Regulation of Cellulase and Xylanase Production by Basidiomycetes: Comparison
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Please note this is a comparison between Version 2 by Catherine Yang and Version 1 by Aza Kobakhidze.

The potential of wood-rotting and litter-deconstructing basidiomycetes to convert lignocellulose into a wide variety of products has been extensively studied. In particular, wood-rotting basidiomycete secretomes are attracting much attention from researchers and biotechnology companies due to their ability to produce extracellular hydrolytic and oxidative enzymes that effectively degrade cellulose, hemicellulose, and lignin of plant biomass.

  • basidiomycetes
  • lignocellulose
  • fermentation
  • cellulase
  • xylanase

1. Introduction

Polysaccharides of lignocellulosic biomass are cheap, abundant, and renewable resources used for their microbial or enzymatic conversion in biofuels and a wide range of chemicals. Polysaccharide-hydrolyzing enzymes (PHEs) are produced by a wide range of saprophytic microbes that grow on dead and decaying plant materials. Complete hydrolysis of cellulose to glucose monomers provides a synergistic action of endoglucanase (EC 3.2.1.4), exoglucanase (EC 3.2.1.91), and β-glucosidase (EC 3.2.1.21) [1,2][1][2]. Enzymatic hydrolysis of hemicelluloses, consisting mainly of xylan, galactoglucomannan, and xyloglucan, occurs under the action of a wide range of enzymes: endo-1,4-β-xylanase, β-xylosidase, α-l-arabinofuranosidase, α-D-glucuronidase, acetyl xylan esterase, feruloyl and coumaroyl esterase, endo-1,4-β-mannanase, β-mannosidase, α-galactosidase, acetyl mannan esterase, and xyloglucanase [3,4][3][4]. Biochemical characterization of cellulases and hemicellulases is presented in several comprehensive reviews [1,3,5][1][3][5].
The demand for the application of PHEs in biofuel production as well as in food, textile, brewery, wine, pulp and paper, and laundry industries and agriculture is growing [6,7][6][7]. The bottleneck in the widespread commercialization of ethanol 2G is thought to be the production cost of the PHEs. Low-cost enzymes with high catalytic activity, stability at elevated temperatures and a certain pH, and high tolerances to end-product inhibition are highly desired for use in these applications. Therefore, the identification of new overproducers of PHEs with complete cellulase and hemicellulases systems, the elucidation of the physiological features of the regulation of these enzyme syntheses, and, on this basis, the development of new approaches to bioprocessing for the maximum expression of the enzymatic activity of microorganisms remain a paramount task. Currently, filamentous fungi belonging to the division Ascomycota, such as Trichoderma, Aspergillus, and Penicillium, are sources of commercial PHEs. Analysis of the existing literature data shows that several species of Basidiomycota fungi are promising but still unexploited as producers of novel and potent PHEs. Indeed, wood-rotting fungi are one of the best decomposers of lignocellulosic materials owing to their ability to secrete a variety of hydrolytic and oxidative enzymes suited for the depolymerization of cellulose, hemicelluloses, and lignin, and provide fungal mycelium with energy and nutrients. However, the enzymes of basidiomycetes involved in the degradation of polysaccharides have received less attention than those of ascomycetes. In particular, few researchers have focused on systematic studies of the environmental factors that modulate the expression of PHEs during submerged and solid-state fermentation (SSF) of plant materials.

