Abstract

Ruminants metabolize fibrous materials through microbial fermentation to extract the essential energy required for diverse biological processes. In the case of dairy cattle, the incorporation of dietary fiber enhances the fat content of milk by elevating the concentration of rumen acetate, which serves as a precursor for the biosynthesis of milk fat. A significant challenge in maximizing the nutrient and energy availability from fiber lies within the lignocellulosic structure of forages. A variety of methodologies, including physical, chemical, biological, and genetic approaches, have been devised to augment the efficacy of forage fiber utilization. Mechanical or physical processing techniques reduce particle size and gut fill, thereby facilitating increased feed intake. Among chemical interventions, several alkaline substances are known to enhance fiber digestibility. Innovative methods such as AFEX (Ammonia-fiber expansion) are capable of disrupting lignocellulosic bonds more effectively than ammonia alone by employing elevated temperatures, moisture levels, and pressure. One of the most dependable and effective strategies for enhancing fiber consumption has been the implementation of genetic advancements, such as brown-midrib mutants (BMR) characterized by diminished lignin content. To enhance the reproducibility, efficacy, cost-effectiveness, and practical application of technologies aimed at improving fiber utilization, further research is imperative.

Keywords:Dietary fiber; Digestion; Forages; Ruminants

Abbreviations:AFEX: Ammonia-fiber expansion; BMR: brown-midrib mutants; EFE: Exogenous fibrolytic enzymes; SFE: seedling-leaf-ferulate-ester mutation

Introduction

As the global populace continues to increase and dietary habits evolve, it becomes imperative to augment livestock production to satisfy the growing need for animal-derived products. The strategic enhancement of feed through the incorporation of feed additives optimizes the utilization of feed resources, thereby improving production efficiency in ruminant species [1]. The dietary regimens of ruminants are characteristically constituted of lignocellulosic substrates, predominantly in developing countries where agricultural byproducts serve as a fundamental component of ruminant nutrition. The rumen itself is a specialized compartment that encompasses a diverse assemblage of microorganisms, including bacteria, anaerobic fungi, protozoa, and methanogens [2]. In ruminants, the fermentation process occurring within the rumen is of paramount significance for the digestion of fibrous feed and its subsequent utilization. In contemporary research, attention has increasingly been directed towards improving the digestibility of lignocellulosic feed through the manipulation of ruminal lignocellulolytic microbial communities, which has resulted in a positive impact on rumen fermentation dynamics [3]. The current review focuses on the utilization of dietary fiber and various technologies to improve the nutritive value and digestion of fiber by the ruminant species.

Fiber in ruminant feedstuff

Fiber can be defined as the “indigestible and slowly digesting, or incompletely available, fractions of feeds that occupies space in the gastrointestinal tract” [4]. Fiber constitutes the major component of the plant cell wall, predominantly consisting of carbohydrates. The fundamental constituents of fiber encompass cellulose, hemicellulose, and lignin. From a chemical perspective, cellulose is characterized by linear arrangements of the monosaccharide. Starch, recognized as the carbohydrate reservoir in cereals, is likewise composed of glucose units. In cellulose, the glucose units are interconnected via a β-1,4 glycosidic bond, while in starch, they are linked by an α-1,4 glycosidic bond. Starch is classified as an α-glucan, in contrast to cellulose, which is categorized as a β-glucan. The digestion of the β-1,4 linked glucose present in cellulose is facilitated solely by microbial enzymes. Hemicellulose similarly relies on microbial enzymes for its degradation due to its intricate structure, which is predominantly constituted of the sugar xylose, also linked by β-1,4 bonds. Hemicellulose exhibits a close association with lignin, which exerts a pronounced negative effect on the digestibility of fiber [5].

