α-l-Arabinofuranosidases

June 6, 2017 | Autor: Badal Saha | Categoria: Engineering, Technology, Molecular Biology, Biotechnology, Biological Sciences
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Biotechnology Advances 18 (2000) 403–423

Research review paper

␣-L-Arabinofuranosidases: biochemistry, molecular biology and application in biotechnology Badal C. Saha* Fermentation Biochemistry Research Unit, National Center for Agricultural Utilization Research, U.S. Department of Agriculture 1, Agricultural Research Service, Peoria, IL 61604, USA

Abstract Interest in the ␣-L-arabinofuranosidases has increased in recent years because of their application in the conversion of various hemicellulosic substrates to fermentable sugars for subsequent production of fuel alcohol. Xylanases, in conjunction with ␣-L-arabinofuranosidases and other accessory enzymes, act synergistically to degrade xylan to component sugars. The induction of ␣-L-arabinofuranosidase production, physico-chemical characteristics, substrate specificity, and molecular biology of the enzyme are described. The current state of research and development of the arabinofuranosidases and their role in biotechnology are presented. © 2000 Published by Elsevier Science Inc. Keywords: ␣-L-Arabinofuranosidase; Arabinoxylan; Arabinan; Arabinanase; Arabinosidase; Arabinose

1. Introduction Hemicelluloses, the most abundant renewable biomass polymer next to cellulose, represent about 20–35% of lignocellulosic biomass (Ward and Moo-Young, 1989). L-Arabinosyl residues are widely distributed in some hemicelluloses, such as arabinan, arabinoxylan, gum arabic, and arabinogalactan. ␣-L-Arabinofuranosidase (␣-L-arabinofuranoside arabinofuranohydrolase, EC 3.2.1.55, AF) is an accessory enzyme involved in arabinose release from these substrates. In this review, the author gives an account of the biochemistry and molecular biology of various AFs and their potential uses in biotechnology.

* Tel: ⫹1-309-681-6276; fax: ⫹1-309-681-6427. E-mail address: [email protected] (B.C. Saha). 1 Names are necessary to report factually on available data; however, the USDA neither guarantees nor warrants the standard of the product, and the use of the name by USDA implies no approval of the product to the exclusion of others that may also be suitable. 0734-9750/00/$ – see front matter © 2000 Published by Elsevier Science Inc. PII: S0 7 3 4 - 9 7 5 0 ( 0 0 ) 0 0 0 4 4 -6

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2. Structure of arabinose-containing hemicelluloses Arabinans occur in various plant tissues and are composed of L-arabinofuranosyl residues that are ␣-1,5-linked. A varying number of these are substituted with other ␣-L-arabinofuranosyl residues at the C2 and/or C3 position (Beldman et al., 1993). In ␤-1,4-arabinogalactans, the galactopyranose backbone is substituted at the O-3 and O-6 positions by ␣-L-arabinofuranose side chains with varying degrees of polymerization (Luonteri et al., 1998). Hemicelluloses are heterogeneous polymers of pentoses (D-xylose, L-arabinose), hexoses (D-mannose, D-glucose, D-galactose) and sugar acids. Unlike cellulose, hemicelluloses are not chemically homogeneous. Hardwood hemicelluloses contain mostly xylans, whereas softwood hemicelluloses contain mostly glucomannans (McMillan, 1993). Xylans of many plant materials are heteropolysaccharides with homopolymeric backbone chains of 1,4linked ␤-D-xylopyranose units. Besides xylose, xylans may contain arabinose, glucuronic acid, or its 4-O-methyl ether, and acetic, ferulic, and p-coumaric acids. The frequency and composition of the branches are dependent on the source of xylan (Aspinall, 1980). Xylans from different sources, such as grasses, cereals, softwood, and hardwood, differ in composition. Birch wood (Roth) xylan contains 89.3% xylose, 1% arabinose, 1.4% glucose, and 8.3% anhydrouronic acid (Kormelink and Voragen, 1993). Rice bran neutral xylan contains 46% xylose, 44.9% arabinose, 6.1% galactose, 1.9% glucose, and 1.1% anhydrouronic acid (Shibuya and Iwasaki, 1985). Wheat arabinoxylan contains 65.8% xylose, 33.5% arabinose, 0.1% mannose, 0.1% galactose, and 0.3% glucose (Gruppen et al., 1992). Corn fiber hemicellulose contains 48–54% xylose, 33–35% arabinose, 5–11% galactose and 3–6% glucuronic acid (Doner and Hicks, 1997; Hespell, 1998). Arabinoxylans often contain ferulic and p-coumaric acids, which are bound to C5 of the arabinofuranosyl side groups. The backbone of maize bran heteroxylan is composed of ␤-1,4 linked xylose residues. About 80% of this backbone is highly substituted with monomeric side-chains of arabinose or glucuronic acid linked to O-2 and/or O-3 of xylose residues, and also by oligomeric side chains containing arabinose, xylose, and sometimes galactose residues (Fig. 1; Chanliaud et al., 1995; Saulinier et al., 1995). A model for the maize bran cell wall is shown in Fig. 2 (Saulnier and Thibault, 1999). The heteroxylans, which are probably highly crosslinked by diferulic bridges, constitute a network in which the cellulose microfibrils may be imbedded. Structural wall proteins might be crosslinked together by isodityrosine bridges and with feruloylated heteroxylans, thus forming an insoluble network (Hood et al., 1991). In softwood heteroxylans, arabinofuranosyl residues are esterified with p-coumaric acids and ferulic acids (Mueller-Hartley et al., 1986). In hardwood xylans, 60–70% of the xylose residues are acetylated (Timell, 1967). 3. Enzymatic hydrolysis of heteroxylan The total hydrolysis of xylan by enzymes requires endo-␤-1,4-xylanase, ␤-xylosidase, and several accessory enzymes, such as AF, ␣-glucuronidase, acetylxylan esterase, ferulic acid esterase, and p-coumaric acid esterase, which are necessary for hydrolyzing various substituted xylans. Table 1 lists the enzymes involved in the degradation of xylan and their modes of action. A hypothetical plant heteroxylan fragment and sites of attack by xylanolytic en-

