they haveeveral advantages including the lack of energy-intensive phasehanges or potentially expensive solvents or adsorbents as well ashe potential for the simultaneous separation and concentration ofactic acid (Li et al., 2008).

.3. Difficulties in using lignocellulosic biomass for efficient lacticcid production by LAB

The effective utilization of lignocellulosic biomass has somenherent limitations due to its seasonal availability, scattered dis-ributions, and the high costs of storage and transportation (Linnd Tanaka, 2006; Polman, 1994). In addition, the main problemsncountered in the efficient conversion of lignocellulosic biomasso lactic acid are: (a) the resistant nature of biomass and pre-reatment problems; (b) high cost enzymes and their feedbacknhibition; (c) formation of by-products due to the heterofermen-ation of pentose sugars; and (d) carbon catabolite repressionaused by the heterogeneity of hydrolysate-sugar composition.hese obstacles are briefly discussed as follows:

.3.1. Resistant nature of biomass and pretreatment problemsCrystalline nonreactivity and, in particular, resistance to hydrol-

sis are the major problems for efficient lignocellulose utilizationKumar et al., 2008). Although various pretreatment proceduresave been evaluated, its utilization is a major drawback and affectshe total economy of the bioconversion of lignocellulosic biomassZhang et al., 2009). Pretreatment is an expensive step and has a

ajor influence on the cost of the enzymatic hydrolysis and fer-

entation processes (Lynd et al., 1996; Wooley et al., 1999). Also,

ignin limits the rate of cellulose hydrolysis by acting as a physi-al barrier that prevents the digestible parts of the substrate fromeing hydrolyzed (Chang and Holtzapple, 2000; Esteghlalian et al.,

otechnology 156 (2011) 286– 301

2001). Different strategies have been examined to overcome thenonproductive adsorption of lignin to cellulase by alkali extractionand the addition of proteins or other additives, e.g., polyethyleneglycol 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 thereleased compounds depends not only on the type of lignocellu-losic material and the chemistry but also on the characteristics ofthe pretreatment process. These inhibitory compounds interferewith the hydrolysis of cellulosic substrates by cellulase (Mes-Hartree et al., 1987). In addition, many potentially inhibitorycompounds released by pretreatment processes have been iden-tified for the microorganisms used for fermentation (Mussattoand Roberto, 2004; Palmqvist and Hahn-Hägerdal, 2000). Althoughdetoxification methods such as bioabatement (Lopez et al., 2004;Nichols et al., 2005) and overliming (Nilvebrant et al., 2003) havebeen proposed, the efficiency of fermentation is still in need ofimprovement. The isolation of superior LAB strains or geneticallyengineered strains that are resistant to inhibitors, and advancesand improvements in the pretreatment of lignocellulose are stillneeded to reduce the overall cost. Recently, wild-type Lactobacillusbrevis S3F4 was shown to have strong resistance to fermentationinhibitors such as ferulic acid and furfural (Guo et al., 2010). Biolog-ical delignification with white rot fungi, which selectively degradelignin and leave cellulosic materials, also has potential advantagessuch as low-capital cost, low-energy input, no chemical require-ments, mild environmental conditions, and high yields withoutgenerating polluting by-products (Chaudhary et al., 1994; Kuhadand Johri, 1992; Kumar et al., 2009). However, drawbacks of thisprocess 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 inhibitionThe 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 commercialapplication of lignocellulose hydrolysis as a lignocellulosic-lactateindustry (Himmel et al., 1999; Wooley et al., 1999). During cellu-lose saccharification, the sugar end products of hydrolysis do notaccumulate quickly because the saccharified glucose and cellobioseinhibit 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 cellulasesystem (Shen and Xia, 2004), removing the released sugars dur-ing hydrolysis by ultrafiltration or simultaneous saccharificationand fermentation (SSF) (Rezaei et al., 2008), optimizing cellulaseenzyme conditions (i.e., temperature, pH, and enzyme loadingamounts) (Sun and Cheng, 2002; Ou et al., 2009), or supplying �-Gduring hydrolysis to avoid cellobiose accumulation (Caminal et al.,1985; Moldes et al., 2001; Ramos and Saddler, 1994). Studies toremove such forms of inhibition are still in progress.

2.3.3. Formation of by-products due to the heterofermentation ofpentose sugars

Lignocellulosic hydrolysates contain not only hexoses but alsopentoses. Hexoses can easily be fermented by LAB, while pen-tose sugars cannot be fermented by most LAB (Hofvendahl andHahn-Hägerdal, 2000; Tanaka et al., 2002). In general, a few LABmetabolize 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 acidalso results in an increase of the lactic acid purification cost (Garde

l of Bi

edoty(tpthen

2o

a(decgbTstr(ptdhdLmcffe

3

3m

sppttt

cc(cbtst2cce

M.A. Abdel-Rahman et al. / Journa

t al., 2002; Patel et al., 2006); therefore, this approach is not con-ucive for the industrial fermentation of pentoses to lactic acid. Tovercome this obstacle, we previously isolated a LAB strain, Lac-ococcus lactis IO-l, which could utilize xylose with a high lactateield and low acetate production (Tanaka et al., 2002). Okano et al.2009a,b) engineered the LAB Lb. plantarum strain to produce lac-ic acid from xylose and arabinose via the pentose phosphate (PP)athway, leading to homolactate production. Recently, we reportedhat a novel LAB, Enterococcus mundtii QU 25, consumed xyloseomofermenatively without acetate production (Abdel-Rahmant al., 2010a, 2011b); therefore, the purification cost will be sig-ificantly decreased with this strain.

.3.4. Carbon catabolite repression caused by the heterogeneityf the hydrolysate-sugar composition

One of the major obstacles in using lignocellulosic biomass as feedstock is the inherent heterogeneity of its sugar compositionKim et al., 2010a). To achieve maximum product yield and pro-uctivity, the complete utilization of these sugars is essential (Kimt al., 2010b; Saha, 2003). In many LAB, fermentation of mixedarbohydrates is achieved sequentially, whereby the utilization oflucose represses the consumption of alternative sugars due to car-on catabolite repression (Saier, 1998; Stulke and Hillen, 1999;itgemeyer and Hillen, 2002). This sequential utilization of mixedugars makes the fermentation process complex and often reduceshe yield and productivity (Bothast et al., 1999). Carbon cataboliteepression by LAB has been reported in many strains, e.g., Lb. caseiGosalbes et al., 1999; Veyrat et al., 1994; Viana et al., 2000), Lb.entosus (Chaillou et al., 1999, 2001; Mahr et al., 2000), Lb. plan-arum (Marasco et al., 1998), Lb. sakei (Zuniga et al., 1998), and Lb.elbrueckii (Morel et al., 1999; Schick et al., 1999). A few LAB strainsave been reported to simultaneously consume lignocellulose-erived sugars, e.g., Lb. brevis (Guo et al., 2010; Kim et al., 2009),b. plantrum (Guo et al., 2010), and our newly isolated strain E.undtii QU 25 (Abdel-Rahman et al., 2010a,b, 2011a). Mixed LAB

ultures have also been used to maximize the yield and productivityrom mixed sugars (Cui et al., 2011; Taniguchi et al., 2004). There-ore, it is essential to isolate LAB strains or to establish geneticallyngineered strains for efficient lignocellulose utilization.

. Fermentative lactic acid production by LAB

.1. Improvement of lactic acid production by LAB in the field oficrobial technology

It has generally been observed that pH, nutrient concentration,ubstrate concentration, end products concentration, and tem-erature significantly affect the growth of LAB and lactic acidroduction. These factors may decrease cell density and the lac-ic acid titer, yield, and productivity in some cases. Researchers inhe field of microbial technology have conducted numerous studieso establish an efficient method of lactic acid production by LAB.

In lactic acid fermentation, low pH has an inhibitory effect onellular metabolism and lactic acid production. The majority of LABannot grow below pH 4, although the pKa of lactic acid is 3.78Adachi et al., 1998); therefore, neutralizing agents such as cal-ium carbonate, sodium hydroxide, or ammonium hydroxide muste added to keep the pH at a constant value in order to reducehe inhibitory effects of low pH. pH-controlled batch fermentationignificantly improves lactic acid production, yield, and produc-ivity by different LAB strains, e.g., Lb. delbrueckii (Tashiro et al.,

011), E. mundtii QU 25 (Abdel-Rahman et al., 2011a,b), and E. fae-ium (Shibata et al., 2007). Batch fermentation is a simple closedulture system that contains an initial and limited amount of nutri-nt, and nothing is added during fermentation except possibly acid

otechnology 156 (2011) 286– 301 291

or alkali for pH control. The low levels of nutrient limit the cellconcentration, final lactic acid concentration, and productivity. Itwas reported that the addition of nutrients to a culture broth of E.mundtii QU 25 during batch fermentation increased the cell massand 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 productionhas 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/Ld-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; Oshiroet al., 2009). To overcome or reduce substrate inhibition, fed-batchcultures were a better fermentation system than batch and contin-uous cultures because they allow for an increased maximum viablecell concentration and prolonged culture lifetime, which result inproduct accumulation to a higher concentration. Bai et al. (2004)developed a process for the production of ammonium lactate withLb. lactis in pH-controlled fed-batch fermentation with 161.2 g/Lof lactic acid. Ding and Tan (2006) developed a high lactic acidconcentration 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 exponentialfeed rate fed-batch fermentations. They generated up to 210 g/L oflactic acid and a 97% yield with an exponential rate of feeding glu-cose solution and yeast extract (Ding and Tan, 2006). However, inall fed-batch technologies, the substrate concentration in the fer-mentation broth is unstable, thereby generating more stress on theproducing strain. Recently, a method was developed to control theconcentration of the substrate through the automatic adjustmentof pH. Using this method, 96.3 g/L and 170 g/L of lactic acid wereobtained with Lb. lactis-11 (Zhang et al., 2010b) and Lb. rhamnosusLA-04-1 (Li et al., 2010), respectively. Chang et al. (2011) suggestedmulti-stage continuous high cell density culture as a new produc-tion platform for obtaining high lactic acid titers (212.9 g/L) andproductivity (10.6 g L−1 h−1) with Lb. rhamnosus. In addition to fed-batch fermentation, continuous and semi-continuous fermentationprocesses have been used for lactic acid production by reducingsubstrate inhibition (Amrane and Prigent, 1996; Nolasco-Hipolitoet al., 2002; Tashiro et al., 2011). The choice of the most suitable fer-mentation process will depend upon the kinetic properties of theLAB species used, the type of substrates, and the economic aspectsof the process.

High productivity was achieved with a high LAB cell densitywithout reducing the yield (Ohleyer et al., 1985). Many reportsshowed that high cell density by cell recycling through filtrationdrastically 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, alongwith repeated batch and continuous processes, generated a highcell concentration and productivity in these processes (Kwon et al.,2001; Oh et al., 2003). The immobilization of cells has been oneof 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 Güvenc , 1999; Senthuranet 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, itmust be selectively removed from the fermentation broth. Manyattempts have been directed to develop processes that removelactic acid from the fermentation broth, e.g., extraction from the

2 l of Bi

fLt2Jbacrpdbtlyppchb(

rdp34a

3a

samoeadl(ppoot(ehaL2

LrmsgJttne(i

92 M.A. Abdel-Rahman et al. / Journa

ermentation broth (Hano et al., 1993; Honda et al., 1995; Iyer andee, 1999a,b; Yabannavar and Wang, 1991; Ye et al., 1996), elec-rodialysis (Boyaval et al., 1987; Hongo et al., 1986; Kim and Moon,001; Min-Tian et al., 2005; Nomura et al., 1998; van Nispen andonker, 1991; Vonktaveesuk et al., 1994), and nanofiltration mem-ranes and ion exchange resins (Jeantet et al., 1996; Monteagudond Aldavero, 1999; Srivastava et al., 1992; Vaccari et al., 1993). Theontinuous removal of lactic acid with extraction or electrodialysisesults in even higher lactic acid concentrations and yields com-ared to conventional batch fermentation processes. Li et al. (2004)eveloped a bioreactor combining conventional electrodialysis andipolar membrane electrodialysis for product removal and pH con-rol in lactic acid fermentation. Min-Tian et al. (2005) achieved highactic acid productivity and yields with a continuous electrodial-sis fermentation system. Even though these methods lower theurification cost, the price of the membranes and decreases in theermeate flow rate make the process less cost efficient and are stillonsiderable drawbacks. Other methods, e.g., two phase systems,ave been developed; however, the extracting material must beiocompatible and not harm the organism in order to be efficientPlanes, 1998).

