Original Paper
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Acta Biochim Biophys
Sin 2007, 39: 811828
doi:10.1111/j.1745-7270.2007.00348.x
Feruloyl Esterases as
Biotechnological Tools: Current and Future Perspectives
Ahmed E FAZARY and Yi-Hsu JU*
Department of Chemical Engineering,
National Taiwan University of Science and Technology, Taipei 106-07, Taiwan,
China
Received: April 18, 2007
Accepted: June 16, 2007
*Corresponding author: Tel,
886-2-27376612; Fax, 886-2-2737 6644; E-mail, [email protected]
Abstract Feruloyl esterases represent a diverse
group of hydrolases catalyzing the cleavage and formation of ester bonds
between plant cell wall polysaccharide and phenolic acid. They are widely
distributed in plants and microorganisms. Besides lipases, a considerable
number of microbial feruloyl esterases have also been discovered and
overexpressed. This review summarizes the latest research on their
classification, production, and biophysicochemical properties. Special emphasis
is given to the importance of that type of enzyme and their related phenolic
ferulic acid compound in biotechnological processes, and industrial and
medicinal applications.
Keywords microbial feruloyl esterase; classification; production;
biophysicochemical property; application
In the past decade, microbial feruloyl esterases (FAEs) have become
important materials with considerable roles in biotechnological processes for
many industrial and medicinal applications. Thus, discovery of new FAEs with
novel properties continues to be an important research area. The amount of
research effort directed towards FAEs has increased dramatically since 1990.
For example, over the periods 1990–2000 and 2001–2006, the average number of
refereed publications describing research involving FAEs as a major component
(within abstract, title, and keywords; estimated using Elsevier SDOS search
engine) was 24 and 44, respectively. It is interesting to note that the
dramatic increase in publications concerned with FAEs observed between 2001
(four documents) and 2006 (11 documents) coincides with the most recent
discoveries on isolation, purification, and characterization of FAEs including
fungal and bacterial FAEs. There were also striking increases in the number of
publications concerned with ferulic acid (the related compound to FAEs). The
average number of documents was 242 for the period (1990–2000), while for
the period 2001–2006, the average number was 329 using the same search engine
(Elsevier SDOS). To date and to the best of our knowledge, the following is a concise
and complete review of the previous relevant studies conducted in nature,
chemistry, and biochemistry of ferulic acid, and FAEs about carbohydrate
esterase type, and their classification, crystal structure, microbial
production, biophysicochemical properties, and finally their biotechnological
applications in life.
Nature, Chemistry and
Biochemistry of Ferulic Acid
Ferulic acid (C10H10O4) is the most abundant, ubiquitous hydroxycinnamic acid derived from
phytochemical phenolic compounds [1], distributed widely throughout the plant
kingdom (spices, vegetables, grains, pulses, legumes, cereals, and fruits),
their by-products (tea, cider, oil, and beverages) and medicinal plants [1–10]. It is a
renewable resource for the biocatalytic or chemical conversion to other useful
aromatic chemicals from agricultural by-products in nature [11–15]. Ferulic acid is a phenylpropenoid derived from the cinnamic acid
3-(4-hydroxy-3-methoxyphenyl)-2-propenoic acid, 4-hydroxy-3-methoxycinnamic
acid, or coniferic acid (Fig. 1). It shows two isomers: cis (a
yellow oily liquid) and trans (crystalline) [3].Its nomenclature comes from Umbelliferae Ferula foetida from which
this active compound was isolated for the first time in 1866. Its functions
within living bodies include seed bud break suppression, indoleacetate enzyme
inhibition, dopa deoxidant enzyme inhibition, and protection against
microorganisms and pests [11–15].It is said that ferulic acid supplies hydrogens to free radicals
with phenolic-OH groups to provide the antioxidation effect. Ferulic acid also
has an active oxygen erasing function and the effect has been reported to be
similar to superoxide dismutase, known as the enzyme that protects living
bodies from the toxicity of active oxygen. Ferulic acid is believed to suppress
melanin generation by antagonizing tyrosine because their chemical structures
are similar. It is also believed to powerfully absorb the harmful long wave
ultraviolet (UV) band. It is listed as an “oxidation inhibitor” in
the “Food additive list” and expected to be used as an anti-oxidant
or anti-discoloration agent with many patents. Thus, ferulic acid has a wide
variety of applications because it has radical and active oxygen erasing
effects, absorbs UV causing active oxygen generation, and is a natural
substance. It seems to be particularly effective for cosmetic use as a
whitening agent and sunscreen, making use of its powerful long wave UV
absorbing function. It has been reported that the ferulic acid ester of vitamin
E drastically decreased melanin generation, with an expectation that it can be
a promising UV pigmentation depressor [14]. Many in vivo and in vitro
studies in humans, animals, and cell culture [1–17] have provided evidences
for the following actions of ferulic acid: (1) inhibition or prevention of
cancers of the breast, colon, lung, stomach, and tongue; (2) prevention of
brain damage by Alzheimer’s proteins; (3) inhibiting prostate growth; (4)
strengthening of bone; (5) prevention of diabetes-induced free radical
formation; (6) expansion of pancreatic islets; (7) reduction of elevated lipid,
triglyceride, and blood glucose levels; (8) lowering cholesterol production; (9)
prevention of hot flashes; (10) prevention of free radical damage to cell
membranes; (11) protection of skin from aging effects of UV light; (12)
stimulation of the immune system; and, finally, (13) stimulation of retinal
cell growth in degenerative retinal diseases.The polysaccharide network can be strengthened by further
hydroxycinnamate oligomers, for example, ferulic acid trimers or tetramers. Due
to the reactive nature of ferulic acid and the polymerization reactions of cell
wall peroxidases, it is most likely that trimers and large polymeric compounds
are formed by the radical coupling of plant ferulic acid. Because of the
chemical nature of the radical-generated polymerization, the extent of linkage
could continue until the reaction is limited either by the exhaustion of
substrate or the physical nature of the cell wall controlling movement and
flexibility of feruloylated polysaccharides. Fry et al. published
evidence for higher oligomers in maize suspension culture but did not present
defined structures [18]. It has been postulated that soluble feruloylated
arabinoxylans in bread dough are prevented from interfering with the formation
of the gluten protein network by oxidative coupling with free ferulic acid
[10]. It is due to the complexity of these compounds that only with the aid of
modern analytical equipment, such as mass spectrometry and 2-D nuclear magnetic
resonance spectroscopy, can the structure of such compounds be elucidated.