The inclusion of fiber is critically significant in the context of ruminant nutrition. It is imperative for sustaining animal health and is necessary for preserving optimal rumen functionality and physiological processes [6]. The incorporation of fibrous components into the diet enhances its volume and ensures optimal ruminal function by promoting both rumination and salivation. The ruminal system of ovine and caprine species operates most efficiently when their daily nutritional intake comprises a substantial proportion of slowly fermentable fiber sources, commonly referred to as roughage. Prolonged mastication of such fibrous substances aids in maintaining the pH levels within the rumen at an optimal range conducive to the proliferation of fiber-degrading microorganisms. This phenomenon is frequently characterized as the process of cud-chewing. The digestive engagement with fiber incites the musculature within the ruminal wall to rhythmically contract and relax, thereby facilitating the agitations of the contents present in the rumen [7]. These forage products include any type of hay, silage, or fresh forage. Cottonseed and soybean hulls are frequently used as a type of fiber in feed formulations [8].

Technologies to enhance fiber digestion in ruminants

In recent years, advancements in animal nutrition, microbiology, and biotechnology have opened up new avenues for improving fiber digestibility in ruminants. These technologies aim to enhance the rumen microbial ecosystem, optimize the breakdown of plant fibers, and ultimately increase the efficiency of nutrient use. Several approaches, including physical, chemical, biological, and genetic methods, are utilized to improve the digestibility of fiber in ruminants, which are explained as follows:
• Physical or mechanical processing: Mechanical processing is a crucial complementary step in forage production due to its effect on forage physical properties that cause gut fill and limit feed intake. Forage particle size is critically important in dairy cattle diets, which must contain sufficient physically effective NDF [9], a combination of both physical (i.e., particle size) and chemical (i.e., NDF concentration) fiber characteristics [10], to stimulate chewing and salivation and reduce gut fill, without reducing digestibility. Physical method includes grinding, chopping, shredding, pelleting, steam treatment and harvesting time.
• Chemical processing: Processing of forages by chemical processes involves alkali treatment, ammoniation, ammonia fiber expansion (AFEX) technology and acid treatment. These processes increase cell wall degradability and enable ruminal microorganisms to attack the structural carbohydrates and increase degradation of hemicellulose and cellulose [11]. Various alkalis including ammonia, sodium hydroxide (NaOH), calcium oxide (CaO), and calcium hydroxide [Ca(OH)2] have been used to increase fiber digestion and hence nutritive value of low quality forages, particularly crop residues [12]. Ammoniation is one of the most studied chemical treatments for improving forage quality as it improves forage digestibility due to hydrolytic action of the alkali on linkages between lignin and structural polysaccharides [13].

An alternative to direct ammoniation alone that combines chemical and physical treatments is AFEX. The method involves ammoniating low-quality forages at high temperature and pressure, with subsequent pressure release and ammonia removal or recycling [14]. The main advantages of AFEX treatment over traditional ammoniation method include safety, as the pellets generated are benign, ease of transport due to density of the pellets, and recycling of the ammonia. However, unlike traditional ammoniation in stacks or bales, which is possible on farms, AFEX treatment occurs in reactors, which makes it difficult for onfarm application and avoidance of transport costs, which can be substantial.

The acid treatment is effective at hydrolyzing hemicellulose, decreasing cellulose crystallinity, and increasing the porosity of treated biomass [15]. Although pretreatment by acid is effective at improving the nutritive value of low-quality feed, it is not widely used for livestock production because of the cost, health hazards, and corrosive nature of the acids. To foster ease of handling and cost effectiveness, dilute acid treatment is preferred [16].
• Exogenous fibrolytic enzymes (EFE): Limited understanding of the composition and mode of action of EFE has restricted the development of effective EFE preparations that consistently improve fiber digestion and the performance of cattle [17]. The cellulase-xylanase and ferulic acid esterase are used as exogenous fibrolytic enzymes.
• Bacterial inoculant treatment: Applying microbial inoculants to forages at ensiling is beneficial as they may hydrolyze plant cell walls into sugars that serve as fermentation substrates, thus improving silage fermentation, nutrient preservation, and utilization of the silage by animals [18]. Consequently, some silage inoculant preparations contain fibrolytic enzymes, mainly cellulases or xylanases, and some studies have reported increased NDFD due to application of such products [19].
• Expansin treatment: Expansins are nonhydrolytic proteins with the unique ability to induce cell-wall relaxation or loosening [20]. They are relatively small proteins (between ~26 to 28 kDa) with disruptive activity that weakens cellulose fibers [21].

