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By , over 14, fungal species capable of degrading cellulose had been isolated, but only a few of them were subjected to in-depth studies [ 23 ]. Obviously, fungi contribute significantly to the decay of lignocellulosic residues in nature by producing many different lignocellulolytic enzymes. Most fungal strains produce various enzymes in large amounts which are released in the environment and act in a synergistic manner.

The breakdown of lignocellulosic biomass involves the formation of long-chain polysaccharides, mainly cellulose and hemicellulose, and the subsequent hydrolysis of these polysaccharides into their component 5- and 6-carbon chain sugars. In biofuel production, these sugars can be converted to bioethanol through fermentation processes [ 24 ]. The primary challenge in biomass conversion to bioethanol is achieving yields that make it cost-competitive with the current fossil-based fuels. Cellulose in the plant cell wall is not readily available to enzymatic hydrolysis cellulases due primarily to; 1 low accessibility of micro- crystalline cellulose fibers, which prevents cellulases from working efficiently, and 2 the presence of lignin mainly and hemicellulose on the surface of cellulose, which prevents cellulases from accessing the substrate efficiently [ 25 ].

Thus, pretreatment of lignocellulosic residues before hydrolysis is a prerequisite and this can be performed by different methods discussed in section 3. High temperature and acid have been used initially for chemical cellulose degradation and they are still involved in pretreatment of lignocellulosic residues at industrial scales. However, this approach is expensive, slow and inefficient [ 26 ]. In addition, the overall yield of the fermentation process will be decreased because this pretreatment releases inhibitors such as weak acids, furan and phenolic compounds [ 27 ].

Some of these problems could be overcome by applying microorganisms such as fungi. For example, thermophilic fungal species such as Sporotrichum thermophile [ 28 ], Thermoascus aurantiacus [ 29 ] and Thielavia terrestris [ 30 ] have been proposed as good candidates for bioconversion of lignocellulosic residues to sugars and offer the great potential to be used at industrial scales. Applying thermophilic fungal species at industrial scales also allows energy savings because the costly cooling after steam pre-treatment is avoided and saccharification rates are improved.

These fungi have been shown to produce cellulases and to degrade native cellulose; however, the enzyme activity in thermophilic organisms e. The initial conversion of biomass into sugars is a key bottleneck in the process of biofuel production and new biotechnological solutions are needed to improve their efficiency, which would lower the overall cost of bioethanol production. Despite the fact that some fungal strains have the advantages of being thermostable and producing cellulases, most of these fungal strains do not produce sufficient amounts of one or more lignocellulolytic enzymes required for efficient bioconversion of lignocellulosic residues to fermentable sugars.

Wild-type T. These rate-limiting steps in the bioconversion of lignocellulosic residues to ethanol remain one of the most significant hurdles to producing economically feasible cellulosic ethanol. Improving fungal hydrolytic activity and finding stable enzymes capable of tolerating extreme conditions has become a priority in many recent studies.

This review focuses on lignocellulosic bioconversion by the application of different lignocellulolytic enzyme-producing fungi. In addition, this review addresses recent efforts to create robust fungal strains using mutagenesis, co-culturing and heterologous gene expression techniques and how these robust organisms can help overcome some of the critical issues in biofuel production.

Lignocellulolytic enzymes-producing fungi are widespread, and include species from the ascomycetes e. Fomitopsis palustris and finally a few anaerobic species e. Orpinomyces sp. Biomass degradation by these fungi is performed by complex mixtures of cellulases [ 33 ], hemicellulases [ 31 ] and ligninases [ 7 , 34 ], reflecting the complexity of the materials. Cellulases and most hemicellulases belong to a group of enzymes known as glycoside hydrolases GH.

Currently more than GH have been identified and classified into families for more information please visit the CAZy web page; www. Interestingly, the same enzyme family may contain members from bacteria, fungi and plants with several different activities and substrate specifications. Table 2 summarizes a few different fungi producing different lignocellulolytic enzymes. All GH 12 cellulases, for example, hydrolyze glycosidic bonds by the retaining mechanism whereas family 6 cellulases use the inverting mechanism [ 33 , 36 ].