Diferulates and larger products make the major contribution to cross-linking of
wall polysaccharides in cultured maize cells [18]. Four different
dehydrotrimers of ferulic acid have recently been identified in maize bran [19–22]. The amount
of diferulate in maize bran varies from 0.0075% to 0.01% of the dry weight of
maize cell walls [22] in comparison to 1.3% of total diferulate levels and 2.6%
monomeric ferulic acid [23] in the same cereal bran. White asparagus cell walls have been shown to contain large amounts
of phenolics, including ferulic acid and its dimers and trimers. It has been
suggested that these phenolic compounds are mainly responsible for
cross-linking the different cell wall polymers related to asparagus hardening
[24]. During post-harvest storage, the asparagus texture and the amount of cell
wall phenolics increased significantly. The effect of post-harvest storage
conditions on the accumulation of ferulic acid and its derivatives were
investigated. Three different storage conditions were used: keeping the spears
in aerobic conditions at room temperature and at 4 ?C, and in anaerobic
conditions at room temperature. A direct relationship between phenol
accumulation and increases in texture was observed, and these changes were
dependent on temperature and storage atmosphere. An increase in temperature led
to a high amount of cell wall phenolics and the absence of oxygen in the
storage atmosphere delayed the accumulation [24].Two new dehydrotriferulic acids and two dehydrotetraferulic acids
were isolated from saponified maize bran insoluble fiber using size exclusion
chromatography on Bio-Beads S-X3 followed by Sephadex LH-20 chromatography and
semipreparative phenyl-hexyl reversed phase high performance liquid
chromatography (HPLC) [25]. The structures were identified on the basis of UV
spectroscopy, mass spectrometry, and 1- and 2-D nuclear magnetic resonance
equipment. [25].There are three kinds of pathways to extract ferulic acid from
natural resources: (1) from low-molecular-weight ferulic conjugates; (2) from
plant cell walls; and (3) from tissue culture or microbial fermentation.
Ferulic acid can also be synthesized chemically by the condensation reaction of
vanillin with malonic acid catalyzed by piperidine [26]. However, this method
produces ferulic acid as a mixture of trans– and cis-isomers. The
yield is high, but it takes as long as three weeks to complete the reaction.
Ferulic acid is one of the most abundant phenolic acids in plants, varying from
5 g/kg in wheat bran and corn kernel, 9 g/kg in sugar beet pulp [22,27], and 15–28 g/kg of rice
bran oil [28]. Today, the commercial natural ferulic acid is mainly produced from g-oryzanol in
rice bran oil, although plant cell wall materials contain more ferulic acid.
One of the main reasons is that ferulic acid cross-links with polysaccharides,
such as arabinoxylans in grasses, pectin in spinach and sugar beet, and
xyloglucans in bamboo, and it is not easy to release ferulic acid from
polysaccharides and purify it. Fortunately, two methods were developed [29] to
break the cross-link and release ferulic acid from plant cell wall materials.
One is an enzymatic method using FAEs. Although there was extensive research on
the preparation of ferulic acid using FAEs, and in some cases in combination
with polysaccharide hydrolases, this is not a practical way to produce
commercial ferulic acid because of high cost in the production of the enzyme by
microorganisms, and the long reaction time required to hydrolyze the bound
ferulic acid. Alkaline hydrolysis is another way to release ferulic acid from
polysaccharides and was often used to determine the content of ferulic acid in
bran [30], which could totally release the bound ferulic acid in short time at
high alkaline concentration and high temperature. However, it is difficult to
purify ferulic acid from the hydrolysate because it contains many components
and is a deep brown color. Using activated charcoal(carbon) to adsorb ferulic
acid could purify it from enzymatic solution, but it is not a feasible way to
purify ferulic acid in alkaline hydrolysate, because activated charcoal
strongly adsorbed the color substances produced during alkaline hydrolysis and
could be also washed out using alcohol or sodium hydroxide as the elute.
Previous studies found that anion macroporous resin had high capacity for
adsorbing ferulic acid in enzyme-hydrolysate from wheat bran and could be
washed out by solutions of ethanol-acetic acid-water, suggesting that it is a
choice to purify ferulic acid from alkaline hydrolysate [31]. Sugarcane is one
of the most important crops in the tropics, with global production now
estimated at 1.25 billion tons a year. It contains 73–76 g liquid/100 g and the
remaining 24–27 g/100 g is fiber discarded as bagasse. Sugarcane bagasse contains
more cellulose and less hemicellulose compared to wheat bran and maize bran,
thus the alkaline hydrolysate solution would not be viscous after treatment by
sodium hydroxide or potassium hydroxide [32]. Moreover, sugarcane bagasse
contains 1.36%2.58% ferulic acid [33,34], indicating that it is a suitable
resource for the preparation of ferulic acid by alkaline hydrolysis. However,
anion macroporous resin exchange chromatography can not be directly used to
purify ferulic acid in alkaline hydrolysate from the bagasse, as NaCl formed
during neutralization after NaOH hydrolysis would greatly decrease the
purification efficiency [35]. The similarity of chemical structures between ferulic acid and
vanillin has led to the development of a biotechnological way to transform
ferulic acid into vanillin [36–38]. In the process, ferulic acid was released from raw materials by
enzymatic treatment, and was biotransformed into vanillin by two different
white rot basidiomycetes. Aspergillus niger first transformed ferulic
acid into vanillic acid, and vanillic acid was then metabolized into vanillin
by Pycnoporus cinnabarinus. Vanillin obtained in this manner could be
considered as “natural” according to European and American
legislations. The release of ferulic acid from various raw materials was
studied with some commercial enzyme mixtures. For example, SP 584 (Novozymes,
Bagsvaerd, Denmark) was shown to be able to solubilize a high percentage of
ferulic acid present in sugar beet pulp to give both free and esterified
ferulic acid forms [39,40].