2. Diversity and Distinctions of Basidiomycetes Producing PHEs

Basidiomycota is one of two large divisions that, together with the Ascomycota, constitute the subkingdom Dikarya within the kingdom Fungi. Depending on the mode of feeding, Basidiomycota can be divided into saprobic, symbiotic, and parasitic groups. Saprobic fungi decomposing wood and leaf litter have received much attention for applications in biocatalysis and biorefinery. In nature, Basidiomycota species inhabit diverse ecological niches, and colonize and use a wide range of lignocellulosic materials to grow, including dead and living trees, forest litter, grasses, plant debris in the soil, and plant roots. More than 90% of wood-destroying basidiomycetes are white rot fungi [11][8], which are capable of destroying all polymers in plant cell walls due to the presence of a hydrolytic enzymatic system for the degradation of polysaccharides and an oxidative enzymatic system for the deconstruction of lignin. Unlike the white-rot basidiomycetes (WRBs), brown rot fungi (BRBs) use PHEs and highly reactive oxidizing agents to depolymerize plant polysaccharides [8,12][9][10]. Although a very limited amount of BRB has been evaluated for cellulase production to date, it has been found that these fungi produce endoglucanase but rarely secrete exoglucanase activity. Only some of them, in particular, Glaeophyllum trabeum [13][11] and Fomitopsis palustris [14][12], are able to decompose crystalline cellulose. Interestingly, G. trabeum produces processive endoglucanase, which hydrolyzes microcrystalline cellulose, compensating for the absence of cellobiohydrolase during cellulose degradation. The production of cellulases and xylanase is reported for a dozen genera and hundreds of species and strains belonging to different taxonomic groups and isolated from a wide variety of ecological niches. It is rather difficult to compare the activity of PHEs obtained from different fungal cultures due to differences in the composition of the medium, especially due to the content of different lignocellulosic growth substrates, and sometimes due to different methods for determining enzyme activity. Moreover, some authors have expressed enzymatic activity in SSF experiments in U/g biomass, others in U/mL. Nevertheless, the selected results presented in Table 1 and Table 2 make it possible to draw several important conclusions. First, these results clearly show both interspecific and intraspecific differences in the ability and potential of basidiomycetes to express cellulase and xylanase activities. For example, in the submerged fermentation of cellulosic materials, basidiomycetes CMCase activity varied from 0.2 U/mL in cultures of Coniophora puteana [15][13] and Pycnoporus sanguineus [16][14] to 122 U/mL in Pseudotrametes gibbosa [17][15]. Moreover, in the SSF of wheat straw, different strains of Pleurotus ostreatus expressed CMCase and xylanase activities from 0.7 U/g [18][16] to 166.9 U/g and 47.6 U/g [19][17], respectively. On the contrary, no differences in CMCase activity were found when plant substrates were fermented with strains of Pleurotus eryngii [20][18] (Table 2). This leads to the second conclusion that, along with the geographical and ecological origin of the fungal strain, the growth substrate plays a critical role in maximizing its biosynthetic potential, as will be discussed in the next section. It is clear that for a correct assessment and comparison of the cellulase activity of fungi belonging to different taxonomic and physiological groups, it is necessary to cultivate them using the same substrate and fermentation method. 
Table 1.
Cellulase and xylanase activity of individual basidiomycetes under the submerged fermentation of lignocellulosic materials.
Fungi Growth Substrate Enzyme Activity (U/mL) * References
CMCase Xylanase FPA
sp. secreted 75 U/g of CMCase and 4.2 U/g FPA during SSF of soybean meal [44][42], while Piptoporus betulinus accumulated 58.4 U/g CMCase and 7.4 U/g FPA during SSF of rice straw [45][43] (Table 2). 
Table 2.
Cellulase and xylanase activities (U/g) of individual basidiomycetes during SSF of lignocellulosic materials.
Fungal Species Growth Substrate Enzyme Activity (U/g) References
CMCase Xylanase FPA
Agaricus arvensis Rice straw 0.3
Bjerkandera adusta Sunflower mealND 0.5 12.9 3.7 ND[21][19]
[46][44] Agaricus brunnescens Crop straw 19.9 ND
  Brewer’s spent grainND ** 18.4[ 2.822 ND][20]
Bjerkandera adusta Corn stover 8.8 25.5 ND [23][21]
  Soybean meal 5.1 0.4 ND Coniophora puteana Wheat bran 0.2 1.2
 0.02 [15][13]
Spent coffee residue 1.2 1.0 ND Coprinus comatus Crop straw 29.4 ND ND [21][19]
Cotylidia pannosa
Calocybe indica Wheat bran 1.7 0.8 ND [47][45] Wheat bran 20.0 17.0 ND [24
Coprinus cinereus Sisal leaf biomass 2.1] 1.2[22]
ND [48][46] Dichomitus squalens Avicel 3.2 6.5 ND [
Coriolus versicolor12] Sweet sorghum bagasse[10]
2.2 11.9 6.7 [49][47] Fomes fomentarius IBB 9 Mandarin peels 4.0 7.0 ND [17][15]
Coriolus versicolor Oak sawdust, coconut husks, soybean oil, corn bran, and coffee husks 78.8 124.2 ND [50][48] F. fomentarius IBB 38 Mandarin peels 52.0 78.0 ND [17][15]
Fomes fomentarius Sunflower meal 1.5 16.8 ND [46][44]   Vinasse 88.0 195.0 ND  
  Apple pomace 4.0 7.0 ND  
  Brewer’s spent grain 1.4 15.9 ND    Grape pomace 5.0 4.0 ND  
  Maple leaves 19.0 26.0 ND  
  Soybean meal 1.0 5.7 ND  
  Spent coffee residues 1.3 0.9 ND  
Fomitopsis sp. Corn cob 2.2 ND 0.2 [44][42] Ganoderma applanatum Cellulose 3.3 8.2 ND [25][23]
  Corn stover 3.7 ND 0.2   Irpex lacteus Avicel 53.7 66.8 5.1 [26][24]
  Wheat straw   Mandarin pomace (MP) 18.1 20.3 1.9  
2.4 ND 0.2  
  Prosopis juliflora 1.1 ND 0.7     Wheat straw 23.0 29.1 2.3  
  Wheat bran 71.5 ND 3.3     Avicel + MP 76.2 106.2 6.8
  
