Cellulosome and cellulosome-like multienzyme complexes from anaerobic and aerobic microorganisms. (This table is adapted from Doi & Kosugi, 2004).
\r\n\t
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Plant biomass contains a complex mixture of polysaccharides, mainly cellulose and hemicellulose (mainly xylan), and other polysaccharides (Aspinall, 1980). The hemicelluloses, as well as the aromatic polymer lignin, interact with the cellulose fibrils, creating a rigid structure strengthening the plant cell wall. Therefore, complete and rapid hydrolysis of these polysaccharides requires not only cellulolytic enzymes but also the cooperation of xylanolytic enzymes (Thomson, 1993). Many microorganisms that produce enzymes capable of degrading cellulose and hemicellulose have been reported and characterized. Two enzyme systems are known for their degradation of lignocellulose by microorganisms. In many aerobic fungi and bacteria, endoglucanase, exoglucanase, and ancillary enzymes are secreted individually and can act synergistically on lignocellulose. The most thoroughly studied enzymes are the glycosyl hydrolases of Trichoderma reesei (Dashtban et al., 2009). On the other hand, several anaerobic cellulolytic microorganisms such as Clostridium thermocellum (Lamed & Bayer, 1988), C. cellulovorans (Doi et al., 2003), C. josui (Kakiuchi et al., 1998) and C. cellulolyticum (Gal et al., 1997) are known to produce a cell-associated, large extracellular polysaccharolytic multicomponent complex called the cellulosome, in which several cellulolytic and xylanolytic enzymes are tightly bound to a scaffolding protein (core protein). Thus, the cellulosome provides for a large variety of enzymes and attractive enzymatic properties for the degradation of recalcitrant plant biomass. So far, anaerobic microorganisms have been identified as producing the multienzyme complex, cellulosome (Doi & Kosugi, 2004; Demain et al., 2005). However, when compared with aerobic enzymes, production of those enzymes by anaerobic culture presents a high cost because of the high price of medium, slow rate of growth and low yield of enzyme, while only a little information has been reported on cellulosome-like multienzyme complex produced by aerobic bacteria (Kim & Kim, 1993; Jiang et al,, 2004; van Dyk et al., 2009). Therefore, the multienzyme complexes, cellulosomes, produced by aerobic bacteria show great potential for improving plant biomass degradation. A facultatively anaerobic bacterium, P. curdlanolyticus strain B-6, is unique in that it produces extracellular xylanolytic-cellulolytic multienzyme complex under aerobic conditions (Pason et al., 2006a, 2006b; Waeonukul et al., 2009b). In the following years, the characteristics, function, genetics and mechanism of the xylanolytic-cellulolytic enzymes system of this bacterium has been the subject of considerable research. In light of new findings in this field, this review will describe the state of knowledge about the multienzyme complex of strain B-6 and its potential biotechnological exploitations.
Lignocellulosic biomass is composed mainly of plant cell walls, with the structural carbohydrates, cellulose and hemicelluloses and heterogeneous phenolic polymer lignin as its primary components (Fig. 1). However, their proportions vary substantially, depending on the type, the species, and even the source of the biomass (Aspinall et al., 1980; Pérez et al., 2002; Pauly et al., 2008).
Structure of lignocellulosic plant biomass. (This figure is adapted from Tomme et al., 1995).
Cellulose: Cellulose, the main constituent of the plant cell wall, is a polysaccharide composed of linear glucan chains linked together by β-1,4-glycosidic bonds with cellobiose residues as the repeating unit at different degrees of polymerization, depending on resources. The cellulose chains are grouped together to form microfibrils, which are bundled together to form cellulose fibers. The cellulose microfibrils are mostly independent but the ultrastructure of cellulose is largely due to the presence of covalent bonds, hydrogen bonds and Van der Waals forces. Hydrogen bonding within a cellulose microfibril determines ‘straightness’ of the chain but inter-chain hydrogen bonds might introduce order (crystalline) or disorder (amorphous) into the structure of the cellulose (Klemm et al., 2005). In the latter conformation, cellulose is more susceptible to enzymatic degradation (Pérez et al., 2002). In nature, cellulose appears to be associated with other plant compounds and this association may affect its biodegradation.
Hemicelluloses: Hemicelluloses are the second most abundant polymers and differ from cellulose in that they are not chemically homogeneous. Hemicelluloses are branched, heterogenous polymers of pentoses (xylose, arabinose), hexoses (mannose, glucose, galactose) and acetylated sugars. They have lower molecular weight compared to cellulose and branches with short lateral chains that are easily hydrolysed (Saha, 2003; Scheller & Ulvskov, 2010). Hemicelluloses differ in composition. Hemicelluloses in agricultural biomass like straws and grasses are composed mainly of xylan, while softwood hemicelluloses contain mainly glucomannan. In many plants, xylans are heteropolysaccharides with backbone chains of 1,4-linked β-D-xylopyranose units. In addition to xylose, xylan may contain arabinose, glucuronic acid, or its 4-O-methyl ether, acetic acid, ferulic and p-coumaric acids. Hemicelluloses are bound via hydrogen bonds to the cellulose microfibrils in the plant cell wall, crosslinking them into a robust network. Hemicelluloses are also covalently attached to lignin, forming together with cellulose to form a highly complex structure.
Lignin: Lignin is the third most abundant polymer in nature. It is present in plant cell walls and confers a rigid, impermeable, resistance to microbial attack and oxidative stress. Lignin is a complex network formed by polymerization of phenyl propane units and constitutes the most abundant non-polysaccharide fraction in lignocelluloses (Pérez et al., 2002; Sánchez, 2009). The three monomers in lignin are p-coumaryl alcohol, coniferyl alcohol and sinapyl alcohol; they are joined through alkyl–aryl, alkyl–alkyl and aryl–aryl ether bonds. Lignin embeds the cellulose thereby offering protection against microbial and enzymatic degradation. Furthermore, lignin is able to form covalent bonds to some hemicelluloses, e.g. benzyl ester bonds with the carboxyl group of 4-O-methyl-D-glucuronic acid in xylan. More stable ether bonds, also known as lignin carbohydrate complexes, can be formed between lignin and arabinose, or between galactose side groups in xylans and mannans.
Several biological methods for lignocellulose recycling based on the enzymology of cellulose, hemicelluloses, and lignin degradation have been developed. To date, processes that use lignocellulolytic enzymes or microorganisms could lead to promising, environmentally friendly technologies. The relationship between cellulose and hemicellulose in the cell walls of higher plants is much more intimate than was previously thought. It is possible that molecules at the cellulose-hemicellulose boundaries, and those within the crystalline cellulose, require different enzymes for efficient hydrolysis.
Cellulase: Cellulases responsible for the hydrolysis of cellulose are composed of a complex mixture of enzymes with different specificities to hydrolyze the β-1,4-glycosidic linkages (Fig. 2A). Cellulases can be divided into three major enzyme activity classes (Goyal et al., 1991; Rabinovich et al., 2002). These are endoglucanases or endo-1-4-β-glucanase (EC 3.2.1.4), exoglucanase or cellobiohydrolase (EC 3.2.1.91), and β-glucosidase (EC 3.2.1.21). Endoglucanases, are thought to initiate attack randomly at multiple internal sites in the amorphous regions of the cellulose fiber, which opens-up sites for subsequent attack by the cellobiohydrolases. Cellobiohydrolases remove cellobiose from the ends of both sides of the glucan chain. Moreover, cellobiohydrolase can hydrolyze highly crystalline cellulose. β-glucosidase hydrolyzes cellobiose and in some cases short chain cellooligosaccharides to glucose.
Enzyme systems involved in the degradation of cellulose (A) and xylan (B). (This figure is adapted from Aro et al., 2005).