Carbohydrate Esterases
Through evolution, enzymes have acquired the ability to attack ester
linkages between hydroxycinnamic acids and carbohydrates in the process of
biodegradation of plant cell walls [41]. Plant cell walls constitute the
largest source of renewable energy on earth. They are composed of an intricate
network of polysaccharides that are among the most complex structures known.
For the complete breakdown of these polysaccharides, microorganisms require a
battery of specific enzymes. These polysaccharides that complex together with
polymers, such as lignin and cellulose, modulate the plant cell wall material
[41]. Complex highly-branched polysaccharides (arabinoxylans, pectin), are the
main compounds of the cell wall. Cinnamic acid derivatives such as ferulic or
coumaric acids are covalently bound to these polysaccharides through ester
linkages, increasing the complexity of these polysaccharidic structures [42].The complete degradation of plant cell wall polymers requires an
array of enzymes with different activities. The hydrolysis of hydroxycinnamate
esters in plant cell walls is catalyzed by cinnamoyl esterases (CEs; such as
cinnamoyl ester hydrolases, feruloyl/p-coumaroyl esterases, and ferulic/p-coumaric
acid esterases). CEs are a subclass of the carboxylesterases (EC 3.1.1.1) and
characterized by a relatively high activity on various hydroxycinnamate esters,
for example, methyl ferulate or [5-O-(trans-feruloyl)-a–L-arabinofuranosyl]-[(13)-b–D-xylopyranosyl-(14)-dxylopyranose,
compared to that of short chain alkyl esters (e.g., p-nitrophenyl/a-naphthyl
acetate) [43]. We might consider two classes: those in which sugar plays the
role of the ?cid,
such as pectin methyl esters; and those in which sugar behaves as the alcohol,
such as in acetylated xylan [44]. A number of possible reaction mechanisms
could be involved. The most common is a Ser-His-Asp catalytic triad catalyzed
deacetylation analogous to the action of classical lipase and serine proteases.
Other mechanisms such as a Zn2+ catalyzed deacetylation might
also be considered for some families [45].Two enzymes, feruloyl and cinnamoyl esterases (FAE-B), purified from
A. niger strains, have different physicochemical characteristics and
catalytic properties against cinnamoyl model substrates, such as methyl
derivatives of hydroxycinnamic esters and soluble feruloylated oligosaccharides
derived from plant cell wall [46]. These enzymes are exocellular and the
corresponding expression is inducible. A new strain of A. niger I-1472
was shown to produce numerous polysaccharide-degrading enzymes as well as
esterases that released ferulic acid from natural feruloylated
oligosaccharides, when grown on sugar beet pulp and maize bran [47].In 2002, it was reported that ferulic acid had been shown to link
hemicellulose and lignin. Cross-linking of ferulic acids within cell wall
components influences wall properties such as extensibility, plasticity, and
digestibility, and limits the access of polysaccharidaes to their substrates
[48]. The degradation of these cell wall polymers requires several hydrolytic
enzymes such as hemicellulases, xylanases, pectinases, and esterases [49].
Classification of FAEs Enzymes
FAEs (EC 3.1.1.73), including cinnamoyl esterases and cinnamic acid
hydrolases, are a subclass of the carboxylic acid esterases (EC 3.1.1) that
play a key physiological role in the degradation of the intricate structure of
the plant cell wall by hydrolyzing the ferulate ester groups involved in the
cross-linking between hemicelluloses and between hemicellulose and lignin
[50,51].Sugar beet pulp is an important source of ferulic acid with a dry
weight content of approximately 1% [52]. FAE occurs as a
single catalytic module and also as a part of a multimodular protein structure.
Some enzymes contain carbohydrate-binding modules and others are a part of a
multimodular complex. The fusion of a carbohydrate binding module to a
catalytic domain improves the catalytic efficiency of FAEs [53,54].The use of multiple alignments of sequences or domains that show FAE
activity, as well as related sequences, helped to construct a
neighborhood-joining phylogenic tree. The outcome of this genetic comparison
supported substrate specificity data and allowed FAEs to be sub-classified into
four types, A, B, C, and D [55–62], based on their substrate specificities towards synthetic methyl
esters of hydroxycinnamic acids (ferulic acid, diferulic acids, p-coumaric
acid, sinapinic acid, and caffeic acid) for substitutions on the phenolic ring,
and on their amino acid sequence identity (protein sequence), indicating an
evolutionary relationship among FAEs, acetyl xylan esterases, and certain
lipases. The nomenclature of FAEs follows both the source of the enzyme and the
type of FAE (Table 1) [63,64]. The classification of carbohydrate
esterases including acetyl xylan esterases and FAEs is available on the
Carbohydrate Active Enzymes database (http://www.cazy.org) [65].
FAE Specificity
FAEs from mesophilic and thermophilic sources [66] show substrate
specificity in accordance with their classification over a wide range of
phenylalkanoate substrates. Within types, however, differences can be observed
with respect to the position of certain substitutions, together with the
necessity for a specific group to be present at a specific location, for
example, the type C enzyme, StFaeC, requires a hydroxyl group to be present at
C-4 of the benzoic ring. Thermophilic FAEs in general had a lower catalytic
efficiency than the mesophilic counterparts, but released more ferulic acid
from plant cell walls within a short time interval at comparable temperatures. Studies indicate that type C FAEs show specificity for soluble
feruloylated arabinoxylans, whereas type A FAEs act more efficiently with
xylanases on water-unextractable wall material [67]. FAEs have enhanced
activity with family 11 xylanases for the release of monomeric ferulic acid,
but family 10 xylanases show preferential activity on diferulates. This might
be linked to the location of these ester-linkages on the arabinoxylan chain. As
preliminary results show that type C FAEs are effective bread improvers, and
are more specific for water-extractable arabinoxylans, the role of water-extractable
arabinoxylans in the process might require re-examination [56]. At present, the
lack of highly conserved sequences within the sequenced esterases does not
permit further classification of the FAEs, other than that their primary amino
acid sequences place the majority of these enzymes in carbohydrate esterase
family 1 of the Carbohydrate Active Enzymes database [65].