In both mechanisms, two catalytic carboxylate residues are involved and catalyze the reaction by acid-base catalysis. Many different fungal species have the ability to degrade cellulose by producing extracellular fungal cellulose-degrading enzymes including endo-cleaving endoglucanases and exo-cleaving cellobiohydrolases. Endoglucanases can hydrolyze glycosidic bonds internally in cellulose chains whereas cellobiohydrolases act preferentially on chain ends. Cellulases mostly have a small independently folded carbohydrate binding module CBM which is connected to the catalytic domain by a flexible linker.

The CBMs are responsible for binding the enzyme to the crystalline cellulose and thus enhance the enzyme activity [ 33 ]. Currently many CBMs have been identified and classified into 54 families, however only 20 families 1, 13, 14, 18, 19, 20, 21, 24, 29, 32, 35, 38, 39, 40, 42, 43, 47, 48, 50 and 52 have been found in fungi. Different fungal cellulolytic enzymes and their main features are summarized in Table 3. Endoglucanases EG are also referred to as carboxymethylcellulases CMCase , named after the artificial substrate used to measure the enzyme activity. EG initiate cellulose breakdown by attacking the amorphous regions of the cellulose, making it more accessible for cellobiohydrolases by providing new free chain ends.

This has been shown by the effect of the enzyme on carboxymethylcellulose and amorphous cellulose [ 8 ]. Fungal EGs are generally monomers with no or low glycosylation and have an open binding cleft. They mostly have pH optima between 4. Studies have shown that many fungi produce multiple EGs. For example, T. For example, four of five EGs in T.

CBHs have been shown to create a substrate-binding tunnel with their extended loops which surround the cellulose [ 58 , 59 ]. Studies have shown that some CBHs can act from the non-reducing ends and others from the reducing ends of the cellulosic chains, which increases the synergy between opposite-acting enzymes. Cellobiose, the end product of CBHs, acts as a competitive inhibitor, which can limit the ability of the enzymes to degrade all of cellulose molecules in a system [ 36 , 44 , 60 ].

BGLs have been placed in families 1 and 3 of glycoside hydrolases based on their amino acid sequences [ 64 ]. BGLs show the most variability among the cellulolytic enzymes due to their structure and localization. While some BGLs have a simple monomeric structure with around 35 kDa molecular mass e. Regarding localization, BGLs can be grouped into three different types including intracellular, cell wall-associated and extracellular [ 67 ]. Moreover, BGL production in T. Attempts with some success have been made to improve BGL activity in T. More recently, the production of T. Several different enzymes are needed to hydrolyze hemicelluloses, due to their heterogeneity [ 10 ].

Similar to cellulases, hemicellulases are usually modular proteins and have other functional modules, such as CBM, in addition to their catalytic domains. Also similarly to cellulases, most of the hemicellulases are glycoside hydrolases GHs , although some hemicellulases belong to carbohydrate esterases CEs which hydrolyze ester linkages of acetate or ferulic acid side groups [ 71 , 72 ]. Hemicellulases belong to 20 different GH families 1, 2, 3, 4, 5, 8, 10, 11, 26, 27, 36, 39, 43, 51, 52, 53, 54, 57, 62 and 67 and all of them except for 4 families 4, 8, 52 and 57 have been found in fungi.

All but 1 family 7 of the 7 different CE families 1, 2, 3, 4, 5, 6 and 7 reported for hemicellulases have been found in fungi [ 35 ]. Similarly to cellulases, aerobic fungi such as Trichoderma and Aspergillus secrete a wide variety of hemicellulases in high concentrations 8 and 12 hemicellulases, respectively and these work in a synergistic manner [ 71 ]. These include two ligninolytic families; i phenol oxidase laccase and ii peroxidases [lignin peroxidase LiP and manganese peroxidase MnP ] [ 74 ].