Hemicellulase: Xylan is the main carbohydrate found in hemicelluloses. Its complete degradation requires the cooperative action of a variety of hydrolytic enzymes (Fig. 2B). Xylanases are frequently classified according to their action on distinct substrates: endo-1,4-β-xylanase (endoxylanase) (EC 3.2.1.8) generates xylooligosaccharides from the cleavage of xylan while 1,4-β-xylosidase (EC 3.2.1.37) produces xylose from xylobiose and short chain xylooligosaccharides. In addition, xylan degradation needs accessory enzymes, such as α-L-arabinofuranosidase (EC 3.2.1.55), α-4-O-methyl-D-glucuronidase (EC 3.2.1.39), acetyl xylan esterase (EC 3.1.1.72), ferulic acid esterase (EC 3.1.1.73), and p-coumaric acid esterase (EC 3.1.1.-), acting synergistically, to efficiently hydrolyze wood xylans. In the case of acetyl-4-O-methylglucuronoxylan, which is one of the most common hemicelluloses, four different enzymes are required for degradation: endo-1,4-β-xylanase, acetyl esterase (EC 3.1.1.6), α-glucuronidase, and β-xylosidase. The degradation of O-acetyl galactoglucomannan starts with the rupture of the polymer by endomannanase (EC 3.2.1.78). Acetylglucomannan esterase (EC 3.1.1.-) removes acetyl groups, and α-galactosidase (EC 3.2.1.22) eliminates galactose residues. Finally, β-mannosidase (EC 3.2.1.85) and β-glucosidase break down the endomannanase-generated oligomeric β-1,4 bonds (Thomson, 1993; Li et al., 2000; Pérez et al., 2002).
The enzyme systems for the lignocellulose degradation by microorganisms can be generally regarded as non-complexed or complexed enzymes (Lynd et al., 2002). In the case of aerobic fungi and bacteria, the cellulase enzymes are free and mostly secreted. In such organisms, by the very nature of the growth of the organisms, they are able to reach and penetrate the cellulosic substrate and, hence, the secreted cellulases are capable of hydrolyzing the substrate. The enzymes in these cases are not organized into high molecular weight complexes and are called non-complexed (Fig. 3A). The polysaccharide hydrolases of the aerobic fungi are largely described based on the examples from Trichoderma, Penicillum, Fusarium, Humicola, Phanerochaete, etc., where a large number of the cellulases are encountered (Dashtban et al., 2009; Sánchez, 2009). In contrast, various cellulases and hemicellulases from several anaerobic cellulolytic microorganisms, are tightly bound to a scaffolding protein, as core protein and organized to form structures on the cell surfaces; these systems are called complexed enzymes or cellulosomes (Fig. 3B). The cellulosome is thought to allow concerted enzyme activities in close proximity to the bacterial cell, enabling optimum synergism between the enzymes presented on the cellulosome. Concomitantly, the cellulosome also minimizes the distance over which hydrolysis products must diffuse, allowing efficient uptake of these oligosaccharides by the host cells (Bayer et al., 1994; Schwarz, 2001; Lynd et al., 2002).
Biotechnological applications in terms of hydrolysis efficiency for complexed enzyme systems might have an advantage over non-complexed enzyme systems. The high efficiency of the cellulosome has been attributed to (i) the correct ratio between catalytic domains that optimize synergism between them, (ii) appropriate spacing between the individual components to further favor synergism, (iii) the presence of different enzymatic activities (cellulolytic or hemicellulolytic enzymes) in the cellulosome that can remove “physical hindrances” of other polysaccharides in heterogeneous plant cell materials (Lynd et al., 2002), and (iv) the presence of carbohydrate-binding modules (CBMs) that can increase the rate of hydrolysis by bringing the cellulosome into intimate and prolonged association with its recalcitrant substrate (Shoseyov et al., 2006). Thus, the complexed enzyme system, cellulosome, may provide great potential for the degradation of plant biomass.
Simplified schematic of the hydrolysis of amorphous and microcrystalline celluloses by non-complexed (A) and complexed (B) cellulase systems. (This figure is adapted from Lynd et al., 2002).
The cellulosome was first identified in 1983 from the anaerobic, thermophilic, spore-forming Clostridium thermocellum (Lamed et al., 1983). The cellulosome of C. thermocellum is commonly studied along with cellulosomes from the anaerobic mesophiles, C. cellulovorans (Doi et al., 2003), C. josui (Kakiuchi et al., 1998) and C. cellulolyticum (Gal et al., 1997). All cellulosomes share similar characteristics, they all contain a large distinct protein, referred to as the scaffoldin which allows binding of the whole complex to microcrystalline cellulose via CBM. Also, the cellulosome scaffoldin expresses type I cohesins which allow binding of a wide variety of cellulolytic and hemicellulolytic enzymes within the complex via the expression of complementary type I dockerins on enzymes. Similarly, at the C-terminal the scaffoldin expresses type II cohesins, which allow the binding of the cellulosome to the cell through type II dockerins on surface layer homology proteins (SLH) (Fig. 4).
Cellulosomes are produced mainly by anaerobic bacteria, mostly from the class clostridia, and some anaerobic fungi such as genus Neocallimastix (Dalrymple et al., 1997), Piromyces (Teunissen et al., 1991) and Orpinomyces (Li et al., 1997). However, evidence suggests the presence of cellulosomes or cellulosome-like multienzyme complexes in a few aerobic microorganisms (Table 1). It is speculated that several other cellulolytic bacteria may also produce cellulosomes not yet described.
Simplified schematic of general cellulosome components and connection with cell surface based on knowledge of Clostridium cellulosome. (This figure is adapted from Bayer et al., 1994).
Anaerobic | Aerobic | ||||
Microorganism | Source | Ref. | Microorganism | Source | Ref. |
Bacteria | Bacteria | ||||
Acetivibrio cellulolyticus | Sewage | Ding et al., 1999 | Bacillus circulans F-2 | Potato starch granules | Kim and Kim, 1993 |
Amorocellulobacter alkalithermophilum | Soil | Watthanalarm-lort et al., 2012 | Bacillus licheniformis SVD1 | Bioreactor | van Dyk et al., 2009 |
Bacteroides cellulosolvens | Sewage | Ding et al., 2000 | Paenibacillus curdlanolyticus B-6 | Anaerobic digester | Pason et al., 2006b |
Bacteroides sp. strain P-1 | Anaerobic digester | Ponpium et al., 2000 | Sorangium cellulosum | Soil | Hou, et al., 2006 |
Butyrivibrio fibrisolvens | Rumen | Berger et al., 1990 | |||
Clostridium acetobutylicum | Soil | Sabathé et al.,2002 | |||
Clostridium cellobioparum | Rumen | Lamed et al., 1987 | Actinomycetes | ||
Clostridium cellulolyticum | Compost | Pagès et al., 1997 | Streptomyces olivaceoviridis E-86 | Soil | Jiang et al., 2004 |
Clostridium cellulovorans | Fermenter | Sleat et al., 1984 | |||
Clostridium josui | Compost | Kakiuchi et al., 1998 | Fungi | ||
Clostridium papyrosolvens | Paper mill | Pohlschröder et al., 1994 | Chaetomium sp. Nov. MS-017 | Rotted wood | Ohtsuki et al., 2005 |
Clostridium thermocellum | Sewage soil | Lamed et al., 1983 | |||
Eubacterium cellulosolvens | Rumen | Blair and Anderson, 1999b | |||
Ruminococcus albus | Rumen | Ohara et al., 2000 | |||
Ruminococcus flavefaciens | Rumen | Ding et al., 2001 | |||
Tepidimicrobium xylanilyticum BT14 | Soil | Phitsuwan et al., 2010 | |||
Thermoanaerobacterium thermosaccharolyticum NOI-1 | Soil | Chimtong et al., 2011 | |||
Fungi | |||||
Neocallimastix patriciarum | Rumen | Dalrymple et al., 1997 | |||
Orpinomyces joyonii | Rumen | Qiu et al., 2000 | |||
Orpinomyces PC-2 | Rumen | Borneman et al., 1989 | |||
Piromyces equi | Rumen | Teunissen et al., 1991 | |||
Piromyces E2 | Faeces | Teunissen et al., 1991 |
Cellulosome and cellulosome-like multienzyme complexes from anaerobic and aerobic microorganisms. (This table is adapted from Doi & Kosugi, 2004).
Efficient enzymatic degradation of lignocellulosic biomass requires a tight interaction between the enzymes and their substrates, and the cooperation of multiple enzymes to enhance the hydrolysis due to the complex structure. Multienzyme complexes, cellulosomes from anaerobic cellulolytic microorganisms, are dedicated to hydrolyzing lignocellulosic substances efficiently because of a large variety of cellulases and hemicellulases in complexes, useful enzymatic properties, and binding ability to insoluble cellulose and/or xylan via CBMs (Bayer et al., 2004; Doi and Kosugi, 2004; Schwarz et al., 2001; Shoham et al., 1999). When compared with aerobic enzymes, they produce several individual enzymes, but microorganisms are not binding to insoluble substrates. However, P. curdlanolyticus B-6 was found to produce a multienzyme complex under aerobic conditions (Pason et al., 2006a, 2006b). Little information has been reported on cellulosome-like multienzyme complexes produced by aerobic bacterium (Kim & Kim, 1993; Jiang et al., 2004; van Dyk et al., 2009). Therefore, the multienzyme complex produced by strain B-6 is critical for improving plant biomass degradation.