Crystal Structure of FAE
Enzymes
There are only 17 protein database entries in that type of enzyme
found in the Comprehensive Enzyme Information System (http://www.brenda-enzymes.info/).
One of the most thoroughly studied FAEs is type A (FAE-A) from A. niger
[42,46,68]. The crystal sequence analysis of FAE-A indicates that the enzyme is
a/b-hydrolase with
a serine, histidine, and aspartic acid catalytic triad. The protein with the
highest sequence similarity, not including the very similar FAEs with more than
93% identity from A. awamori and A. tubingensis, is the lipase
from Rhizomucor miehei [69], with an overall sequence identity of 32%.
FAE-A contains the characteristic lipase serine active site motif and, given
the sequence similarities, it was predicted that FAE-A would have considerable
structural homology and a similar catalytic mechanism to fungal lipases.
However, FAE-A has been shown not to possess lipase activity [70,71].The crystal studies show that many FAEs are modular, comprising of a
catalytic domain covalently linked to a non-catalytic carbohydrate-binding module
[54,65,60,71–75]. The structures of two bacterial FAEs have been published:
FAE_XynZ from Clostridium thermocellum [74]; and FAE_Xyn10B [63], also
from C. thermocellum. Both structures displayed the canonical
eight-strand a/b-fold of an esterase with the catalytic triad at the heart of the
active site. FAE is a compact globular protein (Fig. 2) [64,68]. The
C-terminal polyhistidine purification tag is clearly observed in the density
and has been modeled along with five cadmium ions per protein monomer that
coordinate the tag [64]. Although these enzymes have similar functionality to
FAE-A, there is no apparent sequence homology. Therefore, to examine the
structure of the enzyme and its substrate specificity, FAE-A has been
crystallized and the crystallographic structures solved for the native enzyme
and for the enzyme in complex with ferulic acid. The overall topology of the
protein is a classical a/b-hydrolase fold based on an eight-stranded b-sheet surrounded by a– helices. In
FAEs, six of the strands are parallel, with a pair of antiparallel strands at
the C-terminal side of the fold. There have also been reports of FAEs that are part of large
multidomain structures, such as cellulosomes [76]. Furthermore, fungal chimeric
enzymes composed of the sequences encoding the FAE-A fused to the endoxylanase
B of A. niger has also been constructed [65]. This fusion of naturally
free cell wall hydrolases onto bifunctional enzymes enabled the increase of the
synergistic effect on the degradation of complex substrates such as corn and
wheat bran compared to the result obtained using the free enzymes for both
substrates. Relatively few studies have been carried out to elucidate the
functional relationships between sequence-diverse FAEs. These FAEs have a
common a/b hydrolase fold and a catalytic triad (Ser-His-Asp) as shown in
lipases [64]. Faulds et al. [77] solved the crystal structure of an
inactive mutant of the FAE-A, AnFaeA (S133A), in complex with a feruloylated
trisaccharide and showed that, in agreement with the work of Schubot et al.
[74], tight binding of the carbohydrate was not required for catalysis. In
contrast to FAEs, the determination of the crystal structure of a family 10
xylanase from Thermoascus aurantiacus in complex with xylobiose
containing an arabinofuranosyl-ferulate side-chain revealed that the distal
glycone subsite of the enzyme makes extensive direct and indirect interactions
with the arabinose side-chain, whereas the ferulate moiety is solvent-exposed
[78].Generally, FAEs display broad substrate specificities, although the
structural motifs that discriminate the various enzymatic targets remain to be
elucidated. The first indication of the molecular determinants controlling the
substrate specificity of the cellulosomal FAE module of Xyn10B was achieved by
Prates et al. [63]. It is suggested that the presence of at least one
m-methoxy group in the substrate is required for binding, which explains why
the enzyme can not recognize methyl coumarate or caffeic acid. Considering the
remarkable impact of FAEs in various industrial and medical applications, it is
anticipated that these structural studies will provide an initial framework for
the rational design of novel enzymes with improved biotechnological potential
[63].
