Journal of Biotechnology 156 (2011) 286301

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

Review

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

a r t i c l e

i n f o

a b s t r a c t
Lactic acid is an industrially important product with a large and rapidly expanding market due to its attractive and valuable multi-function properties. The economics of lactic acid production by fermentation is dependent on many factors, of which the cost of the raw materials is very signicant. It is very expensive when sugars, e.g., glucose, sucrose, starch, etc., are used as the feedstock for lactic acid production. Therefore, lignocellulosic biomass is a promising feedstock for lactic acid production considering its great availability, sustainability, and low cost compared to rened sugars. Despite these advantages, the commercial use of lignocellulose for lactic acid production is still problematic. This review describes the conventional processes for producing lactic acid from lignocellulosic materials with lactic acid bacteria. These processes include: pretreatment of the biomass, enzyme hydrolysis to obtain fermentable sugars, fermentation technologies, and separation and purication of lactic acid. In addition, the difculties associated with using this biomass for lactic acid production are especially introduced and several key properties that should be targeted for low-cost and advanced fermentation processes are pointed out. We also discuss the metabolism of lignocellulose-derived sugars by lactic acid bacteria. 2011 Elsevier B.V. All rights reserved.

Article history: Received 2 February 2011 Received in revised form 31 May 2011 Accepted 17 June 2011 Available online 23 June 2011 Keywords: Lignocellulose-derived sugar Lactic acid production Lactic acid bacteria (LAB) Metabolic pathways Designed biomass

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

Corresponding author at: Laboratory of Microbial Technology, Division of Applied Molecular Microbiology and Biomass Chemistry, Department of Bioscience and Biotechnology, Faculty of Agriculture, Kyushu University, 6-10-1 Hakozaki, Higashi-ku, Fukuoka 812-8581, Japan. Tel.: +81 92 642 3019; fax: +81 92 642 3019. E-mail address: sonomoto@agr.kyushu-u.ac.jp (K. Sonomoto). 0168-1656/$ see front matter 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.jbiotec.2011.06.017

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3.

4. 5.

Fermentative lactic acid production by LAB . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Improvement of lactic acid production by LAB in the eld of microbial technology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Lactic acid production by LAB using lignocellulosic biomass and lignocellulose-derived sugars . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Metabolism of lignocellulose-derived sugars by LAB . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Designed biomass study and conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

291 291 292 295 296 297

1. Introduction Lactic acid (2-hydroxypropanoic acid, CH3 CH(OH)COOH) is a natural organic acid with a long history of use in the food and non-food industries, including the cosmetic and pharmaceutical industries, and for the production of oxygenated chemicals, plant growth regulators, and special chemical intermediates (Oshiro et al., 2009; Singhvi et al., 2010; Tashiro et al., 2011). Currently, there is an increased demand for lactic acid as a feedstock for the production of biopolymer poly-lactic acid (PLA), which is a promising biodegradable, biocompatible, and environmentally friendly alternative to plastics derived from petrochemicals. PLA has many uses in surgical sutures, orthopedic implants, drug delivery systems, and disposable consumer products (Adnan and Tan, 2007), and its use would signicantly alleviate waste disposal problems. The physical properties of PLA depend on the isomeric composition of lactic acid. Pure isomers, l- and d-lactic acid, are more valuable than the racemic dl form because each isomer has its own specic industrial application. l-Lactic acid is used for the synthesis of poly l-lactic acid (PLLA), a semi-crystalline biodegradable and thermostable polymer that has a potentially large market in goods packaging. PLLA has high tensile strength and low elongation with a high modulus that makes it suitable for medical products used in orthopedic xation (e.g., pins, rods, ligaments, etc.), cardiovascular applications (e.g., stents, grafts, etc.), dental applications, intestinal applications, and sutures (John et al., 2006a). d-Lactic acid is used for the production of poly d-lactic acid (PDLA) (John et al., 2009). These pure polymers are relatively heat sensitive, while stereocomplexes of PLLA and PDLA have a melting point 50 C higher than their respective pure polymers (Ikeda et al., 1987; Tsuji and Fukui, 2003) and are more biodegradable (de Jong et al., 2001; Tashiro et al., 2011). The ratio of l- and d-lactic acids inuences the properties and the degradability of PLA (Kharras et al., 1993). Lactic acid can be produced either by chemical synthesis or by microbial fermentation. Chemical synthesis from petrochemical resources always results in racemic mixture of dl-lactic acid, which is a major disadvantage of this approach (Hofvendahl and Hahn-Hgerdal, 2000). Conversely, microbial lactic acid fermentation offers an advantage in terms of the utilization of renewable carbohydrate biomass, low production temperature, low energy consumption, and the production of optically high pure lactic acid by selecting an appropriate strain (Ilmen et al., 2007; Pandey et al., 2001). Presently, almost all lactic acid produced globally is manufactured by fermentation routes. In particular, there have been numerous studies of lactic acid production by lactic acid bacteria (LAB) in comparison with other microorganisms. The demand for lactic acid has increased considerably due to its wide range of applications; however, the high cost of the raw materials, e.g., starch and rened sugars, which accounts for the highest portion of the production cost, represents one of the most serious obstacles for the fermentative production of lactic acid to compete with chemical synthesis (Datta et al., 1995). Cheap raw materials are essential for the feasibility of the biotechnological production of lactic acid because polymer producers and other industrial users usually require large quantities of lactic acid at a relatively low cost. The use of low-cost non-food materials for lactic acid production appears to be more attractive because they do not have

any impact on the human food chain. Nowadays, lignocellulosic materials from agricultural, agro-industrial, and forestry sources represent a potentially inexpensive and renewable carbohydrate feedstock for the large-scale fermentation of lactic acid due to their abundance, low price, high polysaccharide content, and renewability (Duff and Murray, 1996; Parajo et al., 1996; Taniguchi et al., 2005; Wyman, 1999). However, the cellulose and hemicellulose in lignocellulose are not directly available for bioconversion to lactic acid because of their intimate association with lignin (Schmidt and Thomsen, 1998) and the lack of hydrolytic enzymes in LAB (Tokuhiro et al., 2008). There have been numerous investigations on the development of biotechnological processes for lactic acid production, with the ultimate objective of making the process more effective and economical. In this review, we focus on the conventional processes for lactic acid fermentation by LAB from lignocellulosic biomass and lignocellulose-derived sugars. Moreover, we describe the limitations of lactic acid production using such materials. We also describe fermentative processes and technologies with practical examples, the metabolism of biomass-derived sugars, and the promising prospects of lactic acid fermentation. 2. Overview of lactic acid production from lignocellulosic biomass 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 820 109 tons of the primary biomass remains potentially accessible (Lin and Tanaka, 2006). Lignocellulosic biomass is organic material derived from a biological origin, and represents the most abundant global source of biomass that has been largely unutilized (Lin and Tanaka, 2006). It is mainly composed of cellulose (insoluble bers of -1,4-glucan), hemicellulose (noncellulosic polysaccharides including xylans, mannans, and glucans), and lignin (a complex polyphenolic structure), which form 90% of the dry matter, plus lesser amounts of minerals, oils, and other components (Balat, 2011; Molina-Sabio and Rodrguez-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 lignocellulosic material has varying amounts of these components because of genetic and environmental inuences and their interactions (Demirbas, 2005). The proportion of biomass constituents varies between species, and there are distinct differences between hardwoods and softwoods. The total content of cellulose and hemicellulose is higher in hardwoods (78.8%) than in softwoods (70.3%), but the total content of lignin is higher in softwoods (29.2%) than in hardwoods (21.7%) (Balat, 2009). As shown in Table 1, the cellulose, hemicellulose, and lignin content depends on the type of lignocellulosic biomass, which indicates that an appropriate material should be selected for the corresponding fermentation. Cellulose, the major component of plant biomass (3060% of total feedstock dry matter), is a homopolysaccharide composed of -d-glucopyranose units, linked by -(1 4)-glycosidic bonds.