Plant expansins can be divided in 2 major families: α-expansins and β-expansins. The α family has cell wall relaxing or loosening activity during acid growth (i.e., growth under acidic conditions), whereas β has been identified as a family of pollen allergens [22].
• Yeast or yeast culture supplementation: Yeast products are used as feed additives throughout the world to improve animal performance. They include live yeast or fermentation products that can be fabricated from various strains of Saccharomyces cerevisiae. Various studies have shown that yeast products improved fiber utilization and animal performance [23].
• White and Brown rot fungi: White-rot fungi achieve lignin depolymerization through the activity of their ligninolytic enzymes, which include lignin peroxidase, manganese peroxidase, versatile peroxidase, laccase, and H2O2-forming enzymes [such as (methyl) glyoxal oxidase and aryl alcohol oxidase] [24]. These fungi improve digestibility and nutritive value of low-quality forages such as wheat straw and bermudagrass [25].

Brown-rot fungi can degrade lignocellulose polysaccharides by supposedly modifying rather than removing lignin [26] and producing enzymes that selectively depolymerize cellulose and hemicellulose, leaving a brown-colored rot [27]. Brown-rot fungi metabolize amorphous cellulose associated with lignin, leaving the crystalline cellulose [28].
• Genetic improvements: Improvements to fiber digestibility of forages are often accomplished by reducing lignin or indigestible NDF concentrations [29]. Brown midrib (BMR) mutant forages (corn, sorghum, and pearl millet) consistently have lower lignin concentrations compared with conventional forages, which has resulted in greater milk production when the BMR forages are fed [30]. Corn hybrids with seedling-leaf-ferulateester mutation (SFE) can have greater NDFD than the wild type. Feeding cows SFE-corn silage instead of isogenic CCS increased DMI and milk and 3.5% FCM yields [31].

Transgenic manipulation of plants to express fibrolytic enzymes may decrease the cost of production of exogenous fibrolytic enzymes (EFE) and is also an efficient method to increase hydrolysis or saccharification of forage biomass [32]. When transgenic corn plants with the ability to express an endocellulase from Acidothermus cellulolyticus were tested, expression of the enzyme during cell wall construction reduced the defiance of the cell walls, increasing acid digestion and saccharification, but did not affect the plant morphology and growth compared with wild types [33].

Conclusion

The demand for livestock products is on the rise due to the increasing human population; therefore, it is imperative to facilitate scientific advancements in fodder crop development through the provision of genetically modified plants and the creation of high-yield cultivars to enhance the supply of fodder. To augment the nutritional quality and fiber utilization in plants, the employment of BMR hybrids represents one of the most dependable, cost-effective, and prevalent methodologies. Various biological treatment approaches, such as the application of enzymes, inoculants, and yeast derivatives, have demonstrated significant improvements in fiber digestion and increased milk production in dairy cows. Combination treatments (such as AFEX) may reduce fiber strength and enhance digestibility, yet their feasibility for practical farm application remains uncertain. Further investigation into economically viable methods for improving fiber digestion is warranted to ensure their straightforward adaptation.