Microbial Production of FAEs
All microbial FAEs are secreted into the culture medium. They are
sometimes called hemicellulose accessory enzymes, because they help xylanases
and pectinases to break down plant cell wall hemicellulose. Most research on
the microbial production of FAEs to date involve the isolation, purification,
and characterization of FAEs derived from a wide range of microorganisms (fungi
and bacteria), as well as the enzymatic release of the products from cell wall
degradation.Summary experimental observations, with the knowledge of the
specific microorganisms and kind of esterase required, suggest that an
appropriate fermentation technique is required for the production of a specific
esterase. Esterases like FAEs and cinnamic acid esterases are produced from Aspergillus
sp. using either solid state or submerged fermentations. There are many
bioprocesses used for the production of enzymes. Many studies show that
solid-state fermentation (SSF) is attractive because it presents many
advantages for fungal cultivations [79]. SSF is defined as a fermentation
process in which microorganisms grow on solid materials without the presence of
free liquid. Water is present in an absorbed form within the solid matrix of
the substrate [80,81]. In SSF, productivity per reactor volume is much higher
than that in submerged culture [82]. Operational cost is also lower because
simpler plant and machinery are required [83]. Solid culture processes are
practical for complex substrates including agricultural, forestry, and food processing
residues and wastes, used as inducing carbon sources for the production of
FAEs. A. niger [84,85], different Penicillium sp. [84–87] and the
thermophilic fungus Sporotrichum thermophile [88] were capable of
producing FAEs when grown on agricultural residues such as sugar beet pulp,
wheat bran, wheat straw and brewer? spent grain under SSF. Penicillium brasilianum [85] was the
more effective FAE producer under SSF. However, in all of these fermentations,
other hydrolytic enzymes, such as cellulases and hemicellulases, are also
produced that incur severe costs in downstream separation.The choice of the appropriate substrate is of great importance for
the successful production of esterases. The substrate not only serves as a
source of carbon and energy, but also provides the necessary inducing compounds
for microorganisms. Monosaccharides and disaccharides such as glucose, xylose,
lactose, maltose, and xylitol generally do not support the production of FAEs
at all. This might be due to glucose catabolite repression and/or the induction
mechanism that has not been completely elucidated. Complex carbon sources that
contain high amounts of esterified ferulic acid such as de-starched wheat bran
[89–93],
maize bran [94–96], brewer’s spent grain [85,97], sugar beet pulp [55,60,83,84] and
wheat bran [58,59,83,98–101] have been efficiently used for the microbial production of FAEs
(Table 2). Several FAE enzymes have been purified and characterized from
aerobic and anaerobic microorganisms that use plant cell wall carbohydrates.
FAE activities have also been detected in mammalian cells and plants, but these
enzymes have yet to be purified and their protein sequences determined for
comparison with the microbial enzymes [102,103]. Over the end of the last decade, FAEs and xylanase have also been
produced by the lignocellulolytic actinomycete Streptomyces avermitilis
CECT 3339 [92,93] during growth on de-starched wheat bran and sugar beet
pulp as the carbon sources.
Although the production of FAEs from mesophilic microorganisms
has been well documented, a limited number of thermophilic microorganisms have
been reported to produce FAEs [92,93].Generally, FAE enzymes are produced (purified and characterized)
from several microorganisms (various bacteria and fungi) (Table 2),
including Streptomyces C254, Streptomyces C248, Streptomyces
olivochromogenes NRCC 2258 [89], S. thermophile ATCC 34628
[100,104], Strep. avermitilis CECT 3339 [92],
Schizophyllum commune ATCC 38548
[91], S. avermitilis UAH 30 [93], Neocallimastix MC-2
[105], P. brasilianum IBT 20888 [85], Penicillium
pinophilum CMI 87160ii [86], Trichoderma reesei QM 9414 [106],
Streptomyces sp. S10 [107], Talaromyces stipitatus CBS
375.48 [108], Piromyces MC-1 [109], Penicillium
funiculosum IMI-134756 [54], Piromyces brevicompactum,
Piromyces expansum [61], A. awamori IFO4033 [99], A.
awamori VTTD-71025, A. foetidus VTTD-71002 [98], A. niger [57,83],
A. niger CBS 120.49 [55], A. flavipes [97], A. niger CS 180
(CMICC 298302) [110], A. oryzae VTTD-85248, A. niger VTTD-77050 [98], A. niger NRCC 401127 [89],
A. niger NRRL3 [111], A. niger CS 180 (CMICC 298302), A.
niger 1-1472 [59,60,110], Aureobasidium pullulans NRRLY
23311-1 [112], Bacillus subtilis ATCC 7661, B. subtilis FMCCDL1,
B. subtilis NCIMB 3610 [113], Clostridium stercorarium NCIMB
11754 [112], Neurospora crassa ST A(74 A) [58], C.
stercorarium [112], C. thermocellum [114], Humicola insolens
[115], Sporo. thermophile [107,104,116,117], and Fusarium oxysporum
[106,108].
Action, Synergism, and Organic
Synthesis of FAEs
In 2000, six novel feruloyl esters of triterpene alcohols and
sterols, two trans-ferulates (cycloeucalenol and 24-methylenecholesterol
trans-ferulates), and four cis-ferulates, (cycloartenol,
24-methyelenecycloartanol, 24-methylcholesterol, and sitosterol cis-ferulates),
as well as five known trans-ferulates (cycloartenol,
24-methylenecycloartanol, 24-methylcholesterol, sitosterol, and stigmastanol trans-ferulates),
and one known cis-ferulate (stigmastanol cis-ferulate), were
isolated from the methanol extract of edible rice bran [118]. The synthesis of
pentylferulate was achieved using a water-in-oil microemulsion system
containing an FAE from A. niger [83]. Although some reports describe the
enzymatic synthesis of alkyl and glyceride ferulates, there are few papers
concerning enzymatic preparation of feruloylated carbohydrates [119]. Ferulic acid was also efficiently released from wheat bran by a
mixture of Trichoderma viride xylanase and A. niger
ferulate esterase FAE-A [120–122]. In addition, the release of ferulic acid from maize bran by
commercial enzymes was low and autoclaving treatment of the bran improved the
solubilization of feruloylated oligosaccharides, which are substrates for FAEs
[60,65]. However, the use of cell wall-degrading enzymes and FAEs involved
either dependence on commercially available mixtures or numerous steps of
purification of the enzymes, as in the case of FAE-A.Recently, FAEs from Humicola insolens [123] catalyzed the
transesterification of secondary alcohols with excellent enantioselectivity,
which are substrates that bear no structural similarity to the natural
substrates of this enzyme [124]. The observations of feruloyl and p-coumaroyl
esterase activities of the cleavage of ester cross-linkage have led to the
purification and partial characterization of FAEs from various sources
[55,87,120–122,125,126]. Several studies on the release of ferulic acid from
feruloylated polymers by FAE have indicated that the participation of a much
more complicated enzymatic system is needed [86,127–129]. However, previous
studies on the interactions of FAEs have been mainly focused on enzymes such as
xylanase and b-xylosidases [120,121,130–134], and there is little information on
xylan-debranching enzymes such as a–L-arabinofuranosidase or on the effect
of the co-existence of xylanase and arabinofuranosidase on FAEs.It has been documented that FAEs are inducible
[89,90,92,93,125,135,136]. The expression of the FAE-encoding gene from
eukaryotic A. niger is regulated by xylose, arabinose and ferulic acid.