The influence of temperature on lactic acid fermentation iselated to the growth kinetic parameters of LAB, lactic acid pro-uction, and substrate consumption. Among LAB, most lactic acidroductivity studies have been conducted at temperatures of0–43 ◦C. We recently isolated a new LAB strain, Lb. delbrueckii QU1, that exhibits a high thermotolerance and produces d-lactic acidt temperatures ≥50 ◦C (Tashiro et al., 2011).

.2. Lactic acid production by LAB using lignocellulosic biomassnd lignocellulose-derived sugars

Separate hydrolysis and fermentation (SHF) is a process witheparate enzymatic hydrolysis and fermentation steps. The maindvantage of SHF is the ability to carry out each step under opti-al conditions for each process. However, the main disadvantage

f this method is the feedback inhibition of saccharified sugars,.g., glucose, xylose, cellobiose, and other oligosaccharides, on thectivity of hydrolytic enzyme during the hydrolysis process, whichemands lower loadings of the lignocellulosic biomass and higher

oadings of the hydrolytic enzymes to achieve reasonable yieldsJeffries and Jin, 2000; Philippidis, 1996). In addition, this 2-steprocess increases the total processing time. To overcome theseroblems, SSF for lactic acid production by LAB has been devel-ped as described in detail below. In comparison with SHF, SSFffers many advantages, including: (1) reduced reactor volume dueo the usage of only a single reactor; (2) rapid processing time;3) reduced feedback inhibition; (4) increased productivity; (5)nhanced rate of hydrolysis; (6) lower enzyme loading; and (7)igher lactic acid yields (Ehrman and Himmel, 1994; Hofvendahlnd Hahn-Hägerdal, 2000; Iyer and Lee, 1999a,b; John et al., 2006c;inko and Javanainen, 1996; Moritz and Duff, 1996; Sun and Cheng,002; Tsai and Moon, 1998; Zheng et al., 1998).

SSF technology is a good strategy for lactic acid production byAB from renewable bioresources such as lignocellulosic mate-ials. In SSF, cellulases and xylanases convert the lignocellulosicaterials to fermentable sugars. These enzymes are notoriously

usceptible to feedback inhibition by the saccharified sugars, e.g.,lucose, xylose, cellobiose, and other oligosaccharides (Jeffries andin, 2000). As described above, one of the advantages of SSF is thathe immediate consumption of sugars by microorganism maintainshe sugar concentration at a low level in the bioreactor, thereby sig-

ificantly reducing feedback inhibition (Balat et al., 2008; Mosiert al., 2005). In SSF, hydrolysis is usually the rate-limiting processPhilippidis and Smith, 1995). SSF with cellulose has been stud-ed with Lb. delbrueckii (Abe and Takagi, 1991) and Lb. rhamnosus

otechnology 156 (2011) 286– 301

(Parajo et al., 1997; Schmidt and Padukone, 1997). Other studieshave reported lactic acid production by SSF from lignocellulosicbiomasses such as corncob, waste wood, wheat straw, and alfalfafiber (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; Romaniet 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., thesaccharification 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 andfermentation (Krishna et al., 2001; Huang et al., 2005), and the inhi-bition of enzyme function by lactic acid. In general, the optimalconditions for enzymatic hydrolysis and lactic acid fermentationare 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 temperatureclose to the optimal hydrolysis temperature, as have succeededin high lactic acid production with SSF technology by thermotol-erant Bacillus coagulans (Ou et al., 2009, 2011). In addition, Iyerand Lee (1999a) studied the effect of lactic acid on the enzy-matic hydrolysis of cellulose in SSF. They found that the enzymaticdigestibility 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 lacticacid, they observed a 50% inhibition of the digestibility. However,the inhibition of enzymatic hydrolysis by lactic acid is much lowerthan 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 lignocellulosicbiomass as well as cellulose, which yields pentose sugars suchas xylose and arabinose by saccharification. The majority of LABstrains, 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 nothemicellulose-derived sugars. Others are capable of utilizing pen-tose sugars for lactic acid production, including Lb. pentosus ATCC8041 (Bustos et al., 2005; Zhu et al., 2007), Lb. bifermentans DSM20003 (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-Rahmanet al., 2010a, 2011b). Recently, Okano et al. (2009a,b) succeededin replacing the PK pathway with the PP pathway in Lb. plan-tarum �ldhL1 in order to obtain a higher yield and production ofd-lactic acid from xylose and arabinose with very low amounts ofby-products. Among the LAB reported so far, only the wild-type E.mundtii QU 25 (Abdel-Rahman et al., 2011a,b) and the geneticallymodified Lb. plantarum �ldhL1 (Okano et al., 2009a,b) can performhomo-lactate fermentation of pentose sugars, which is expected togenerate 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 haveexamined lactic acid production from xylooligosaccharides and cel-looligosaccharides. Leu. lactis SHO-47 and SHO-54 were reported toassimilate xylooligosaccharides from disaccharides to hexasaccha-rides to produce d-lactic acid (Ohara et al., 2006). Recently, lacticacid 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 ofcellotriose, 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-phosphate3 ate kid ) 6-phi d dash

it

t

-epimerase; (8) xylose isomerase; (9) xylulokinase; (10) phosphoketolase; (11) acetrogenase; (15) lactate dehydrogenase; (16) transketolase; (17) transaldolase; (18

somerase. Solid lines indicate the homofermentative pathway. Thick-solid lines an

fied Lb. plantarum for cellotriose and cellopentaose fermentationo produce lactic acid.

As mentioned above, lignocellulosic biomass yields severalypes of sugars by hydrolysis, e.g., glucose, cellooligosaccharides,

nase; (12) phosphotransacetylase; (13) aldehyde dehydrogenase; (14) alcohol dehy-osphofructokinase; (19) fructose-bisphosphate aldolase; and (20) triosephosphateed lines indicate PP/glycolytic pathway and PK pathway, respectively.

xylose, and xylooligosaccharides; therefore, the mixed sugars inlignocellulose hydrolysates need to be utilized simultaneously foreffective fermentation. Lb. buchneri NRRL B-30929 simultaneouslyand completely ferments lignocellulosic hydrolysates (glucose

294M

.A.

Abdel-R

ahman

et al.

/ Journal

of Biotechnology

156 (2011) 286– 301Table 2Lactic acid production from lignocellulosic biomass materials and lignocellulose-derived sugars by lactic acid bacteria.

Microorganism Substrate Ferment. process CLAa (g/L) YLA

b (g/g) PLAc (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., 2004Lb. bifermentans DSM 20003 Wheat bran hydrolysate Batch with cell

immobilization62.8 0.83 1.17 Givry et al. (2008)

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)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., 2009Lb. 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 withcell-recycle

27.0 0.9 6.7 Wee and Ryu (2009)

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(Xylooligosaccharides)

Batch 2.3 – – Ohara et al. (2006)

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– 301 295

ion fro

a(ct(noaiAt0brm(Rscm2bwi

hustnpdssmst

Fig. 3. A flow chart of the approaches used for useful substance product

nd xylose) with the production of lactate, acetate, and ethanolLiu et al., 2009). Lc. lactis IO-1 has been used to convert glu-ose, xylose, and arabinose in sugarcane bagasse hydrolysateso a mixture of lactic acid, acetic acid, formic acid, and ethanolLaopaiboon et al., 2010). Marques et al. (2008) used Lb. rham-osus ATCC 7469 to produce lactic acid from short fiber cellulosef paper sludge by SSF without any pretreatment, and obtained

lactic acid yield of 0.97 g/g carbohydrates and a productiv-ty of 2.9 g L−1 h−1 (Marques et al., 2008). SSF of Lb. rhamnosusTCC 9595 with kraft pulp mill biosludge also produced lac-

ic acid with a yield of 0.38 g/g biosludge and a productivity of.87 g L−1 h−1 (Romani et al., 2008). Several authors have reportediotechnological lactic acid production from lignocellulosic mate-ials, agricultural waste, and forestry, industrial, or municipal solidaterials, e.g., unpolished rice (Lu et al., 2009), defatted rice bran

Tanaka et al., 2006), and waste cardboard (Yanez et al., 2005).ecently, in order to increase the conversion efficiency of sub-trates, co-cultures of LAB (e.g., E. casseliflavus and Lb. casei or Lb.asei and Lc. lactis) have been reported from lignocellulose-derivedixed sugars (Cui et al., 2011; Nancib et al., 2009; Taniguchi et al.,

004). Lactic acid fermentation from various types of lignocellulosiciomass materials and lignocellulose-derived sugars by LAB strainsere achieved with different fermentation modes, as summarized

n Table 2.As a result of these kinds of fermentation, cellulose- and

emicellulose-derived sugars from lignocellulosic biomass can betilized with higher efficiency and productivity; however mixedugar cultures have not been used on an industrial scale because ofheir many limitations. In mixed sugar cultures, the strains used doot always have similar optimum culture conditions for pH, tem-erature, nutrients, oxygen demand, etc.; therefore, it is not easy toefine the optimum condition or to maintain stable conditions foruch cultures during fermentation, and corresponding studies are

carce. The discovery of LAB that have the capability to homofer-entatively utilize a wide range of sugars, including C5 and C6

ugars, and can resist the inhibitory compounds generated duringhe pretreatment process is still a major challenge in fermenta-

m renewable resources in a recent study and a designed biomass study.

tion technology for the production of lactic acid from lignocellulosicbiomass.

4. Metabolism of lignocellulose-derived sugars by LAB

LAB can be classified into 2 groups on the basis of the end productof their fermentation: homofermentative and heterofermentative.Homofermentative LAB virtually produce only lactic acid, whereasother products are generated by heterofermentative LAB along withlactic 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, theyare consumed by the Streptococcus, Lactococcus, Enterococcus, andPediococcus genera and some Lactobacillus species to produce lacticacid homofermentatively (Naveena, 2004), while additional prod-ucts, e.g., carbon dioxide, ethanol, and acetic acid, are produced byheterofermentative LAB, the Leuconostoc genera, and certain Lacto-bacillus species (Carr et al., 2002; Cowan and Steel, 1965; Schillingerand 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 thetheoretical yield of lactic acid to glucose is 1.0 g/g or 2.0 mol/mol.On the other hand, heterofermentative LAB possess the pentosemonophosphate pathway, in which glucose 6-phosphate (6 car-bons) is initially converted to ribulose 5-phosphate (5 carbons) andcarbon dioxide (1 carbon) catalyzed by several enzymes (Reddyet al., 2008). The resulting ribulose 5-phosphate is cleaved to 1 molof glyceraldehyde 3-phosphate (GAP) and acetyl phosphate (acetyl-P). GAP is further metabolized to lactic acid (3 carbons), whilethe acetyl-P is reduced to ethanol (2 carbons) via acetyl-CoA andacetaldehyde intermediates (Zaunmuller et al., 2006) and/or con-verted to acetate via acetate kinase. Therefore, the theoretical yieldof 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 fermentationfrom pentose sugars by LAB (Fred et al., 1919; Patel et al., 2006).Some species of LAB can metabolize pentose sugars as a substrate to

2 l of Bi

lSe2Laaow5iaaopLtfo(2w2eTwshiP

sdlctusacccwwo

5

ebiaaufcisfnbdum

96 M.A. Abdel-Rahman et al. / Journa

actic acid, e.g., Lc. lactis IO-1 (Oshiro et al., 2009; Tanaka et al., 2002),treptococcus sp. (Enterococcus sp.) and Lb. thermophilus T1 (Fukuit al., 1957), Lactobacillus strain MONT4 (Barre, 1978), E. mundtii QU5 (Abdel-Rahman et al., 2011b), Lb. pentosus (Bustos et al., 2005),b. brevis (Chaillou et al., 1998), Lb. plantarum (Helanto et al., 2007),nd Leu. lactis (Ohara et al., 2006). Two different pathways, the PKnd PP/glycolic pathways, are proposed as the metabolic pathwaysf pentoses in LAB (Fig. 2) (Tanaka et al., 2002). In the PK pathway,hich is used by the majority of pentose-utilizing LAB, xylulose

-P (5 carbons) is cleaved to GAP and acetyl-P. The resulting GAPs converted to pyruvic acid and then to lactic acid (3 carbons) as

final product, while acetyl-P is metabolized to synthesize aceticcid or ethanol (both 2 carbons). As a result, the theoretical yieldf pentose sugars to lactic acid is 0.6 g/g or 1.0 mol/mol via the PKathway (Patel et al., 2006). On the other hand, a few species ofAB possess the PP/glycolic pathway for the metabolism of pen-ose sugars. The PP/glycolic pathway produces 5 mol of lactic acidrom 3 mol of pentose without carbon loss, thereby providing a the-retical yield of lactic acid to pentose of 1.0 g/g or 1.67 mol/moli.e., homo-lactate fermentation) (Oshiro et al., 2009; Tanaka et al.,002). Therefore, to improve the lactate yield, the PP/glycolic path-ay is more useful and valuable than the PK pathway (Oshiro et al.,

009). Among wild-type LAB, E. mundtii QU 25 (Abdel-Rahmant al., 2011b), Streptococcus sp. (Enterococcus sp.), Lb. thermophilus1 (Fukui et al., 1957), and Lactobacillus strain MONT4 (Barre, 1978)ere reported to only show homo-lactate fermentation of pentose

ugars. In addition, Okano et al. (2009a,b) recently demonstratedomo-lactate fermentation with arabinose and xylose using genet-

cally modified Lb. plantarum by replacing the PK pathway with theP pathway.