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Fig. 1. Schematic structure of heteroxylan from maize bran. (Reprinted from Saulnier et al., 1995, with permission from Elsevier Science.)

zymes are shown in Fig. 3 (Wood et al., 1992). The endo-xylanase attacks the main chains of xylans and ␤-xylosidase hydrolyzes xylooligosaccharides to xylose. AF and ␣-glucuronidase remove the arabinose and 4-O-methyl glucuronic acid substituents, respectively, from the xylan backbone. Esterases hydrolyze the ester linkages between xylose units of the xylan and acetic acid (acetylxylan esterase) or between arabinose side chain residues and phenolic acids, such as ferulic acid (ferulic acid esterase) and p-coumaric acid (p-coumaric acid esterase). The presence of large amounts of substituents may hinder the formation of enzyme– substrate complexes, and thus impede enzymic hydrolysis (Kormelink and Voragen, 1993). Synergistic action between depolymerizing and side-group cleaving enzymes has been verified using acetylated xylan as a substrate (Poutanen and Puls, 1989). Bachmann and McCarthy (1991) reported significant synergistic interaction among endo-xylanase, ␤-xylosidase, AF, and acetylxylan esterase of the thermophilic actinomycete Thermomonospora fusca. Some xylanases do not cleave glycosidic bonds between xylose units that are substituted. The side chains must be cleaved before the xylan backbone can be completely hydrolyzed (Lee and Forsberg, 1987). On the other hand, several accessory enzymes only remove side chains from xylooligosaccharides. These enzymes require a partial hydrolysis of xylan before the side chains can be cleaved (Poutanen et al., 1991). Although the structure of xylan is more complex than cellulose, and requires several different enzymes with different specificities for complete hydrolysis, the polysaccharide does not form tightly packed crystalline structures like cellulose, and is thus more accessible to enzymatic hydrolysis (Gilbert and

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Fig. 2. Model for the maize bran cell walls. (Reprinted from Saulnier and Thibault, 1999, with permission from Elsevier Science.)

Hazlewood, 1993). Many microorganisms, such as Penicillium capsulatum and Talaromyces emersonii, possess complete xylan-degrading enzyme systems (Filho et al., 1991). 4. Types of AFs AFs are exo-type enzymes, which hydrolyze terminal nonreducing residues from arabinose-containing polysaccharides. These enzymes can hydrolyze (1→3)- and (1→5)-␣-arabinosyl linkages of arabinan (Fig. 4). The AFs are part of microbial xylanolytic systems necessary for complete breakdown of arabinoxylans (Bachmann and McCarthy, 1991; Greve et al., 1984; Lee and Forsberg, 1987; Poutanen, 1988; Saha and Bothast, 1999a). AFs warrant substantial research efforts because they represent potential rate limiting enzymes in xylan degradation, particularly those substrates from agricultural residues such as corn fiber, corn stover, and rice straw (Saha and Bothast, 1999b). There is another group of enzymes which degrade arabinan by endo-fashion and are called endo-1→5-␣- L-arabinanases (1→5␣-L-arabinan1→5-␣-L-arabinanohydrolase, EC 3.2.1.99). The AFs have been classified into

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Table 1 Enzymes involved in the hydrolysis of heteroxylans Enzyme

Mode of action

Endo-xylanase Exo-xylanase ␤-Xylosidase ␣-Arabinofuranosidase ␣-Glucuronidase Acetylxylan esterase Ferulic acid esterase p-Coumaric acid esterase