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Table 1 The contents of cellulose, hemicellulose, and lignin in various types of lignocellulosic biomass (% dry weight).a Lignocellulosic materials Algae (green) Aspen hardwood Birch Hardwood Chemical pulps Coastal Bermuda grass Corn cobs Cornstalks Cotton seed hairs Cotton, ax, etc. Grasses Hardwood Hardwood barks Hardwood stems Leaves Newspaper Nut shells Paper Pine softwood Primary wastewater solids Softwood Softwood barks Softwood stems Solid cattle manure Sorted refuse Spruce softwood Swine waste Switch grass Waste papers from chemical pulps Wheat straw Willow Hardwood Cellulose (%) 2040 51 40 6080 25 45 3947 8095 8095 2540 45 2 2240 4055 1520 4055 2530 8599 44 815 42 2 1838 4550 1.64.7 60 43 6.0 45 6070 3741 37 Hemicellulose (%) 2050 29 39 2030 35.7 35 2631 520 520 2550 30 5 2038 2440 8085 2540 2530 0 26 NAb 27 2 1533 2535 1.43.3 20 26 28 31.4 1020 2732 23 Lignin (%) NAb 16 21 210 6.4 15 35 0 NAb 1030 20 4 3055 1825 0 1830 3040 015 29 2429 28 3 3060 2535 2.75.7 20 29 NAb 12.0 510 1315 21

Lignocellulosic biomass

Chemical/physical Pretreatment

Lignin

Hydrolyzed Hemicellulose

Cellulose

Enzymatic hydrolysis Mainly Pentoses Mainly Glucose

Fermentation

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

Separation

Lactic acid
The orientation of the linkages and additional hydrogen bonding make the polymer rigid and difcult to break. Hemicellulose (2040% of total feedstock dry matter) is a short, highly branched heterogeneous polymer consisting of pentose (xylose and arabinose), hexose (galactose, glucose, and mannose), and acid sugars (Saha, 2000). Mannose is the dominant hemicellulose sugar in softwoods, while xylose is dominant in hardwoods and agricultural residues (Taherzadeh and Karimi, 2008). Hemicellulose is more readily hydrolyzed compared to cellulose because of its branched and amorphous nature. Lignin (1525% of total feedstock dry matter) is an aromatic polymer synthesized from phenylpropanoid precursors. The phenylpropane units of lignin (primarily syringyl, guaiacyl, and phydroxy phenol) are bonded together by a set of linkages to form a very complex matrix (Demirbas, 2008). This complex matrix consists of a variety of functional groups, e.g., hydroxyl, methoxyl, and carbonyl groups, which impart a high polarity to the lignin macromolecule (Feldman et al., 1991). Lignin is considered to be difcult to use as a fermentation substrate because it makes the biomass resistant to chemical and biological degradation (Taherzadeh and Karimi, 2008). 2.2. Conventional processes for lactic acid production by LAB from lignocellulosic biomass Despite the advantages in its sustainability and availability, the commercial use of lignocellulose in lactic acid production is still problematic due to its complexity. The biochemical conversion of lignocellulosic biomass requires several processing steps designed to convert structural carbohydrates to monomeric sugars, e.g., glucose, xylose, arabinose, and mannose. These sugars
Fig. 1. A general ow chart of the conventional process for lactic acid production from lignocellulosic biomass materials.

can be fermented to lactic acid by wild-type and breeding strains, with varying degrees of effectiveness. Once the technologies are established and commercialized, a wide range of valuable products could be produced from lignocellulosic biomass. The conventional processes for producing lactic acid from lignocellulosic biomass include the following 4 main steps (Fig. 1): (1) Pretreatmentbreaking down the structure of the lignocellulosic matrix. (2) Enzymatic hydrolysisdepolymerizing lignocellulose to fermentative sugars, such as glucose and xylose, by means of hydrolytic enzymes. (3) Fermentationmetabolizing the sugars to lactic acid, generally by LAB. (4) Separation and purication of lactic acidpurication of lactic acid to meet the standards of commercial applications. 2.2.1. Pretreatment methods The enzymatic susceptibility of native lignocellulose is difcult and slow due to the association of cellulose and hemicellulose with lignin (Schmidt and Thomsen, 1998). The main goals of pretreatment are to remove lignin, separate cellulose and hemicellulose, increase the accessible surface area, partially depolymerize cellulose, and increase the porosity of the materials to aid in the subsequent access of the hydrolytic enzymes (Chandel et al., 2007; Hendriks and Zeeman, 2009; Kumar et al., 2009; Sun and

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Cheng, 2002; Taherzadeh and Karimi, 2007; Zhang et al., 2009). The hemicellulose should be removed or altered without degradation for a high ultimate yield of sugars (Mosier et al., 2005). Pretreatment includes physical (milling and grinding), chemical (alkali, dilute acid, oxidizing agents, and organic solvents), physicochemical (steam explosion/autohydrolysis, hydrothermolysis, and wet oxidation), and biological methods. Some methods disrupt the lignincarbohydrate complex, and other disrupts the highly ordered crystalline cellulose structure (Sun et al., 1995). Different pretreatment methods have been extensively developed, including ammonia ber explosion and ammonia recycle percolation (Jorgensen et al., 2007), lime (Kaar and Holtzaple, 2000), organosolv (Pan et al., 2006), liquid hot water (Antal, 1996), ionic liquid (Dadi et al., 2006), alkaline pretreatment (Lau et al., 2008), dilute acid and steam explosion (Laser et al., 2002; Mosier et al., 2005; Parisi, 1989; Yang and Wyman, 2008), and enzymatic treatment (Anderson et al., 2005; Converse, 1993; Hayn et al., 1993; Ladisch et al., 1983). Among these methods, dilute acid pretreatment is still the method of choice in several model processes (Wyman et al., 2005). The initial pretreatment reaction involves a mild acid-catalyzing hydrolysis of the glycosidic bonds of hemicellulose and the ether linkages in lignin (Fengel and Wegener, 1989), in which the organic acids, formed by the cleavage of labile ester groups, catalyze the hydrolysis of hemicellulose. Fractionation is achieved by the enlargement of the inner surface. The effects of different pretreatment methods upon different lignocellulosic materials, e.g., corn stover (Chen et al., 2009), wheat straw (Sun and Chen, 2008), switchgrass (Esteghlalian et al., 1997), rice straw (Zhang and Cai, 2008), and sugarcane bagasse (Rabelo et al., 2009), have been investigated. The pretreatment process is a very critical stage in lignocellulose bioconversion. If pretreatment is not sufciently efcient, the resultant residue is not easily saccharied by hydrolytic enzymes and, if it is too severe, toxic compounds can be produced that inhibit microbial metabolism and growth (Kodali and Pogaku, 2006). Therefore, pretreatment has a great potential to inuence the downstream costs by determining fermentation toxicity, enzymatic hydrolysis rates, enzyme loading, mixing power, product concentrations, product purication, waste treatment demands, power generation, and other process variables. An effective pretreatment process should meet the following requirements: (1) highly digestible pretreated solid; (2) no signicant degradation of sugars; (3) good recovery of high sugar concentrations; (4) sugar formation by subsequent enzymatic hydrolysis; (5) effective at low moisture contents; (6) form minimal or no microbial inhibitory by-products; (7) require minimal energy input; (8) high degree of simplicity; (9) not require biomass size reduction; (10) low cost materials for the construction of pretreatment reactors and to be easily managed at large volumes; (11) produce less residues; (12) consume few and cheap chemicals; and (13) have environmentally acceptable features (Galbe and Zacchi, 2007; Lynd, 1996; Sun and Cheng, 2002; Wu et al., 2011; Yang and Wyman, 2008). 2.2.2. Enzymatic hydrolysis Enzymatic hydrolysis is the most promising means to yield fermentable sugars from pretreated lignocellulosic biomass, and is necessary to allow LAB to utilize polysaccharides as a carbon source (Hinman et al., 1992; Lin and Tanaka, 2006; Lynd et al., 1996; Ogier et al., 1999; Taniguchi et al., 2005; Yu and Zhang, 2004). The goal of enzymatic hydrolysis is to depolymerize the polysaccharides in the water-insoluble solid fraction that remains after pretreatment. There are 2 general categories of enzymes necessary to convert cellulose and hemicellulose into soluble sugars: cellulases and hemicellulases, respectively. To maximize enzymatic hydrolysis, mixtures of these enzymes are needed to increase hemicellulose hydrolysis and thus increase the access of cellulase, leading to a