In human, fecal inoculum FAE activity could be induced by fine bran cell wall
material, but the induction of FAE activity in intestinal microflora is largely
unknown [27]. Using Novozym 435 as catalyst, the syntheses of ethyl ferulate
from ferulic acid (4-hydroxy 3-methoxy cinnamic acid) and ethanol, and octyl
methoxycinnamate from p-methoxycinnamic acid and 2-ethyl hexanol were
successfully achieved recently in our laboratory [137].In 2001, it was reported that the solubilization of A. niger FAE-A
in a cetyltrimethylammonium bromide water-in-oil microemulsion offered a number
of advantages for the enzymatic synthesis of ferulate esters [138]: (1) a good
yield of pentylferulate was obtained (60%); (2) the pentylferulate yield was
independent of the water content of the microemulsion system; (3) a high
substrate (n-pentanol) concentration was achievable; and (4) an increased
stability of FAE-A in cetyltrimethylammonium bromide water-in-oil microemulsion
was observed when compared with the correspondent stability in water.
Activity Assays of Microbial
FAEs
Several methods have been reported for measuring the activity of the
purified microbial FAEs. Most are based on HPLC techniques, using enzymatic
hydrolysis of ferulic acid esters [139,140], plant polysaccharides
[92,93,109,130], their fragments [141] and fragment analogs [142], as well as
chlorogenic acid or hydroxycinnamic tartrate-containing materials [139]. The
assay was based on the measurement of ferulic acid released from ethyl
ferulate. One volume of enzyme solution was mixed with 3 volumes of 1.33 mM
ethyl ferulate in 0.05 M potassium phosphate buffer, pH 6.5. Both solutions
were preheated to 40 ?C before mixing. The final mixture was incubated at the
same temperature. At various time intervals, 0.3 ml aliquots of the reaction
mixture were withdrawn and mixed with 0.1 ml of 0.35 M H2SO4 to stop the reaction. This was followed by
the addition of 0.3 ml of 1.0 mM benzoic acid as the internal standard and 0.1
ml of 0.7 M NaOH. The solution was mixed by vortexing, passed through a 0.45 mm syringe
filter, and analyzed by HPLC. The acidic components of the samples were eluted
with a mixture of water : acetic acid : 1-butanol (350:1:7; V/V/V)
with a flow rate of 1 ml/min. A linear gradient of methanol (ramped up to 100%
methanol in 5 min) was used to wash off the unreacted ethyl ferulate. All ethyl
ferulate, ferulic acid, and benzoic acid were dissolved in minimal volume of
ethanol prior to mixing with buffer or water. Unfortunately, these HPLC methods require expensive equipment, are
time-consuming, and not suitable for rapid analysis of large numbers of
samples. Some of these methods require the isolation of natural substrates,
which adds another laborious step. Capillary zone electrophoresis [87] and gas
chromatography [109] have also been applied to FAE assays using natural
substrates, their analogs and hydroxycinnamic methyl esters, but these methods
possess similar disadvantages.Spectrophotometric analysis for FAE activity described in published
reports relies on the use of differences in spectral properties of free ferulic
acid and its natural esters [143,144] or their analogs [142]. Such methods
measure relatively low changes of absorbance and have not become generally
adopted. A new spectrophotometric method [145] for determining FE activity
using 4-nitrophenyl ferulate, a cheap substrate that is easy to prepare [146],
was used. The method is simple and is based on the measurement of 4-nitrophenol
released upon enzyme action. The main drawback in using such a substrate is its
low solubility in aqueous buffer solutions. Inspired by the method for lipase
assays, dimethyl sulfoxide and a detergent, Triton X-100, were used to create transparent
emulsions stable for several hours, enabling the measurement of FAE activity
spectrophotometrically [147]. A variety of natural substrates such as
feruloylated oligosaccharides [61,114] and de-starched wheat bran [148] have
been used to assay the enzymes. Synthetic esters of various cinnamic acids and
short chain alcohols, such as methyl and ethyl ferulates, were also introduced
for assaying FAEs [27,131]. In all cases, FAE activity was determined by
measuring the rate of hydrolysis of model substrates such as methyl esters of
hydroxycinnamic acids, that is, methyl ferulate, methyl sinapinate, methyl
p-coumarate, and methyl caffeate. One unit of FAE activity was defined as the
amount of enzyme required for releasing 1 mM ferulic acid per min at pH 6.0 at 37 ?C.
Biophysical and Biochemical
Properties of Microbial FAEs
From 1991 to 2006, more than 40 FAEs were purified and characterized
from microorganisms such as C. stercorarium [126], C. thermocellum [114],
Sporo. thermophile [121], S. olivochromogenes [127], A.