White-rot basidiomycetes such as Coriolus versicolor [ 73 ], P. Interestingly, LiP is able to oxidize the non-phenolic part of lignin, but it was not detected in many lignin degrading fungi. In addition, it has been widely accepted that the oxidative ligninolytic enzymes are not able to penetrate the cell walls due to their size. Thus, it has been suggested that prior to the enzymatic attack, low-molecular weight diffusible reactive oxidative compounds have to initiate changes to the lignin structure as discussed below [ 76 , 77 ].

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A few decades ago, non-enzymatic degradation mechanisms for plant cell-wall polysaccharide degradation were also considered and over the time more evidence for these was found. These free radicals attack polysaccharides as well as lignin in plant cell walls in a nonspecific manner providing some cleavages which make it easier for the lignocellulolytic enzymes to penetrate [ 80 , 81 ]. CDH, an extracellular monomeric protein with some glycosylation has been identified in a number of wood- and cellulose-degrading fungi including basidiomycetes mostly white-rot fungi and ascomycetes growing on cellulose.

In addition, CDH with in ascomycetes or without CBM in basidiomycetes have been identified however even in the absence of CBM they are able to bind to cellulose through hydrophobic interactions [ 82 ]. It has been shown in some fungi that under cellulolytic conditions CDH production increases which helps cellulases and hemicellulases [ 83 , 84 ]. It is now widely accepted that CDH are able to degrade and modify all three major components of the lignocellulosic residues cellulose, hemicelluloses and lignin by producing free hydroxyl radicals in a Fenton-type reaction for detailed information please refers to the review by Baldrin and Valaskova, [ 44 ].

It has been shown that white and brown-rot fungi produce low molecular weight chelators which are able to penetrate into the cell wall. For example Gloeophyllum trabeum produces a low molecular weight peptide known as short fiber generating factor, SFGF which can degrade cellulose into short fibers by an oxidative reaction [ 81 , 85 ]. It has also been reported that some of these low molecular weight compounds are quinones which have to be converted to hydroquinones by some fungal enzymes Table 4 and then through Fenton reaction, free hydroxyl radicals will be produced [ 73 ].

Different glycopeptides with different molecular weight ranging from 1. Similar to the other mechanisms, glycopeptides are able to catalyze redox reactions and thus produce free hydroxyl radicals. Anaerobic fungi represent a special group of microorganisms inhabiting the gastro-intestinal tract of ruminants and most non-ruminant herbivores. These fungi, along with some anaerobic bacteria mainly from the class Clostridia e.

Clostridium thermocellum [ 92 ] , produce a range of cellulolytic and hemicellulolytic enzymes in a multienzyme complex known as cellulosome. The first anaerobic gut fungi able to break down ingested lignocellulosic residues were identified in by Orpin [ 93 ] and since then 6 genera and 18 species have been identified some of which are shown in Table 2. The cellulosome, however, was initially discovered in anaerobic bacteria Clostridium thermocellum in [ 94 ], and then first described in anaerobic fungi in Neocallimastix frontalis [ 95 ].

However, in anaerobic fungi such as N. All hydrolytic enzymes in the cellulosome are bound together by noncatalytic scaffolding proteins. Interestingly, 50 fungal FDDs have been identified so far which present different amino acid sequences than those found in bacterial dockerins [ 31 , 97 ]. Anaerobic fungi efficiently hydrolyze cellulose and hemicellulose by producing many lignocellulolytic enzymes.

Most of the enzymes are associated with the cellulosome; however, some free enzymes also have been identified. In Piromyces sp. Interestingly, FDD has been reported only for 11 of the genes, which indicates that these cellulases are cellulosome-associated. Moreover, CBM has been identified only in three of those 17 genes, including two cellulases and one hemicellulase [ 31 ].