decreased hydrolysis time and process cost (hgren et al., 2007; Tu and Saddler, 2010; Zhang et al., 2010a). The rate of the enzymatic hydrolysis of cellulose is greatly affected by its degree of polymerization (Chang and Holtzapple, 2000; Cohen et al., 2005; Kumar et al., 2008). Efcient degradation and saccharication of cellulose require a synergistic reaction of the following 3 classes of cellulolytic enzymes: (a) Endo--1,4-glucanases (EG; EC 3.2.1.3): randomly hydrolyze accessible intramolecular -1,4-glucosidic bonds of cellulose chains and insert a water molecule in the -(1,4) bond, creating a new reducing and non-reducing chain end pair. (b) Exo--1,4-glucanases or cellobiohydrolases (CBH; EC 3.2.1.91): cleave cellulose chains at the ends of the polymer, releasing soluble cellobiose or glucose. (c) -Glucosidases (-G; EC 3.2.1.21) (cellobiases): complete the hydrolysis by cleaving cellobiose into 2 glucose molecules (Lynd et al., 2002) and thus relieve the system from end-product inhibition (Fujii et al., 1995). They are also active on cellooligosaccharides (Kumar et al., 2008). Individual cellulases have very limited hydrolytic activity, while a mixture of cellulases can exhibit a synergistic effect (Nidetzky et al., 1994; Zhang et al., 2007). Extensive research has been performed to improve the hydrolytic efciency of such enzymes (Baker et al., 1998; Mais et al., 2002; Selig et al., 2008). In addition to these 3 major groups of cellulases, accessory or helper enzymes that attack hemicellulose (Berlin et al., 2005) and lignin (Palonen and Viikari, 2004) may also play a role in hydrolysis by clearing the access of the main enzymes to cellulose. Unlike cellulose, xylans are chemically quite complex, and their degradation requires multiple enzymes. Enzymatic hydrolysis of hemicellulose requires endo-1,4--xylanase, -xylosidase, glucuronidase, -l-arabinofuranosidase, and acetylxylan esterase, which act on xylan degradation and saccharication (Carvalheiro et al., 2008; Saha, 2004), and -mannanase and -mannosidase, which cleave the glucomannan polymer backbone (Kumar et al., 2008). Although more enzymes are required for xylan hydrolysis than for cellulose hydrolysis, the substrate is more easily accessible because xylan does not form tight crystalline structures (Keshwani and Cheng, 2009). The hydrolytic efciency of a multi-enzyme mixture in the process of lignocellulose hydrolysis depends on the properties of the individual enzymes and their ratio in the multi-enzyme cocktail (Irwin et al., 1993; Zhou et al., 2009). Recently, Lin et al. (2011) constructed a cellulase cocktail for a more efcient enzymatic hydrolysis of lignocellulose and a more rational utilization of enzymes by using combinations of the 3 enzymes, 2 cellulases, and 1 xylanase. 2.2.3. Fermentation process with LAB The hydrolysate of a lignocellulosic biomass is a mixture of hexoses (e.g., glucose) and pentoses (e.g., xylose and arabinose). Lignin cannot be used for lactic acid fermentation. The effective utilization of cellulose- and hemicellulose-derived sugars can reduce the production cost of biomaterials by as much as 25% (Hinman et al., 1989). Fermentation technologies must be cost competitive with chemical synthesis to validate the use of biotechnological processes on an industrial scale (Bustos et al., 2007). The key economic drivers in the fermentation process are high product yields, productivity, and the concentration of products formed, which strongly inuences the product recovery costs. In order to achieve maximum lactic acid yield and productivity, a large number of studies have investigated lactic acid fermentation by LAB from lignocellulosic biomass in the eld of microbial technology, as described

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in detail in Section 3.2. Biomass materials have been used as substrates for lactic acid production by LAB, including lignocellulose/hemicellulose hydrolysates (Karel et al., 1997), cottonseed hulls (Vickroy, 1985), corncob (Guo et al., 2010; Moldes et al., 2006; Shen and Xia, 2006; Wang et al., 2010), corn ber hydrolysates and stalks (Saha and Nakamura, 2003; Vickroy, 1985), apple pomace (Gullon et al., 2008), wood hydrolysate (Wee et al., 2004), beet molasses (Gksungur and Gvenc , 1999; Kotzamanidis et al., 2002), sugar cane press mud and bagasse (Xavier and Lonsane, 1994; Laopaiboon et al., 2010), cassava bagasse (John et al., 2006a,b; Rojan et al., 2005), cellulose (Venkatesh, 1997; Singhvi et al., 2010), paper sludge (Marques et al., 2008), carrot processing waste (Pandey et al., 2001), molasses spent wash (Sharma et al., 2003), and wheat bran (John et al., 2006c; Naveena et al., 2005a,b). 2.2.4. Separation and purication of lactic acid In the traditional chemical separation process, the fermentation broth is rst neutralized by calcium carbonate. The calcium lactatecontaining broth is then ltered to remove cells, carbon treated, decolored, evaporated, and acidied with sulfuric acid to produce lactic acid and insoluble calcium sulfate (Datta and Henry, 2006). Pure lactic acid is further obtained by hydrolysis, esterication, and distillation. The disadvantages of this process include the production of a large amount of calcium sulfate (gypsum) as a by-product and high sulfuric acid consumption (Qin et al., 2010). Other alternative lactic acid separation technologies such as adsorption (Chen and Ju, 1998), reactive distillation (Kumar et al., 2006), ultraltration and electrodialysis (Choi et al., 2002; Datta and Henry, 2006; Hbov et al., 2004; Kim and Moon, 2001; Madzingaidzo et al., 2002), and nanoltration (Gonzalez et al., 2008; Li and Shahbazi, 2006) have also been studied as lactic acid separation and purication processes that do not yield salt waste. These separation processes are more cost and energy efcient when compared with traditional chemical separation processes. In addition, they have several advantages including the lack of energy-intensive phase changes or potentially expensive solvents or adsorbents as well as the potential for the simultaneous separation and concentration of lactic acid (Li et al., 2008). 2.3. Difculties in using lignocellulosic biomass for efcient lactic acid production by LAB The effective utilization of lignocellulosic biomass has some inherent limitations due to its seasonal availability, scattered distributions, and the high costs of storage and transportation (Lin and Tanaka, 2006; Polman, 1994). In addition, the main problems encountered in the efcient conversion of lignocellulosic biomass to lactic acid are: (a) the resistant nature of biomass and pretreatment problems; (b) high cost enzymes and their feedback inhibition; (c) formation of by-products due to the heterofermentation of pentose sugars; and (d) carbon catabolite repression caused by the heterogeneity of hydrolysate-sugar composition. These obstacles are briey discussed as follows: 2.3.1. Resistant nature of biomass and pretreatment problems Crystalline nonreactivity and, in particular, resistance to hydrolysis are the major problems for efcient lignocellulose utilization (Kumar et al., 2008). Although various pretreatment procedures have been evaluated, its utilization is a major drawback and affects the total economy of the bioconversion of lignocellulosic biomass (Zhang et al., 2009). Pretreatment is an expensive step and has a major inuence on the cost of the enzymatic hydrolysis and fermentation processes (Lynd et al., 1996; Wooley et al., 1999). Also, lignin limits the rate of cellulose hydrolysis by acting as a physical barrier that prevents the digestible parts of the substrate from being hydrolyzed (Chang and Holtzapple, 2000; Esteghlalian et al.,