awamori [149], F. oxysporum [122,127], Fusarium proliferatum [111],
N. crassa [58,150], A. nidulans [149], Aureo. pullulans [112],
A. niger [151], Piromyces equi [61], Cellvibrio japonicus
[106], and Tal. stipitatus [59,108]
(Table 3). The biophysical and biochemical characteristics of the purified FAEs
show significant variations in chemical characteristics such as molecular
weight (27–210 kDa), isoelectric point, and optimum hydrolytic reaction
conditions (pH 3.0–9.5) (Table 3). There is no correlation between the
biochemical characteristics of the FAEs and their optimal reaction conditions
found to date. Microbial FAEs have a broad range of pH and temperature
dependence, with optimal activities occurring between pH 5.0 and8.0, and between
30 ?C and 65 ?C.Results obtained from the biophysico-chemical studies on FAEs will help
to advance the use of that type of enzyme in food processing and agricultural
industries. In addition, knowledge of their biophysical and biochemical
properties should be useful for research workers in the biomedicine field
Applications of Microbial FAEs
There has recently been considerable interest in a large number of
potential applications of these enzymes due to their roles in many
biotechnological processes, in various industries (chemicals, fuel, animal
feed, textile and laundry, pulp and paper, food and agriculture, and
pharmaceutical), also in their potential applications in obtaining ferulic acid
from agro-industrial waste materials such as those produced by milling,
brewing, and sugar industries. The prospect of broad applications of FAEs has
fueled much interest in these enzymes, as shown by the increasing number of
FAEs discovered in microbial organisms in recent years. FAEs could be used in pulp and paper processes [152,153] and as
animal feed additives [3,4,120–122] to facilitate nutrient assimilation. In addition, ferulic acid,
which is the most abundant cinnamic acid in plant cell walls, is a precursor
for vanillin and its access through biotechnological methods is crucial in the
quest for natural vanillin [1–8]. As well as being exploited as a hydrolase, FAE was shown to be a
good catalyst in synthesizing sugar-phenolic esters [3,4,120–122], and could
also be used to functionalize sugar polymers by adding phenolic derivatives
onto the natural biopolymers.Generally, FAEs benefit microorganisms, industry, and biochemists.
Some of the ester-linked substituents on plant cell wall polysaccharides retard
or inhibit microbial infection [154]. There are many examples in published
reports concerning the antimicrobial nature of the phenolic compounds towards
some microorganisms. Phenolic components of the plant cell wall, especially
p-coumaric acid, ferulic acid, and p-hydroxybenzaldehyde, inhibit the growth of
rumen microorganisms [155,156] and phenolic acids derived from plant cell walls
have long been used as food preservatives [69] to inhibit microbial growth. Magnaporthe
grisea, a rice blast fungus, produces a xylanase and an arabinofuranosidase
that act synergistically to release arabinoxylo-oligosaccharides from rice cell
walls. These compounds contain esterified ferulic acid, and the release leads
to the death (presumably programmed cell death) of surrounding rice cells. In
vitro removal of the ferulic acid moiety (i.e., to give phenolic and
oligosaccharide separately) destroyed more than 95% of this killing ability,
which would enhance the chances of the colonization of the rice cell wall by
the pathogen in the presence of a cinnamoyl esterase [157]. As phenolic acid sugar esters have clear antitumor activity and the
potential to be used to formulate antimicrobial, antiviral, and/or
anti-inflammatory agents [1,108], specific FAEs could be used in the tailored
synthesis of such pharmaceuticals [158–160]. The FAE system of Talaromyces
stipitatus has been studied and three discrete FAEs, including a type C
esterase, with broad specificity against hydroxycinnamate esters [161,162] have
been found. The re-establishments of efficient use of cheap agricultural waste
materials, with their synergistic action with other lignocellulose-degrading
enzymes, are promising tools in various agro-industrial processes [163]. Other
potential applications include production of important medicinal compounds,
improvement of bread quality, pulp treatment, juice clarification, improvement
of quality of animal feedstock, production of biofuel, and synthesis of
oligosaccharides [156]. Therefore, effective FAEs production is a vital prerequisite
for successful applications in various industries. To achieve this goal, it is
necessary to use FAEs, as well as defined polysaccharides and oligosaccharides
from different agricultural raw materials.Hemicellulases and cellulases offer alternatives to augment chemical
and mechanical paper-pulping methods, and there is a large amount of published
work on this subject [60,156]. Acetylxylan esterases and FAEs might enhance
this process by removing substitutions and linkages between polymers during
pulping, thus making the solubilization of lignin-carbohydrate complexes easier
[50,51,56,57,60,61,110,156]. After the removal of acetyl groups, the
hemicellulases crystallize and form more cellulose-like structures thus
affecting polysaccharide solubility and cohesiveness. Ferulic acid is
postulated to form cross-links with proteins in wheat, which is important in
the rheology of doughs. Pretreatment of lignocellulosic material by secreted
fungal enzymes leads to de-esterification, which increased the rate of in
vitro digestion by ruminal microorganisms by approximately 80%
[50,51,56,57,60,61,110,156]. FAEs are potential analytical aids in modern carbohydrate chemistry.
In combination with other plant cell wall-degrading enzymes, the esterases will
provide important tools in understanding the fine structure and linkage
patterns that exist in the plant cell wall, but the science is at an early
stage and ripe for exploitation [50,51,56,57,60,61,110,156]. Arabinoxylans and b-glucans in the
cell walls of barley have been shown to be associated either together or to a
common component through an ester bond, as shown by specific hydrolysis by a
pure cinnamoyl esterase [164]. The exact nature of the covalent bond between
lignin and carbohydrate polymers in the cell wall matrix of various plants has
still to be determined, although evidence is beginning to accrue on these
structures. FAEs could provide a useful tool in helping to determine this link
[165]. FAEs are secreted by a number of bacterial and fungal organisms that
exploit plants either to enter the plant cell or to use the cell wall material
as a nutritional resource. The complete degradation of plant cell wall polymers
requires multi-enzyme complex systems. Most FAEs have been shown to act
synergistically with xylanases, cellulases, and pectinases to break down
complex plant cell wall carbohydrates [166,167]. Products of the maize industry are ideal stock materials for
biotechnology processes. An example is ferulic acid, an aromatic food
anti-oxidant that can be isolated from maize fiber after wet milling and is
converted to valuable compounds such as vanillin, an important flavourant used
extensively in foodstuffs [168]. Apart from its use in flavoring, vanillin is
also required for the synthesis of pharmaceutical drugs and is used extensively
in the perfume and metal plating industries. In agriculture it has herbicidal
action, and can be used as a ripening agent to increase the yield of sucrose in
sugar cane [169].The demand for ethanol has generated the most significant market,
where it is used either as a chemical feedstock or as an octane enhancer or
petrol additive. Global crude oil production is predicted to decline from 25
billion barrels to approximately 5 billion barrels in 2050 [164]. In the USA,
fuel ethanol has been used in gasohol or oxygenated fuels since the 1980s.