The conversion of pyruvic acid to lactate can be affected bytereospecific NAD-dependent enzymes of l- or d-lactate dehy-rogenase. Both enzymes have been found to be active in most

actobacilli, for example, Lb. plantarum (Ferain et al., 1996) and Lb.asei (Viana et al., 2005). The stereospecificity and optical purity ofhe lactic acid produced depends on the type of LAB, whose enzymesed in its production. In addition, when xylose was used as theole carbon source, substrate concentration has been shown to be

factor for the metabolic flux of lactic acid production in the batchulture of E. mundtii QU 25 (Abdel-Rahman et al., 2011b) and theontinuous culture of Lc. lactis IO-1 (Tanaka et al., 2002); a higheroncentration of xylose and a higher yield of lactic acid to xyloseas obtained. Thus, further investigations of culture conditionsith LAB are suggested to be necessary for the efficient conversion

f lignocellulosic biomass to lactic acid.

. Designed biomass study and conclusions

Currently, the fermentative production of useful substances,.g., biomaterials and biofuels, from various renewable resourcesy microorganisms has become more attractive. For this purpose,

t is essential that the used strain should consume the renew-ble resources as substrates to produce the useful substances. In

number of recent studies, a targeted substrate is initially decidedpon, e.g., several types of biomass and by-products from industrialactories. Two main approaches are then applied to achieve effi-ient bioconversion (Fig. 3). One approach is a screening method tosolate wild-type strains from natural sources. The isolated strainhould show a great potential in terms of its degrading enzymeor the targeted substrate, broad substrate specificity for compo-ents derived from renewable resources, high product yield, low

y-product yield, capacity for high product concentration and pro-uctivity, and so on. An efficient process can then be investigatedsing the isolated strain, e.g., batch, fed-batch, or continuous fer-entation, SHF, or SSF. The second approach is breeding a strain

otechnology 156 (2011) 286– 301

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 alsosignificant for the highly efficient bioconversion of renewableresources to useful substances. Recently, we proposed a “designedbiomass study” for this purpose. “Designed biomass” refers tocompetent substances that can be designed for the correspondingfermentation, conversion processes, etc. In this type of study, all thetechnologies and engineering methods developed to date can beused, 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 notonly several types of components (mono-, oligo-, or polysaccha-rides) derived from various non-edible biomass sources but alsoorganic 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; Tashiroet al., 2007), both are produced fermentatively, were indicated asdesigned biomass material for acetone–butanol–ethanol fermen-tation by using the Clostridium saccharoperbutylacetonicum N1-4strain. In terms of lactic acid fermentation, we assessed sago starchas a designed biomass for E. faecium from among several starchesderived from different plants (Shibata et al., 2007). Of course, ourconcept also involves investigations on pretreatments and enzy-matic hydrolysis of renewable resources, as mentioned in Section2.2.

In this review, we mainly described fermentative lactic acid pro-duction processes by LAB. Other microorganisms can be consideredas genetically modified hosts for industrial lactic acid productionsuch as yeasts and Escherichia coli, which generally produce littlelactic acid (Okano et al., 2010b). Yeasts can grow in simpler syn-thetic media and are more tolerant to low pHs than LAB, whichcan 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 recombinantyeasts has been reported in Saccharomyces cerevisiae (Tokuhiroet al., 2008; van Rooyen et al., 2005), Kluyveromyces lactis (Bianchiet 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 asimple mineral salt medium, and the easy and reproducible meth-ods of genetic manipulation have been established in E. coli (Zhouet al., 2006). Very recently, there have been a few interesting reportson the direct productions of PLA and its copolymers from glucoseusing recombinant E. coli strains equipped with several genes forthe 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 followedby chemical process for PLA synthesis. Therefore, the constructedE. coli can develop a novel strategy for PLA production by one-stepprocess. Although recombinant yeasts and E. coli as described abovecould not utilize lignocellulose-derived sugars efficiently, furtherresearches should have potential and application for lactic acidproduction from lignocellulosic materials.

In conclusion, we described many studies and the findings oflactic acid fermentation by LAB from lignocellulosic materials andalso compared the features of LAB with other microorganisms.Nevertheless, industrial lactic acid production from lignocellulosicmaterials has not been sufficiently profitable. One of the reasonsfor 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 directlyto lactic acid, and the development of genetically modified LABthat have hydrolytic enzymes with high activity should be con-

l of Bi

tt

R

A

A

A

A

A

A

A

A

A

A

A

A

A

A

A

B

B

B

B

B

B

B

B

B

B

B

B

M.A. Abdel-Rahman et al. / Journa

inued. Designed biomass studies using those LAB would facilitatehe industrial production of lactic acid.

eferences

bbott, D.A., Zelle, R.M., Pronk, J.T., van Maris, A.J.A., 2009. Metabolic engineering ofSaccharomyces cerevisiae for production of carboxylic acids: current status andchallenges. FEMS Yeast Res. 9, 1123–1136.

bdel-Rahman, M.A., Tashiro, Y., Zendo, T., Hanada, K., Shibata, K., Sonomoto, K.,2011b. Efficient homofermentative l-(+)-lactic acid production from xylose bya novel lactic acid bacterium, Enterococcus mundtii QU 25. Appl. Environ. Micro-biol. 77, 1892–1895.

bdel-Rahman, M.A., Tashiro, Y., Zendo, T., Shibata, K., Sonomoto, K., 2011a. Isola-tion and characterization of lactic acid bacterium for effective fermentation ofcellobiose into optically pure homo l-(+)-lactic acid. Appl. Microbiol. Biotechnol.89, 1039–1049.

bdel-Rahman, M.A., Tashiro, Y., Zendo, T., Sonomoto, K., 2010a. Isolation and char-acterization of novel lactic acid bacterium for efficient production of l (+)-lacticacid from xylose. J. Biotechnol. 150 (S1), 347.

bdel-Rahman, M.A., Tashiro, Y., Zendo, T., Sonomoto, K., 2010b. Effective l (+)-lactic acid production by co-fermentation of mixed sugars. J. Biotechnol. 150(S1), 347–348.

be, S., Takagi, M., 1991. Simultaneous saccharification and fermentation of celluloseto lactic acid. Biotechnol. Bioeng. 37, 93–96.

dachi, E., Torigoe, M., Sugiyama, M., Nikawa, J., Shimizu, K., 1998. Modificationof metabolic pathways of Saccharomyces cerevisiae by the expression of lactatedehydrogenase and deletion of pyruvate decarboxylase genes for the lactic acidfermentation at low pH value. J. Ferment. Bioeng. 86, 284–289.

denis, L., Woiciechowski, A.L., Soccol, C.R., Ramos, L.P., Pandey, A., 1999. Experimen-tal design to enhance the production of l-(+)-lactic acid from steam-explodedwood hydrolyzate using Rhizopus oryzae in a mixed-acid fermentation. ProcessBiochem. 34, 949–955.

dnan, A.F.M., Tan, I.K.P., 2007. Isolation of lactic acid bacteria from Malaysian foodsand assessment of the isolates for industrial potential. Bioresour. Technol. 98,1380–1385.

dsul, M.G., Varma, A.J., Gokhale, D.V., 2007a. Lactic acid production from wastesugar cane bagasse derived cellulose. Green Chem. 9, 58–62.

dsul, M.G., Khire, J.M., Bastawade, K.B., Gokhale, D.V., 2007b. Lactic acid productionfrom cellobiose and cellotriose by Lactobacillus delbrueckii mutant Uc-3. Appl.Environ. Microbiol. 73, 5055–5057.

mrane, A., Prigent, Y., 1996. A novel concept of bioreactor: specialized function two-stage continuous reactor, and its application to lactose conversion into lacticacid. J. Biotechnol. 45, 195–203.

nderson, W.F., Peterson, J., Akin, D.E., Morrison, W.H., 2005. Enzyme pretreatmentof grass lignocellulose for potential high-value co-products and an improvedfermentable substrate. Appl. Biochem. Biotechnol. 121, 303–310.

ntal Jr., M., 1996. Water: a traditional solvent pregnant with new applications. In:White Jr., H.J. (Ed.), Proceedings of the 12th International Conference on theProperties of Water and Steam. Begell House, New York, pp. 24–32.

xelsson, L.T., 1993. Lactic acid bacteria: classification and physiology. In: Salminen,S., Wright, A. (Eds.), Lactic Acid Bacteria. Marcel Dekker, New York, USA, pp. 1–63.

ai, D.M., Wei, Q., Yan, Z.H., Wei, Q., Zhao, X.M., Li, X.G., Xu, S.M., 2004. Ammoniumlactate production by Lactobacillus lactis BME5-18M in pH-controlled fed-batchfermentations. Biochem. Eng. J. 19, 47–51.

aker, J.O., Ehrman, C.I., Adney, W.S., Thomas, S.R., Himmel, M.E., 1998. Hydrol-ysis of cellulose using ternary mixtures of purified cellulases. Appl. Biochem.Biotechnol. 70, 395–403.

alat, M., 2009. Gasification of biomass to produce gaseous products. Energy Source31, 516–526.

alat, M., 2011. Production of bioethanol from lignocellulosic materials via the bio-chemical pathway: a review. Energy Convers. Manage. 52, 858–875.

alat, M., Balat, H., Öz, C., 2008. Progress in bioethanol processing. Prog. Energ.Combust. 34, 551–573.

arre, P., 1978. Identification of thermobacteria and homofermentative, ther-mophilic, pentose-utilizing Lactobacilli from high temperature fermentinggrape musts. J. Appl. Bacteriol. 44, 125–129.

erlin, A., Gilkes, N., Kilburn, D., Bura, R., Markov, A., Skomarovsky, A., Okunev, O.,Gusakov, A., Maximenko, V., Gregg, D., 2005. Evaluation of novel fungal cellulasepreparations for ability to hydrolyze softwood substrates—evidence for the roleof accessory enzymes. Enzyme Microb. Technol. 37, 175–184.

ianchi, M., Tizzani, L., Destruelle, M., Frontali, L., Wesolowski-Louvel, M., 1996.The “petite-negative” yeast Kluyveromyces lactis has a single gene expressionpyruvate decarboxylase activity. Mol. Microbiol. 19, 27–36.

örjesson, J., Engqvist, M., Sipos, B., Tjerneld, F., 2007. Effect of poly (ethylene gly-col) on enzymatic hydrolysis and adsorption of cellulase enzymes to pretreatedlignocellulose. Enzyme Microb. Technol. 41, 186–195.

othast, R.J., Nichols, N.N., Dien, B.S., 1999. Fermentations with new recombinantorganisms. Biotechnol. Prog. 15, 867–875.

oyaval, P., Corre, C., Terre, S., 1987. Continuous lactic acid fermentation with con-centrated product recovery by ultrafiltration and electrodialysis. Biotechnol.

Lett. 9, 207–212.

ustos, G., de la Torre, N., Moldes, A.B., Cruz, J.M., Dominguez, J.M., 2007. Revaloriza-tion of hemicellulosic trimming vine shoots hydrolyzates trough continuousproduction of lactic acid and biosurfactants by L. pentosus. J. Food Eng. 78,405–412.

otechnology 156 (2011) 286– 301 297

Bustos, G., Moldes, A.B., Cruz, J.M., Domínguez, J.M., 2004. Production of fermentablemedia from vine-trimming wastes and bioconversion into lactic acid by Lacto-bacillus pentosus. J. Sci. Food. Agric. 84, 2105–2112.