Hydrolyzes mainly interior ␤-1,4-xylose linkages of the xylan backbone Hydrolyzes ␤-1,4-xylose linkages releasing xylobiose Releases xylose from xylobiose and short chain xylooligosaccharides Hydrolyzes terminal nonreducing ␣-arabinofuranose from arabinoxylans Releases glucuronic acid from glucuronoxylans Hydrolyzes acetylester bonds in acetyl xylans Hydrolyzes feruloylester bonds in xylans Hydrolyzes p-coumaryl ester bonds in xylans

four families of glycanases (families 43, 51, 54, and 62) on the basis of amino acid sequence similarities (Henrissat and Bairoch, 1996). The two families (51 and 54) of AFs also differ in substrate specificity for arabinose-containing polysaccharides. Beldman et al. (1997) summarized the AF classifications based on substrate specificities: (1) AFs, not active toward polymers; (2) AFs, active toward polymers; and (3) arabinofuranohydrolases, specific for arabinoxylans. The N-terminal sequence of the first 50 amino acids of AF from Bacillus stearothermophilus T-6 showed high homology with the N-terminal region of AF from Streptomyces lividans 66 (Gilead and Shoham, 1995; Manin et al., 1994). Another type of arabinan-degrading enzyme has been reported from Erwinia carotovora (Kaji and Shimokawa,

Fig. 3. Representative plant xylan and the sites of cleavage by xylan-degrading enzymes. Ac, acetyl group; Araf, L-arabinofuranosidase, MeGlcA, 4-O-methyl-D-glucuronic acid; Xyl, D-xylose; Fe, ferulic acid; Coum, p-coumaric acid. [Reprinted (in modified form) from Wood et al., 1992, with permission from Elsevier Science.]

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1984). It released arabinose trisaccharides from the nonreducing end of 1,5-␣-L-arabinan, and did not show activity on synthetic ␣-L-arabinosides. 5. Microbial production of AFs Karimi and Ward (1989) screened a variety of microorganisms for AF and arabinase production. Thermoascus aurantiacus and several Bacillus species were the most active producers of AF. The induction of extracellular arabinases in Aspergillus niger occurred with arabinose and arabitol but not with xylose or xylitol (van der Veen et al., 1993). Arabitol, in particular, was found to be an inducer for AFs and endo-arabinase activities, playing an important role in the induction of AFs in A. nidulans (van der Veen and Visser, 1993). The highest levels of enzyme (1.0 U per ml) were obtained when arabitol was used as a carbon source for growth of Penicillium purpurogenum, while 0.85 and 0.7 U per ml are produced with sugar beet pulp and oat spelt xylan, respectively (De loannes et al., 2000). In the case of Aureobasidium pullulans, arabinose was most effective for production of both whole-broth and extracellular AF activity, followed by arabitol (Saha and Bothast, 1998a). Oat spelt xylan, sugar beet arabinan, xylose, xylitol, and wheat arabinoxylan were intermediate in their ability to support the AF production. Formation of AF was induced in Trichoderma reesei RUT C-30 by growing the fungus on arabinose or dulcitol, and by adding arabinose, arabitol, galactose, or dulcitol to nongrowing mycelia (Kristufek et al., 1994). L-Sorbose, an excellent inducer of cellulase and xylanase from T. reesei PC-3-7, also induced AF activity (Nogawa et al., 1999). In wild-type A. niger, AF A, AF B, endo-arabinases, L-arabinose reductase, and L-arabitol dehydrogenase were induced during growth on arabinose, but addition of glucose prevented this induction (Ruijter et al., 1997). Repression was relieved to varying degrees in the CreA mutants, showing that biosynthesis of AF is under the control of CreA. In the presence of arabitol, A. terreus CECT 2663 produced three AFs with molecular mass of 90, 82, and 78.5 kDa. The synthesis of these enzymes is under carbon catabolic repression (Le Clinche et al., 1997). The production of AF was investigated by solid-state cultivation of T. aurantiacus on a leached sugar beet pulp-based medium. The optimal medium composition for maximum AF production by solid-state cultivation of T. aurantiacus was sugar beet pulp containing 77.8% moisture after being wetted with a mineral solution at pH 9.5, containing 1.2% yeast extract as the nitrogen source (Roche et al., 1994). The highest levels of AF were generated when cultures of A. nidulans were grown on 1% (w/v) purified beet pulp arabinan at 30⬚C and at an initial pH of 7.0 (Fernandez-Espinar et al., 1994). B. stearothermophilus T-6 produced an AF

Fig. 4. Primary structure of arabinan.