2001). Different strategies have been examined to overcome the nonproductive adsorption of lignin to cellulase by alkali extraction and the addition of proteins or other additives, e.g., polyethylene glycol and Tween (Brjesson et al., 2007; Pan et al., 2005). Another obstacle is the release of inhibitory compounds during the pretreatment process. Although the composition of the released compounds depends not only on the type of lignocellulosic material and the chemistry but also on the characteristics of the pretreatment process. These inhibitory compounds interfere with the hydrolysis of cellulosic substrates by cellulase (MesHartree et al., 1987). In addition, many potentially inhibitory compounds released by pretreatment processes have been identied for the microorganisms used for fermentation (Mussatto and Roberto, 2004; Palmqvist and Hahn-Hgerdal, 2000). Although detoxication methods such as bioabatement (Lopez et al., 2004; Nichols et al., 2005) and overliming (Nilvebrant et al., 2003) have been proposed, the efciency of fermentation is still in need of improvement. The isolation of superior LAB strains or genetically engineered strains that are resistant to inhibitors, and advances and improvements in the pretreatment of lignocellulose are still needed to reduce the overall cost. Recently, wild-type Lactobacillus brevis S3F4 was shown to have strong resistance to fermentation inhibitors such as ferulic acid and furfural (Guo et al., 2010). Biological delignication with white rot fungi, which selectively degrade lignin and leave cellulosic materials, also has potential advantages such as low-capital cost, low-energy input, no chemical requirements, mild environmental conditions, and high yields without generating polluting by-products (Chaudhary et al., 1994; Kuhad and Johri, 1992; Kumar et al., 2009). However, drawbacks of this process include its long treatment period and low hydrolysis rate (Kumar et al., 2008; Sun and Cheng, 2002). 2.3.2. High-cost enzymes and their feedback inhibition The high costs of enzyme production, feedback inhibition, and the excessive enzymatic dosages necessary to hydrolyze pretreated biomass are some of the drawbacks limiting the commercial application of lignocellulose hydrolysis as a lignocellulosic-lactate industry (Himmel et al., 1999; Wooley et al., 1999). During cellulose saccharication, the sugar end products of hydrolysis do not accumulate quickly because the saccharied glucose and cellobiose inhibit the EG and CBH activities by feedback inhibition (Adsul et al., 2007b; Ghosh and Das, 1971; Holtzapple et al., 1990; Lee and Fan, 1983). Several methods have been developed to reduce this inhibition, including the improvement of -G activity in the cellulase system (Shen and Xia, 2004), removing the released sugars during hydrolysis by ultraltration or simultaneous saccharication and fermentation (SSF) (Rezaei et al., 2008), optimizing cellulase enzyme conditions (i.e., temperature, pH, and enzyme loading amounts) (Sun and Cheng, 2002; Ou et al., 2009), or supplying -G during hydrolysis to avoid cellobiose accumulation (Caminal et al., 1985; Moldes et al., 2001; Ramos and Saddler, 1994). Studies to remove such forms of inhibition are still in progress. 2.3.3. Formation of by-products due to the heterofermentation of pentose sugars Lignocellulosic hydrolysates contain not only hexoses but also pentoses. Hexoses can easily be fermented by LAB, while pentose sugars cannot be fermented by most LAB (Hofvendahl and Hahn-Hgerdal, 2000; Tanaka et al., 2002). In general, a few LAB metabolize pentose sugars via the phosphoketolase (PK) pathway, which exhibits heterofermentation with equimolar amounts of lactic acid and acetic acid produced and reaches only 0.60 C-mol/C-mol in terms of the theoretical yield of lactic acid to pentose sugars (Abdel-Rahman et al., 2011b; Oshiro et al., 2009; Patel et al., 2006; Tanaka et al., 2002). This co-production of acetic acid and lactic acid also results in an increase of the lactic acid purication cost (Garde

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et al., 2002; Patel et al., 2006); therefore, this approach is not conducive for the industrial fermentation of pentoses to lactic acid. To overcome this obstacle, we previously isolated a LAB strain, Lactococcus lactis IO-l, which could utilize xylose with a high lactate yield and low acetate production (Tanaka et al., 2002). Okano et al. (2009a,b) engineered the LAB Lb. plantarum strain to produce lactic acid from xylose and arabinose via the pentose phosphate (PP) pathway, leading to homolactate production. Recently, we reported that a novel LAB, Enterococcus mundtii QU 25, consumed xylose homofermenatively without acetate production (Abdel-Rahman et al., 2010a, 2011b); therefore, the purication cost will be signicantly decreased with this strain. 2.3.4. Carbon catabolite repression caused by the heterogeneity of the hydrolysate-sugar composition One of the major obstacles in using lignocellulosic biomass as a feedstock is the inherent heterogeneity of its sugar composition (Kim et al., 2010a). To achieve maximum product yield and productivity, the complete utilization of these sugars is essential (Kim et al., 2010b; Saha, 2003). In many LAB, fermentation of mixed carbohydrates is achieved sequentially, whereby the utilization of glucose represses the consumption of alternative sugars due to carbon catabolite repression (Saier, 1998; Stulke and Hillen, 1999; Titgemeyer and Hillen, 2002). This sequential utilization of mixed sugars makes the fermentation process complex and often reduces the yield and productivity (Bothast et al., 1999). Carbon catabolite repression by LAB has been reported in many strains, e.g., Lb. casei (Gosalbes et al., 1999; Veyrat et al., 1994; Viana et al., 2000), Lb. pentosus (Chaillou et al., 1999, 2001; Mahr et al., 2000), Lb. plantarum (Marasco et al., 1998), Lb. sakei (Zuniga et al., 1998), and Lb. delbrueckii (Morel et al., 1999; Schick et al., 1999). A few LAB strains have been reported to simultaneously consume lignocellulosederived sugars, e.g., Lb. brevis (Guo et al., 2010; Kim et al., 2009), Lb. plantrum (Guo et al., 2010), and our newly isolated strain E. mundtii QU 25 (Abdel-Rahman et al., 2010a,b, 2011a). Mixed LAB cultures have also been used to maximize the yield and productivity from mixed sugars (Cui et al., 2011; Taniguchi et al., 2004). Therefore, it is essential to isolate LAB strains or to establish genetically engineered strains for efcient lignocellulose utilization. 3. Fermentative lactic acid production by LAB 3.1. Improvement of lactic acid production by LAB in the eld of microbial technology It has generally been observed that pH, nutrient concentration, substrate concentration, end products concentration, and temperature signicantly affect the growth of LAB and lactic acid production. These factors may decrease cell density and the lactic acid titer, yield, and productivity in some cases. Researchers in the eld of microbial technology have conducted numerous studies to establish an efcient method of lactic acid production by LAB. In lactic acid fermentation, low pH has an inhibitory effect on cellular metabolism and lactic acid production. The majority of LAB cannot grow below pH 4, although the pKa of lactic acid is 3.78 (Adachi et al., 1998); therefore, neutralizing agents such as calcium carbonate, sodium hydroxide, or ammonium hydroxide must be added to keep the pH at a constant value in order to reduce the inhibitory effects of low pH. pH-controlled batch fermentation signicantly improves lactic acid production, yield, and productivity by different LAB strains, e.g., Lb. delbrueckii (Tashiro et al., 2011), E. mundtii QU 25 (Abdel-Rahman et al., 2011a,b), and E. faecium (Shibata et al., 2007). Batch fermentation is a simple closed culture system that contains an initial and limited amount of nutrient, and nothing is added during fermentation except possibly acid