Bustos, G., Moldes, A.B., Cruz, J.M., Domínguez, J.M., 2005. Influence of themetabolism pathway on lactic acid production from hemicellulosic trimmingvine shoots hydrolyzates using Lactobacillus pentosus. Biotechnol. Prog. 21,793–798.

Buyukgungor, H., Bueschelberger, H.G., 1986. Production of lactic acid fromlactose by free and immobilized Lactobacillus bulgaricus. Biotech-Forum. 3,80–85.

Caminal, G., Lbpez-Santin, J., Sola, C., 1985. Kinetic modeling of the enzymatic hydrol-ysis of pretreated cellulose. Biotechnol. Bioeng. 27, 1282–1290.

Carr, F.J., Chill, D., Maida, N., 2002. The lactic acid bacteria: a literature survey. Crit.Rev. Microbiol. 28, 281–370.

Carvalheiro, F., Duarte, L.C., Giri, F.M., 2008. Hemicellulose biorefineries: a reviewon biomass pretreatments. J. Sci. Ind. Res. 67, 849–864.

Chaillou, S., Bor, Y.C., Batt, C.A., Postma, P.W., Pouwels, P.H., 1998. Molecular cloningand functional expression in Lactobacillus plantarum 80 of xylT, encoding thed-xylose-H+ symporter of Lactobacillus brevis. Appl. Environ. Microbiol. 64,4720–4728.

Chaillou, S., Postma, P.W., Pouwels, P.H., 2001. Contribution of the phosphoenolpyru-vate: mannose phosphotransferase system to carbon catabolite repression inLactobacillus pentosus. Microbiology 147, 671–679.

Chaillou, S., Pouwels, P.H., Postma, P.W., 1999. Transport of d-xylose in Lacto-bacillus pentosus, Lactobacillus casei, and Lactobacillus plantarum: evidence fora mechanism of facilitated diffusion via the phosphoenolpyruvate: mannosephosphotransferase system. J. Bacteriol. 181, 4768–4773.

Chandel, A.K., ES, C., Rudravaram, R., Narasu, M.L., Rao, L.V., Ravindra, P., 2007. Eco-nomics and environmental impact of bioethanol production technologies: anappraisal. Biotechnol. Mol. Biol. Rev. 2, 14–32.

Chang, H.N., Kim, N.J., Kang, J., Jeong, C.M., Choi, J.D., Fei, Q., Kim, B.J., Kwon, S.,Lee, S.Y., Kim, J., 2011. Multi-stage high cell continuous fermentation for highproductivity and titer. Bioprocess Biosyst. Eng. 34, 419–431.

Chang, V.S., Holtzapple, M., 2000. Fundamentals factors affecting biomass reactivity.Appl. Biochem. Biotechnol. 84–86, 5–37.

Chaudhary, L.C., Singh, R., Kamra, D.N., 1994. Biodelignification of sugar cane bagasseby Pleurotus florida and Pleurotus cornucopiae. Indian J. Microbiol. 34, 55–57.

Chen, C.C., Ju, L.K., 1998. Adsorption characteristics of polyvinylpyridine andactivated carbon for lactic acid recovery from fermentation of Lactobacillus del-brueckii. Sep. Sci. Technol. 33, 1423–1437.

Chen, M., Zhao, J., Xia, L., 2009. Comparison of four different chemical pretreat-ments of corn stover for enhancing enzymatic digestibility. Biomass Bioenergy33, 1381–1385.

Chen, R., Lee, Y.Y., 1997. Membrane-mediated extractive fermentation for lacticacid production from cellulosic biomass. Appl. Biochem. Biotechnol. 63–65,435–448.

Choi, J.H., Kim, S.H., Moon, S.H., 2002. Recovery of lactic acid from sodium lactate byion substitution using ion-exchange membrane. Sep. Purif. Technol. 28, 69–79.

Cohen, R., Suzuki, M.R., Hammel, K.E., 2005. Processive endoglucanase active incrystalline cellulose hydrolysis by the brown rot basidiomycete Gloeophyllumtrabeum. Appl. Environ. Microbiol. 71, 2412–2417.

Converse, A.O., 1993. Substrate factors limiting enzymatic hydrolysis. In: Saddler, J.N.(Ed.), Bioconversion of Forest and Agricultural Plant Residues. CAB International,Wallingford, UK, pp. 93–106.

Cotton, J.C., Pometto, A.L., Gvozdenovic-Jeremic, J., 2001. Continuous lactic acidfermentation using plastic composite support biofilm reactor. Appl. Microbiol.Biotechnol. 57, 626–630.

Cowan, S.T., Steel, K.J., 1965. Manual for the Identification of Medical Bacteria. Cam-bridge University Press, New York, pp. 44–60.

Cui, F., Li, Y., Wan, C., 2011. Lactic acid production from corn stover using mixedcultures of Lactobacillus rhamnosus and Lactobacillus brevis. Bioresour. Technol.102, 1831–1836.

Dadi, A.P., Varanasi, S., Schall, C.A., 2006. Enhancement of cellulose saccharificationkinetics using anionic liquid pretreatment step. Biotechnol. Bioeng. 95, 904–910.

Datta, R., Henry, M., 2006. Lactic acid: recent advances in products, processes andtechnologies—a review. J. Chem. Technol. Biotechnol. 81, 1119–1129.

Datta, R., Tsai, S.P., Bonsignor, P., Moon, S., Frank, J., 1995. Technological and eco-nomical potential of polylactic acid and lactic acid derivatives. FEMS Microbiol.Rev. 16, 221–231.

de Jong, S.J., van Eerdenbrugh, B., van Nostrum, C.F., Kettenes-van den Bosch, J.J.,Hennink, W.E., 2001. Physically crosslinked dextran hydrogels by stereocomplexformation of lactic acid oligomers: degradation and protein release behavior. J.Control. Release 71, 261–275.

Demirbas, A., 2008. Products from lignocellulosic materials via degradation pro-cesses. Energy Source 30, 27–37.

Demirbas, A., 2005. Bioethanol from cellulosic materials: a renewable motor fuelfrom biomass. Energy Source 27, 327–337.

Ding, S.F., Tan, T.W., 2006. l-Lactic acid production by Lactobacillus casei fer-mentation using different fed-batch feeding strategies. Process Biochem. 41,1451–1454.

Duff, S.J.B., Murray, W.D., 1996. Bioconversion of forest products industry waste

cellulosics to fuel ethanol: a review. Bioresour. Technol. 55, 1–33.

Dumbrepatil, A., Adsul, M., Chaudhari, S., Khire, J., Gokhale, D., 2008. Utilizationof molasses sugar for lactic acid production by Lactobacillus delbrueckii subsp.delbrueckii mutant Uc-3 in batch fermentation. Appl. Environ. Microbiol. 74,333–335.

2 l of Bi

E

E

E

F

F

F

F

F

F

G

G

G

G

G

G

G

G

G

G

H

H

H

H

H

H

H

H

H

H

H

H

98 M.A. Abdel-Rahman et al. / Journa

hrman, C.I., Himmel, M.E., 1994. Simultaneous saccharification and fermentationof pretreated biomass: improving mass balance closure. Biotechnol. Tech. 8,99–104.

steghlalian, A., Hashimoto, A.G., Fenske, J.J., Penner, M.H., 1997. Modeling and opti-mization of the dilute-sulfuric-acid pretreatment of corn stover, poplar andswitchgrass. Bioresour. Technol. 59, 129–136.

steghlalian, A.R., Svivastava, V., Gilkes, N., Gregg, D.J., Saddler, J.N., 2001. Anoverview of factors influencing the enzymatic hydrolysis of lignocellulosic feed-stocks. In: Himmel, M.E., Baker, W., Saddler, J.N. (Eds.), Glycosyl Hydrolases forBiomass Conversion. ACS, pp. 100–111.

eldman, D., Banu, D., Natansohn, A., Wang, J., 1991. Structure–properties relationsof thermally cured epoxy-lignin polyblends. J. Appl. Polym. Sci. 42, 1537–1550.

engel, D., Wegener, G., 1989. Wood Chemistry, Ultrastructure, Reactions. Walter deGruyter, Berlin New York, pp. 437–466.

erain, T., Hobbs Jr., J.N., Richardson, J., Bernard, N., Garymn, D., Hols, P., Allen, N.E.,Delcour, J., 1996. Knockout of the two ldh genes has major impact on peptidogly-can precursor synthesis in Lactobacillus plantarum. J. Bacteriol. 178, 5431–5437.

red, E.B., Peterson, W.H., Davenport, A.J., 1919. Acid fermentation of xylose. J. Biol.Chem. 39, 347–383.

ujii, M., Mori, J.I., Homma, T., Taniguchi, M., 1995. Synergy between an endoglu-canase and cellobiohydrolases from Trichoderma koningii. Chem. Eng. J. Biochem.Eng. J. 59, 315–319.

ukui, S., Oi, A., Obayashi, A., Kitahara, K., 1957. Studies on the pentose metabolismby microorganism. 1. A new type-lactic acid fermentation of pentose by lacticacid bacteria. J. Gen. Appl. Microbiol. 3, 258–268.

albe, M., Zacchi, G., 2007. Pretreatment of lignocellulosic materials for efficientbioethanol production. Adv. Biochem. Eng. Biotechnol. 108, 41–65.

arde, A., Jonsson, G., Schmidt, A.S., Ahring, B.K., 2002. Lactic acid production fromwheat straw hemicellulose hydrolysate by Lactobacillus pentosus and Lactobacil-lus brevis. Bioresour. Technol. 81, 217–223.

atje, G., Gottschalk, G., 1991. Limitation of growth and lactic acid productionin batch and continuous cultures of Lactobacillus helveticus. Appl. Microbiol.Biotechnol. 34, 446–449.

hosh, T.K., Das, K., 1971. Kinetics of hydrolysis of insoluble cellulose by cellulase.Adv. Biochem. Eng. 1, 49–55.

ivry, S., Prevot, V., Duchiron, F., 2008. Lactic acid production from hemicellulosichydrolyzate by cells of Lactobacillus bifermentans immobilized in Ca-alginateusing response surface methodology. World J. Microbiol. Biotechnol. 24,745–752.

öksungur, Y., Güvenc , U., 1999. Production of lactic acid from beet molasses by cal-cium alginate immobilized Lactobacillus delbrueckii IFO 3202. J. Chem. Technol.Biotechnol. 74, 131–136.

onzalez, M.I., Alvarez, S., Riera, F.A., Alvareza, R., 2008. Lactic acid recovery fromwhey ultrafiltrate fermentation broths and artificial solutions by nanofiltration.Desalination 228, 84–89.

osalbes, M.J., Monedero, V., Perez-Martinez, G., 1999. Elements involved in catabo-lite repression and substrate induction of the lactose operon in Lactobacilluscasei. J. Bacteriol. 181, 3928–3934.

ullon, B., Yanez, R., Alonso, J.L., Parajo, J.C., 2008. l-Lactic acid production fromapple pomace by sequential hydrolysis and fermentation. Bioresour. Technol.99, 308–319.

uo, W., Jia, W., Li, Y., Chen, S., 2010. Performances of Lactobacillus brevis for produc-ing lactic acid from hydrolysate of lignocellulosics. Appl. Biochem. Biotechnol.161, 124–136.