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when grown in the presence of arabinose, sugar beet arabinan, or oat spelt xylan. At the end of fermentation, about 40% of the activity was extracellular, and enzyme activity in the cellfree supernatant reached 25 U/ml (Gilead and Shoham, 1995). The filamentous fungus Cochliobolus carbonum produced AF when grown on maize cell walls. Low concentrations of sucrose in a medium containing other carbon sources stimulated production, while high sucrose concentration partially repressed enzyme production (Ransom and Walton, 1997). AF was the main enzyme produced at a rate of 433 U per g of dry fermented medium at the end of solid-state culture (165 h) on sugar beet pulp (63 U per mg of soluble protein) by T. reesei (Roche et al., 1995). Roche and Durand (1996) studied the fungal solubilization of cell wall components of sugar beet pulp during solid-state fermentation of T. aurantiacus. In 120 h, more than 60% of the main sugar beet polysaccharides, including arabinose-containing polysaccharides, were rapidly brought into solution by the fungus. AF was found to be one of the highest enzyme activities present. Both arabinoxylan arabinofuranohydrolases (AXH-d3 and AXH-m23) from Bifidobacterium adolescentis were induced when grown on xylose and arabinoxylan-derived oligosaccharides (Van Laere et al., 1999). Wheat bran was the best inducer for the production of AF by Streptomyces diastaticus (Tajana et al., 1992). Pretreated corn cob was the best substrate for production of extracellular AF (4.2 U/ml) by Sclerotium rolfsii (Chinnathambi and Lachke, 1995). Arabinan, as the carbon source, was the most effective substrate for the production of AF by Corticium rolfsii (Kaji and Yoshihara, 1970). 6. Physico-chemical characteristics of AFs Multiple forms of AF have been detected in the culture broth of A. awamori (Kaneko et al., 1998a), A. nidulans (Ramon et al., 1993), A. niger (Rombouts et al., 1988), A. terreus (Luonteri et al., 1995), P. capsulatum (Filho et al., 1996), P. purpurogenun, Sclerotina fructigena (Laborda et al., 1973), and S. diastaticus (Tajana et al., 1992). The AF I and AF II purified from the culture filtrate of A. awamori had MWs of 81 000 and 62 000 and pIs of 3.3 and 3.6, respectively (Kaneko et al., 1998a). The AF from A. pullulans is a homodimer with an apparent native MW of 210 000 and a subunit MW of 105 000 (Saha and Bothast, 1998b). Komae et al. (1982) showed that the MW of AF from S. purpurascens IFO 3389 is about 495 000, and the enzyme contains eight equal subunits of MW 65 000. The MW of AF of Butyrivibrio fibrisolvens GS113 is 240 000 and it consists of eight subunits of MW 31 000 (Hespell and O’Bryan, 1992). The enzyme from Clostridium acetobutylicum ATCC 824 is a single polypeptide with a MW of 94 000 (Lee and Forsberg, 1987). The intracellular AF from A. niger is a monomer with a MW of 67 000 (Kaneko et al., 1993). One AF from P. purpurogenun is a monomer of 58 kDa, with a pI of 6.5 (De loannes et al., 2000). The AF (MW 110 000) from B. stearothermophilus L1 consists of two subunits (MWs 52 500 and 57 500), that (MW 256 000) from B. stearothermophilus T-6 consists of four identical subunits (MW 64 000) (Bezalel et al., 1993; Gilead and Shoham, 1995). The AF III from Monillinia frucigena is a monomer of MW 40 000 (Kelly et al., 1987). Microbial AFs have a broad range of pH and temperature dependence, with optimal activities occurring between pH 3.0–6.9 and 40–75⬚C (Bezalel et al., 1993; Fernandez-Espinar et al., 1993; Filho et al., 1996; Kaji, 1984; Lee and Forsberg, 1987; Saha and Bothast, 1998b). The purified enzyme from Rhodotorula flava is highly acid stable, retaining 82% of its activ-

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ity after being maintained for 24 h at pH 1.5 and at 30⬚C (Uesaka et al., 1978). Optimum activity of this enzyme is at pH 2.0. The AF from Corticium rolfsii had an optimum activity at pH 2.5 toward beet arabinan (Kaji and Yoshihara, 1971). The AF from Talaromyces emersonii is a dimer (MW 210 000), with a pH and temperature optima of 3.2 and 70⬚C, respectively (Tuohy et al., 1994).

7. Substrate specificity of AFs The AFs from A. pullulans (Saha and Bothast, 1998b), Streptomyces sp. strain 17-1 (Kaji et al., 1981) and B. subtilis 3–6 (Komae et al., 1982) have hydrolytic activity for both ␣-(1→ 3) and ␣-(1→5)-linked, nonreducing, terminal residues. They do not act on internal ␣-arabinosyl linkages. The AFs from A. niger (Kaji and Tagawa, 1970) and S. purpurascens IFO 3389 (Luonteri et al., 1998) hydrolyze either (1→5) or (1→3)-arabinosyl linkages of arabinan. The enzyme purified from S. purpurascens is inactive against arabinans and arabinogalactans (Komae et al., 1982). Kormelink et al. (1991) described another type of AF (AXH) from A. awamori that was highly specific for arabinoxylans, and unlike other AFs, did not show any activity toward pNP-␣-L-arabinofuranoside, arabinans, and arabinogalactans. Arabinoxylan-derived oligosaccharides were treated with AXH from A. awamori and two types of AF from A. niger (Kormelink et al., 1993). All these enzymes acted on arabinoxylan oligosaccharides. Van Laere et al. (1997) described a new arabinofuranohydrolase from B. adolescentis able to remove arabinosyl residues from double-substituted xylose units in arabinoxylan. The enzyme showed no activity toward sugar beet arabinan, soy arabinogalactan, arabinooligosaccharides, and arabinogalacto-oligosaccharides. The AF from S. lividans exhibited no activity against oat spelt xylan or arabinogalactan (Manin et al., 1994). It acted slowly on arabinan and arabinoxylans by releasing arabinose after prolonged incubation. The limit of hydrolysis of arabinan by the AF from B. subtilis 3–6 was only 15%, even when the enzyme was present in excess (Kaneko et al., 1994). The AF from P. purpurogenum is highly specific for ␣-L-arabinofuranosides and liberates arabinose from arabinoxylan (De loannes et al., 2000). The AF I from A. awamori preferentially hydrolyzed the (1→5) linkage of branched arabinotrisaccharide, whereas AF II from the same organism preferentially hydrolyzed (1→3) linkage in the same substrate (Kaneko et al., 1998a). The AF I released arabinose from the nonreducing terminus of arabinan, whereas AF II preferentially hydrolyzed the arabinosyl side chain linkage of arabinan. The enzyme from Cytophaga xylanolytica released arabinose from rye, wheat, corn cob, and oat spelt arabinoxylans, and sugar beet arabinan but not from arabinogalactan (Renner and Breznak, 1998). All three AFs isoforms from A. terreus preferred branched pectic polysaccharides such as sugar beet arabinan and ␤-1,4-arabinogalactans as substrates, but were able to release arabinose from linear arabinan, ␤-1,3/ 1,6-arabinogalactans and different arabinoxylans (Luonteri et al., 1998). Feruloyl substituents limited the hydrolysis of arabinoxylan and arabinan oligosaccharides by an AF from A. terreus but only if the feruloyl group was esterified to the terminal nonreducing arabinose (Luonteri et al., 1999). The AF from T. reesei preferentially cleaved the arabinosyl side chain from the arabinan rather than the terminal arabinosyl residues of the arabinan backbone