Among several Bacillus strains, isolated from various sources and cultivated under aerobic conditions, P. curdlanolyticus strain B-6 shows important evidences for multienzyme complex producing bacterium (Pason et al., 2006a) as follows: high production of cellulase and xylanase, presence of CBMs that have ability to bind to insoluble substances, adhesion of bacterial cells to insoluble substances, and production of multiple cellulases and xylanases in the form of a high molecular weight complex. Thus, strain B-6 exhibits great promise bacterium in the production of multienzyme complex under aerobic conditions. Some properties of bacterial cells and cellulase and xylanase from strain B-6 compared with other Bacillus spp. are shown in Table 2.
Strain (Bacillus sp.) and growth condition | Specific activity (U/mg protein) | Enzyme binding ability to insoluble substances (%) | Adhesion of cells to insoluble substances (%) | Zymogram analysis | ||||
CMCase | Xylanase | Avicel | Xylan | Avicel | Xylan | CMCase band | Xylanase band | |
1. Strain B-6 | ||||||||
Avicel grown | 0.16 | 1.12 | 57.1 | 64.3 | 28.0 | 39.9 | 11 | 13 |
Xylan grown | 0.12 | 7.19 | 39.1 | 51.5 | 13.6 | 74.7 | 9 | 15 |
2. Strain H-4 | ||||||||
Avicel grown | 0.15 | 1.10 | 50.0 | 50.0 | 0 | 0 | 2 | 2 |
Xylan grown | 0.09 | 4.23 | 31.1 | 38.5 | 0 | 0 | 1 | 3 |
3. Strain S-1 | ||||||||
Avicel grown | 0.15 | 0.90 | 43.4 | 49.1 | 0 | 0 | 3 | 2 |
Xylan grown | 0.09 | 4.49 | 37.9 | 45.8 | 0 | 0 | 2 | 3 |
4. Strain X-11 | ||||||||
Avicel grown | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
Xylan grown | 0.05 | 3.29 | 29.2 | 45.0 | 0 | 0 | 0 | 2 |
5. Strain X-24 | ||||||||
Avicel grown | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
Xylan grown | 0.06 | 3.19 | 29.6 | 36.1 | 0 | 0 | 0 | 2 |
6. Stain X-26 | ||||||||
Avicel grown | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
Xylan grown | 0.04 | 3.10 | 28.2 | 38.2 | 0 | 0 | 0 | 2 |
Production of carboxymethyl cellulase (CMCase) and xylanase by Bacillus strains; binding ability of enzymes to insoluble substances; adherence of bacterial cells to insoluble substances; and zymograms analysis in culture supernatant.
P. curdlanolyticus strain B-6 was a facultative, spore-forming, Gram-positive, motile, rod-shaped organism and produced catalase. Thus, this bacterium was identified as a member of the genus Bacillus according to Bergey’s Manual of Systematic Bacteriology (Sneath, 1986). The bacterium was also identified by 16S rRNA gene sequence analysis. The use of a specific PCR primer designed for differentiating the genus Paenibacillus from other members of the Bacillaceae showed that this strain had the same amplified 16S rRNA gene fragment as a member of the genus Paenibacillus. Based on these observations, it is reckoned that this strain was transferred to the genus Paenibacillus (Shida et al., 1997). The 16S rDNA sequence of this strain had 1,424 base pairs and 97% similarity with Paenibacillus curdlanolyticus (Innis & Gelfand, 1990).
During growth of P. curdlanolyticus B-6 on Berg’s mineral salt medium containing 0.5% xylan as carbon sources, the protein concentration in the medium was low up to the late stationary growth phase. CMCase and xylanase activities could be detected in the culture medium after the late exponential phase (Pason et al., 2006b). At the declining growth phase, the extracellular xylanase and CMCase rapidly increased due to the release of enzymes from the cell surfaces into the culture medium. These phenomena were different from the growth patterns of other aerobic bacteria, which grew and produced extracellular enzymes into culture supernatant immediately, but similar to those of the anaerobic bacteria which produced multienzyme complexes (cellulosomes) around the cell surfaces and adhered to these substrates and secreted into culture supernatant later (Bayer & Lamed, 1986; Lamed & Bayer, 1988). The observation of cell surfaces at the late exponential growth phase by scanning electron microscopy (SEM) revealed that the cells adhered to xylan (Fig. 5A), similar to the cells of the cellulosome producing anaerobic bacterium, C. thermocellum, which is a cell associated entity that mediates the adhesion of the bacterium to cellulose (Lamed et al., 1987; Mayer et al., 1987), whereas the surface of the cells of strain B-6 at the late stationary growth phase lacked such structures because the multienzyme complex was released into the medium from the cell surfaces (Fig. 5B). In addition, the pattern of multienzyme complex in the culture medium at the late stationary growth phase was determined. Native-polyacrylamide gel electrophoresis (native-PAGE) exhibited a high molecular weight band at the top of the gel (Fig. 6, lane 1). This protein band was dissociated into major and minor components through treatment by boiling in sodium dodecyl sulphate (SDS) solution, showing at least 18 proteins with molecular masses in the range of 29 to 280 kDa (Fig. 6, lane 2). Among those protein bands, at least 15 bands showed xylanase activities (Fig. 6, lane 3) and at least 9 bands showed CMCase activities (Fig. 6, lane 4) on zymograms. These multiple cellulases and xylanases are assembled into the high molecular weight complexes and released from the cell surfaces into medium at the late stationary growth phase. In C. thermocellum, the cellulosome consisted of many different types of glycosyl hydrolases, including cellulases, hemicellulases, and carbohydrate esterases, which served to promote their synergistic action (Lamed et al., 1983). These evidences confirm that the strain B-6 can produce xylanolytic-cellulolytic enzyme system that exists as multienzyme complex under aerobic conditions.
SEM of the cell surfaces of P. curdlanolyticus B-6 harvested at the late exponential growth phase showing adhesion of cell to xylan (A) and the cell harvested at the late stationary growth phase showing no adhesion of cell to xylan (B).
Proteins and enzymes patterns of multienzyme complex in culture supernatant at the late stationary growth phase; Native-PAGE (lane 1), SDS-PAGE (lane 2), and zymograms analysis of xylanase activity (lane 3), and CMCase activity (lane 4).
The effect of polymeric substances such as cellulose, xylan, corn hull, and sugarcane bagasse, and of soluble sugars such as L-arabinose, D-galactose, D-glucose, D-xylose, and cellobiose on the induction of multienzyme complexes in a facultatively anaerobic bacterium, P. curdlanolyticus B-6, was investigated under aerobic conditions (Waeonukul et al., 2008; 2009b). Cells grown on each carbon source adhered to cellulose. Hence strain B-6 cells from all carbon sources must have an essential component responsible for anchoring the cells to the substrate surfaces. Native–PAGE, SDS–PAGE, zymograms analysis, and enzymatic assays revealed that many proteins having xylanolytic and cellulolytic activities from P. curdlanolyticus B-6 grown on each carbon source were produced as multienzyme complex into the culture supernatants. These results indicated that strain B-6 produced multienzyme complexes when grown on both polymeric substances and soluble sugars. However, the subunits expressed in the multienzyme complex of strain B-6 depended on the carbon sources. These observations are consistent with previous reports that the enzymatic activities and enzyme compositions of the cellulosomes of C. thermocellum (Bayer et al., 1985; Bhat et al., 1993; Nochur et al., 1993), C. cellulolyticum (Mohand-Oussaid et al., 1999), and C. cellulovorans (Kosugi et al., 2001; Han et al., 2004; 2005) and the xylanosome of S. olivaceoviridis E-86 (Jiang et al., 2004) were affected by carbon sources in the media.
Many investigators have reported that the synthesis of cellulosome assemblies requires the presence of crystalline cellulose under anaerobic conditions, and that synthesis hardly occurs in growth on glucose or other soluble carbohydrates (Nochur et al., 1992; Blair & Anderson; 1999a; Bayer 2004; Doi & Kosugi, 2004). Some strains of C. thermocellum (Bayer et al., 1985; Bhat et al., 1993), however, can induce cellulosome synthesis when grown on cellobiose. P. curdlanolyticus B-6 differs from most cellulosome-producing microorganisms in that it produces multienzyme complex when grown on both polymeric substances and soluble sugars under aerobic conditions. Therefore, the mechanism of multienzyme complex formation by strain B-6 must be different from that of other microorganisms.