ábová, V., Melzoch, K., Rychtera, M., Sekavová, B., 2004. Electrodialysis as a usefultechnique for lactic acid separation from a model solution and a fermentationbroth. Desalination 162, 361–372.

ano, T., Matsumoto, M., Uenoyama, S., Ohta, T., Kawano, Y., Miura, S., 1993. Sepa-ration of lactic acid from fermented broth by solvent extraction. Bioseparation3, 321–326.

ayn, M., Steiner, W., Klinger, R., Steinmtiller, H., Sinner, M., Esterbauer, H., 1993.Basic research and pilot studies on the enzymatic conversion of lignocellulosics.In: Saddler, J.N. (Ed.), Bioconversion of Forest and Agricultural Plant Residues.CAB International, Wallingford, UK, pp. 33–72.

elanto, M., Kiviharju, K., Leisola, M., Nyyssölä, A., 2007. Metabolic engineering ofLactobacillus plantarum for production of l-ribulose. Appl. Environ. Microbiol.73, 7083–7091.

endriks, A.T., Zeeman, G., 2009. Pretreatments to enhance the digestibility of lig-nocellulosic biomass. Bioresour. Technol. 100, 10–18.

immel, M.E., Ruth, M.F., Wyman, C.E., 1999. Cellulase for commodity products fromcellulosic biomass. Curr. Opin. Biotechnol. 10, 358–364.

inman, N.D., Schell, D.J., Riley, C.J., Bergeron, P.W., Walter, P.J., 1992. Preliminaryestimate of the cost of ethanol production for SSF technology. Appl. Biochem.Biotechnol. 34/35, 639–649.

inman, N.D., Wright, J.D., Hoagland, W., Wyman, C.E., 1989. Xylose fermentation,an economic analysis. Appl. Biochem. Biotechnol. 20–21, 391–401.

ofvendahl, K., Hahn-Hägerdal, B., 2000. Factors affecting the fermentative lac-tic acid production from renewable resources. Enzyme Microb. Technol. 26,87–107.

oltzapple, M., Cognata, M., Shu, Y., Hendrickson, C., 1990. Inhibition of Trichodermareesei cellulase by sugars and solvents. Biotechnol. Bioeng. 36, 275–287.

onda, H., Toyama, Y., Takahashi, H., Nakazeko, T., Kobayashi, T., 1995. Effectivelactic acid production by two-stage extractive fermentation. J. Ferment. Bioeng.79, 589–593.

ongo, M., Nomura, Y., Iwahara, M., 1986. Novel method of lactic acid productionby electrodialysis fermentation. Appl. Environ. Microbiol. 52, 314–319.

otechnology 156 (2011) 286– 301

Huang, L.P., Jin, B., Lant, P., Zhou, J.T., 2005. Simultaneous saccharification and fer-mentation of potato starch wastewater to lactic acid by Rhizopus oryzae andRhizopus arrhizus. Biochem. Eng. J. 23, 265–276.

Ikeda, Y., Jamshidi, K., Tsuji, H., Hyon, S.H., 1987. Stereocomplex formation betweenenantiomeric poly(lactides). Macromolecules 20, 904–906.

Ikushima, S., Fujii, T., Kobayashi, O., Yoshida, S., Yoshida, A., 2009. Genetic engineer-ing Candida utilis yeast for efficient production of l-lactic acid. Biosci. Biotechnol.Biochem. 73, 1818–1824.

Ilmen, M., Koivuranta, K., Ruohonen, L., Suominen, P., Penttila, M., 2007. Efficientproduction of l-lactic acid from xylose by Pichia stipitis. Appl. Environ. Microbiol.73, 117–123.

Irwin, D.C., Spezio, M., Walker, L.P., Wilson, D.B., 1993. Activity studies of eight puri-fied cellulases: specificity, synergism, and binding domain effects. Biotechnol.Bioeng. 42, 1002–1013.

Iyer, P.V., Lee, Y.Y., 1999b. Simultaneous saccharification and extractive fer-mentation of lignocellulosic materials into lactic acid in a two-zonefermentor–extractor system. Appl. Biochem. Biotechnol. 78, 409–419.

Iyer, P.V., Lee, Y.Y., 1999a. Product inhibition in simultaneous saccharification andfermentation of cellulose into lactic acid. Biotechnol. Lett. 21, 371–373.

Iyer, P.V., Thomas, S.A., Lee, Y.Y., 2000. High-yield fermentation of pentoses intolactic acid. Appl. Biochem. Biotechnol. 84–86, 665–677.

Jeantet, R., Maubois, J.L., Boyaval, P., 1996. Semicontinuous production of lactic acidin a bioreactor coupled with nano-filtration membranes. Enzyme Microb. Tech-nol. 19, 614–619.

Jeffries, T.W., Jin, Y.S., 2000. Ethanol and thermotolerance in the bioconversion ofxylose by yeasts. Adv. Appl. Microbiol. 47, 221–268.

John, R.P., Anisha, G.S., Nampoothiri, K.M., Pandey, A., 2009. Direct lactic acid fer-mentation: focus on simultaneous saccharification and lactic acid production.Biotechnol. Adv. 27, 145–152.

John, R.P., Nampoothiri, K.M., Pandey, A., 2006a. Simultaneous saccharification andfermentation of cassava bagasse for l-(+)-lactic acid production using Lacto-bacilli. Appl. Biochem. Biotechnol. 134, 263–272.

John, R.P., Nampoothiri, K.M., Pandey, A., 2006b. Solid-state fermentation for l-lactic acid production from agro wastes using Lactobacillus delbrueckii. ProcessBiochem. 41, 759–763.

John, R.P., Nampoothiri, K.M., Pandey, A., 2006c. Simultaneous saccharification and l-(+)-lactic acid fermentation of protease treated wheat bran using mixed cultureof lactobacilli. Biotechnol. Lett. 28, 1823–1826.

John, R.P., Nampoothiri, K.M., Pandey, A., 2007. Fermentative production of lacticacid from biomass: an overview on process developments and future perspec-tives. Appl. Microbiol. Biotechnol. 74, 524–534.

Jorgensen, H., Kristensen, J.B., Felby, C., 2007. Enzymatic conversion of lignocelluloseinto fermentable sugars: challenges and opportunities. Biofuels Bioprod. Bioref.1, 119–134.

Joshi, D.S., Singhvi, M.S., Khire, J.M., Gokhale, D.V., 2010. Strain improvement ofLactobacillus lactis for d-lactic acid production. Biotechnol. Lett. 32, 517–520.

Jun, L., Liming, L., Wenxu, W., Peilin, C., 1998. Kinetics of cellulose enzymatic hydrol-ysis and simultaneous saccharification and lactic acid fermentation process. J.Chem. Ind. Eng. 49, 161–169.

Jung, Y.K., Kim, T.Y., Park, S.J., Lee, S.Y., 2010. Metabolic engineering of Escherichia colifor the production of PLA and its copolymers. Biotechnol. Bioeng. 105, 161–171.

Jung, Y.K., Lee, S.Y., 2011. Efficient production of polylactic acid and its copolymersby metabolically engineered Escherichia coli. J. Biotechnol. 151, 94–101.

Kaar, W.E., Holtzaple, M.T., 2000. Using lime pretreatment to facilitate the enzymatichydrolysis of corn stover. Biomass Bioenergy 18, 189–199.

Karel, M., Jaroslav, V., Vera, H., Mojmir, R., 1997. Lactic acid production in a cellretention continuous culture using lignocellulosic hydrolysate as a substrate. J.Biotechnol. 56, 25–31.

Keshwani, D.R., Cheng, J.J., 2009. Switchgrass for bioethanol and other value-addedapplications: a review. Bioresour. Technol. 100, 1515–1523.

Kharras, G.B., Sanchez-Riera, F., Severson, D.K., 1993. Polymers of lactic acid. In:Molby, D.B. (Ed.), Plastics from Microbes: Microbial Synthesis of Polymers andPolymer Precursors. Hanser Publ., pp. 93–137.

Kim, J.H., Mills, D.A., Block, D.E., Shoemaker, S.P., 2010a. Atypical ethanol pro-duction by carbon catabolite derepressed lactobacilli. Bioresour. Technol. 101,8790–8797.

Kim, J.H., Mills, D.A., Block, D.E., Shoemaker, S.P., 2010b. Conversion of rice strawto biobased chemicals: an integrated process using Lactobacillus brevis. Appl.Microbiol. Biotechnol. 86, 1375–1385.

Kim, J.H., Shoemaker, S.P., Mills, D.A., 2009. Relaxed control of sugar utilization inLactobacillus brevis. Microbiology 155, 1351–1359.

Kim, Y.H., Moon, S.H., 2001. Lactic acid recovery from fermentation broth using onestage electrodialysis. J. Chem. Technol. Biotechnol. 76, 169–178.

Kodali, B., Pogaku, R., 2006. Pretreatment studies of rice bran for the effective pro-duction of cellulose. Electron J. Environ. Agric. Food Chem. 5, 1253–1264.

Kotzamanidis, C., Roukas, T., Skaracis, G., 2002. Optimization of lactic acid productionfrom beet molasses by Lactobacillus delbrueckii NCIMB 8130. World J. Microbiol.Biotechnol. 18, 441–448.

Krishna, S.H., Reddy, T.J., Chowdary, G.V., 2001. Simultaneous saccharification andfermentation of lignocellulosic wastes to ethanol using a thermotolerant yeast.Bioresour. Technol. 77, 193–196.

Kuhad, R.C., Johri, B.N., 1992. Fungal decomposition of peddy straw: light and scan-ning microscopic study. Indian J. Microbiol. 32, 255–258.

Kulozik, U., Wilde, J., 1999. Rapid lactic acid production at high cell concentrationsin whey ultrafiltrate by Lactobacillus helveticus. Enzyme Microb. Technol. 24,297–302.

l of Bi

K

K

K

K

L

L

L

L

L

L

L

L

L

L

L

L

L

L

L

L

L

L

L

L

M

M

M

M

M

M

M

M.A. Abdel-Rahman et al. / Journa

umar, R., Singh, S., Singh, O.V., 2008. Bioconversion of lignocellulosic biomass: bio-chemical and molecular perspectives. J. Ind. Microbiol. Biotechnol. 35, 377–391.

umar, P., Barrett, D.M., Delwiche, M.J., Stroeve, P., 2009. Methods for pretreatmentof lignocellulosic biomass for efficient hydrolysis and biofuel production. Ind.Eng. Chem. Res. 48, 3713–3729.

umar, R., Nanavati, H., Noronha, S.B., Mahajani, S.M., 2006. A continuous process forthe recovery of lactic acid by reactive distillation. J. Chem. Technol. Biotechnol.81, 1767–1777.

won, S., Yoo, I.K., Lee, W.G., Chang, H.N., Chang, Y.K., 2001. High-rate continuousproduction of lactic acid by Lactobacillus rhamnosus in a two-stage membranecell-recycle bioreactor. Biotechnol. Bioeng. 73, 25–34.

adisch, M.R., Lin, K.W., Voloch, M., Tsao, G.T., 1983. Process considera-tions in the enzymatic hydrolysis of biomass. Enzyme Microb. Technol. 5,82–102.

aopaiboon, P., Thani, A., Leelavatcharamas, V., Laopaiboon, L., 2010. Acid hydrol-ysis of sugarcane bagasse for lactic acid production. Bioresour. Technol. 101,1036–1043.

aser, M., Schulman, D., Allen, S.G., Lichwa, J., Antal, M.J., Lynd, L.R., 2002. A com-parison of liquid hot water and steam pretreatments of sugar cane bagasse forbioconversion to ethanol. Bioresour. Technol. 81, 33–44.

au, M.W., Dale, B.E., Balan, V., 2008. Ethanolic fermentation of hydrolysates fromammonia fiber expansion (AFEX) treated corn stover and distillers grain withoutdetoxification and external nutrient supplementation. Biotechnol. Bioeng. 99,529–539.

ee, S.M., Koo, Y.M., Lin, J., 2004. Production of lactic acid from paper sludge bysimultaneous saccharification and fermentation. Adv. Biochem. Eng. Biotechnol.87, 173–194.

ee, Y.H., Fan, L.T., 1983. Kinetic studies of enzymatic hydrolysis insoluble cellulose(II). Biotechnol. Bioeng. 25, 959–966.

i, H., Mustacchi, R., Knowles, C.J., Skibar, W., Sunderland, G., Dalrymple, L., Jack-man, S.A., 2004. An electrokinetic bioreactor: using direct electric currentfor enhanced lactic acid fermentation and product recovery. Tetrahedron 60,655–661.

i, Y., Shahbazi, A., Williams, K., Wan, C., 2008. Separate and concentrate lacticacid using combination of nanofiltration and reverse osmosis membranes. Appl.Biochem. Biotechnol. 147, 1–9.

i, Y.B., Shahbazi, A., 2006. Lactic acid recovery from cheese whey fermentation brothusing combined ultrafiltration and nanofiltration membranes. Appl. Biochem.Biotechnol. 132, 985–996.

i, Z., Lu, J., Zhao, L., Xiao, K., Tan, T., 2010. Improvement of l-lactic acid produc-tion under glucose feedback controlled culture by Lactobacillus rhamnosus. Appl.Biochem. Biotechnol. 162, 1762–1767.

in, Y., Tanaka, S., 2006. Ethanol fermentation from biomass resources: current stateand prospects. Appl. Microbiol. Biotechnol. 69, 627–642.