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(Kaneko et al., 1998b). The enzyme from B. polymyxa was only active on (1→5)-␣-L-arabinooligosaccharides but not on linear (1→5)-␣-L-arabinan, arabinogalactan, and arabinoxylan (Morales et al., 1995a). However, it was able to release arabinose from arabinoxylan when an endoxylanase was also present in hydrolysis assays. The purified AF II from Bacillus sp. No. 430 liberated arabinose from beet arabinan, arabinogalactan, and arabinoxylan (Yasuda and Tokuzato, 1988). Using this purified enzyme, xylans of high purity were obtained from enzyme reaction with sugar cane bagasse or galactans from coffee and soybean. The AFs from two species of A. niger hydrolyzed arabinan and debranched arabinan at almost the same rate (Kaneko et al., 1998c). Enzymatic dearabinosylation of an arabinogalactan protein isolated from a cider apple juice with a purified AF released 95% of arabinose (Brillouet et al., 1996). Ferulated arabinans in sugar beet pulp are readily available for hydrolysis by arabinan degrading enzymes (Kroon and Williamson, 1996). A novel property of AF from A. awamori was its capacity to release a substantial portion (42%) of feruloyl arabinose from intact wheat straw arabinoxylan (Wood and McCrae, 1996). Arabinose-substituted oligosaccharides were better substrates for this AF. The AF from S. diastatochromogenes 065 released only the terminal arabinose of arabinoxylo-oligosaccharides (Kaneko et al., 1998d). The enzyme hydrolyzed methyl arabinofuranobiosides to arabinose and methyl arabinofuranosides in the order of (1→2) ⬎ (1→3) ⬎ (1→5) linkages. It preferentially hydrolyzed the (1→3) linkages over the (1→5) linkages of methyl arabinofuranotrioside. Similar substrate specificities have been reported for the AF from B. subtilis 3–6 (Kaneko and Kusakabe, 1995) and A. niger 5–16 (Kaneko et al., 1998c). An arabinoxylan arabinofuranohydrolase (AXH) from wheat bran and germinated wheat was active toward polymeric substrate but was unable to hydrolyze p-nitrophenyl-␣-L-arabinofuranoside (Beldman et al., 1996). A bifunctional protein with ␤-xylosidase and AF activities from B. fibrisolvens has been reported (Utt et al., 1991). In Bacteroides ovatus, AF and ␤-xylosidase activities were suggested to be catalyzed by a bifunctional protein or two proteins of very similar molecular weight (Whitehead and Hespell, 1990). One AF from P. capsulatum was competitively inhibited by arabinose with a Ki of 16.4 mM (Filho et al., 1996). Arabinose, at 80 mM concentration, caused a 40% reduction of the hydrolytic activity of AF from A. nidulans (Fernandez-Espinar et al., 1994). The enzyme from A. pullulans was not inhibited by 1.2 M (21.6%) arabinose (Saha and Bothast, 1998b). Pitson et al. (1996) studied the stereochemical course of hydrolysis catalyzed by arabinofuranosyl hydrolases. The AFs from A. niger, A. aculeatus, P. capsulatum, B. subtilis, A. awamori, M. fructigena, and Humicola insolens catalyzed the glycosyl transfer reaction to methanol with retention of configuration and, therefore, probably operate via double displacement hydrolytic mechanisms. It was predicted that all members of glycosyl hydrolase family 51 and 54 catalyze hydrolysis with net retention of anomeric configuration. Studies with (1→4)-␤-D-arabinoxylan arabinohydrolases from A. awamori, T. reesei, and B. adolescentis only enabled their tentative classification as inverting enzymes on the basis of their lack of glycosyl transfer to methanol. The endo-arabinases from A. niger and A. aculeatus hydrolyzed linear arabinan with inversion of configuration and may, therefore, act via a single displacement mechanism. These enzymes are classified in glycosyl hydrolase family 43 (Henrissat and Bairoch, 1996). Comparative properties of some fungal, bacterial, and plant AF are presented in Tables 2, 3, and 4, respectively.