Despite many advantages of cellulosomes such as synergistic activity between the components and efficient hydrolytic activity on both cellulose and hemicellulose, fungal cellulosomes are much less well characterized compared to bacterial cellulosomes. The bioconversion of lignocellulosic residues to valuable materials such as ethanol is more complicated than the bioconversion of starch based residues and thus requires four steps of processing, of which the first three are bio-related processes and the fourth is primarily a chemical engineering process that will not be discussed in great detail in this review; i pretreatment ii de-polymerization saccharification of cellulose and hemicelluloses to soluble monomer sugars hexoses and pentoses by a process known as hydrolysis, iii conversion of these monomeric sugars to valuable products such as ethanol in a fermentation process and iv separation and purification of the products Figure 1.

In order to improve the yield, each step in the bioconversion process has to be optimized. In addition, process integration has to be considered in order to minimize process energy demand [ 22 ]. Pretreatment of the lignocellulosic residues is necessary because hydrolysis of non-pretreated materials is slow, and results in low product yield.

Some pretreatment methods increase the pore size and reduce the crystallinity of cellulose Figure 1. Pretreatment also makes cellulose more accessible to the cellulolytic enzymes, which in return reduces enzyme requirements and thus the cost [ 99 ]. Many different pretreatment methods have been used, but they can be categorized into three broad groups: chemical e. In the chemical pretreatment method using acid for example, hemicelluloses will be targeted whereas in alkali-catalyzed pretreatment mainly lignin is removed [ 22 ].

It has been suggested that, there will probably not be a general pretreatment procedure and that different raw materials will require different pretreatments [ 22 ]. Biological pretreatment uses microorganisms and their enzymes selectively for delignification of lignocellulosic residues and has the advantages of a low-energy demand, minimal waste production and a lack of environmental effects [ ]. White-rot basidiomycetes possess the capabilities to attack lignin.

Other basidiomycetes such as Phlebia radiata , P. Ceriporiopsis subvermispora , however, lacks cellulases cellobiohydrolase activity but produces manganese peroxide and laccase, and selectively delignifies several different wood species [ ]. After pretreatment, cellulose and hemicelluloses are hydrolyzed to soluble monomeric sugars hexoses and pentoses using cellulases and hemicellulases, respectively Figure 1. As mentioned earlier, many fungal species such as Trichoderma , Penicillium , Aspergillus and T.

High temperature and low pH tolerant enzymes are preferred for the hydrolysis due to the fact that most current pretreatment strategies rely on acid and heat [ ]. In addition, thermostable enzymes have several advantages including higher specific activity and higher stability which improve the overall hydrolytic performance [ ]. Ultimately, improvement in catalytic efficiencies of enzymes will reduce the cost of hydrolysis by enabling lower enzyme dosages.

Some fungal strains such as T. Due to the promising thermostability and acidic tolerance of thermophilic fungal enzymes, they have good potential to be used for hydrolysis of lignocellulosic residues at industrial scales. Schematic picture for the conversion of lignocellulosic biomass to ethanol, including the major steps. Hydrolysis and fermentation can be performed separately SHF, indicated by broken arrows or as simultaneous saccharification and fermentation SSF. In consolidated bioprocessing CBP however, all bioconversion steps are minimized to one step in a single reactor using one or more microorganisms.

For reduction of production cost, ethanol production can be integrated with a combined heat and power plant using lignin. In the fermentation process, the hydrolytic products including monomeric hexoses glucose, mannose and galactose and pentoses xylose and arabinose will be fermented to valuable products such as ethanol Figure 1. Among these hydrolytic products, glucose is normally the most abundant, followed by xylose or mannose and other lower concentration sugars.

Saccharomyces cerevisiae is the most frequently and traditionally used microorganism for fermenting ethanol from starch-based residues at industrial scales [ 22 ]. However, S. To make industrial lignocellulosic bioconversion more economically feasible, it is necessary to choose microorganisms capable of fermenting both glucose and xylose. Therefore, many successful attempts have been made to improve xylose fermentation in S. These efforts can be classified within two major groups: recombinant e. These improvements have reached the point where the deficient xylose-fermenting S.