in, Z.X., Zhang, H.M., Ji, Z.J., Chen, J.W., Huang, H., 2011. Hydrolytic enzyme of cellu-lose for complex formulation applied research. Appl. Biochem. Biotechnol. 164,23–33.

inko, P., Stenroos, S.L., Linko, Y., Koistinen, T., Harju, M., Heikonen, M., 1984. Appli-cations of immobilized lactic acid bacteria. Ann. N. Y. Acad. Sci. 434, 406–417.

inko, Y.Y., Javanainen, P., 1996. Simultaneous liquefaction, saccharification, andlactic acid fermentation on barley starch. Enzyme Microb. Technol. 19, 118–123.

iu, S., Bischoff, K.M., Hughes, S.R., Leathers, T.D., Price, N.P., Qureshi, N., Rich, J.O.,2009. Conversion of biomass hydrolysates and other substrates to ethanol andother chemicals by Lactobacillus buchneri. Lett. Appl. Microbiol. 48, 337–342.

opez, M.J., Nichols, N.N., Dien, B.S., Moreno, J., Bothast, R.J., 2004. Isolation ofmicroorganisms for biological detoxification of lignocellulosic hydrolysates.Appl. Microbiol. Biotechnol. 64, 125–131.

u, Z., Lu, M., He, F., Yu, L., 2009. An economical approach for d-lactic acid productionutilizing unpolished rice from aging paddy as major nutrient source. Bioresour.Technol. 100, 2026–2031.

ynd, L.R., Weimer, P.J., van Zyl, W.H., Pretorius, I.S., 2002. Microbial cellulose utiliza-tion: fundamentals and biotechnology. Microbiol. Mol. Biol. Rev. 66, 506–577.

ynd, L.R., 1996. Overview and evaluation of fuel from cellulosic biomass. Annu. Rev.Energy Environ. 21, 403–465.

ynd, L.R., Elander, R.T., Wyman, C.E., 1996. Likely features and costs of maturebiomass ethanol technology. Appl. Biochem. Biotechnol. 57/58, 741–761.

adzingaidzo, L., Danner, H., Braun, R., 2002. Process development and optimisationof lactic acid purification using electrodialysis. J. Biotechnol. 96, 223–239.

ahr, K., Hillen, W., Titgemeyer, F., 2000. Carbon catabolite repression in Lactobacil-lus pentosus: analysis of the ccpA region. Appl. Environ. Microbiol. 66, 277–283.

ais, U., Esteghlalian, A.R., Saddler, J.N., Mansfield, S.D., 2002. Enhancing the enzy-matic hydrolysis of cellulosic materials using simultaneous ball milling. Appl.Biochem. Biotechnol. 98, 815–832.

arasco, R., Muscariello, L., Varcamonti, M., De Felice, M., Sacco, M., 1998. Expressionof the bglH gene of Lactobacillus plantarum is controlled by carbon cataboliterepression. J. Bacteriol. 180, 3400–3404.

arques, S., Santos, J.A.L., Girio, F.M., Roseiro, J.C., 2008. Lactic acid productionfrom recycled paper sludge by simultaneous saccharification and fermentation.Biochem. Eng. J. 41, 210–216.

cCaskey, T.A., Zhou, S.D., Britt, S.N., Strickland, R., 1994. Bioconversion of municipalsolid waste to lactic acid by Lactobacillus species. Appl. Biochem. Biotechnol.

45–46, 555–563.

elzoch, K., Votruba, J., Habova, V., Rychtera, M., 1997. Lactic acid production in a cellretention continuous culture using lignocellulosic hydrolysate as a substrate. J.Biotechnol. 56, 25–31.

otechnology 156 (2011) 286– 301 299

Mes-Hartree, M.M., Yu, E.K.C., Reid, I.D., Saddler, J.N., 1987. Suitability of aspen woodbiologically delignified with Pheblia tremellosus for fermentation of ethanol orbutanol. Appl. Microbiol. Biotechnol. 26, 120–125.

Min-Tian, G., Koide, M., Gotou, R., Takanashi, H., Hirata, M., Hano, T., 2005. Devel-opment of a continuous fermentation system for production of lactic acid byLactobacillus rhamnosus. Process Biochem. 40, 1033–1036.

Miura, S., Arimura, T., Itoda, N., Dwiarti, L., Feng, J.B., Bin, C.H., Okabe, M., 2004.Production of L-lactic acid from corncob. J. Biosci. Bioeng. 97, 153–157.

Moldes, A.B., Alonso, J.L., Parajo, J.C., 2001. Strategies to improve the bioconver-sion of processed wood into lactic acid by simultaneous saccharification andfermentation. J. Chem. Technol. Biotechnol. 76, 279–284.

Moldes, A.B., Torrado, A., Converti, A., Dominguez, J.M., 2006. Complete biocon-version of hemicellulosic sugars from agricultural residues into lactic acid byLactobacillus pentosus. Appl. Biochem. Biotechnol. 135, 219–227.

Moldes, B.N., Alonso, L.J., Parajo, C.J., 1999. Cogeneration of cellobiose and glucosefrom pretreated wood and bioconversion to lactic acid: a kinetic study. J. Biosci.Bioeng. 87, 787–792.

Molina-Sabio, M., Rodríguez-Reinoso, F., 2004. Role of chemical activation in thedevelopment of carbon porosity. Colloid Surf. A Physicochem. Eng. Aspect. 241,15–25.

Monteagudo, J.M., Aldavero, M., 1999. Production of l-lactic acid by Lactobacillusdelbrueckii in chemostat culture using an ion exchange resins system. J. Chem.Technol. Biotechnol. 74, 627–634.

Monteagudo, J.M., Rodriguez, L., Rincon, J., Fuertes, J., 1997. Kinetics of lactic acid fer-mentation by Lactobacillus delbrueckii grown on beet molasses. J. Chem. Technol.Biotechnol. 68, 271–276.

Morel, F., Frot-Coutaz, J., Aubel, D., Portalier, R., Atlan, D., 1999. Characterization ofa prolidase from Lactobacillus delbrueckii subsp. bulgaricus CNRZ 397 with anunusual regulation of biosynthesis. Microbiology 145, 437–446.

Moritz, J.W., Duff, S.J.B., 1996. Simultaneous saccharification and extractive fermen-tation of cellulosic substrates. Biotechnol. Bioeng. 49, 504–511.

Mosier, N., Wyman, C., Dale, B., Elander, R., Holtzapple, Y.Y.L.M., Ladisch, M., 2005.Features of promising technologies for pretreatment of lignocellulosic biomass.Bioresour. Technol. 96, 673–686.

Mussatto, S.I., Fernandes, M., Mancilha, I.M., Roberto, I.C., 2008. Effects of mediumsupplementation and pH control on lactic acid production from brewer’s spentgrain. Biochem. Eng. J. 40, 437–444.

Mussatto, S.I., Roberto, I.C., 2004. Alternatives for detoxification of diluted acid lig-nocellulosic hydrolysates for use in fermentative process: a review. Bioresour.Technol. 93, 1–10.

Nancib, A., Nancib, N., Boudrant, J., 2009. Production of lactic acid from date juiceextract with free cells of single and mixed cultures of Lactobacillus casei andLactococcus lactis. World J. Microbiol. Biotechnol. 25, 1423–1429.

Naveena, B.J., 2004. Amylolytic bacterial l(+) lactic acid production in solid statefermentation and molecular identification of the strain. Ph.D. thesis, OsmaniaUniversity, Hyderabad, India.

Naveena, B.J., Altaf, M., Bhadrayya, K., Madhavendra, S.S., Reddy, G., 2005b. Directfermentation of starch to l(+) lactic acid in SSF by Lactobacillus amylophilus GV6using wheat bran as support and substrate—medium optimization using RSM.Process Biochem. 40, 681–690.

Naveena, B.J., Altaf, M., Bhadriah, K., Reddy, G., 2005a. Selection of medium com-ponents by Plackett–Burman design for production of l(+) lactic acid byLactobacillus amylophilus GV6 in SSF using wheat bran. Bioresour. Technol. 96,485–490.

Nichols, N.N., Dien, B.S., Guisado, G.M., López, M.J., 2005. Bioabatement to removeinhibitors from biomass-derived sugar hydrolysates. Appl. Biochem. Biotechnol.121, 379–390.

Nidetzky, B., Steiner, W., Hayn, M., Claeyssens, M., 1994. Cellulose hydrolysis bythe cellulases from Trichoderma reesei: a new model for synergistic interaction.Biochem. J. 298, 705–710.

Nilvebrant, N.O., Person, P., Reimann, A., Sousa, F.D., Gorton, L., Jonsson, L.J., 2003.Limits for alkaline detoxification of dilute-acid lignocellulose hydrolysates. Appl.Biochem. Biotechnol. 107, 615–628.

Nolasco-Hipolito, C., Matsunaka, T., Kobayashi, G., Sonomoto, K., Ishizaki, A., 2002.Synchronised fresh cell bioreactor system for continuous l-(+)-lactic acid pro-duction using Lactococcus lactis IO-1 in hydrolysed sago starch. J. Biosci. Bioeng.93, 281–287.

Nomura, Y., Iwahara, M., Hallsworth, J.E., Tanaka, T., Ishizaki, A., 1998. High-speedconversion of xylose to l-lactate by electrodialysis bioprocess. J. Biotechnol. 60,131–135.

Nomura, Y., Iwahara, M., Hongo, M., 1987. Lactic acid production by electrodialysisfermentation using immobilized growing cells. Biotechnol. Bioeng. 30, 788–793.

Ogier, J.C., Ballerini, D., Leygue, J.P., Rigal, L., Pourquie, J., 1999. Ethanol productionfrom lignocellulosic biomass. Oil Gas Sci. Technol. 54, 67–94.

Oh, H., Wee, Y.J., Yun, J.S., Ryu, H.W., 2003. Lactic acid production through cell-recyclerepeated batch bioreactor. Appl. Biochem. Biotechnol. 105, 603–613.

Ohara, H., Owaki, M., Sonomoto, K., 2006. Xylooligosaccharide fermentation withLeuconostoc lactis. J. Biosci. Bioeng. 101, 415–420.

Öhgren, K., Bura, R., Saddler, J., Zacchi, G., 2007. Effect of hemicellulose and ligninremoval on enzymatic hydrolysis of steam pretreated corn stover. Bioresour.Technol. 98, 2503–2510.

Ohleyer, E., Blanch, H.W., Wilke, C.R., 1985. Continuous production of lactic acid ina cell recycle reactor. Appl. Biochem. Biotechnol. 11, 317–332.

Okano, K., Tanaka, T., Ogino, C., Fukuda, H., Kondo, A., 2010b. Biotechnologi-cal production of enantiomeric pure lactic acid from renewable resources:

3 l of Bi

O

O

O

O

O

O

O

O

O

P

P

P

P

P

P

P

P

P

P

P

P

P

P

P

Q

R

R

00 M.A. Abdel-Rahman et al. / Journa

recent achievements, perspectives, and limits. Appl. Microbiol. Biotechnol. 85,413–423.

kano, K., Yoshida, S., Tanaka, T., Fukuda, H., Kondo, A., 2009a. Homo d-lactic acidfermentation from arabinose by redirection of phosphoketolase pathway to pen-tose phosphate pathway in l-lactate dehydrogenase gene-deficient Lactobacillusplantarum. Appl. Environ. Microbiol. 75, 5175–5178.

kano, K., Yoshida, S., Yamda, R., Tanaka, T., Ogino, C., Fukuda, H., Kondo, A.,2009b. Improved production of homo-d-lactic acid via xylose fermentationby introduction of xylose assimilation genes and redirection of the phospho-ketolase pathway to pentose phosphate pathway in l-lactate dehydrogenasegene-deficient Lactobacillus plantarum. Appl. Environ. Microbiol. 75, 7858–7861.

kano, K., Zhang, Q., Yoshida, S., Tanaka, T., Ogino, C., Fukuda, H., Kondo,A., 2010a. d-Lactic acid production from cellooligosaccharides and �-glucan using genetically modified l-lactate dehydrogenase gene-deficient andendoglucanase-secreting Lactobacillus plantarum. Appl. Microbiol. Biotechnol.85, 643–650.

lsson, L., Hahn-Hägerdal, B., 1996. Fermentation of lignocellulosic hydrolyzates forethanol production. Enzyme Microb. Technol. 18, 312–331.

sawa, F., Fujii, T., Nishida, T., Tada, N., Ohnishi, T., Kobayashi, O., Komeda, T., Yoshida,S., 2009. Efficient production of l-lactic acid by Crabtree-negative yeast Candidaboidinii. Yeast 26, 485–496.