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8. Molecular biology of AFs A fully secreted AF was cloned from the homologous expression system of S. lividans (Vincent et al., 1997). The purified enzyme has a specific arabinofuranose debranching activity on xylan from Gramineae, acts synergistically with the S. lividans xylanases, and binds specifically to xylan. From small arabinoxylooligosides, it liberates arabinose and, after prolonged incubation, the purified enzyme exhibits some xylanolytic activity as well. The AF gene (ABF2) of A. niger was expressed successfully in Saccharomyces cerevisiae, and functional AF was secreted from yeast cells (Crous et al., 1996). The ABF2 nucleotide sequence is 94% identical to the AF B of A. niger N400. A recombinant wine yeast strain was constructed expressing the gene coding for AF B from A. niger (Sanchez-Torres et al., 1996). The protein was efficiently secreted by the recombinant yeast. Attempts have been made to construct A. nidulans recombinant strains, which secrete both AF and ␤-glucosidase activities suitable to increase wine aroma (Sanchez-Torres et al., 1998). The gene encoding AF and ␤-xylosidase from T. reesei RutC-30 was cloned and expressed in S. cerevisiae (Margolles-Clark et al., 1996). Both enzymes produced in yeasts displayed hydrolytic properties similar to those of the corresponding enzymes purified from T. reesei. Two polypeptides exhibiting AF I activity were purified to homogeneity from culture supernatants of a B. subtilis clone harboring xynD gene from B. polymyxa (Morales et al., 1995b). Arabinose was the unique product released from arabinoxylans by both I forms. Gene arfB, which encodes AF B (ArfB) of the cellulolytic thermophile, Clostridium stercorarium, was expressed in Escherichia coli from a 2.2-kb EcoR1 DNA fragment (Schwarz et al., 1995). The identity of the N-terminal amino acid sequence indicates that the recombinant AF corresponds to the major AF present in the culture supernatant of C. stercorarium. The nucleotide sequence of the AF gene arfB from C. stercorarium is homologous to AFs of glycosyl hydrolase family 51 (Zverlov et al., 1998). Sakka et al. (1993) reported the nucleotide sequence of the C. stercorarium xylA gene encoding a bifunctional protein with ␤-D-xylosidase and AF activities. The genes encoding the enzyme arabinoxylan arabinofuranohydrolase, which releases arabinose from arabinoxylan, have been cloned from the closely related fungi A. niger and A. tubingensis, and were shown to be functional in A. niger (Gielkens et al., 1997). Integration of multiple copies in the genome resulted in overexpression of the enzymes. Kim et al. (1998) cloned and sequenced arfI and arfII, two genes encoding AF in C. xylanolytica. Products of both cloned genes liberated arabinose from arabinan and arabinoxylan. The deduced amino acid sequences of ArfI and ArfII revealed numerous regions that were identical to each other and to regions of homologous proteins from B. ovatus (Whitehead, 1995) and C. stercorarium (Zverlov et al., 1998). Using a DNA fragment containing the A. niger abfB gene as a probe, the homologous A. nidulans gene, designated abfB, has been cloned from a genomic library containing sizeselected HindIII fragments (Gielkens et al., 1999). The nucleotide sequence of the A. nidulans abfB gene shows strong homology with the A. niger abfB, T. reesei abf-1, and T. koningii AF/␤-xylosidase. Flipphi et al. (1993a,b,c) cloned the three arabinase-encoding genes from A. niger and analyzed the structure of these two genes, abnA encoding ABN A and abfB encoding ABF B. Flipphi et al. (1994) also studied arabinase expression induced by sugar

I II

I II III

I II

3.5 3.6 3.9 7.5 8.3 8.5 — — 6.1

67 000 53 000 34 300 39 000 59 000 59 000 210 000 63 000 160 000 ⫺240 000 60 000 64 500 62 700 63 000 58 000 53 000 5.1 4.15 4.54 7.5 6.5 7.5

3.3 3.6 3.3

pI

81 000 62 000 65 000

Molecular weight

60 60 55 — 50

60 — 50 — — — 75 50 45

60 60 65

Optimum temperature (⬚C)