In addition to xylose, S. Therefore, recombinant S. The latest recombinant S. During fermentation of lignocellulosic-based biomass, S. Thus, it is necessary to detoxify hydrolytic products before the fermentation which increases process cost in addition to sugar loss [ ]. Interestingly, S.

In a recent study for example, glucose and xylose, the hydrolytic products of steam-pretreated corn stover were efficiently co-fermented to ethanol without detoxification using the recombinant S. It is also possible to adopt recombinant xylose-fermenting S. Attempts have been taken to reduce by-product inhibition. In a recent study for example, wheat straw pellets were subjected to wet explosion pretreatment using three different oxidizing agents, H 2 O 2 , O 2 and air [ ]. Interestingly, the pretreatment with O 2 has been shown to be the most efficient in enhancing conversion of the raw material to sugars.

Ammonia fiber explosion AFEX pretreatment also has been shown to be a good candidate since it does not produce some inhibitory by-products such as furans. However, the disadvantage of the method is that some of the phenolic compounds in lignin may remain on the pretreated material, which then needs to be washed. This creates wastewater, which causes the process to become environmentally unfriendly [ ]. The last two steps of bioconversion of pretreated lignocellulolytic residues to ethanol hydrolysis and fermentation can be performed separately SHF or simultaneously SSF Figure 1.

In the separate hydrolysis and fermentation SHF , the hydrolysate products will be fermented to ethanol in a separate process. The advantage of this method is that both processes can be optimized individually e. However, its main drawback is the accumulation of enzyme-inhibiting end-products cellobiose and glucose during the hydrolysis. In simultaneous saccharification and fermentation SSF , however, the end-products will be directly converted to ethanol by the microorganism. However, the main drawback of SSF is the need to compromise processing conditions such that temperature and pH are suboptimal for each individual step.

However, the development of recombinant yeast strains i. Further process integration can be achieved by a process known as consolidated bioprocessing CBP which aims to minimize all bioconversion steps into one step in a single reactor using one or more microorganisms. In order to increase ethanol yield in the bioconversion process, both cellulose and hemicellulose have to be completely hydrolyzed with minimum sugar degradation. Moreover, all monomeric sugars produced during hydrolysis have to be efficiently fermented to ethanol.

Technologies required for bioconversion of lignocelluloses to ethanol and other valuable products are currently available but need to be developed further in order to make biofuels cost competitive compared to other available energy resources such as fossil fuels. Many attempts have been made to improve the overall process yield and cost with a main focus on enzyme production and activity. Not surprisingly, the application of different strains and processes which are selected on the basis of the biomass residues used make comparisons difficult, if not impossible.

Many fungal strains have been subjected to extensive mutagenesis studies due to their ability to secrete large amounts of cellulose-degrading enzymes. It has been four decades since Mandels and Weber late s screened over wild-type strains of Trichoderma species to isolate the best cellulolytic strain and came up with T.

Cellulolytic activity of T. Other studies in different laboratories have also made significant contributions to strain improvements using mutagenesis techniques, leading to development of the mutant strains M7, NG14 [ ] and RUT-C30 [ ]. Moreover, T. These T. Cellulase and xylanase activities in Penicillium verruculosum 28K mutants were improved about 3-fold using four cycles of UV mutagenesis.

The enzyme production was further improved by 2- to 3-fold in a two-stage fermentation process using wheat bran, yeast extract medium and microcrystalline cellulose as the inducer [ ]. However, caution has to be taken during strain improvement by mutagenesis. Studies have shown that the best T. On the other hand, site-directed mutagenesis SDM has played a central role in the characterization and improvement of cellulases including their putative catalytic and binding residues.

Different site-directed mutagenesis methods such as saturation mutagenesis, error-prone PCR and DNA shuffling have been used to improve specific enzyme properties. For example, by the application of SDM it was found that Glu and are the catalytic nucleophile and acid-base residues in Hypocrea jecorina anamorph T. All mutants were resistant to thermal inactivation at alkaline pH.