Soybean meal 75.0 ND 4.2     Wheat straw + MP 40.3 34.2 2.5  
Ganoderma lucidum Sugarcane bagasse and wheat bran 17.6 16.3 4.9 [51][49] Inonotus obliquus Rice straw
Gloeophyllum trabeum1.4 307.0 0.4 [27][25]
Pinus taeda wood chips 0.1 1.2 0.1 [52][50]   Wheat straw
G. trabeum Jerusalem artichoke stalk1.3 283.0 0.5  
6.3 37.2 ND [53][51]   Corn stover 1.2 288.0 0.3  
Inonotus obliquus Wheat bran 27.2 ND 3.2 [54][52] Peniophora sp. Rice straw 0.2% 6.0 ND ND [
Lentinula edodes Oak sawdust, coconut husks, soybean oil, corn bran, and coffee husks 66.9 107.5 ND28][26]
[50][48]   Rice straw 0.6% 17.4 ND ND  
Lentinula edodes Wheat straw 0.8 ND ND [55][53   Potato infusion 10% 24.0 ND ND  
]
  Reed grass 1.0 ND ND   Potato infusion 80% 100.0 ND ND  
  Beanstalk 0.9 ND ND   Pholiota adiposa Rice straw 26.0 ND 1.2 [29][27]
Microporus xanthopus Green tea waste 81.8 ND ND [56][54] Pleurotus ostreatus Crop straw 28.2 ND ND [22][20]
Phanerochaete chrysosporium Sugarcane bagasse 63.8 220.0 13.1 [57][55] Pleurotus ostreatus Cottonseeds 1.7 1.6 ND [30][28]
Sugarcane Barbojo 126.3 227.6 19.3   Postia placenta Wheat bran 0.4 1.0 0.1 [15][13]
Pseudotrametes gibbosa Mandarin peels 120.0 37.0 ND [17][15]
  Vinasse 112.0 48.0 ND  
  Apple pomace 39.0 32.0 ND  
Pycnoporus coccineus Avicel
Grass powder 188.7 427.0 30.2  
  Corn straw 114.0 32.0 11.2  
  Rice straw 33.6 112.0 5.3  
Phanerochaete chrysosporium Rice bran 182.2 293.0 11.1 [19][17] 63.0 31.0 4.6 [26][24]
Paddy straw 34.3 81.9 16.7     Mandarin pomace (MP) 19.0 14.0 2.2  
Wheat straw 97.8 124.3 13.3     Wheat straw 22.0 18.0 1.9
Sorghum straw 
132.2 302.2   Avicel + MP 82.0 65.0 5.7  
  Wheat straw + MP 27.0 19.0 2.2  
16.6  
Bajra straw 77.8 113.5 19.3   Pycnoporus sanguineus
Sorghum hay 95.5 84.7 28.2   Orange peels 0.2 0.1 ND [16][14]
Maize straw 113.3 118.4 16.7   Pycnoporus sanguineus Palm oil mill effluent and oil palm frond 18.2 ND 13.4 [31][29]
Phlebia radiata Spruce wood 0.1 ND ND [58][56] Schizophyllum commune Rice straw 44.4
Piptoporus betulinus Rice straw1.1 0.6 [ 58.432 ND][ 7.430]
[45][43] S. commune Avicel 39.0 626.0 2.1
Pleurotus eryngii 160[26][24]
Cotton sake 0.2 ND ND [20][18]   Mandarin pomace (MP) 23.0 531.0 3.0  
  Barley oats straw 0.1 ND ND     Wheat straw 8.0 120.0 1.3  
Pleurotus eryngii 163 Poplar wood sawdust 0.2 ND ND [20][18]   Avicel + MP 39.0 740.0 4.2  
  Barley oats straw 0.2 ND ND [20][18]   Wheat straw + MP 14.0
Pleurotus eryngii528.0 1662.2  
Barley oats straw 0.1 ND ND [20][18] Sistotrema brinkmannii Rice straw 9.8 ND 0.3
Pleurotus eryngii 173[21] Barley oats straw[19]
0.1 ND ND [20][18 Sporotrichum pulverulentum Corn stover 6.6 33.5 ND [23][21]
]
Pleurotus florida Typha weed 307.0 358.0 ND [59][57] Trametes hirsuta Avicel 34.3 48.8 2.5 [33][31]
Pleurotus ostreatus Wheat straw 0.7 0.7 ND [18][16]   Avicel + mandarin peels 64.6 73.0 5.3  