3.5 4.0 4.0 4.0–4.5 4.0 4.0

4.0 4.0 5.0 3.5–4.5 3.5–4.5 3.5–4.5 4.0–4.5 3.5–4.0 5.8

4.0 4.0 4.0

Optimum pH

BA, AX BA, AX, AXO BA, AX, AXO BA, AX AX AX, AXO

OSX, RAX, AGX, BA OSX, RAX, AGX, BA OSC, RAX, AGX, BA BA, AX, OSX BA, AX AX, BA

BA BA, AX

BA BA

Polymer attackeda

Baker et al., 1979 De loannes et al., 2000 Poutanen, 1998

Brillouet et al., 1985 Filho et al., 1996

Saha and Bothast, 1998b Ransom and Walton, 1997 Renner and Breznak, 1998

Kaneko et al., 1993 Kaji and Tagawa, 1970 Kimura et al., 1995 Luonteri et al., 1995

Ramon et al., 1993

Kaneko et al., 1998a

Reference

AX, arabinoxylan; BA, beet arabinan; CX, corn endosperm xylan; OSX, oatspelt xylan; AXO, arabinoxylan oligosaccharides; RAX, rye arabinoxylan; AGX, arabinoglucuronoxylan.

a

Sclerotinia sclerotiorum Penicillium purpurogenum Trichoderma reesei

Dichomitus squalens Penicillium capsulatum

Aureobasidium pullulans Cochliobolus carbonum Cytophaga xylanolytica

Aspergillus nidulans Aspergillus niger 5–16 Intracellular Extracellular Aspergillus sojae Aspergillus terreus

Aspergillus awamori

Organism

Table 2 Comparative properties of some fungal ␣-arabinofuranosidases

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50 30–40 55

— 70

Optimum temperature (⬚C)

6.0 6.5

5.5–6.0 6.0 6.0–6.5 5.0–5.5 6.9 6.0 5.0–6.5 5.0–6.5

6.5

— 7.0

Optimum pH

BA A2, A3

AXO only AX only BA, AX, OSX BA AH BA, AX, AG AX AX

AXO only Used for delignification BA

Polymer attackeda

Higashi et al., 1983 Komae et al., 1982

Hespell and O’Bryan, 1992 Lee and Forsberg, 1987 Greve et al., 1994 Kaji et al., 1981 Tajana et al., 1992

Schyns et al., 1994

Weinstein and Albershein, 1979

Morales et al., 1995a Bezalel et al., 1993

Reference

a AX, arabinoxylan; BA, beet arabinan; CX, corn endosperm xylan; OSX, oatspelt xylan; AXO, arabinoxylan oligosaccharides; A2, arabinobiose; A3, arabinotriose.

3.9

73 000 495 000

364 000 (61 000)

Bacteroides xylanolyticus

5.3

6.0 8.2 3.8 4.4 8.8 8.3

65 000

Bacillus subtilis

4.7 —

pI

240 000 94 000 310 000 92 000 38 000 60 000

166 000 110 000

Bacillus polymyxa Bacillus stearothermophilus

Bifidobacterium adolescents Butyrivibrio fibrisolvens Clostridium acetobutylicum Ruminococcus albus Streptomyces sp. 17–1 Streptomyces diastaticus C1 C2 Streptomyces diastaatochromogenes 065 Streptomyces purpurascens

Molecular weight

Organism

Table 3 Comparative properties of some bacterial ␣-arabinofuranosidases

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415

Table 4 Comparative properties of some plant ␣-arabinofuranosidases Source

Spinach leaf

Carrot cell culture Radish seeds Soybean seeds Japanese pear fruit a

I II

Molecular weight

pI

118 000 68 000

4.8 4.2

84 000 64 000 87 000 42 000

5.6 4.7 4.8

Optimum temperature (⬚C)

Optimum pH

Polymer attackeda

Reference

Hirano et al., 1994 4.8 55

3.8

5.0

BA BA, AG

Konno et al., 1994 Hata et al, 1992 Hatanaka et al, 1991 Tateishi et al., 1996

BA, beet arabinan; AG, arabinogalactan.

beet pulp or L-arabitol as a function of time both in wild-type A. niger and transformed A. niger strains containing multiple copies of either the abfA or the abfB gene. Upon comparison of the three arabinase genes, common sequence elements were identified that might be involved in regulation of arabinase gene expression in A. niger. Gasparic et al. (1995) isolated a gene from Prevotella ruminicola B14 containing activities against p-NP arabinofuranoside and p-NP-xyloside. Recently, Kimura et al. (2000) cloned the AF gene from A. sojae. The deduced amino acid sequence of the catalytic domain of the mature enzyme exhibits extensive identity with the catalytic domains of S. coelicolor (74%), A. niger (75%), S. lividans (74%), and A. tubingensis (75%), which are enzymes that belong to family 62 of the glycosyl hydrolases. Debeche et al. (2000) isolated the AF-encoding gene, abfD3 from Thermobacillus xylanilyticus. The recombinant AF (56 071-Da enzyme) produced in E. coli could be assigned to family 51 of the glycosyl hydrolase classification system (Henrissat and Bairoch, 1996). The enzyme is localized within a distinct phylogenic cluster that contains three other AFs from taxonomically related bacterial sources [B. subtilis (Kaneko et al., 1994), C. stercorarium (Schwartz et al., 1995), and B. stearothermophilus (Gilead and Shoham, 1995)]. The AF I from Streptomyces chartreusis belongs to family 51, whereas AF II from the same organism belongs to family 43 of the glycoside hydrolase family (Matsuo et al., 2000). Sequence alignment of some AFs from glycosyl hydrolase family 51 is given in Fig. 5. 9. Application in biotechnology In recent years, xylan-degrading enzymes have received much attention because of their practical applications in various agro-industrial processes, such as efficient conversion of hemicellulosic biomass to fuels and chemicals, delignification of paper pulp, digestibility enhancement of animal feedstock, clarification of juices, and improvement in the consistency of beer (Campbell and Bedford, 1992; Vikari et al., 1993; Wong et al., 1988; Zeikus et al., 1991). During Japanese pear fruit ripening, the AF activity in the fruit increased dramatically (Tateishi et al., 1996).