Recently, the structures and mechanisms for assembly of multienzyme complexes, cellulosomes, in anaerobic cellulolytic microorganisms are clear (Bayer et al., 2004, 2007; Doi & Kosugi, 2004). Generally, the key feature of the cellulosome is a scaffoldin that integrates the various catalytic subunits into the complex by self-assembly by cohesion-dockerin interaction. However, the structure and mechanism of the multienzyme complex produced by a facultatively anaerobic bacterium, such as P. curdlanolyticus B-6 is still unknown. In order to describe features of the multienzyme complex system produced by strain B-6, the multienzyme complex was purified by four kinds of chromatography (cellulose affinity, gel filtration, anion-exchange and hydrophobic-interaction chromatographys) (Fig. 7).
Isolation and purification of multienzyme complex of P. curdlanolyticus strain B-6.
The multienzyme complex of P. curdlanolyticus strain B-6 with molecular mass of 1,450 (G1) was isolated from culture supernatant at the late stationary growth phase through cellulose affinity and Sephacryl S-300 gel filtration chromatographys (Pason et al., 2006b). Basically, the individual cellulosomes from anaerobic bacteria show 600 kDa to 2.1 MDa complexes size and show cohesion-dockerin domain as a signature protein (Bayer et al., 2004; Doi & Kosugi, 2004). While, multienzyme complexes from aerobic microorganisms, were range in mass from about 468 kDa to 2 MDa (with contained 5-12 protein subunits) (Table 3) and has no report of cohesion-dockerin domain. Here, the multienzyme complex produced by strain B-6 under aerobic conditions was the first report on characterization.
Multienzyme complex | Mol. Mass (kDa) | Protein subunits | Ref. |
Aerobic microorganisms | |||
Paenibacillus curdlanolyticus B-6 | 1450 | 11 | Pason et al.,2006b |
Bacillus circulans F-2 | 669 | 7 | Kim and Kim, 1993 |
Bacillus licheniformis SVD1 | 2000 | 12 | van Dyk et al., 2009 |
Sorangium cellulosum | 1000-2000 | 10 | Hou et al., 2006 |
Streptomyces olivaceoviridis E-86 | 1200 | 5 | Jiang et al., 2004 |
Chaetomium sp. Nov. MS-017 | 468 | 12 | Ohtsuki et al., 2005 |
Anaerobic microorganisms | |||
Clostridium acetobutylicum | 665 | 11 | Sabathé et al.,2002 |
Clostridium cellulolyticum | 600 | 14 | Gal et al., 1997 |
Clostridium cellulovorans | 900 | 10 | Shoseyov & Doi 1990 |
Clostridium josui | 700 | 14 | Kakiuchi et al., 1998 |
Clostridium popyrosolvens | 600 | 15 | Pohlschröder et al., 1994 |
Clostridium thermocellum | 2100 | 14 | Lamed et al., 1983 |
Ruminococcus albus | 1500 | 15 | Ohara et al., 2000 |
Molecular weights and protein subunits of multienzyme complexes from aerobic and anaerobic microorganisms.
Elucidation of the purified multienzyme feature of P. curdlanolyticus strain B-6 was followed by anion-exchange and hydrophobic-interaction chromatographys (Pason et al., 2010). The complex G1 from gel filtration chromatography (1,450 kDa) was purified by anion-exchange chromatography and showed at least five large protein complexes or aggregates, namely F1-F5. Among the fractions obtained from anion-exchange chromatography, F1 was apparently the most suited fraction to study on the organization and function of the multienzyme system of strain B-6 because F1 formed one clear band on the top of native PAGE, had the highest xylanase activity, and its subunit composition was clearly shown on SDS-PAGE. In the final step, complex F1 was separated to one major complex (H1) and two minor protein components (H2 and H3) by hydrophobic-interaction chromatography. The multienzyme complex (H1) was composed of a 280 kDa protein with xylanase activity, a 260 kDa protein that is a truncated form on the C-terminal side of the 280 kDa protein, two xylanases of 40 and 48 kDa, and 60 and 65 kDa proteins having both xylanase and CMCase activities (Fig. 8). The two components (280 and 40 kDa) of the multienzyme complex has characteristics similar to the cellulosome of C. thermocellum in that it is composed of a scaffolding protein and a catalytic subunit (Bayer et al., 1998; Demain et al., 2005). The 280 kDa protein resembled the scaffolding proteins of the multienzyme complex based on its migratory behavior in polyacrylamide gels and as a glycoprotein. The 280 kDa protein and a 40 kDa major xylanase subunit are the key components of multienzyme complex of the strain B-6.
Native-PAGE (A) and SDS-PAGE (B) in isolated complex from culture supernatant at the late stationary growth phase (lane Cr), affinity column (lane A1), gel filtration column (lane G1), anion-exchange column (lane F1) and hydrophobic-interaction column (lane H1). All samples contained 200 g of protein.
These apparently propose that P. curdlanolyticus B-6 produced multienzyme complex, which consisted of many subunit compositions. The large protein (280 kDa) may function as a scaffoldin-like protein that allowed the enzyme subunits, majority is 40 kDa, binding to form a multienzyme complex. The key components, 280 and 40 kDa, are identified in the next topic.
P. curdlanolyticus B-6 produces an extracellular xylanolytic-cellulolytic multienzyme complex mainly comprised of xylanases under aerobic conditions. To understand the xylanase system, a genomic library of the strain B-6 was constructed and screened for high xylanase activity. Recently, six xylanase genes, S1 (Pason et al., 2010), xyn10A (Waeonukul et al., 2009a), xyn10B (Sudo et al., 2010), xyn10C (unpublished data), xyn10D (Sakka et al., 2011) and xyn11A (Pason et al., 2010) were cloned, and the translated products were characterized (Table 4).
Enzyme | Modular structure | GH family | Mol. Mass (kDa) | GenBank accession No. |
S1 | U | 91 | - | |
Xyn10A | 10 | 142 | EU418764 | |
Xyn10B | 10 | 40 | AB570291 | |
Xyn10C | 10 | 35 | AB688987 | |
Xyn10D | 10 | 61 | AB600191 | |
Xyn11A | 11 | 40 | FJ956758 |
Modular structure xylanases of P. curdlanolyticus strain B-6.
S1 protein: From the early research, the 280 kDa subunit (S1) plays a role of scaffoldin in assembling the enzyme complex and shows xylanase activity (Pason et al., 2010). The S1 gene consists of 2,589 nucleotides and encodes 863 amino acids with a molecular weight of 91,000 Da, indicating that the 280 kDa subunit is highly glycosylated. Sequence analysis revealed that S1 did not have significant homology with any proteins in the databases except for two surface layer homology (SLH) domains in its N-terminal region. Surprisingly, the recombinant S1 exhibits xylanase activity, and cellulose- and xylan-binding ability, suggesting that the S1 should be a novel xylanase and CBM(s) with new functions (unpublished data).
Xylanase Xyn10A: The xyn10A gene consists of 3,828 nucleotides encoding a protein of 1,276 amino acids with a predicted molecular weight of 142,726 Da. Xyn10A is a multidomain enzyme comprised of nine domains in the following order: three family-22 CBMs, a family-10 catalytic domain of glycosyl hydrolases (GH), a family-9 CBM, a glycine-rich region, and three SLH domains. Xyn10A can effectively hydrolyze insoluble xylan and natural biomass without pretreatment such as sugarcane bagasse, corn hull, rice bran, rice husk and rice straw. Xyn10A binds to various insoluble polysaccharides such as cellulose, xylan and chitin. The SLH domains functioned in Xyn10A by anchoring this enzyme to the cell surfaces of P. curdlanolyticus B-6. Removal of the CBMs from Xyn10A strongly reduced the ability of binding and plant cell wall hydrolysis. Therefore, the CBMs of Xyn10A play an important role in the hydrolysis of native biomass materials (Waeonukul et al., 2009a).
Xylanase Xyn10B: The xyn10B gene consists of 1,047 nucleotides encoding a protein of 349 amino acids with a predicted molecular weight of 40,480 Da. Xyn10B consists of only a family-10 catalytic of GH. Xyn10B is an intracellular endoxylanase (Sudo et al., 2010).