Pleurotus ostreatus Sugarcane bagasse and wheat bran 19.9 8.7 6.7 [51][49] T. hirsuta Orange peel 0.5 45.0 ND
Pleurotus ostreatus Oak sawdust, coconut husks, soybean oil, corn bran, and coffee husks 47.3[34][32]
80.5 ND [50][48] Trametes pubescens Mandarin peels 74.0 32.0 ND [17][15]
Pleurotus ostreatus Rice bran 79.5 56.3 30.1 [19][17] T. pubescens Wheat bran 1.6
  Paddy straw4.8 ND 39.4 39.9 19.1[35][33]
  Trametes spp. Avicel 0.4 ND
  Wheat straw 148.5 13.9ND [36][34]
19.8   T. trogii Corn stover 6.5 45.4 ND [
 23] Sorghum straw[21]
137.2 47.6 30.7   T. versicolor Carboxymethyl cellulose 1.6
  Bajra straw4.5 ND [37][35]
Tricholoma giganteum Pithecellobium Dulce wood ND 338.0 0.3 [38][36]
  Tamarindus Indica wood ND 375.0 0.3  
* In Tables and Figures one unit of enzyme activity is defined as the amount of enzyme, releasing 1 µmol of reducing sugars per minute. ** ND - not determined.
Thirdly, not all WRBs and BRBs are efficient producers of cellulase or xylanase, only a few of them can accumulate significant enzymatic activity, and some Basidiomycota strains have shown exceptional potential for the production of certain groups of hydrolytic enzymes under appropriate cultivation conditions. Thus, Coprinellus disseminatus produced 469 U/mL of alkali-thermotolerant xylanase along with negligible cellulase activity [39][37] while Armillaria gemina secreted up to 146 U endoglucanase/mL, 15 U β-glucosidase/mL, and 1.72 U FPA/mL [40][38]. Further, Jagtap et al. [29][27] achieved very high β-glucosidase activity (45.2 U/mL) in the submerged cultivation of Pholiota adiposa in a medium containing rice straw and corn steep powder. During the extensive screening of wood and litter-deconstructing basidiomycetes for lignocellulolytic enzyme production, Fomes fomentarius, Panus lecometei, Pseudotrametes gibbosa, Trametes versicolor [17[15][39],41], Irpex lacteus, and Schizophyllum commune [33][31] were revealed as especially promising cellulases and xylanases producers in the submerged fermentation of cellulose or plant raw materials (Table 1). Among these fungi, S. commune appeared to be an outstanding producer of xylanase and β-glucosidase, producing 740 U/mL and 18.6 U/mL, respectively [26][24]. Interestingly, under SSF conditions, as high as 512 U/g endoglucanase activity was achieved utilizing poplar wood as the growth substrate for Trametes trogii [42][40], and 10196 U/g xylanase was achieved under SSF conditions using rice straw as the growth substrate for Schizophyllum commune [43][41]. In contrast to WRBs, a very limited number of BRBs strains have been evaluated for cellulase and xylanase activities, although their ability to produce these enzymes has been well documented and some of them may be excellent producers of PHEs. For example, Fomitopsis
166.9
7.5
14.8
 