shiro, M., Hanada, K., Tashiro, Y., Sonomoto, K., 2010. Efficient conversion of lac-tic acid to butanol with pH-stat continuous lactic acid and glucose feedingmethod by Clostridium saccharoperbutylacetonicum. Appl. Microbiol. Biotechnol.87, 1177–1185.

shiro, M., Shinto, H., Tashiro, Y., Miwa, N., Sekiguchi, T., Okamoto, M., Ishizaki,A., Sonomoto, K., 2009. Kinetic modeling and sensitivity analysis of xylosemetabolism in Lactococcus lactis IO-1. J. Biosci. Bioeng. 108, 376–384.

u, M.S., Ingram, L.O., Shanmugam, K.T., 2011. l-(+)-Lactic acid production fromnon-food carbohydrates by thermotolerant Bacillus coagulans. J. Ind. Microbiol.Biotechnol. 38, 599–605.

u, M.S., Mohammed, N., Ingram, L.O., Shanmugam, K.T., 2009. Thermophilic Bacilluscoagulans requires less cellulases for simultaneous saccharification and fermen-tation of cellulose to products than mesophilic microbial biocatalysts. Appl.Biochem. Biotechnol. 155, 379–385.

almqvist, E., Hahn-Hägerdal, B., 2000. Fermentation of lignocellulosic hydrolysates.II: inhibitors and mechanisms of inhibition. Bioresour. Technol. 74, 25–33.

alonen, H., Viikari, L., 2004. Role of oxidative enzymatic treatments on enzymatichydrolysis of softwood. Biotechnol. Bioeng. 86, 550–557.

an, X., Gilkes, N., Kadla, J., Pye, K., Saka, S., Gregg, D., Ehara, K., Xie, D., Lam, D.,Saddler, J., 2006. Bioconversion of hybrid poplar to ethanol and coproducts usingan organosolv fractionation process: optimization of process yields. Biotechnol.Bioeng. 94, 851–861.

an, X., Arato, C., Gilkes, N., Gregg, D., Mabee, W., Pye, K., Xiao, Z.Z., Zhang, X., Saddler,J., 2005. Biorefining of softwoods using ethanol organosolv pulping: preliminaryevaluation of process streams for manufacture of fuel-grade ethanol and co-products. Biotechnol. Bioeng. 90, 473–481.

andey, A., Soccol, C.R., Rodriguez-Leon, J.A., Nigam, P., 2001. Production of organicacids by solid state fermentation. In: solid state fermentation in biotechnology:fundamentals and applications. Asiatech Publishers, New Delhi, p. 127.

arajo, J.C., Alonso, J.L., Moldes, A.B., 1997. Production of lactic acid from lignocel-lulose in a single stage of hydrolysis and fermentation. Food Biotechnol. 11,45–58.

arajo, J.C., Alonso, J.L., Santos, V., 1996. Lactic acid from wood. Process Biochem. 31,271–280.

arisi, F., 1989. Advances in lignocellulosics hydrolysis and in the utilization of thehydrolysates. Adv. Biochem. Eng. Biotechnol. 38, 53–87.

atel, M.A., Ou, M.S., Harbrucker, R., Aldrich, H.C., Buszko, M.L., Ingram, L.O., Shan-mugam, K.T., 2006. Isolation and characterization of acid-tolerant, thermophilicbacteria for effective fermentation of biomass-derived sugars to lactic acid. Appl.Environ. Microbiol. 72, 3228–3235.

hilippidis, G.P., Smith, T.K., 1995. Limiting factors in the simultaneous sacchari-fication and fermentation process for conversion of cellulosic biomass to fuelethanol. Appl. Biochem. Biotechnol. 51–52, 117–124.

hilippidis, G., 1996. Cellulose bioconversion technology. In: Wyman, C.E. (Ed.),Handbook on Bioethanol: Production and Utilization. Taylor & Francis, Wash-ington, DC, pp. 253–285.

lanes, J., 1998. Lactic acid production: extractive fermentation in aqueous two-phase systems. University of Lund, PhD., Thesis, Lund, Sweden.

olman, K., 1994. Review and analysis of renewable feedstocks for the productionof commodity chemicals. Appl. Biochem. Biotechnol. 45, 709–722.

orro, D., Bianchi, M.M., Brambilla, L., Menghini, R., Bolzani, D., Carrera, V., Lievense,J., Liu, C.L., Ranzi, B.M., Frontali, L., Alberghina, L., 1999. Replacement of ametabolic pathway for large scale production of lactic acid from engineeredyeasts. Appl. Environ. Microbiol. 65, 4211–4215.

ortilla, O.M., Rivas, B., Torrado, A., Moldes, A.B., Domingues, J.M., 2008. Revalorisa-tion of vine trimming wastes using Lactobacillus acidophilus and Debaryomyceshansenii. J. Sci. Food Agric. 88, 2298–2308.

in, J., Wang, X., Zheng, Z., Ma, C., Tang, H., Xu, P., 2010. Production of l-lactic acid bya thermophilic Bacillus mutant using sodium hydroxide as neutralizing agent.Bioresour. Technol. 101, 7570–7576.

abelo, S.C., Filho, R.M., Costa, A.C., 2009. Lime pretreatment of sugarcane bagassefor bioethanol production. Appl. Biochem. Biotechnol. 153, 139–153.

amos, L.P., Saddler, J.N., 1994. Enzyme recycling during fed-batch hydrolysis ofcellulose derived from steam-exploded Eucalyptus viminalis. Appl. Biochem.Biotechnol. 45–46, 193–207.

otechnology 156 (2011) 286– 301

Reddy, G., Altaf, M.D., Naveena, B.J., Venkateshwar, M., Vijay Kumar, E., 2008. Amy-lolytic bacterial lactic acid fermentation—a review. Biotechnol. Adv. 26, 22–34.

Rezaei, F., Richard, T.L., Logan, B.E., 2008. Enzymatic hydrolysis of cellulose cou-pled with electricity generation in a microbial fuel cell. Biotechnol. Bioeng. 101,1163–1169.

Rojan, P.J., Nampoothiri, K.M., Nair, A.S., Pandey, A., 2005. l(+)-Lactic acid produc-tion using Lactobacillus casei in solid-state fermentation. Biotechnol. Lett. 27,1685–1688.

Romani, A., Yanez, R., Garrote, G., Alonso, J.L., 2008. SSF production of lactic acid fromcellulosic biosludges. Bioresour. Technol. 99, 4247–4254.

Saha, B.C., Nakamura, L.K., 2003. Production of mannitol and lactic acid by fer-mentation with Lactobacillus intermedius NRRL B-3693. Biotechnol. Bioeng. 82,865–871.

Saha, B.C., 2000. Alpha-l-arabinofuranosidases—biochemistry, molecular biologyand application in biotechnology. Biotechnol. Adv. 18, 403–423.

Saha, B.C., 2003. Hemicellulose bioconversion. J. Ind. Microbiol. Biotechnol. 30,279–291.

Saha, B.C., 2004. Lignocellulose biodegradation and applications in biotechnology.ACS Symp. Ser. 889, 2–34.

Saier, M.H., 1998. Multiple mechanisms controlling carbon metabolism in bacteria.Biotechnol. Bioeng. 58, 170–174.

Schick, J., Weber, B., Klein, J.R., Henrich, B., 1999. PepR1, a CcpA-like transcriptionregulator of Lactobacillus delbrueckii subsp. lactis. Microbiology 145, 3147–3154.

Schillinger, U., Lücke, F.K., 1987. Identification of lactobacilli from meat and meatproducts. Food Microbiol. 4, 199–208.

Schmidt, A.S., Thomsen, A.B., 1998. Optimization of wet oxidation pretreatment ofwheat straw. Bioresour. Technol. 64, 139–151.

Schmidt, S., Padukone, N., 1997. Production of lactic acid from wastepaper as acellulosic feedstock. J. Ind. Microbiol. Biotechnol. 18, 10–14.

Selig, M.J., Knoshaug, E.P., Adney, W.S., Himmel, M.E., Decker, S.R., 2008. Synergisticenhancement of cellobiohydrolase performance on pretreated corn stover byaddition of xylanase and esterase activities. Bioresour. Technol. 99, 4997–5005.

Senthuran, A., Senthuran, V., Hatti-Kaul, R., Mattiasson, B., 1999. Lactic acid produc-tion by immobilized Lactobacillus casei in recycle batch reactor: a step towardsoptimization. J. Biotechnol. 73, 61–70.

Sharma, N., Wati, L., Singh, D., 2003. Production of lactic acid during bioremediationof anaerobically digested molasses spent wash. Indian J. Microbiol. 43, 119–121.

Shen, X., Xia, L., 2004. Production and immobilization of cellobiase from Aspergillusniger ZU-07. Process Biochem. 39, 1363–1367.

Shen, X.L., Xia, L.M., 2006. Lactic acid production from cellulosic material bysynergetic hydrolysis and fermentation. Appl. Biochem. Biotechnol. 133,251–262.

Shibata, K., Flores, D.M., Kobayashi, G., Sonomoto, K., 2007. Direct l-lactic acidfermentation with sago starch by a novel amylolytic lactic acid bacterium, Ente-rococcus faecium. Enzyme Microb. Technol. 41, 149–155.

Singhvi, M., Joshi, D., Adsul, M., Varma, A., Gokhale, D., 2010. d-(−)-Lactic acid pro-duction from cellobiose and cellulose by Lactobacillus lactis mutant RM2-24.Green Chem. 12, 1106–1109.

Singleton, P., Sainsbury, D., 1987. Dictionary of Microbiology and Molecular Biology,2nd ed. John Wiley & Sons, New York.

Skory, C.D., 2003. Lactic acid production by Saccharomyces cerevisiae expressing aRhizopus oryzae lactate dehydrogenase gene. J. Ind. Microbiol. Biotechnol. 30,22–27.

Sreenath, H.K., Moldes, A.B., Koegel, R.G., Straub, R.J., 2001. Lactic acid production bysimultaneous saccharification and fermentation of alfalfa fiber. J. Biosci. Bioeng.92, 518–523.

Srivastava, A., Roychoudbury, P.K., Sashi, V., 1992. Extractive lactic acid fermentationusing ion-exchange resin. Biotechnol. Bioeng. 39, 607–613.

Stamer, J.R., 1976. Lactic acid bacteria. In: Defigueiredo, M.P., Spllittstoesser, D.F.(Eds.), Food Microbiology. Public Health and Spoilage Aspects, AVI PublishingCo. Inc., Westport, Connecticut, pp. 404–426.

Stulke, J., Hillen, W., 1999. Carbon catabolite repression in bacteria. Curr. Opin.Microbiol. 2, 195–201.

Sun, F., Chen, H., 2008. Enhanced enzymatic hydrolysis of wheat straw by aqueousglycerol pretreatment. Bioresour. Technol. 99, 6156–6161.

Sun, R., Lawther, J.M., Banks, W.B., 1995. Influence of alkaline pretreatments on thecell wall components of wheat straw. Ind. Crops Prod. 4, 127–145.

Sun, Y., Cheng, J., 2002. Hydrolysis of lignocellulosic materials for ethanol produc-tion: a review. Bioresour. Technol. 83, 1–11.

Taherzadeh, M.J., Karimi, K., 2007. Enzymatic-based hydrolysis processes for ethanolfrom lignocellulosic materials: a review. BioResources 2, 707–738.

Taherzadeh, M.J., Karimi, K., 2008. Pretreatment of lignocellulosic wastes to improveethanol and biogas production: a review. Int. J. Mol. Sci. 9, 1621–1651.

Takagi, M., 1984. Inhibition of cellulase by fermentation products. Biotechnol. Bio-eng. 26, 1506–1507.

Tanaka, K., Komiyama, A., Sonomoto, K., Ishizaki, A., Hall, S.J., Stanbury, P.F., 2002.Two different pathways for d-xylose metabolism and the effect of xylose con-centration on the yield coefficient of l-lactate in mixed-acid fermentation bythe lactic acid bacterium Lactococcus lactis IO-1. Appl. Microbiol. Biotechnol. 60,160–167.

Tanaka, T., Hoshina, M., Tanabe, S., Sakai, K., Ohtsubo, S., Taniguchi, M., 2006. Pro-

duction of d-lactic acid from defatted rice bran by simultaneous saccharificationand fermentation. Bioresour. Technol. 97, 211–217.