or alkali for pH control. The low levels of nutrient limit the cell concentration, nal lactic acid concentration, and productivity. It was reported that the addition of nutrients to a culture broth of E. mundtii QU 25 during batch fermentation increased the cell mass and lactic acid production and productivity (Abdel-Rahman et al., 2011a). In addition, batch fermentation was superior to continuous fermentation in some respects, particularly lactic acid titer (Buyukgungor and Bueschelberger, 1986; Hofvendahl and HahnHgerdal, 2000; Nomura et al., 1987). High lactic acid production has been obtained with batch fermentation of LAB with the production of 150 g/L l-lactate from glucose (Bai et al., 2004), 87.2 g/L d-lactate from glucose (Tashiro et al., 2011), and 119 g/L l-lactate (Abdel-Rahman et al., 2011a) and 80 g/L d-lactate (Joshi et al., 2010) from cellobiose. Substrate inhibition always occurs at high sugar concentrations (Ding and Tan, 2006; Gatje and Gottschalk, 1991; Oshiro et al., 2009). To overcome or reduce substrate inhibition, fed-batch cultures were a better fermentation system than batch and continuous cultures because they allow for an increased maximum viable cell concentration and prolonged culture lifetime, which result in product accumulation to a higher concentration. Bai et al. (2004) developed a process for the production of ammonium lactate with Lb. lactis in pH-controlled fed-batch fermentation with 161.2 g/L of lactic acid. Ding and Tan (2006) developed a high lactic acid concentration process using 4 different fed-batch feeding strategies with Lb. casei: pulse fed-batch, constant feed rate fed-batch, constant residual glucose concentration fed-batch, and exponential feed rate fed-batch fermentations. They generated up to 210 g/L of lactic acid and a 97% yield with an exponential rate of feeding glucose solution and yeast extract (Ding and Tan, 2006). However, in all fed-batch technologies, the substrate concentration in the fermentation broth is unstable, thereby generating more stress on the producing strain. Recently, a method was developed to control the concentration of the substrate through the automatic adjustment of pH. Using this method, 96.3 g/L and 170 g/L of lactic acid were obtained with Lb. lactis-11 (Zhang et al., 2010b) and Lb. rhamnosus LA-04-1 (Li et al., 2010), respectively. Chang et al. (2011) suggested multi-stage continuous high cell density culture as a new production platform for obtaining high lactic acid titers (212.9 g/L) and productivity (10.6 g L1 h1 ) with Lb. rhamnosus. In addition to fedbatch fermentation, continuous and semi-continuous fermentation processes have been used for lactic acid production by reducing substrate inhibition (Amrane and Prigent, 1996; Nolasco-Hipolito et al., 2002; Tashiro et al., 2011). The choice of the most suitable fermentation process will depend upon the kinetic properties of the LAB species used, the type of substrates, and the economic aspects of the process. High productivity was achieved with a high LAB cell density without reducing the yield (Ohleyer et al., 1985). Many reports showed that high cell density by cell recycling through ltration drastically increased lactic acid productivity with Lb. helveticus (Kulozik and Wilde, 1999), E. faecium (Shibata et al., 2007), and Lb. delbrueckii (Tashiro et al., 2011). The cell recycling system, along with repeated batch and continuous processes, generated a high cell concentration and productivity in these processes (Kwon et al., 2001; Oh et al., 2003). The immobilization of cells has been one of the means used for high cell retention in bioreactors; however, many studies were not very successful in terms of yield and productivity (Cotton et al., 2001; Gksungur and Gvenc , 1999; Senthuran et al., 1999; Zhang et al., 2011). One of the major problems associated with lactic acid production by fermentation is end-product inhibition; therefore, to decrease the inhibitory effect of lactic acid during fermentation, it must be selectively removed from the fermentation broth. Many attempts have been directed to develop processes that remove lactic acid from the fermentation broth, e.g., extraction from the

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fermentation broth (Hano et al., 1993; Honda et al., 1995; Iyer and Lee, 1999a,b; Yabannavar and Wang, 1991; Ye et al., 1996), electrodialysis (Boyaval et al., 1987; Hongo et al., 1986; Kim and Moon, 2001; Min-Tian et al., 2005; Nomura et al., 1998; van Nispen and Jonker, 1991; Vonktaveesuk et al., 1994), and nanoltration membranes and ion exchange resins (Jeantet et al., 1996; Monteagudo and Aldavero, 1999; Srivastava et al., 1992; Vaccari et al., 1993). The continuous removal of lactic acid with extraction or electrodialysis results in even higher lactic acid concentrations and yields compared to conventional batch fermentation processes. Li et al. (2004) developed a bioreactor combining conventional electrodialysis and bipolar membrane electrodialysis for product removal and pH control in lactic acid fermentation. Min-Tian et al. (2005) achieved high lactic acid productivity and yields with a continuous electrodialysis fermentation system. Even though these methods lower the purication cost, the price of the membranes and decreases in the permeate ow rate make the process less cost efcient and are still considerable drawbacks. Other methods, e.g., two phase systems, have been developed; however, the extracting material must be biocompatible and not harm the organism in order to be efcient (Planes, 1998). The inuence of temperature on lactic acid fermentation is related to the growth kinetic parameters of LAB, lactic acid production, and substrate consumption. Among LAB, most lactic acid productivity studies have been conducted at temperatures of 3043 C. We recently isolated a new LAB strain, Lb. delbrueckii QU 41, that exhibits a high thermotolerance and produces d-lactic acid at temperatures 50 C (Tashiro et al., 2011). 3.2. Lactic acid production by LAB using lignocellulosic biomass and lignocellulose-derived sugars Separate hydrolysis and fermentation (SHF) is a process with separate enzymatic hydrolysis and fermentation steps. The main advantage of SHF is the ability to carry out each step under optimal conditions for each process. However, the main disadvantage of this method is the feedback inhibition of saccharied sugars, e.g., glucose, xylose, cellobiose, and other oligosaccharides, on the activity of hydrolytic enzyme during the hydrolysis process, which demands lower loadings of the lignocellulosic biomass and higher loadings of the hydrolytic enzymes to achieve reasonable yields (Jeffries and Jin, 2000; Philippidis, 1996). In addition, this 2-step process increases the total processing time. To overcome these problems, SSF for lactic acid production by LAB has been developed as described in detail below. In comparison with SHF, SSF offers many advantages, including: (1) reduced reactor volume due to the usage of only a single reactor; (2) rapid processing time; (3) reduced feedback inhibition; (4) increased productivity; (5) enhanced rate of hydrolysis; (6) lower enzyme loading; and (7) higher lactic acid yields (Ehrman and Himmel, 1994; Hofvendahl and Hahn-Hgerdal, 2000; Iyer and Lee, 1999a,b; John et al., 2006c; Linko and Javanainen, 1996; Moritz and Duff, 1996; Sun and Cheng, 2002; Tsai and Moon, 1998; Zheng et al., 1998). SSF technology is a good strategy for lactic acid production by LAB from renewable bioresources such as lignocellulosic materials. In SSF, cellulases and xylanases convert the lignocellulosic materials to fermentable sugars. These enzymes are notoriously susceptible to feedback inhibition by the saccharied sugars, e.g., glucose, xylose, cellobiose, and other oligosaccharides (Jeffries and Jin, 2000). As described above, one of the advantages of SSF is that the immediate consumption of sugars by microorganism maintains the sugar concentration at a low level in the bioreactor, thereby signicantly reducing feedback inhibition (Balat et al., 2008; Mosier et al., 2005). In SSF, hydrolysis is usually the rate-limiting process (Philippidis and Smith, 1995). SSF with cellulose has been studied with Lb. delbrueckii (Abe and Takagi, 1991) and Lb. rhamnosus