 
Sorghum hay
140.8
44.5
11.4
 
 
Maize straw
109.4
29.5
15.8
 
Pleurotus ostreatus
Grape pomace
0.1
ND
ND
[
60
]
[
58
]
Pleurotus
pulmonarius
Grape pomace
0.1
ND ND [60][58]
Pleurotus sajor caju, Rice bran 36.9 66.5 27.2 [19][17]
  Paddy straw 46.5 24.1 16.9  
  Wheat straw 59.1 87.0 14.8  
  Sorghum straw 45.3 45.0 15.5  
  Bajra straw 25.3 65.9 19.1  
  Sorghum hay 44.2 27.6 15.5  
  Maize straw 14.8 63.1 12.7  
Porodaedalea pini Picea jezoensis wood samples 4.2 5.4 ND [61][59]
Schizophyllum commune Rice straw ND 10196 ND [43][41]
S. commune Jerusalem artichoke stalk 15.2 106.5 ND [53][51]
S. commune Sunflower meal 13.2 2.5 ND [46][44]
  Brewerʼs spent grain 17.5 1.2 ND  
  Soybean meal 1.9 0.7 ND  
  Spent coffee residue 6.2 0.8 ND  
Trametes trogii Poplar wood 512.2 ND ND [42][40]
T. versicolor Sugarcane bagasse and wheat bran 56.5 36.7 9.5 [51][49]
T. versicolor Oak sawdust, coffee husk, and corn bran ND 9.1 11.6 [62][60]
Fourthly, the ratio of cellulase and xylanase activities varies greatly depending on the fungus species. Although most fungal species are capable of producing approximately equal amounts of cellulase and xylanase activity, Pseudotrametes gibbosa [17][15] and especially Schizophyllum commune [32][30] predominantly produce endoglucanase in submerged fermentation of lignocellulosic materials whereas Inonotus obliquus [27][25], T. hirsuta [34][32], and T. trogii [23][21] secrete many times higher xylanase activity compared to endoglucanase (Table 1). It should be noted that the ratio of cellulase and xylanase activities largely depends on the type and chemical composition of the lignocellulosic growth substrate, as will be discussed below. Finally, some fungal strains, such as Pycnoporus sanguineus [31][29], Irpex lacteus [33][31], Phanerochaete chrysosporium [57][55], and Pleurotus ostreatus [19][17] probably possess a well-balanced cellulolytic system, exhibit high filter paper activity (FPA), and, therefore, are promising candidates for use in biorefining processes.

3. Effect of Carbon Source on Cellulase and Xylanase Production

Developing a highly productive fermentation process to enhance the ability of fungi to produce a complete cellulase system is challenging [63][61]. PHEs production by Basidiomycota fungi is strongly influenced by the availability of nutrients such as carbon and nitrogen sources, growth factors, and microelements, as well as medium pH, fermentation temperature, aeration, and other factors. Various approaches have been used to enhance the production of cellulases and xylanase in submerged and SSF fermentation of lignocellulosic materials. It is clear that optimizing the medium composition that provides nutrients and energy for the growing organism and establishing favorable environmental factors are necessary to achieve both maximum enzymatic activity and productivity. In this case, careful selection of the carbon source (and potential inducer of PHEs synthesis) in the presence of which the enzyme producer grows is of paramount importance. For PHEs production by basidiomycetes, the growth medium usually includes pure cellulose, which serves as a source of carbon and as an inducer of the synthesis of enzymes that decompose biomass polysaccharides. To gain insight into the peculiarities of PHEs production by individual wood- and litter-degrading basidiomycetes, several research groups tested the effects of various mono-, di-, and polysaccharides along with lignocellulosic substrates. For example, cellulose had the most significant inducing effect on cellulase and xylanase production by Ganoderma applanatum LPB MR-56, but CMC and xylose were also effective in inducing these enzymatic activities [25][23]. Altaf et al. [64][62] reported that the values of xylanase activity of the basidiomycetes Flammulina velutipes and Pleurotus eryngii using xylose as a carbon source were higher than those produced with xylan. Among four chemically pure carbon sources, Avicel provided the highest FPA and β-glucosidase activity of Agaricus arvensis 0.18 U/mL and 7.2 U/mg protein, respectively, while in the presence of CMC, xylan, and cellobiose FPA was equal to 0.06–0.08 U/mL and β-glucosidase activity achieved 5.5, 2.3, and 0.5 U/mg protein, respectively [65][63]. Kumar et al. [66][64] compared CMCase and FPA of Schizophyllum CMCase and FPA activities of the fungal culture were as high as in the medium with wheat bran, but many times higher than those observed in media containing rice straw, rice husk, wheat straw, and sugarcane bagasse. It is interesting that this fungus secreted significant CMCase activity in the cultivation of this strain in a medium containing sucrose. When cultivating BRBs, a completely different picture of the fungal response to the presence of various carbon sources in the nutrient medium was revealed. In this case, active secretion of cellulase and xylanase was observed during the cultivation of G. abietinum 89 and P. aurivella 437 in the presence of both polymeric compounds and easily metabolizable carbon sources indicating that these fungi produce cellulase and xylanase constitutively. Cellobiose ensured the highest volumetric enzyme activity of G. abietinum 89 while even glucose was a suitable carbon source for cellulase and xylanase production by P. aurivella 437 although crystalline cellulose was the best source of carbon for the production of volumetric cellulase and xylanase activity by this fungus. The most interesting finding is that carboxymethyl cellulose, which provided very poor growth of all fungi, promoted the expression of the activity of both enzymes by BRBs so that the specific cellulase and xylanase activities of P. aurivella 437 in media with Avicel and CMC were comparable, while in the cultivation of G. abietinum 89, the fungus enzymatic activities in medium with CMC turned out to be two times higher than those in the medium with crystalline cellulose. These results and the literature data [69,70][65][66] indicate that the characteristic feature of brown-rot fungi is a constitutive synthesis of cellulase and xylanase, even in the presence of glucose as the only source of carbon and energy. However, no formation of cellulolytic enzymes was observed during the growth of Coniophora puteana on glucose alone, although this fungus secreted four endocellulases and two exo-cellobiohydrolases in the presence of amorphous cellulose as the sole carbon source [71][67]. 