Xylanase Xyn10C: The xyn10C gene consists of 957 nucleotides and encodes 318 amino acid residues with a predicted molecular weight of 35,123 Da. Xyn10C is a single module enzyme consisting of a signal peptide and a family-10 catalytic module of GH (unpublished data).
Xylanase Xyn10D: The xyn10D gene consists of 1,734 nucleotides and encodes 577 amino acid residues with a calculated molecular weight of 61,811 Da. Xylanase Xyn10D is a modular enzyme consisting of a family-10 catalytic module of the GH, a fibronectin type-3 homology (Fn3) module, and family-3 CBM, in that order, from the N terminus. The CBM3 in Xyn10D has an affinity for cellulose and xylan, and plays an important role in hydrolysis of arabinoxylan and native biomass materials (Sakka et al., 2011).
Xylanase Xyn11A: The xyn11A gene consists of 1,150 bp and encodes a protein of 385 amino acids with a molecular weight of 40,000 Da. Xyn11A is composed of two major functional domains, a catalytic domain belonging to family-11 GH and a CBM classified as family-36. A glycine- and asparagine-repeated sequences existed between the two domains. Xyn11A has been identified to be one of the major xylanase subunit in the multienzyme complex of strain B-6 (Pason et al., 2010).
Simplified schematic view of the interaction between the P. curdlanolyticus B-6 multienzyme complex system and its substrate, and its connection to the cell surface via an associated anchoring protein. (Abbreviations: CBM, carbohydrate-binding module; CD, catalytic domain, En, enzyme subunit; SLH, surface layer homology domain).
Based on both biochemical and molecular biological findings, a simplistic schematic view of the enzyme system from P. curdlanolyticus B-6 and its interaction with substrate and cell surface was created and presented in Fig. 9. In this assessment, the S1 protein did not have significant homology with any proteins in the databases except for two S-layer homology domains in its N-terminal region. However, the S1 protein that exhibits xylanase activity and cellulose- and xylan-binding ability, and contains cell anchoring function, seems remarkable. The multifunctional protein S1 is also responsible for forming the enzyme subunits into the complex and anchoring the complex into cell surface via the SLH domain. The interaction between S1 protein and enzyme subunits should be a mechanism distinct from the cohesion-dockerin interaction known in cellulosome of anaerobic microorganisms, since cohesion- or dockerin– like sequences were not observed in the S1 protein or the major xylanase subunit, Xyn11A. In addition, strain B-6 also produces cell bound multimodular xylanase Xyn10A that contains the numerous CBMs and SLH domains. Xyn10A can bind to the plant cell wall through CBM, whereas the catalytic module (GH10) is able to access its target substrate. Thus, the CBM greatly increases the concentration of the enzyme in the vicinity of the substrate, leading to the observed increase in polysaccharide hydrolysis. Besides, the presence of the functional CBMs and SLH domains in Xyn10A allows the cells to attach to substrate. Although, the overall structure of the enzyme complex system of the strain B-6 is not entirely clear, the enzyme complex has unique characteristics distinct from multienzyme complex cellulosome of anaerobic microorganisms. However, the mechanism for complex formation, interaction between the S1 protein as scaffoldin and enzyme subunits, needs to be further investigated.
Biological conversion of lignocellulosic materials has been proposed as a renewable and sustainable route for the production of value-added products (Bayer et al., 2007, Doi et al., 2003). There is much interest in exploiting the properties of multienzyme complexes for practical purposes. The facultative bacterium, P. curdlanolyticus strain B-6 produces a unique extracellular multienzyme system under aerobic conditions that effectively degrade cellulose and hemicellulose by gaining access through the protective matrix surrounding the cellulose microfibrils of plant cell walls. Therefore, the multienzyme complex from strain B-6 is a promising enzyme which can potentially be used in many applications, such as enhancing extraction and production of value-added bioproducts by saccharification of cell wall components and application for construction of the modular enzymes creation (Fig. 10).
The multienzyme complex of P. curdlanolyticus strain B-6 for biotechnological applications.
Biological treatment and saccharification using microorganisms and their enzymes selectively for degradation of lignocellulosic residues has the advantages of low energy consumption, minimal waste production, and environmental friendliness (Schwarz, 2001). The catalytic components of the multienzyme complex release soluble sugars, simple 5- and 6-carbon, from lignocellulose providing the primary carbon substrates, which can be subsequently converted into fuels by microorganisms. For enzyme saccharification, the close proximity between cellulolytic and xylanolytic enzymes is key to concerted degradation of the substrate, whereby the activities of the different enzymes facilitate the activities of their counterparts by promoting access to appropriated portions of the rigid insoluble substrates, since the release of sugar products was high. The synergistic action of the combination of enzymes by different modes of actions (xylanases and cellulases) and the presence of xylan- or cellulose-binding ability on lignocellulose enhanced soluble sugars released from the plant cell walls. In practicality, the multienzyme complex produced from P. curdlanolyticus B-6 allows access to lignocellulosic substrate and produces reducing sugar more than non-complexed enzymes from fungi (T. viride and Aspergillus niger) when the same cellulase activity (0.1 unit) was applied for degradation of corn hull and rice straw residues (unpublished data). In addition, the multienzyme complex of strain B-6 has been used to improve the extraction of plant food such as making low-cyanide-cassava starch by using multienzyme complex to enhance linamarin released by allowing more contact between linamarase and linamarin (Sornyotha et. al., 2009). Also, extraction of volatile compounds such as sea food-like flavor from seaweed, served for food supplement. Consequently, enzymatic treatment has advantages for the preparation of β-glucan and acidic α-glucan-protein complex from the fruiting body of mushroom, Pleurotus sajor-caju because the specificity of the multienzyme complex and gentle conditions allow for the recovery of high purity glucans in their native forms with minimal degradation (Satitmanwiwat et al., 2012a,b).
Typically, most plant cell wall degrading enzymes are composed of a series of separate modules (modular enzymes). These domains may fold and function in an independent manner and are normally separated by short linker. P. curdlanolyticus B-6, produces a number of glycosyl hydrolase (GHs) families and CBM families which have different substrates recognition affinity and increase amorphous regions of cellulose by H-bond elimination. Interestingly, modular architecture created by chimeric proteins creation with various tandem CBMs, GHs, and SLH-specific, should make it possible to construct effective lignocellulosic degrading enzymes, strongly binding, targeting enzyme to their substrates and bacterial cell surfaces for enhancing a variety of substrates hydrolysis. The strong carbohydrate-binding property of the cellulose-binding domain and xylan-binding domain, specific degradative activities exhibit important properties of the lignocellulosic material degrading enzymes that can be used in biotechnology.
A facultatively anaerobic bacterium P. curdlanolyticus strain B-6, isolated from an anaerobic digester fed with pineapple wastes, is unique in that it produces extracellular xylanolytic-cellulolytic multienzyme complex capable of efficient degradation of plant biomass materials under aerobic conditions. The production of strain B-6 multienzyme complex under aerobic conditions has several advantages: (i) a simple process, (ii) low price of medium, (iii) high growth rate, (iv) large quantities of extracellular enzymes yields, and (v) safe use with regard to health and environmental aspects. Thus, strain B-6 and its multienzyme complex is a promising tool for an industrial process employing direct hydrolysis for the bioconversion of cellulose as well as hemicellulose in biomass. This review shows that strain B-6 multienzyme complex is a novel enzymatic system known at the biochemical, genetic, and mechanism level. It also stresses that some points still need to be further investigated, mainly (i) the elucidation of scaffolding protein functions, (ii) the characterization of others key enzyme subunits, (iii) the assembly mechanism of the multienzyme complex, (iv) improvement of the efficiency in degradation of biomass of the multienzyme complex, and (v) improvement of the production of the multienzyme complex. The latter will certainly represent a challenge for future research.