(Parajo et al., 1997; Schmidt and Padukone, 1997). Other studies have reported lactic acid production by SSF from lignocellulosic biomasses such as corncob, waste wood, wheat straw, and alfalfa ber (Adenis et al., 1999; Cui et al., 2011; Garde et al., 2002; Jun et al., 1998; Lee et al., 2004; Miura et al., 2004; Moldes et al., 1999; Romani et al., 2008; Sreenath et al., 2001; Yanez et al., 2003). SSF technology with lignocellulosic materials needs to be further improved, including the co-fermentation of multiple sugar substrates, i.e., the saccharication of cellulose to glucose and hemicellulose to xylose, and the fermentation of saccharied glucose and xylose. Compared to SHF, the disadvantages of SSF lie in the different temperatures and pH optima required for saccharication and fermentation (Krishna et al., 2001; Huang et al., 2005), and the inhibition of enzyme function by lactic acid. In general, the optimal conditions for enzymatic hydrolysis and lactic acid fermentation are 50 C and 3743 C, and a pH < 5.0 and 5.07.0, respectively (Hofvendahl and Hahn-Hgerdal, 2000). To perform SSF more efciently, thermotolerant LAB are expected to raise the temperature close to the optimal hydrolysis temperature, as have succeeded in high lactic acid production with SSF technology by thermotolerant Bacillus coagulans (Ou et al., 2009, 2011). In addition, Iyer and Lee (1999a) studied the effect of lactic acid on the enzymatic hydrolysis of cellulose in SSF. They found that the enzymatic digestibility decreased from 79% to 56% as the lactic acid concentration increased from 0 to 90 g/L. At levels higher than 90 g/L lactic acid, they observed a 50% inhibition of the digestibility. However, the inhibition of enzymatic hydrolysis by lactic acid is much lower than the feedback inhibition caused by glucose buildup (Takagi, 1984). Depending on the source of lignocellulosic biomass (Table 1), hemicellulose forms a substantial fraction of the lignocellulosic biomass as well as cellulose, which yields pentose sugars such as xylose and arabinose by saccharication. The majority of LAB strains, e.g., Lb. delbrueckii (Monteagudo et al., 1997), Lb. helveticus (Tango and Ghaly, 2002), and Lb. acidophilus (Portilla et al., 2008), can convert cellulose-derived glucose to lactic acid, but not hemicellulose-derived sugars. Others are capable of utilizing pentose sugars for lactic acid production, including Lb. pentosus ATCC 8041 (Bustos et al., 2005; Zhu et al., 2007), Lb. bifermentans DSM 20003 (Givry et al., 2008), Lb. brevis (Chaillou et al., 1998), Lb. plantarum (Helanto et al., 2007), Leuconostoc lactis (Ohara et al., 2006), Lc. lactis (Tanaka et al., 2002), and E. mundtii QU 25 (Abdel-Rahman et al., 2010a, 2011b). Recently, Okano et al. (2009a,b) succeeded in replacing the PK pathway with the PP pathway in Lb. plantarum ldhL1 in order to obtain a higher yield and production of d-lactic acid from xylose and arabinose with very low amounts of by-products. Among the LAB reported so far, only the wild-type E. mundtii QU 25 (Abdel-Rahman et al., 2011a,b) and the genetically modied Lb. plantarum ldhL1 (Okano et al., 2009a,b) can perform homo-lactate fermentation of pentose sugars, which is expected to generate signicant levels of lactic acid production from lignocellulosic biomass. To date, direct lactic acid fermentation from xylan or cellulose has not been demonstrated, and very few studies have examined lactic acid production from xylooligosaccharides and cellooligosaccharides. Leu. lactis SHO-47 and SHO-54 were reported to assimilate xylooligosaccharides from disaccharides to hexasaccharides to produce d-lactic acid (Ohara et al., 2006). Recently, lactic acid production from cellobiose with LAB has been established, including Lb. delbrueckii mutant Uc-3 (Adsul et al., 2007b), Lb. plantarum (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 lactic acid production from cellooligosaccharides. Adsul et al. (2007b) used the Lb. delbrueckii mutant Uc-3 strain for the utilization of cellotriose, while Okano et al. (2010a) developed genetically mod-

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

ied Lb. plantarum for cellotriose and cellopentaose fermentation to produce lactic acid. As mentioned above, lignocellulosic biomass yields several types of sugars by hydrolysis, e.g., glucose, cellooligosaccharides,

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

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Table 2 Lactic acid production from lignocellulosic biomass materials and lignocellulose-derived sugars by lactic acid bacteria. Microorganism E. mundtii QU 25 Substrate Cellobiose Xylose Glucose/cellobiose Glucose/xylose Glucose/xylose/cellobiose Wood hydrolysate Xylose and glucose Wheat bran hydrolysate Corncob Wheat straw hemicellulose Cassava bagasse Soft wood Cellulose Pretreated cardboard Alfalfa bers Cellulose Defatted rice bran Cellobiose Molasses Cassava bagasse Sugar cane bagasse Brewers spent grain Corn cob residue Date juice Cellobiose -Cellulose Vine shoots Barley bran husks hydrolysates Corncob Vine-trimming wastes Corn stover Alfalfa bers -Glucan/cellopentaose/cellohexaose Ferment. process Batch Batch Batch Batch Batch Batch Batch Batch with cell immobilization Batch Batch Batch SSF Batch SSF Batch SSF SSF SSF SSF Batch Batch Batch SSF Batch SSF Batch Batch/continuous Batch Batch SSF Batch Batch Batch Batch Fed-batch SSF SSF Batch CLA a (g/L) 119 86.7 35.1 93.0 95.0 62.8 39.1 7.1 83.8 21.123.75 54.0 23.4 35.4 65.0 28.0 90.0 166 81.9 67.0 35.5 48.7/44.2 60.3 80.0 73.0 24.0 33.0 26.0 74.8 46.4 1.47/ 1.27/ 1.27 38.6 41.2 20.95 73.0 32.5 39.4 129 27.0 33.26 10.9 2.3 YLA b (g/g) 0.83 0.84 0.91 0.83 0.79 0.93 0.83 0.70 0.95 0.96 0.740.83 0.89 0.56 0.35 0.18 0.28 0.90 0.95 0.94 0.83 0.99 0.95/0.92 0.8 0.73 0.76 0.57 0.53 0.77 0.65 0.46 0.82 0.89 0.70 0.97 0.88 0.36 0.95 0.9 0.68 0.36 PLA c (g L1 h1 ) 1.12 0.90 2.99 3.6d 2.6d 1.7 1.17 0.81 1.40 0.150.23 0.5 0.48 0.75 0.77 2.25 4.15 1.36 0.93 0.59 1.01/5.7 3.2d 1.66 1.52 0.51 0.60 0.34 0.84 0.64 3.78d 1.6d 0.58 2.9 5.41 0.82 2.9 6.7 0.17 Reference Abdel-Rahman et al. (2011a) Abdel-Rahman et al. (2010a, 2011b) Abdel-Rahman et al. (2010b, 2011a) Abdel-Rahman et al. (2010b) Abdel-Rahman et al. (2010b) Wee et al. (2004) Taniguchi et al., 2004 Givry et al. (2008) Guo et al. (2010) Garde et al. (2002) John et al. (2006a) Iyer et al. (2000) Yanez et al. (2003) Yanez et al. (2005) Sreenath et al. (2001) Iyer and Lee (1999a,b) Tanaka et al. (2006) Adsul et al. (2007b) Dumbrepatil et al. (2008) John et al. (2006a) Adsul et al. (2007a) Mussatto et al. (2008) Shen and Xia (2006) Nancib et al., 2009 Singhvi et al. (2010) Singhvi et al. (2010) Moldes et al. (2006) Moldes et al. (2006) Moldes et al. (2006) Bustos et al. (2004) Zhu et al. (2007) Sreenath et al. (2001) Okano et al. (2010a)