4. Role of the Lignocellulosic Growth Substrate

Despite numerous studies of the synthesis of PHEs by basidiomycetes, the general and distinctive features of the production of these enzymes during the cultivation of taxonomically, ecologically, and physiologically different fungi in the presence of chemically different lignocellulosic materials remain insufficiently clear. Microcrystalline cellulose is commonly used for the production of cellulase by filamentous fungi [25,26,33,65,68,73,75,84][23][24][31][63][68][69][70][71]. Undoubtedly, it is the most appropriate growth substrate for the production of PHEs. Nevertheless, cellulose or cellulose derivatives, such as carboxymethyl cellulose, are quite expensive; therefore, more attention has been paid to the use of cellulose-rich biomass instead of expensive cellulose for the production of these enzymes. Lignocellulosic materials are cheap, renewable, and abundant, and their use as growth substrates rich in required nutrients provides the production of hydrolases and, if necessary, other complementary enzymes involved in the degradation of plant biomass. However, it is not clear how the production of enzymes depends on the content of cellulose, hemicellulose, and lignin in the plant substrate. In particular, if any plant material contains cellulose and hemicellulose, then why is the range of cellulase activity so varied (Table 1 and Table 2) when the same fungus is cultivated on different substrates? The structure and chemical composition of the lignocellulosic substrates is critical; they must contain sufficient readily available nutrients and microelements to ensure abundant growth and biosynthetic activity of the fungus to provide enhanced production of PHEs. Likewise, Brijwani and Vadlani [85][72] showed that the physicochemical properties of the substrate, such as porosity and crystallinity, significantly affect the production of cellulase and xylanase. Clearly, a high cellulose content and a low lignin content in the growth substrate are preferable for the active production of PHEs. It should be noted that in materials such as woody residues, the accessibility to cellulose for microbes is poor due to a higher percentage of lignin content; therefore, their pre-treatment is necessary to improve the accessibility of cellulose to microbial enzymes. This probably explains why mainly herbaceous substrates and food industry wastes have been exploited for cellulase production and not woody substrates. Although, this may also be because food industry wastes are produced in significant quantities in many countries and are cheap. It is important to note that when WRBs are used to ferment lignocellulosic growth substrates such as straw and sawdust, there is no particular need for their pretreatment since these fungi can produce both hydrolases and lignin-modifying enzymes. However, in this case, a wide range of extracellular enzymes belonging to different classes are involved in the degradation of lignocellulosic polymers and their synthesis requires significant energy and material resources, while the fermentation of cellulose or xylan requires only a few specific glycoside hydrolases for their hydrolysis. Literature data indicate that some of the substrates significantly stimulate the synthesis of individual PHEs without supplementation of the culture medium with specific inducers [17,27,31][15][25][29]. Some substrates, especially food industry by-products that are low in lignin and contain free sugars and organic acids can stimulate cellulase production. It was found that among the tested lignocellulosic materials, wheat bran provides the maximum production of CMCase (71.5 U/g), FPA (3.3 U/g), and b-glucosidase (50.7 U/g) of Fomitopsis sp. RCK2010 while corn cob was not suitable for enzyme secretion [44][42]. Results in Table 1 and Table 2 show that Basidiomycota strains cultivated on the same substrate express significant differences in cellulase and xylanase activities. However, the same strain of fungus that expresses exceptionally high cellulase activity in the presence of a particular substrate may produce low cellulase activity when cultivated on a different substrate, i.e., fungal growth and enzyme activity expression might be substrate-specific. Thus, Ilić et al. [46][44] showed that the SSF of brewer’s spent grain by F. fomentarius provided the formation of only 1.4 U/g of CMCase activity, whereas in the fermentation of the same substrate by Bjerkandera adusta and S. commune, the enzyme activities achieved 18.4 and 17.5 U/g, respectively. In the same work, the xylanase activity of F. fomentarius varied from 0.9 U/g in the medium with spent coffee residues to 16.8 U/g in the medium containing sunflower meal. The results obtained and the literature data [86][73] (Table 1 and Table 2) evidence that the lignocellulosic substrate appears to determine the type and yield of enzymes produced by a given wood-rotting fungus in a species and strain-specific manner. Moreover, using lignocellulosic substrates with different chemical compositions, it is possible to obtain enzyme complexes with different levels and ratios of individual enzymes. Thus, Shradhdha and Murty [19][17] successfully implemented SSF of rice bran and sorghum straw for the maximum production of both cellulases and xylanase using P. chrysosporium and demonstrated the suitability of paddy straw and sorghum hay for the predominant production of xylanase or cellulase, respectively. Furthermore, Bentil et al. [86][73] summarized the results on the rate of cellulase production and reported that in particular for SSF, the recorded rates of enzyme production range from 0.001 to 72 U/g/day for various fungi and lignocellulosic substrates. Probably the decisive role in the stimulation of PHEs expression belongs to the presence of significant amounts of readily available cellulose in the medium. In any case, it is important to search for a suitable combination of fungal strain and lignocellulosic substrate for maximum production of PHEs.