These gasoline fuels contain up to 10% ethanol by volume. It is estimated that 4.54 billion liters of
ethanol is used by the American transportation sector and that this number will
rise phenomenally as the American automobile manufacturers plan to manufacture
a significant number of flexi-fueled engines which can use a blend of 85%
ethanol and 15% gasoline by volume. The production of fuel ethanol from sugars
or starch impacts negatively on the economics of the process, thus making
ethanol more expensive compared with fossil fuels. Hence the technology
development focus in the production of ethanol has shifted towards the use of
residual lignocellulosic materials to lower production cost. An improved use of
wheat endosperm by-products in this type of ethanol production would generate a
fermentable hydrolysate based on the hemicellulose fraction. Complete enzymatic
hydrolysis of arabinoxylan requires both depolymerizing and side-group cleaving
enzyme activities such as FAEs. Any hemicellulose containing lignocellulose
generates a mixture of sugars upon pretreatment alone or in combination with
enzymatic hydrolysis. In Europe, potable alcohol manufacturing plants are based
on wheat endosperm processing, with the hemicellulosic by-product remaining
after fermentation consisting of approximately 66% (W/W)
arabinoxylan [164]. Fermentable sugars from cellulose and hemicellulose will essentially
be glucose and xylose, which can be released from lignocellulosics by single-
or two-stage hydrolysis, thereby leading to mixtures of glucose and xylose or
separate glucose- and xylose-rich streams. Conventional methods, applied for
bioconversion of cellulose and hemicellulose to ethanol, involve acid or enzyme
hydrolysis of biopolymers to soluble oligosaccharides followed by fermentation
to ethanol. A synergistic effect between cellulases, FAEs and xylanases was
proven under a critical enzymatic concentration, in the saccharification of
steam-exploded wheat straw [170]. In 2004, for the first time, the homologous overexpression of the
FAE-B gene in A. niger was evaluated [100,101]. The main characteristics
of the recombinant FAE-B were in good agreement with those of the corresponding
native protein and new insights were provided in order to present a more
complete description of this enzyme. Sufficient amount of proteins obtained
from the FAE-B overproduction will allow structure-function studies to be
carried out. In addition, these promising results of overproduction will permit
to envisage the first experiments of application and to check the potential of
this enzyme in the pulp and paper industry, or more generally in the
biotransformation of phenolic compounds of agricultural byproducts. The synthetic activity pattern of FAEs for the transesterification
of various methyl esters of cinnamic acids is similar to that of their
hydrolytic action [120–122,133,104,116,117]. The active sites of FAEs from mesophilic and
thermophilic sources were probed using methyl esters of phenylalkanoic acids.
Type B and type A FAEs were found to be appropriate biocatalysts for the
synthesis of hydroxylated phenolic compounds and methoxylated phenolic
compounds, respectively. StFaeC showed maximum hydrolytic activity towards
4-hydroxy-3-methoxy cinnamate, indicating that it might be the most promising
type of FAE as a biocatalyst for the enzymatic feruloylation of aliphatic
alcohols and oligosaccharides or polysaccharides. Many reports show that StFaeC
catalyzed the transfer of the feruloyl group to L-arabinose in a ternary water-organic mixture
consisting of n-hexane, t-butanol, and water system, with an approximately 40%
conversion of L-arabinose
to its feruloylated derivative [120–122,133,104,116,117]. FAEs derived from
non-recombinant producing strains might be important for better acceptance by
consumer? food
related applications. Optimizing FAE production in native producing strains is
therefore important. An increase in biomass production in a bioreactor will
lead to a significant improvement in overall productivity, which will in turn
result in a cost reduction, and thus a more competitive and more accessible
FAE-based enzyme technology [153,170]. A potentially important application of FAE is in the use of vastly
abundant renewable chemical feedstocks, cellulose/lignocellulose. Ferulic acid
bond, which provides the cross-linking between lignin and cellulose, and
between polysaccharide chains, is an important factor that makes plant cell
wall materials recalcitrant and resistant to enzyme hydrolysis. Although
chemical hydrolysis is effective to de-polymerize cellulose and hemicellulose
materials, the harsh conditions it entails often lead to the generation of toxic
by-products that require additional processing steps. The use of enzymes could
avoid such problems but is not currently feasible, as complete hydrolysis has
not been achieved and the cost of enzymes is considered to be inhibitive for
application on a commercial scale [109,171]. Due to the complex nature of the
polymeric material, it is conceivable that its complete hydrolysis will require
synergistic use of a suite of enzymes. FAE, being an enzyme that breaks down
the cross-linking of the polymers chain, is expected to be particularly
important in separating lignin from cellulose, de-polymerizing hemicellulose
into fermentable sugars, and in making polymeric materials more accessible to
other enzymes [172].
Conclusion
Microbial
FAEs acting on plant cell wall polymers represent key tools for degradation of
plant cell wall polysaccharides, modification of physical and chemical
properties of plant cell walls and components, and elucidation of plant cell
wall structures. The field is at an early stage, and there is a lot of work to
be done on the enzymology, especially 3-D structures and site-directed
mutagenesis combined with rigorous kinetics to enhance understanding of binding
sites, substrate recognition, and catalytic mechanisms. Cloning of more enzymes
would allow classes and relationships between these esterases to be identified.
Further work on the structure of the plant cell wall is required, helped by the
existence of highly purified esterases, to improve understanding of the
synergistic interactions between enzymes. There are many unanswered questions
concerning regulation of expression, including full gene sequences, extent of
coordinate regulation, and molecular mechanisms in response to putative
inducers. In summary, future work on FAEs should include: (1) elucidating the
structural characteristics that determine specificity (structure-function
relationships); (2) isolation, characterization and cloning of plant FAEs; (3)
extending the use of existing and novel esterases as probes for cell wall structures;
and (4) production of tailor-made esterases with novel functionalities.
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