Over the past decades, the livestock industry has been revolutionized toward the use of microbial feed additives due to an increasing awareness of the stockholders on the beneficial role of probiotics in production and gut health status [1, 2]. There are several probiotic products that are commercially available and marketed for animal use [3]. Most probiotic products at the moment do not go through pre-market approvals and are commonly used for a much wider range of scenarios in which their efficacy is not well established. Similarly, latest molecular methods such as gene sequencing and phylogenetic analysis are not used to identify the probiotic strains as feed supplements. For the selection of best probiotic product, it is highly important to determine the real probiotic potential of the microbial strain by using latest molecular methods. In this contract, locally isolated and validated probiotic strains will be better than any unauthorized local available strain. The competitive advantage and adaptability to local microbial ecosystem will allow local probiotic strain to grow and adhere well in the local animal breed. Literature showed that probiotic strains should specifically prepare according to purpose and function related to the milk enhancement in local breed [4, 5]. Nowadays, it is highly accepted that probiotic yeast is highly productive in terms of milk and meat for large animals [6, 7]. Probiotic yeast improves the ruminal gut microbiota which may increase the nutrient digestibility and leads to improve animal productivity [8]. In large animals, ingested feed digested by numerous microbial species is present along the gastrointestinal tract [9]. This microbial community consists of 1014 members, mainly composed of fibrolytic bacterial species [10]. Literature highlighted that gut microbiota plays important role in the feed digestion and utilization. The gut microbial populations in cow have been identified in almost 90% of the total microbial community [11]. On the other hand, a certain fraction of the GI tract bacterial community has yet to be identified due to less knowledge of the microbial community in gut microbial ecosystem because majority of the 16S rRNA gene sequences from feces are taken from unidentified species, and many modern methods of genomic analysis of communities to determine changes in microbiota have been used by many scientists [12]. Studies have utilized culture-independent sequencing techniques, 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing and many more have added a new era to determine the microbial diversity of the GI tract [13]. Research noted that the culture-independent methods deliver a comprehensive assessment of the microbial community composition, while the culture-dependent methods provide the structural and functional diversity of the microbial strains [14]. In this chapter, a detailed discussion on the effects of probiotic yeast in ruminant’s well being, production performance, uses of different omics methodologies for the discovery of ideal animal probiotic strains and development of indigenous probiotic yeast for ruminant will be employed.
The Saccharomyces cerevisiae (baker’s yeast) is the first eukaryotic sequenced genome. The sequencing of first whole eukaryotic genome was a challenging task for the scientists, but the efforts of more than 600 scientists from Europe, North America, and Japan made it possible. The entire sequence of the yeast was released in 1996. The size of the baker’s yeast genome is 12.1 Mb containing 16 chromosomes and 5400 coding genes approximately. The sequence information of yeast is available at Saccharomyces Genome Database (SGD), Yeast Protein Database (YPD), and Munich Information Center for Protein Sequences (MIPS) [15] (Table 1).
Yeast genome | |
---|---|
Genome size | 12.1 Mb |
Chromosomes | 16 |
Genes | 5300–5400 |
Base pairs | 12 million base pairs |
Databases | SGD, MIPS, YPD |
Details of first eukaryotic sequenced genome (yeast).
Ruminant nutritionists have been pondering to improvise new methodologies for ameliorating the roles of microflora in ruminants and enhance processes of digestion and fermentation along with augmented nutrients usage and bioavailability using feed supplementation. One of the commonly used methods was the use of growth promoters (antibiotics) to restrict the pathogenic effect on productivity of ruminants [16]. Nevertheless, antibiotics have been reported to cause serious health challenges to consumers and environmental implications. Thus, their usage has been banned in 2006 due to emerging antibiotic resistance. In the light of these concerns, consumer preferred more natural product. A super alternate of feed additives was the use of probiotics [17]. Probiotics are living microorganisms confined in animal feed that affect the host by improving the digestion [18]. Other definition includes probiotics as microorganisms (viable) that functions in gaining weight and feed conversions along with reducing diarrheal incidence [19]. Probiotics have been deployed as one of the recent exploited proposals in ensuring efficiency of production systems and safety to both consumers and environment [20, 21]. In ruminant nutrition, yeast probiotics are commonly being used because of their efficient roles in rumen stabilization and maintaining microbial communities specifically fibrolytic bacteria [22]. The yeast cells function in maintaining throughout viability of the digestive tract [23]. Yeast supplementation as probiotics enhanced feed conversion, efficient fermentation, and fiber digestion in the rumen, maintained ruminal pH, increased milk production [24, 25] and feed intake and production of organic acids and vitamins to activate the growth of the lactic acid bacteria (LAB) [26]. The commonly used yeast probiotic is Saccharomyces cerevisiae. Numerous literatures on Saccharomyces cerevisiae as supplement are available that dated back to the 1950s and continued under study till today [27]. Significant role of yeast supplementation (live) in diet has been stated for lactating and growing ruminants. Recent studies confirmed that they increase the ruminant’s milk production early lactation period by altering the fermentation of food inside the GIT of ruminants[28]. Latest beef and dairy production systems demand active muscle growth and high milk yield via feeding animal at high ruminal ferment ability rates. This would result in increased risk of metabolic disorders such as acidosis due to dysbiosis in ruminal microbial environment resulting in abnormal functioning in rumen which further leads to poor feed intake, health, and decreased productivity [29]. Therefore, yeast supplementation in ruminant diet is beneficial in the ruminal functioning and overall animal health and maintenance. The ameliorating functions of yeast probiotic on digestibility of high forage diets also underscore the potential use of yeast supplementation to optimize the use of lower quality feeds.
Rumen microbial manipulation by using the probiotics to improve the ruminant feed digestion is a promising production improvement strategy. A better understanding of the rumen microbiology is an important step to select and prepare a new yeast strain affecting on functional specific microbes. Latest molecular techniques have provided the opportunity to study the rumen microbiota in detail for development of the ideal probiotic.
Digestive system of ruminant is composed of four parts: reticulum, rumen, omasum and abomasums. The rumen is that part of the digestive system in which fermentation is carried out [30]. The rumen can also be defined as a complex ecosystem in which nutrients consumed by different microorganisms are digested anaerobically. Microbial biomass and volatile fatty acids are most common end products of fermentation which are then used by ruminant host. Interaction of host animal and microorganisms is a symbiotic relationship that helps the ruminant hosts in digestion of fiber-rich and protein-low diets. Rumen microorganisms provide enzymes that are necessary for fermentation processes, which in turn allow ruminants to obtain energy contained in forage [31]. Growth and activity of ruminal microorganisms are influenced by different factors including pH, temperature, osmotic pressure, buffering capacity, and redox potential. These factors are determined by environmental factors. Temperature of the rumen is in the range of 39–39.5°C. But when animal eats, fermentation occurs that generates heat due to which temperature increases up to the limit of 41°C [32, 33]. Short-chain fatty acid generation along with their absorption, saliva production, feed intake level and type, as well as exchange of phosphates and bicarbonates through epithelium of the rumen are the factors that affect pH [34]. In the reticule ruminal environment, these factors determine the buffering capacity as well as pH. There is a constant change in pH but mostly it remains in the range of 5.5–7.0 [35]. When there is an acidic environment in the cell, bacterial intracellular pH decreases. Microbial enzymes are very much sensitive to pH, i.e., bacterial growth is inhibited when there is an acidic pH. This is due to the disproportion of intracellular hydrogen ions [36]. In the rumen, ions and molecules affect osmotic pressure due to which gas tension is created. Fermentation process in the rumen depends upon the environmental factors and the diet due to which these factors also affect rumen osmotic pressure [37] (Figure 1).
Rumen ecosystem: different types of microbial flora present inside the rumen. The most abundant microbes are bacteria.
Bacteria are more in number than any other microbes. It is noted that there are five groups of rumen bacteria: (1) free-living in liquid phase, (2) loosely attached with feed, (3) firmly attached with feed, (4) attached with rumen epithelial lining, and (5) attached with protozoa/fungi. The bacterial species inside the rumen are 99.5% obligatory anaerobic. Mostly rumen bacteria are involved in the fermentation of fibers, starch, and sugar present in the feed and converted into volatile fatty acid, H2, and CO2 [38]. Most of the bacteria are responsible for degradation of different types of dietary components [39] (Table 2).
Bacteria | Species |
---|---|
Carbohydrate-utilizing bacteria | Fibrobacter succinogenes Ruminococcus flavefaciens Ruminococcus albus Clostridium cellobioparum Clostridium longisporum Clostridium lochheadii Eubacterium cellulosolvens Cillobacterium cellulosolvens Butyrivibrio fibrisolvens Prevotella ruminicola Bacteroides ruminicola Eubacterium xylanophilum Bacteroides uniformis |
Nitrogen-utilizing bacteria | Prevotella ruminicola Ruminobacteramylophilus Clostridium bifermentans |
Lipid-utilizing bacteria | Anaerovibriolipolytica |
Bacterial diversity of the rumen microbial ecosystem.