Tango, M.S., Ghaly, A.E., 2002. A continuous lactic acid production system using animmobilized packed bed of Lactobacillus helveticus. Appl. Microbiol. Biotechnol.58, 712–720.

l of Bi

T

T

T

T

T

T

T

T

T

T

V

v

v

V

V

V

V

V

V

W

W

W

W

M.A. Abdel-Rahman et al. / Journa

aniguchi, M., Hoshina, K., Tanabe, S., Higuchi, Y., Sakai, K., Ohtsubo, S., Hoshino,K., Tanaka, T., 2005. Production of l-lactic acid by simultaneous saccharificationand fermentation using unsterilized defatted rice bran as a carbon source andnutrient component. Food Sci. Technol. Res. 11, 400–406.

aniguchi, M., Tokunaga, T., Horiuchi, K., Hoshino, K., Sakai, K., Tanaka, T., 2004.Production of l-lactic acid from a mixture of xylose and glucose by co-cultivationof lactic acid bacteria. Appl. Microbiol. Biotechnol. 66, 160–165.

ashiro, Y., Kaneko, W., Sun, Y., Shibata, K., Inokuma, K., Zendo, T., Sonomoto, K., 2011.Continuous d-lactic acid production by a novel thermotolerant Lactobacillusdelbrueckii subsp lactis QU 41. Appl. Microbiol. Biotechnol. 89, 1741–1750.

ashiro, Y., Shinto, H., Hayashi, M., Baba, S., Kobayashi, G., Sonomoto, K., 2007. Novelhigh-efficient butanol production from butyrate by non-growing Clostridiumsaccharoperbutylacetonicum N1-4 (ATCC 13564) with methyl viologen. J. Biosci.Bioeng. 104, 238–240.

ashiro, Y., Takeda, K., Kobayashi, G., Sonomoto, K., Ishizaki, A., Yoshino, S., 2004.High butanol production by Clostridium saccharoperbutylacetonicum N1-4 in fed-batch culture with pH-stat continuous butyric acid and glucose feeding method.J. Biosci. Bioeng. 98, 263–268.

itgemeyer, F., Hillen, W., 2002. Global control of sugar metabolism: a Gram-positivesolution. Anton. Leeuw. Int. J. G. 82, 59–71.

okuhiro, K., Ishida, N., Kondo, A., Takahashi, H., 2008. Lactic fermentation of cel-lobiose by a yeast strain displaying �-glucosidase on the cell surface. Appl.Microbiol. Biotechnol. 79, 481–488.

sai, S.P., Moon, S.I.L., 1998. An integrated bioconversion process for productionof l-lactic acid from starchy potato feedstocks. Appl. Biochem. Biotechnol. 72,417–428.

suji, H., Fukui, I., 2003. Enhanced thermal stability of poly(lactide)s in the melt byenantiomeric polymer blending. Polymer 44, 2891–2896.

u, M., Saddler, J.N., 2010. Potential enzyme cost reduction with the addition of sur-factant during the hydrolysis of pretreated softwood. Appl. Biochem. Biotechnol.161, 274–287.

accari, G., Gonzalez-Vara, R.A.Y., Campi, A.L., Doci, E., Brigidi, P., 1993. Fermentativeproduction of l-lactic acid by Lactococcus lactis DSM20011 and product recoveryusing ion exchange resins. Appl. Microbiol. Biotechnol. 40, 23–27.

an Nispen, J.G.M., Jonker, R., 1991. Process for the fermentative preparation oforganic acids. US Patent, 5:002,881.

an Rooyen, R., Hahn-Hägerdal, B., La Grange, D.C., van Zyl, W.H., 2005. Construc-tion of cellobiose-growing and fermenting Saccharomyces cerevisiae strains. J.Biotechnol. 120, 284–295.

enkatesh, K.V., 1997. Simultaneous saccharification and fermentation of celluloseto lactic acid. Bioresour. Technol. 62, 91–98.

eyrat, A., Monedero, V., Perez-Martinez, G., 1994. Glucose transport by the phos-phoenolpyruvate: mannose phosphotransferase system in Lactobacillus caseiATCC 393 and its role in carbon catabolite repression. Microbiology 140,1141–1149.

iana, R., Monedero, V., Dossonnet, V., Vadeboncoeur, C., Perez-Martinez, G.,Deutscher, J., 2000. Enzyme I and HPr from Lactobacillus casei: their role in sugartransport, carbon catabolite repression and inducer exclusion. Mol. Microbiol.36, 570–584.

iana, R., Yebra, M.J., Galán, J.L., Monedero, V., Pérez-Martínez, G., 2005. Pleiotropiceffects of lactate dehydrogenase inactivation in Lactobacillus casei. Res. Micro-biol. 156, 641–649.

ickroy, T.B., 1985. Lactic acid. In: Blanch, H.W., Drew, S. (Eds.), ComprehensiveBiotechnology—The Principles, Applications and Regulation of Biotechnologyin Industry, Agriculture and Medicine, vol. 3. Pergamon Press, Toronto, pp.761–776.

onktaveesuk, P., Toyokawa, M., Ishlzaki, A., 1994. Stimulation of the rate of l-lactatefermentation using Lactococcus lactis IO-1 by periodic electrodialysis. J. Ferment.Technol. 77, 508–512.

ang, L., Zhao, B., Liu, B., Yu, B., Ma, C., Su, F., Hua, D., Li, Q., Ma, Y., Xu, P., 2010. Effi-cient production of l-lactic acid from corncob molasses, a waste by-productin xylitol production, by a newly isolated xylose utilizing Bacillus sp. strain.Bioresour. Technol. 101, 7908–7915.

ee, Y.J., Ryu, H.W., 2009. Lactic acid production by Lactobacillus sp. RKY2 in acell-recycle continuous fermentation using lignocellulosic hydrolyzates as inex-pensive raw materials. Bioresour. Technol. 100, 4262–4270.

ee, Y.J., Yun, J.S., Park, D.H., Ryu, H.W., 2004. Biotechnological production of l(+)

lactic acid from wood hydrolyzate by batch fermentation of Enterococcus faecalis.Biotechnol. Lett. 26, 71–74.

ooley, R., Ruth, M., Glassner, D., Sheehan, J., 1999. Process design and costingof bioethanol technology: a tool for determining the status and direction ofresearch and development. Biotechnol. Prog. 15, 794–803.

otechnology 156 (2011) 286– 301 301

Wu, X., Jiang, S., Liu, M., Pan, L., Zheng, Z., Luo, S., 2011. Production of l-lactic acid byRhizopus oryzae using semicontinuous fermentation in bioreactor. J. Ind. Micro-biol. Biotechnol. 38, 565–571.

Wyman, C.E., 1999. Biomass ethanol: technical progress, opportunities, and com-mercial challenges. Annu. Rev. Energy Environ. 24, 189–226.

Wyman, C.E., Dale, B.E., Elander, R.T., Holtzapple, M., Ladish, M.R., Lee, Y.Y., 2005.Coordinated development of leading biomass pretreatment technologies. Biore-sour. Technol. 96, 1959–1966.

Xavier, S., Lonsane, B.K., 1994. Sugarcane pressmud as a novel and inexpensive sub-strate for production of lactic acid in a solid state fermentation system. Appl.Microbiol. Biotechnol. 41, 291–295.

Yabannavar, V.M., Wang, D.I.C., 1991. Extractive fermentation for lactic acid produc-tion. Biotechnol. Bioeng. 37, 1095–1100.

Yanez, R., Alonso, J.L., Parajo, J.C., 2005. d-Lactic acid production from waste card-board. J. Chem. Technol. Biotechnol. 80, 76–84.

Yanez, R., Moldes, A.B., Alonso, J.L., Parajo, J.C., 2003. Production of d-(−)-lacticacid from cellulose by simultaneous saccharification and fermentation usingLactobacillus coryniformis subsp. torquens. Biotechnol. Lett. 25, 1161–1164.

Yang, B., Wyman, C.E., 2008. Pretreatment: the key to unlocking low-cost cellulosicethanol. Biofuels Bioprod. Bioref. 2, 26–40.

Yang, S.J., Kataeva, I., Hamilton-Brehm, S.D., Engle, N.L., Tschaplinski, T.J., Doeppke,C., Davis, M., Westpheling, J., Adams, M.W.W., 2009. Efficient degradation oflignocellulosic plant biomass, without pretreatment, by the thermophilic anaer-obe “Anaerocellum thermophilum” DSM 6725. Appl. Environ. Microbiol. 75,4762–4769.

Yang, T.H., Kim, T.W., Kang, H.Y., Lee, S.H., Lee, E.J., Lim, S.C., Oh, S.O., Song, A.J.,Park, S.J., Lee, S.Y., 2010. Biosynthesis of polylactic acid and its copolymers usingevolved propionate CoA transferase and PHA synthase. Biotechnol. Bioeng. 105,150–160.

Ye, K., Jin, S., Shimizu, K., 1996. Performance improvement of lactic acid fermentationby multistage extractive fermentation. J. Ferment. Bioeng. 81, 240–246.

Yu, Z.S., Zhang, H.X., 2004. Ethanol fermentation of acid-hydrolyzed cel-lulosic hyrolysate with Saccharomyces cerevisiae. Bioresour. Technol. 93,199–204.

Yun, J.S., Wee, Y.J., Kim, J.N., Ryu, H.W., 2004. Fermentative production of dl-lacticacid from amylase treated rice and wheat brans hydrolyzate by a novel lacticacid bacterium, Lactobacillus sp. Biotechnol. Lett. 26, 1613–1616.

Zaunmuller, T., Eichert, M., Richter, H., Unden, G., 2006. Variations in the energymetabolism of biotechnologically relevant heterofermentative lactic acid bac-teria during growth on sugars and organic acids. Appl. Microbiol. Biotechnol. 72,421–429.

Zhang, M.J., Su, R.X., Qi, W., He, Z.M., 2010a. Enhanced enzymatic hydrolysis of lig-nocellulose by optimizing enzyme complexes. Appl. Biochem. Biotechnol. 160,1407–1414.

Zhang, Q., Cai, W., 2008. Enzymatic hydrolysis of alkali-pretreated rice straw byTrichoderma reesei ZM4-F3. Biomass Bioenergy 32, 1130–1135.

Zhang, Y., Cong, W., Shi, S., 2010b. Application of a pH feedback-controlled sub-strate feeding method in lactic acid production. Appl. Biochem. Biotechnol. 162,2149–2156.

Zhang, Y., Cong, W., Shi, S.Y., 2011. Repeated fed-batch lactic acid production ina packed bed-stirred fermentor system using a pH feedback feeding method.Bioprocess Biosyst. Eng. 34, 67–73.

Zhang, Y., Pan, Z., Zhang, R., 2009. Overview of biomass pretreatment for cellulosicethanol production. Int. J. Agric. Biol. Eng. 2, 51–68.

Zhang, Y.H.P., Ding, S.Y., Mielenz, J.R., Cui, J.B., Elander, R.T., Laser, M., Michael, E.,Himmel, M.E., McMillan, J.R., Lynd, L.R., 2007. Fractionating recalcitrant ligno-cellulose at modest reaction conditions. Biotechnol. Bioeng. 97, 214–223.

Zheng, Y.Z., Lin, H.M., Tsao, G.T., 1998. Pretreatment for cellulose hydrolysis bycarbon dioxid explosion. Biotechnol. Prog. 14, 890–896.

Zhou, S., Grabar, T.B., Shanmugam, K.T., Ingram, L.O., 2006. Betaine tripled the vol-umetric productivity of d(−)-lactate by Escherichia coli strain SZ132 in mineralsalts medium. Biotechnol. Lett. 28, 671–676.

Zhou, J., Wang, Y.H., Chu, J., Luo, L.Z., Zhuang, Y.P., Zhang, S.L., 2009. Optimizationof cellulase mixture for efficient hydrolysis of steam-exploded corn stover bystatistically designed experiments. Bioresour. Technol. 100, 819–825.

Zhu, Y.M., Lee, Y.Y., Elander, R.T., 2007. Conversion of aqueous ammonia-treatedcorn stover to lactic acid by simultaneous saccharification and cofermentation.

Appl. Biochem. Biotechnol. 137-140, 721–738.

Zuniga, M., Champomier-Verges, M., Zagorec, M., Perez-Martinez, G., 1998. Struc-tural and functional analysis of the gene cluster encoding the enzymesof the arginine deiminase pathway of Lactobacillus sake. J. Bacteriol. 180,4154–4159.