5. Cultivation Methods for Cellulases Production

Both submerged fermentation (Table 1) and SSF (Table 2) of different lignocellulosic materials can be successfully used for PHEs production by Basidiomycota fungi [10,86,87][73][74][75]. Currently, submerged fermentation is the main industrial process; it ensures controlled cultivation conditions, uniform availability of nutrients and oxygen, the formation of proper fungal pellets, and easy product recovery and reproducibility. Many studies proved that compared to the SSF method, submerged fermentation of plant raw materials provides fast production and a higher yield of cellulase [30,49,88][28][47][76]. However, significantly higher amylase, endoglucanase, and xylanase activities were recorded during the SSF of cassava peel by Trametes polyzona BKW001 than during submerged fermentation [89][77]. The activity of β-glucosidase and exoglucanase was also slightly higher with SSF than with submerged fermentation. In recent years, interest in SSF has increased because, in the cultivation of basidiomycetes, it provides a growth environment similar to their natural habitat and ensures major advantages: (1) high volumetric productivity and product yield, (2) relatively higher concentration of the products, (3) simpler downstream processing, (4) less effluent generation, (5) requirement for simpler fermentation equipment, and (6) opportunities to organize on-site tailor-made enzyme production without requiring large capital investments. It can be assumed that during colonization of the growth substrate under SSF conditions, the rate of substrate uptake is sufficiently high and the accumulation of easily metabolizable products of polysaccharide hydrolysis does not occur, which provides a high rate of PHEs synthesis due to the absence of catabolic repression. Compared to submerged fermentation, in SSF, the fungal mycelium is in direct contact with the lignocellulosic material, it grows on the surface and then penetrates the substrate. The fungal growth rate, biomass, and PHEs yields are directly related to the lignocellulosic substrate chemical composition and structure [87,90][75][78]. Of particular importance is also the porosity and specific surface of the particles of plant material, which determine the efficiency of air diffusion and the water-holding capacity of the substrate. The substrate’s porosity must be sufficient to not limit the supply of necessary oxygen and the removal of carbon dioxide and the resulting metabolic heat [91][79]. In this regard, it is necessary to take into account the thickness and particle size of the substrate. The moisture content in the growth substrate in the range of 65–75% of the total mass is considered the most optimal both for the growth of basidiomycetes and the production of PHEs. A medium containing appropriate nitrogen and mineral salts is usually used to moisten the substrate. It should be noted that a comparative assessment of the effectiveness and benefits of both cultivation methods is difficult since only a few studies used the same fungal species and cellulose substrate for comparison. Okal et al. [10][74] indicated that the majority of WRB produce higher yields of cellulases in submerged fermentation of lignocellulosic biomass than in SSF. Moreover, Tengerdy [92][80] compared the production of cellulase in submerged and SSF systems and indicated that when using SSF, the cost of production is reduced by about 10 times. Undoubtedly, the influence of the cultivation method on the production of cellulases varies depending on the individual peculiarities of the fungal strain and the nature of biomass residues used as a growth substrate. Highly lignified residues like straw and tree leaves are suitable for SSF while nutrient-rich fruit residues are appropriate for submerged fermentation [86][73]. In this regard, it is worth noting that in many studies media of the same composition and concentration were used for both SSF and submerged fermentation of plant materials. However, the volume of the medium used to wet the substrate to a moisture content of 70–75% is limited, and the amount of additional necessary elements may not be enough for both abundant fungal growth and maximum cellulase production. Therefore, it is desirable to increase the concentration of the medium components by 5–10 times for SSF. Undoubtedly, the production of cellulases in the SSF of plant raw materials is promising for scaling up to an industrial level, but innovative knowledge and design solutions are required to create effective systems. This method of basidiomycetes cultivation is especially promising for the organization of on-site enzyme production using, for example, food industry by-products as biomass feedstock. In this case, the entire fermented product enriched with fungal biomass and enzymes can be directly used as a feed additive. This approach is cost-effective, energy-efficient, and more environment-friendly as compared to the off-site production of enzymes [7]. In this regard, a promising and feasible approach to improve the yield of cellulase production approach may be the co-cultivation of two or more strains of WRB fungi. Compared to monocultures, co-cultivation provides a number of advantages, such as better substrate degradation and nutrient supply to the producer as well as higher productivity [6,93][6][81]. In addition, this is a way not only to enhance the expression of the target enzyme but also to supplement enzyme systems with complementary enzymes. However, in order to achieve maximum results, it is necessary to search for compatible fungal strains. Thus, when Schizophyllum commune was co-cultivated with Irpex lacteus, an increase in cellulase activity occurred compared with individual cultures, while co-cultivation of S. commune with Pycnoporus coccineus or Trametes hirsuta had a negative effect on cellulase production [33][31].