Majority of anaerobic rumen fungi is from order Neocallimastigales within the phylum Neocallimastigomycota. On the phylogeny basis, six genera have been identified, which are Piromyces, Neocallimastix, Caecomyces, Anaeromyces, Orpinomyces, and Cyllamyces [40]. In fiber digestion, fungi play a very important role because of the vegetative thallic rhizoids. The main functions of the rumen fungi are the lignin and fiber degradation by producing different types of enzymes [41] (Table 3).
Microbial species | Rumen | Fecal |
---|---|---|
Bacteria | Bulleidia Roseburia Prevotella Ruminococcus Acidaminococcus Megasphaera Succiniclasticum | Bacteroides Bifidobacterium Clostridium Collinsella Blautia Dorea Lactobacillus Peptostreptococcus Treponema Succinivibrio Faecalibacterium |
Fungi | Caecomyces Orpinomyces Piromyces | Caecomyces Orpinomyces Piromyces |
Archaea | Methanobrevibacter Methanosphaera | Methanobrevibacter Methanosphaera |
Bacteria, fungi, and archaea present inside the rumen and feces of dairy cows.
The rumen is the first part of the ruminant stomach which has a well-developed microbial ecosystem containing different types of microbes (bacteria, fungi, protozoa, and bacteriophages). These microbes coexist in ecological equilibrium in unique symbiotic relationship between cows and rumen microbes. The cows supply food to the rumen microbes which in turn digest the feedstuff to provide cows the essential nutrients in the form of microbial protein as organic acid energy sources. The microscopic view of rumen ecosystem showed that it is consisted of a number of bacteria, protozoa and fungi [42]. Bacteria make the largest population in this diverse microbial world. Their function is to digest the fibers, starch, sugar acids, and protein to give useful compounds and elements necessary for the growth and productivity of the cows. The role of protozoa and fungi is less clear. However, these microbes do provide help in digestion of feed. The structure and function of microbial community are influenced by feed composition and mainly by the host genetic potential. Prevotella and Succinivibrionaceae are the dominated rumen bacterial communities, cellulolytic and fibrolytic genera; Neocallimastigaceae are the dominant fecal and rumen fungal communities; and Methanobrevibacter are the dominant fecal and rumen archaeal communities in the adult ruminants. Bacteroidetes and Firmicutes are the dominant phyla of bacterial communities. Bacteroidaceae, Lachnospiraceae, Prevotellaceae, Ruminococcaceae, Succinivibrionaceae, and Veillonellaceae are the most abundant bacterial families in adult ruminant [43]. The term “yeast” is originally derived from the Dutch word gist, which basically refers to the foam that formed during beer fermentation. A variety of roles is played by yeast in veterinary practices, livestock feeding, and medicine as well as in biomedical and pharmaceutical industries [44]. Hayduck first discovered the inhibitory activity of yeast. Probiotics such as yeast or fungi have been extensively used in ruminant feed for the improvement of growth, health, and lactation due to their impact on rumen pH, intake of dry matter, and digestibility of nutrients [45]. Probiotic yeast has potential beneficial effects on the rumen. In the cattle, the ability of live yeast for enhancement of milk yield as well as weight gain is due to the fact that yeast is responsible for stimulating bacterial activity in the rumen [46]. Mechanism of action of yeast mainly stimulates the growth of cellulatic and hemicellulatic bacteria [47]. Increase in the number of bacteria in the rumen is due to the reproducible effects of probiotic yeast. Yeasts remove oxygen from the rumen due to which bacterial performance improves in the rumen. To maintain the metabolic activity, yeast cells consume available oxygen on the surface of freshly ingested feed in the rumen. Few studies showed that there is a significant decrease in redox potential, up to -20 mV by providing yeast supplementation (Figure 2).
Representative scheme of effect of live yeast on the microbial flora of the gastrointestinal tract in ruminants: live yeast improves carbohydrate, protein, and lipid digestion rates by improving the production of cellulolytic, hemi-cellulolytic, and proteolytic and lipolytic bacteria and fungi.
Better conditions have been created by this change for the growth of anaerobic cellulolytic bacteria which in turn stimulates their attachment to forage particles as well as increases the initial rate of cellulolysis. Recalcitrant plant lignocellulosic material is not degraded by ruminants on its own. They rely on rumen microbial flora for its degradation [48]. The main components of the fiber are cellulose, hemicellulose, and lignin. It has been estimated that 20–70% of the ruminant feed is composed of the cellulose and hemicellulose [49]. The most abundant carbohydrate in plant cell wall is the cellulose which makes up to 40% of the plant cell wall. The microbial cellulolytic enzymes have the capability to digest the β-1,4 links present inside the cellulose, glucose molecules [50] (Figure 3).
A scheme describing the mode of action of yeast culture: improved the gut microbial balance is related to the O2 slavering by live yeast cells.
The lower gut microbial population is affected by dietary supplementation of the probiotic yeast. The probiotics provide a desirable microbial balance due to shift in the balance of friendly and pathogenic microbiota. The GIT having healthy microbial populations are often related with improved host performance and its immune system. In the lower gut, the pathogenic microbial species reduces due to the production of the antimicrobial material (bacteriocin) and the attachment of the friendly microbes to the gut wall, via the competitive exclusive method. The most common modulation of the GIT microflora is provided by probiotics [51].
Latest researches have improved our understanding related to the mode of action of probiotic yeast inside the rumen. Well-designed animal studies have verified that target-specific probiotic strains have health and production benefits in the ruminants. These studies have made the livestock industry to accept and understand the probiotic concept [52]. On the other hand, current probiotic has not been chosen for definite purposes in the animal feed. Therefore, some unique molecular methods are needed for selection and characterization of target-specific probiotic strains [53]. It has been noted that during stress conditions, some portion of the live probiotic microbial strain enters in the dormant but metabolically active state called viable but nonculturable (VBNC) state. These microbial cells have an ability to replicate when acclimated to a favorable condition inside the host [54]. Uses of molecular techniques have changed the study of the rumen ecosystem. First is the PCR which is more sensitive than growth on traditional selective media in determining small differences in population sizes in response to dietary changes or upon the inclusion of an additive to the diet and thus may identify changes or shifts within levels of the microbial population which may have been previously overlooked [55] (Figure 4).
Probiotic preparation: general steps for the isolation and characterization of probiotic yeast strains for local animal breed.
In response to various feeding sources, changes within the microbial population can be studied by DNA fingerprinting (DGGE, TTGE, and TGGE). Probiotic can be classified into three different types, like mono-probiotic, poly probiotics, and combined probiotics depending on the probiotic strain function [55] (Figure 5).
Potential characteristics of typical animal probiotic yeast.
Yeasts and fungi are the ideal organisms and have been used in vast genetic studies and comparative genomic studies in eukaryotes because of their small and compact genomes.
We have sketched sampling approaches and finalized the protocols that will guide researchers in identifying the most ideal probiotics for animal use. Livestock is under increasing threat of antimicrobial resistance genes; therefore, continued optimization of protocols is urgently needed so that these threats can be reduced through the use of probiotics. Two sequence-based methods are commonly used for the identification of yeast. The first and the most common method used for the identification is PCR amplification of internal transcribed spacer (ITS) of nuclear ribosomal variable region that has been recognized as the universal barcode for the identification of fungi. The second and the advanced approach to identify fungal species or strains is shotgun metagenomics [56]. Microbes are very vital to life present on the earth. Their significance is increasing day by day as their beneficiary potential has been recognized in the field of health and medicine. There are two methods which have been utilized till now for the identification of the microorganisms present in microbial community.