E. faecalis RKY1 E. casseliavus and Lb. casei Lb. bifermentans DSM 20003 Lb. brevis Lb. brevis and Lb. pentosus Lb. casei NCIMB 3254 Lb. casei subsp rhamnosus Lb. coryniformis ATCC 25600 Lb. coryniformis spp. torquens ATCC 25600 Lb. delbreuckii Lb. delbreuckii NRRL-B445 Lb. delbrueckii IFO 3202 Lb. delbrueckii mutant Uc-3 Lb. delbrueckii NCIM 2025 Lb. delbrueckii subsp. delbrueckii Mutant Uc-3 Lb. delbrueckii UFV H2B20 Lb. delbrueckii ZU-S2 Lb. casei and Lb. lactis Lb. lactis RM 2-24 Lb. pentosus

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Lb. pentosus ATCC 8041 Lb. planlarum Lb. plantarum (Recombinant)

Lb. plantarum (Recombinant) Lb. plantarum (Recombinant) Lb. rhamnosus and Lb. brevis Lb. rhamnosus ATCC 7469 Lb. rhamnosus ATCC 9595 (CECT288) Lactobacillus sp. RKY2

Arabinose Xylose Corn stover Paper sludge Apple pomace Cellulosic biosludge Rice and wheat bran Lignocellulosic hydrolysates Xylose Sugar cane baggase Hydrolyzed xylan (Xylooligosaccharides)

Lc. lactis IO-1 Leuconostoc lactis SHO-47 and SHO-54

Batch Batch SSF Batch SSF Batch SSF Batch Continuous with cell-recycle Batch Batch Batch

Okano et al. (2009a) Okano et al. (2009b) Cui et al. (2011) Marques et al. (2008) Gullon et al. (2008) Romani et al. (2008) Yun et al. (2004) Wee and Ryu (2009) Tanaka et al. (2002) Laopaiboon et al. (2010) Ohara et al. (2006)

E, Enterococcus; Lb, Lactobacillus; Lc, Lactococcus; SSF, simultaneous saccharication 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.

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Fig. 3. A ow chart of the approaches used for useful substance production from renewable resources in a recent study and a designed biomass study.

and xylose) with the production of lactate, acetate, and ethanol (Liu et al., 2009). Lc. lactis IO-1 has been used to convert glucose, xylose, and arabinose in sugarcane bagasse hydrolysates to a mixture of lactic acid, acetic acid, formic acid, and ethanol (Laopaiboon et al., 2010). Marques et al. (2008) used Lb. rhamnosus ATCC 7469 to produce lactic acid from short ber cellulose of paper sludge by SSF without any pretreatment, and obtained a lactic acid yield of 0.97 g/g carbohydrates and a productivity of 2.9 g L1 h1 (Marques et al., 2008). SSF of Lb. rhamnosus ATCC 9595 with kraft pulp mill biosludge also produced lactic acid with a yield of 0.38 g/g biosludge and a productivity of 0.87 g L1 h1 (Romani et al., 2008). Several authors have reported biotechnological lactic acid production from lignocellulosic materials, agricultural waste, and forestry, industrial, or municipal solid materials, e.g., unpolished rice (Lu et al., 2009), defatted rice bran (Tanaka et al., 2006), and waste cardboard (Yanez et al., 2005). Recently, in order to increase the conversion efciency of substrates, co-cultures of LAB (e.g., E. casseliavus and Lb. casei or Lb. casei and Lc. lactis) have been reported from lignocellulose-derived mixed sugars (Cui et al., 2011; Nancib et al., 2009; Taniguchi et al., 2004). Lactic acid fermentation from various types of lignocellulosic biomass materials and lignocellulose-derived sugars by LAB strains were achieved with different fermentation modes, as summarized in Table 2. As a result of these kinds of fermentation, cellulose- and hemicellulose-derived sugars from lignocellulosic biomass can be utilized with higher efciency and productivity; however mixed sugar cultures have not been used on an industrial scale because of their many limitations. In mixed sugar cultures, the strains used do not always have similar optimum culture conditions for pH, temperature, nutrients, oxygen demand, etc.; therefore, it is not easy to dene the optimum condition or to maintain stable conditions for such cultures during fermentation, and corresponding studies are scarce. The discovery of LAB that have the capability to homofermentatively utilize a wide range of sugars, including C5 and C6 sugars, and can resist the inhibitory compounds generated during the pretreatment process is still a major challenge in fermenta-

tion technology for the production of lactic acid from lignocellulosic biomass. 4. Metabolism of lignocellulose-derived sugars by LAB LAB can be classied into 2 groups on the basis of the end product of their fermentation: homofermentative and heterofermentative. Homofermentative LAB virtually produce only lactic acid, whereas other products are generated by heterofermentative LAB along with lactic acid (Axelsson, 1993; Hofvendahl and Hahn-Hgerdal, 2000). Fig. 2 shows the metabolic pathways of hexose and pentose in LAB. When hexose sugars such as glucose are used, they are consumed by the Streptococcus, Lactococcus, Enterococcus, and Pediococcus genera and some Lactobacillus species to produce lactic acid homofermentatively (Naveena, 2004), while additional products, e.g., carbon dioxide, ethanol, and acetic acid, are produced by heterofermentative LAB, the Leuconostoc genera, and certain Lactobacillus species (Carr et al., 2002; Cowan and Steel, 1965; Schillinger and Lcke, 1987; Singleton and Sainsbury, 1987; Stamer, 1976). In the metabolism of homofermentative LAB, glucose is metabolized to lactic acid via the EmbdenMeyerhof pathway, whereby the theoretical yield of lactic acid to glucose is 1.0 g/g or 2.0 mol/mol. On the other hand, heterofermentative LAB possess the pentose monophosphate pathway, in which glucose 6-phosphate (6 carbons) is initially converted to ribulose 5-phosphate (5 carbons) and carbon dioxide (1 carbon) catalyzed by several enzymes (Reddy et al., 2008). The resulting ribulose 5-phosphate is cleaved to 1 mol of glyceraldehyde 3-phosphate (GAP) and acetyl phosphate (acetylP). GAP is further metabolized to lactic acid (3 carbons), while the acetyl-P is reduced to ethanol (2 carbons) via acetyl-CoA and acetaldehyde intermediates (Zaunmuller et al., 2006) and/or converted to acetate via acetate kinase. Therefore, the theoretical yield of lactic acid to glucose reaches only 0.5 g/g or 1.0 mol/mol with heterofermentative LAB. There are very few reports describing lactic acid fermentation from pentose sugars by LAB (Fred et al., 1919; Patel et al., 2006). Some species of LAB can metabolize pentose sugars as a substrate to