6. Influence of Nitrogen Source on the Cellulase and Xylanase Production

The growth rate of basidiomycetes, the yield of fungal biomass, and, accordingly, the production and yield of PHEs are largely dependent on the nitrogen sources present in the fermentation medium. In a synthetic medium containing cellulose, a source of nitrogen is an essential component for optimal fungal growth and enzyme production. Lignocellulosic materials used as a growth substrate, to a certain extent, serve as sources of nitrogen and provide the accumulation of fungal biomass and target enzymes. However, to accelerate both processes, it is necessary to introduce an additional source of nitrogen into the medium, especially when the yield of cellulases correlates with the amount of fungal biomass. Both the nature and concentration of nitrogen sources affect cellulase and xylanase activity in Basidiomycota strains. For example, among various sources of organic nitrogen, urea caused the maximum production of CMCase (81.8 U/g) by Fomitopsis sp. RCK2010 during SSF of wheat bran, while casein and soy flour resulted in the maximum production of FPA (4.7 U/g) and β-glucosidase (69.1 U/g), respectively, while inorganic sources of nitrogen had no significant effect on the increase in enzyme activity [44][42]. An analysis of the literature data shows that peptone is probably the most suitable source of nitrogen, providing a significant growth of most fungi and the production of PHEs. For example, in the SSF of tree leaves, the addition of peptone to the medium as an additional source of nitrogen provided a twofold increase in the P. ostreatus protein content compared to the control medium and an increase in the activity of CMCase and xylanase from 20 U/mL to 28 and 35 U/mL, respectively [88][76]. Replacing peptone with ammonium sulfate reduced the activity of enzymes to 13 and 17 U/mL, respectively, although the increase in fungal biomass protein was comparable to that in the peptone medium. Ammonium sulfate is a physiologically acidic salt, and in its presence, nitrogen consumption is accompanied by the acidification of the medium. It is possible that this circumstance affected both the secretion of enzymes and the stability of the already synthesized enzyme during long-term cultivation. Nevertheless, Coniglio et al. [36][34] found that both peptone and ammonium sulfate as nitrogen sources favored the secretion of cellobiohydrolase activity by Trametes villosa LBM 033. Unfortunately, in most studies of the effect of nitrogen and its concentration on the cellulase activity of fungi, there are no data on the accumulated biomass. As a result, some authors make an incorrect conclusion about the stimulation or inhibition of enzyme production by one or another source of nitrogen. Interestingly, the effect of an additional source of nitrogen on the fungal cellulase activity may depend on the nature and chemical composition of the lignocellulosic substrate. For example, in SSF of beech leaf by P. dryings, peptone was the most suitable source of nitrogen for CMCase production, while in the presence of wheat straw, the maximum activity of the enzyme was detected when (NH4)2SO4 was added to the medium [94][82]. Therefore, to maximize cellulase production, it is necessary to find the right combination of nitrogen source and lignocellulosic substrate for each particular fungal strain. Moreover, Salmon et al. [25][23] showed that the effect of nitrogen source on the activity of Ganoderma applanatum LPB MR-56 xylanase and cellulase depends on the concentration of cellulose used. Yeast extract was found to be the best nitrogen source when using 1% cellulose, while peptone was the best nitrogen source when using 0.5% cellulose.

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