Culture-dependent method
Culture-independent method
Both approaches have their own significance. Culture-based methods are considered effective for the morphological, physiological, and functional characterizations of a particular strain, while culture-independent technology is preferred to unravel the microbial diversity along with genomic and genetic identification of microbial communities. Studies have also indicated that there is a loss of 99% microbes in the laboratory-dependent culturing methods. Culturing-independent method has been recognized as an effective and efficient method to isolate the DNA of a number of microbes from an environmental sample which seems impossible using the cultural methods. The linkage of culture-dependent and culture-independent data has been recognized as a crucial step for the identification of probiotics [57]. For identification of the potential probiotic strains, researchers should use the latest molecular methods, and the probiotic strains should be deposited in some recognized microbial culture collection. Proteomics and metabolomics may also be used for choosing the best yeast species [58]. By utilizing strain’s proteome and metabolome, which are argued to yield a positive influence upon ruminal fermentation, it may be possible to identify specific traits, characteristics, and secondary growth metabolites that play a potential role to enhance the growth of target-specific microorganisms inside the rumen. Even accounting for the potential bias of latest molecular methods, it is obvious that these methods are the dominant tools recently accessible for monitoring the gut for bacterial diversity of dairy animals and developing new yeast strain [59]. Extensive use of molecular methodologies may give insights into the new era where such microbial studies are no longer limited to a handful of laboratories with an abundance of funding and labor. It is noted that the specific yeast strains of known origin act more precisely and efficiently as compared to the yeast strain obtained from any unknown origin [60]. As we note all ruminates live in different parts of the world; therefore, upon the ruminal fermentation different yeast strains may exhibit markedly different effects. Therefore, we should identify new yeast strains for getting best results on the rumen fermentation. Uses of molecular techniques have changed the study of the rumen ecosystem. First is the PCR which is more sensitive than growth on traditional selective media in determining small differences in population sizes in response to dietary changes or upon the inclusion of an additive to the diet and thus may identify changes or shifts within levels of the microbial population which may have been previously overlooked. In response to various feeding sources, changes within the microbial population can be studied by DNA fingerprinting (DGGE, TTGE, and TGGE). To select best yeast strains, proteomics and metabolomics may also be used. By characterizing the proteome and metabolome of microbial isolates endowed with the ability to have a positive impact on the rumen fermentation, it may be possible to identify specific traits, characteristics, and secondary growth metabolites which play genuine role in the improvement of the growth of some important microbial species [61] (Figure 6).
Interlinked factors involved in the application of probiotic in the ruminant nutrition.
Cultural approach is the widely used method in microbiology to grow a microbe in a laboratory. Sampling is the basic and the crucial step for the identification of the indigenous probiotic yeast. The second step is isolation of the pure yeast strain under laboratory conditions which requires a series of inoculation steps of the microbes on the selective media. After purification of the yeast isolate on the OGA media, the biochemical tests are performed to identify the distinct features of the pure isolates. Morphological features of the isolate are determined by using electron microscope. The next step is the molecular identification of the yeast via 18S rRNA gene sequencing. The probiotic characterization is usually performed according to the standards defined by the WHO [62]. The best probiotic strain is retrieved among all the selected potential candidates, and in vivo experiments are performed using an animal model. After functional testing, all technological and safety measures are accessed, and the probiotic yeast strain is ready for probiotic product and packaging [63].
The use of omics approach has been emphasized to study the microbiome of microbes. To identify the potential probiotic strains among the microbial community present in any environment, it is very important to identify all the microorganisms in microbiota and determine their structural and functional differences at genomic level. Below are the currently available omics approaches for the identification, screening, and selection of probiotic strains of indigenous yeast [64] (Figure 7).
Omics approaches to identify the probiotic.
Amplicon sequencing refers to the sequencing of a specific fragment of interest of a microbe using high-throughput sequencing technique. 18S amplicon sequencing is specifically used to determine the most prevalent fungal yeast species present in microbiota [65]. The methodologies used in the recent researches for the identification of bacterial probiotics can be applied in the recognition of indigenous probiotic yeast strains. The comparative and detailed analysis of 18S amplicon sequencing data can help the scientists in the isolation of potential probiotic after the identification of functional and structural characteristics of the indigenous yeast in microbiota. Further experiments and testing would be required to maximize the production and ability of probiotic yeast in the gut of an animal [66]. Furthermore, the 18S amplicon sequencing does not only help in the indigenous yeast identification, but it also reveals the diversity of microeukaryotes when 18S rRNA gene is sequenced [67].
Shotgun metagenomics is one of the most advanced techniques of sequencing in which the entire microbiome of microbiota is sequenced. The data generated using this method provides all the information about the genome of an organism [68]. Metagenomics information unravels the composition of microbial community and also indicates the genes, their functions, and associated genetic pathways. The identification of the indigenous yeast and their probiotic potential and capabilities can also be determined using the metagenomics data. Their relationship within the microbial community and their effect on the host can also be studied on the basis of the retrieved information [69].
Scientists and researchers are using metatrancriptomics to study and analyze the expression profiles of mRNA in a microbial community. The identification of genes, genetic pathways and their regulation, host-microbe interaction, and the symbiotic relation among microbes can easily be determined by using the mRNA expression data. Metatranscriptome approach can be pursued in the identification of indigenous probiotic yeast within the microbiota of an animal. For this purpose the sampling methods and molecular techniques should be improved [70].
Metabolomics refers to the study of the metabolites or final cellular products. This is also considered one of the useful and efficient methods for the identification of probiotic potential of a microorganism within a microbiota of an animal or selected biological sample [71]. Indigenous probiotic potential of yeast can also be determined using this technique. Studies are still needed to fully understand the function of metabolites in context of probiotic potential and other inhibitory functions of metabolic compounds. As metabolites vary in structure and function, so they could be used in the comparative studies of species and populations. A number of species with high probiotic potential could be approached using metabolomics [72].
Yeast probiotics not only help to improve the performance factor of cattle, but it also enhances nutrient digestibility. However, the effectiveness of yeast-supplemented products is variable. Therefore, future studies are required to estimate the potency of these diet products as supplements for finishing beef cattle, with an objective to have healthier and productive animals without negotiating their efficiency and costs.
The animal body is a “supraorganism” and refers to the gastrointestinal tract as a virtual organ of the human body. The ongoing research is mainly on probiotics that are used chiefly for the GI tract, whereas there is an impetus need to evaluate the progress on other regions of the body as well.
Yeast supplementation is an effective strategy; thus, it is vital to ensure the stability and viability of yeast-supplemented diet products by developing practicable and cost-effective technologies (e.g., storage, microencapsulation, etc.), which poses marketing and technological challenges for producers at industrial level. Polysaccharides, lipids, and proteins are chiefly used for encapsulation materials in food industry. However, cost-effective production remains a challenge for production of future probiotics and formulation technologies.
Role of yeast probiotics in combating antibiotic-associated diseases has been extensively reported through control trials and ingestion of yeast probiotics (Saccharomyces boulardii) and has positive therapeutic effects specifically in preventing antibiotic-associated diarrhea (ADD), but validated biomarkers for numerous target diseases are probiotic or antibiotic deficient. Therefore, in the field of probiotic investigation, the defining of validated biomarkers needs to be advanced.
There is a dire need to understand the composition and relationship of microbial community within an animal gut for improving the production of dairy products. Advances in the high-throughput technologies, computational tools, and omics approaches give insights into the molecular and genetic potential of an organism. Studies in the omics arena are still needed to fully understand the genetic mechanisms and pathway analysis.
Every living organism is different in terms of their genetic makeup. The current progresses in sequencing and functional omics techniques have delivered better understandings into the precise mechanisms underlying probiotic functionality. The emerging understanding of the animal gut microbiota allowed accurate characterization of probiotic effects on the commensal microbiota of animal in vivo. Identification of genes vital to probiotic functionality is providing scientists the capacity to genetically tailor probiotics to encounter the requirements for precise applications. The livestock sector has a larger proportion of land consumption than agriculture keeping in view both grain feed intake and grazing. This trend is expected to rise, putting pressure and competencies on land resources in the agriculture sector. Moreover, there is a high demand for quality production which Cannot be attained by traditional practices for feeding ruminants. Quality cereal feed costs high and is uneconomical for large production. Consequently, this creates an imbalance in nutrition which drastically reduces dairy production. Probiotic yeast can overcome dairy production disparity. It augments nutrient uptake and increases Immunity, overall better health and production. Utilization of probiotic yeast for health and production is influenced by many different factors including probiotic strains, age, and breed of cattle. Essentially, yeast probiotics enhance assimilation by balancing the microflora of the rumen. It facilitates fiber digestion via inducing fermentation and stabilizing high pH. Facilitating an environment that flourishes rumen microbes is one factor. Other avenues need to be explored for probiotic yeast. More probiotic yeast strains are needed to be identified. For the preparation of probiotic feed, a complete nutritional profile generation is required. Furthermore, the amino acid profile of milk produced by dairy heifers fed on yeast probiotic should be analyzed.
The recommendations are outlined as follows:
Sampling source should be indigenous for isolation of the probiotic strains.
The identification of the probiotic strains must be based on the international validated molecular methods.
The identified strain name should be deposited in validated microbial culture collection.
The probiotic as well as genetic properties of the probiotic strains should be studied. Good manufacturing practices must be applied with quality assurance and shelf-life conditions established and labeling made clear to include minimum dosage and verifiable health claims.
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