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lactic acid, e.g., Lc. lactis IO-1 (Oshiro et al., 2009; Tanaka et al., 2002), Streptococcus sp. (Enterococcus sp.) and Lb. thermophilus T1 (Fukui et al., 1957), Lactobacillus strain MONT4 (Barre, 1978), E. mundtii QU 25 (Abdel-Rahman et al., 2011b), Lb. pentosus (Bustos et al., 2005), Lb. brevis (Chaillou et al., 1998), Lb. plantarum (Helanto et al., 2007), and Leu. lactis (Ohara et al., 2006). Two different pathways, the PK and PP/glycolic pathways, are proposed as the metabolic pathways of pentoses in LAB (Fig. 2) (Tanaka et al., 2002). In the PK pathway, which is used by the majority of pentose-utilizing LAB, xylulose 5-P (5 carbons) is cleaved to GAP and acetyl-P. The resulting GAP is converted to pyruvic acid and then to lactic acid (3 carbons) as a nal product, while acetyl-P is metabolized to synthesize acetic acid or ethanol (both 2 carbons). As a result, the theoretical yield of pentose sugars to lactic acid is 0.6 g/g or 1.0 mol/mol via the PK pathway (Patel et al., 2006). On the other hand, a few species of LAB possess the PP/glycolic pathway for the metabolism of pentose sugars. The PP/glycolic pathway produces 5 mol of lactic acid from 3 mol of pentose without carbon loss, thereby providing a theoretical yield of lactic acid to pentose of 1.0 g/g or 1.67 mol/mol (i.e., homo-lactate fermentation) (Oshiro et al., 2009; Tanaka et al., 2002). Therefore, to improve the lactate yield, the PP/glycolic pathway is more useful and valuable than the PK pathway (Oshiro et al., 2009). Among wild-type LAB, E. mundtii QU 25 (Abdel-Rahman et al., 2011b), Streptococcus sp. (Enterococcus sp.), Lb. thermophilus T1 (Fukui et al., 1957), and Lactobacillus strain MONT4 (Barre, 1978) were reported to only show homo-lactate fermentation of pentose sugars. In addition, Okano et al. (2009a,b) recently demonstrated homo-lactate fermentation with arabinose and xylose using genetically modied Lb. plantarum by replacing the PK pathway with the PP pathway. The conversion of pyruvic acid to lactate can be affected by stereospecic NAD-dependent enzymes of l- or d-lactate dehydrogenase. Both enzymes have been found to be active in most lactobacilli, for example, Lb. plantarum (Ferain et al., 1996) and Lb. casei (Viana et al., 2005). The stereospecicity and optical purity of the lactic acid produced depends on the type of LAB, whose enzyme used in its production. In addition, when xylose was used as the sole carbon source, substrate concentration has been shown to be a factor for the metabolic ux of lactic acid production in the batch culture of E. mundtii QU 25 (Abdel-Rahman et al., 2011b) and the continuous culture of Lc. lactis IO-1 (Tanaka et al., 2002); a higher concentration of xylose and a higher yield of lactic acid to xylose was obtained. Thus, further investigations of culture conditions with LAB are suggested to be necessary for the efcient conversion of lignocellulosic biomass to lactic acid.

5. Designed biomass study and conclusions Currently, the fermentative production of useful substances, e.g., biomaterials and biofuels, from various renewable resources by microorganisms has become more attractive. For this purpose, it is essential that the used strain should consume the renewable resources as substrates to produce the useful substances. In a number of recent studies, a targeted substrate is initially decided upon, e.g., several types of biomass and by-products from industrial factories. Two main approaches are then applied to achieve efcient bioconversion (Fig. 3). One approach is a screening method to isolate wild-type strains from natural sources. The isolated strain should show a great potential in terms of its degrading enzyme for the targeted substrate, broad substrate specicity for components derived from renewable resources, high product yield, low by-product yield, capacity for high product concentration and productivity, and so on. An efcient process can then be investigated using the isolated strain, e.g., batch, fed-batch, or continuous fermentation, SHF, or SSF. The second approach is breeding a strain

to improve its ability to produce or degrade renewable resources, to modify metabolic pathways and their ux, including their increment or decrement, and to provide de novo degradation enzymes. To date, many breeding strains have been created using mutagenesis with physical or chemical mutagens and genetic manipulation. On the other hand, the active selection of substrates is also signicant for the highly efcient bioconversion of renewable resources to useful substances. Recently, we proposed a designed biomass study for this purpose. Designed biomass refers to competent substances that can be designed for the corresponding fermentation, conversion processes, etc. In this type of study, all the technologies and engineering methods developed to date can be used, i.e., excellent strains or highly efcient processes; thereafter, substrates could be modied or identied for the existing technologies (Fig. 3). The targeted renewable resources should include not only several types of components (mono-, oligo-, or polysaccharides) derived from various non-edible biomass sources but also organic acids or glycerol that are readily available and inexpensive as ready-made waste. On the basis of this concept, lactic acid (Oshiro et al., 2010) and butyric acid (Tashiro et al., 2004; Tashiro et al., 2007), both are produced fermentatively, were indicated as designed biomass material for acetonebutanolethanol fermentation by using the Clostridium saccharoperbutylacetonicum N1-4 strain. In terms of lactic acid fermentation, we assessed sago starch as a designed biomass for E. faecium from among several starches derived from different plants (Shibata et al., 2007). Of course, our concept also involves investigations on pretreatments and enzymatic hydrolysis of renewable resources, as mentioned in Section 2.2. In this review, we mainly described fermentative lactic acid production processes by LAB. Other microorganisms can be considered as genetically modied hosts for industrial lactic acid production such as yeasts and Escherichia coli, which generally produce little lactic acid (Okano et al., 2010b). Yeasts can grow in simpler synthetic media and are more tolerant to low pHs than LAB, which can eliminate a generation of the precipitated lactate by neutralizing agents for pH control during fermentation (Abbott et al., 2009; Skory, 2003). Lactic acid production using several recombinant yeasts has been reported in Saccharomyces cerevisiae (Tokuhiro et al., 2008; van Rooyen et al., 2005), Kluyveromyces lactis (Bianchi et al., 1996; Porro et al., 1999), Candida boidinii (Ikushima et al., 2009; Osawa et al., 2009). On the other hand, E. coli can grow in a simple mineral salt medium, and the easy and reproducible methods of genetic manipulation have been established in E. coli (Zhou et al., 2006). Very recently, there have been a few interesting reports on the direct productions of PLA and its copolymers from glucose using recombinant E. coli strains equipped with several genes for the polymerization (Jung and Lee, 2011; Jung et al., 2010; Yang et al., 2010). Conventionally, PLA is industrially produced by two steps: lactic acid fermentation for lactic acid production and followed by chemical process for PLA synthesis. Therefore, the constructed E. coli can develop a novel strategy for PLA production by one-step process. Although recombinant yeasts and E. coli as described above could not utilize lignocellulose-derived sugars efciently, further researches should have potential and application for lactic acid production from lignocellulosic materials. In conclusion, we described many studies and the ndings of lactic acid fermentation by LAB from lignocellulosic materials and also compared the features of LAB with other microorganisms. Nevertheless, industrial lactic acid production from lignocellulosic materials has not been sufciently protable. One of the reasons for this is the high cost of hydrolytic enzymes for the saccharication of cellulose and hemicellulose. To address this problem, attempts to isolate LAB that can ferment cellulose or xylan directly to lactic acid, and the development of genetically modied LAB that have hydrolytic enzymes with high activity should be con-

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