Fungal Bioconversion of Lignocellulosic Residues; Opportunities & Perspectives

Also, the catalytic efficiency and optimum pH of T. Moreover, the stability of T. Fungal co-culturing offers a means to improve hydrolysis of lignocellulosic residues, and also enhances product utilization which minimizes the need for additional enzymes in the bioconversion process.

However, none of the fungal strains, including the best mutants, are able to produce high levels of the enzymes at the same time. In addition, hemicellulose hydrolysis must also be considered when lignocellulosic residues are subjected to biomass conversion. However, this will be determined by the pretreatment methods. Specifically in an alkali pretreatment method, a part of lignin will be removed and thus hemicellulose has to be degraded by the use of hemicellulases, whereas in acid-catalyzed pretreatment, the hemicellulose layer will be hydrolyzed [ 22 ].

Again, some fungal strains have been shown to work more efficiently on cellulosic residues whereas others produce more hemicellulolytic enzymes and efficiently hydrolyze hemicellulosic portions [ 20 , ]. Conversion of both cellulosic and hemicellulosic hydrolytic products in a single process can be achieved by co-culturing two or more compatible microorganisms with the ability to utilize the materials. In fact, in nature, lignocellulosic residues are degraded by multiple co-existing lignocellulolytic microorganisms.

Co-culturing of two or more fungal strains in mixed culture fermentation is widely used in many biological processes including the production of antibiotics, enzymes and fermented food [ ]. Mixed fungal cultures have many advantages compared to their monocultures, including improving productivity, adaptability and substrate utilization. Improving fungal cellulolytic activity of T.

Moreover, other fungal strains have been co-cultured to obtain better cellulolytic activity such as co-culturing of T. There are a few examples of co-culturing fungal strains for the purpose of combining cellulose and hemicellulose hydrolysis such as co-culturing T. In the both cases, enzyme activity for cellulases and hemicellulases was significantly increased.

The main drawback of co-culturing however is the complexity of growing multiple microorganisms in the same culture [ ]. Alternatively to co-culture, microorganisms can be metabolically engineered, which enable one microorganism to complete an entire task from beginning to end. For example by application of homologous recombination, the production of T. This will permit one fungal strain such as T. Heterologous expression is a powerful technique to improve production yield of enzymes, as well as activity.

The expressed enzyme has been shown to be highly thermostable optimum temperature at In the study for the improvement of biofinishing of cotton, T. The results have shown that the expression of CBHI was increased to 1. In the case of CBHII, however, the expression was increased to 3- to 4-fold using just one additional copy of the gene [ ]. In addition, chimeric proteins with specific applications have been designed using recombinant DNA technology. For example, an endoglucanase from Acidothermus cellulolyticus was fused to T. Moreover, the structural and biochemical information obtained from family GH 12 homologues was used to create a wide range of H.

Lignocellulolytic microorganisms, especially fungi, have attracted a great deal of interest as biomass degraders for large-scale applications due to their ability to produce large amounts of extracellular lignocellulolytic enzymes. Many successful attempts have been made to improve fungal lignocellulolytic activity including recombinant and non-recombinant techniques.

Process integration has also been considered for the purpose of decreasing the production cost, which was partly achieved by performing hydrolysis and fermentation in a single reactor SSF using one or more microorganisms co-culturing. Moreover, recombinant S. These laboratory improvements should now be verified in pilot and demonstration plants, such as the projects completed at the Iogen pilot plant Canada. Scaling up the production of lignocellulosic ethanol, however, requires further reduction of the production cost. Overall, in order to improve the technology and reduce the production cost, two major issues have to be addressed: i improving technologies to overcome the recalcitrance of cellulosic biomass conversion pretreatment, hydrolysis and fermentation and ii sustainable production of biomass in very large amounts.

In the case of large scale biomass production, in addition to forest and crop residues, energy crops such as switchgrass and Miscanthus can be grown to meet the needs. On the other hand, biotechnological approaches including systems biology and computational tools are likely good candidates to overcome these issues. We thank Miranda M.

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