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Fig. 5. Sequence alignment of some arabinofuranosidases of glycosyl hydrolase family 51. (a) Clostridium stercorium ArfB; (b) Bacillus subtilis Abf2; (c) Bacteroides ovatus AsdII; (d) Streptomyces lividans AbfA; (e) Bacillus subtilis AbfA; (f) Aspergillus niger AbfA; (g) B. ovatus AsdI; (h) Bacillus stearothermophilus T-6 ␣-L-arabinofuranosidase N-terminus (Gilead and Shoham, 1995). Areas with high similarity in all sequences are boxed. *Denotes the end of a sequence. Amino acid insertions are indicated by slashes and the number of deleted aa residues. (Reprinted from Zverlov et al., 1998, with permission from Elsevier Science.)

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417

The utilization of hemicellulosic sugars is essential for efficient conversion of lignocellulosic materials to ethanol and other value-added products. Dilute acid pretreatment at high temperatures converts hemicellulose to monomeric sugars (Saha and Bothast, 1999b). However, this pretreatment also produces by-products that are toxic to fermentative microorganisms. Other pretreatments, such as alkali, alkali peroxide, and ammonia fiber explosion (AFEX), solubilize xylans and produce xylooligosaccharides (Saha et al., 1998). These oligo-saccharides are not fermentable, and must be converted to monomeric sugars with enzymes or by other means prior to fermentation. Xylan-degrading enzymes hold great promise in saccharifying various pretreated agricultural and forestry residues to monomeric sugars for fermentation to fuels and chemicals. Enzymes cleaving ␣-L-arabinofuranosidic linkages can act synergistically with xylanases in the hydrolysis of arabinoxylans (Greve et al., 1984; Poutenan, 1988; Suh et al., 1996). Sugar beet pulp can be fractionated into pectin, cellulose, and arabinose by using AF and/or endo-arabinase combined with ultrafiltration (Spagnuolo et al., 1999). The best enzymatic hydrolysis results were obtained when 100 U/g of beet pulp of each enzyme worked synergistically with yields of 100% arabinose and 91.7% pectin. The interaction of endo-xylanases and AFs can facilitate the degradation of arabinoxylans in grasses, and therefore enhance the digestibility of animal feed (Graham and Inborr, 1992). The purified AF from B. stearothermophilus partially delignified softwood kraft pulp (Bezalel et al., 1993). Treatment of the pulp with AF at 65⬚C for 2 h at pH 8.0 led to lignin release of 2.3%. The enzyme acted synergistically with a thermophilic xylanase in the delignification process, yielding a 19.2% release of lignin. Arabinan-degrading enzymes can be used to facilitate processing of fruits and vegetables (Beldman et al., 1993). Some monoterpenes of grape cultivars contribute to the flavor of wine. These compounds are present in must, both as free forms and as aroma precursors (Gunata et al., 1986). Glycosidically bound terpenes can be released by enzymatic hydrolysis in two stages. The AF from A. niger was active against monoterpenyl ␣-L-arabinofuranosylglucosides from grape by liberating monoterpenyl ␤-D-glucosides and arabinose regardless of the structure of the aglycon moiety (Gunata et al., 1990). A ␤-glycosidase then liberated the monoterpenols (Gunata et al., 1988). Spagna et al. (1998) immobilized AF from A. niger on chitin and chitosan for use in the food-processing industry, and in particular, in oenology. Table 5 summarizes the potential applications of AFs in biotechnology. 10. Concluding remarks AF is one of the rate-limiting enzymes in xylan degradation. Ineffectiveness of commercial hemicellulases in degrading arabinoxylans from various agricultural residues as well as Table 5 Application of ␣-L-arabinofuranosidase Bioconversion of lignocellulosic materials to fermentable products Improvement of animal feedstock digestibility Delignification of pulp Hydrolysis of grape monoterpenyl ␣-L-arabinofuranosylglucosides to increase aroma during wine making Clarification and thinning of juices

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production of by-products inhibitory to subsequent microbial fermentation during dilute acid pretreatment are formidable technological barriers that retard the development of various industrial processes. Commercial hemicellulase preparations need to be enriched with several accessory enzymes including AF to effectively convert hemicellulose to simple sugars. With the increase of enzyme usage in animal feed formulations, AFs will find an important role in the enhancement of animal feed digestibility.

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