References

1. Puniya AK, Salem AZ, Kumar S, Dagar SS, Griffith GW, et al. (2015) Role of live microbial feed supplements with reference to anaerobic fungi in ruminant productivity: a review. J Integr Agric 14(3): 550-560.
2. Matthews C, Crispie F, Lewis E, Reid M, O’Toole PW, et al. (2019) The rumen microbiome: a crucial consideration when optimising milk and meat production and nitrogen utilisation efficiency. Gut Microbes 10(2): 115-132.
3. Jyothi C, Muwel N, Nayak S, Khare A, Sharma R, et al. (2024) Anaerobic rumen fungi as a feed additive in ruminants: a review. J Livest Sci 15: 78-85.
4. Martin NP, Russelle MP, Powell JM, Sniffen CJ, Smith SI, et al. (2017) Invited review: Sustainable forage and grain crop production for the US dairy industry. J Dairy Sci 100(12): 9479-9494.
5. Kung L (2006) The role of fiber in ruminant ration formulation.
6. Mirzaei-Aghsaghali A, Maheri-Sis N (2011) Importance of" physically effective fiber" in ruminant nutrition: a review. Ann Biol Res 2(3): 262-270.
7. Adesogan AT, Arriola KG, Jiang Y, Oyebade A, Paula EM, et al. (2019) Symposium review: Technologies for improving fiber utilization. J Dairy Sci 102(6): 5726-5755.
8. Li X (2021) Plant cell wall chemistry: implications for ruminant utilisation. J Appl Anim Nutr 9(1): 31-56.
9. Hall MB, Mertens DR (2017) A 100-year review: carbohydrates—characterization, digestion, and utilization. J Dairy Sci 100(12): 10078-10093.
10. Mertens DR (1997) Creating a system for meeting the fiber requirements of dairy cows. J Dairy Sci 80(7): 1463-1481.
11. Sun R, Lawther JM, Banks WB (1995) Influence of alkaline pre-treatments on the cell wall components of wheat straw. Ind Crop Prod 4(2): 127-145.
12. Singh GP, Klopfenstein TJ (1998) Relative effect of feeding urea supplemented and ammoniated wheat straw of different particle size on the passage rate, particle break down rate and digestibility in sheep. J Dairy Sci 51: 328–334.
13. Dean DB, Adesogan AT, Krueger NA, Littell RC (2008) Effects of treatment with ammonia or fibrolytic enzymes on chemical composition and ruminal degradability of hays produced from tropical grasses. Anim Feed Sci Technol 145(1-4): 68-83.
14. Griffith CL, Ribeiro Jr GO, Oba M, McAllister TA, Beauchemin KA (2016) Fermentation of ammonia fiber expansion treated and untreated barley straw in a rumen simulation technique using rumen inoculum from cattle with slow versus fast rate of fiber disappearance. Front Microbiol 7: 1839.
15. Sun YE, Cheng JJ (2005) Dilute acid pretreatment of rye straw and bermudagrass for ethanol production. Bioresour Technol 96(14): 1599-1606.
16. Torget R, Werdene P, Himmel M, Grohmann K (1990) Dilute acid pretreatment of short rotation woody and herbaceous crops. Appl Biochem Biotechnol 24: 115-126.
17. Adesogan AT, Ma ZX, Romero JJ, Arriola KG (2014) Ruminant Nutrition Symposium: Improving cell wall digestion and animal performance with fibrolytic enzymes. J Anim Sci 92(4): 1317-1330.
18. Muck RE, Bolsen KK (1991) Silage preservation and silage additive products. Field guide for hay and silage management in North America pp: 105-126.
19. Queiroz OCM, Kim SC, Adesogan AT (2012) Effect of treatment with a mixture of bacteria and fibrolytic enzymes on the quality and safety of corn silage infested with different levels of rust. J Dairy Sci 95(9): 5285-5291.
20. Georgelis N, Tabuchi A, Nikolaidis N, Cosgrove DJ (2011) Structure-function analysis of the bacterial expansin EXLX1. J Biol Chem 286(19): 16814-16823.
21. Silveira RL, Skaf MS (2016) Molecular dynamics of the Bacillus subtilis expansin EXLX1: interaction with substrates and structural basis of the lack of activity of mutants. Phys Chem Chem Phys 18(5): 3510-3521.
22. Cosgrove DJ (2015) Plant expansins: diversity and interactions with plant cell walls. Curr Opin Plant Biol 25: 162-172.
23. Jiang Y, Ogunade IM, Arriola KG, Qi M, Vyas D, et al. (2017a) Effects of the dose and viability of Saccharomyces cerevisiae. 2. Ruminal fermentation, performance of lactating dairy cows, and correlations between ruminal bacteria abundance and performance measures. J Dairy Sci 100(10): 8102-8118.
24. Sindhu R, Binod P, Pandey A (2016) Biological pretreatment of lignocellulosic biomass–an overview. Bioresour Technol 199: 76-82.
25. Nayan N, Sonnenberg AS, Hendriks WH, Cone JW (2018) Screening of white‐rot fungi for bioprocessing of wheat straw into ruminant feed. J Appl Microbiol 125(2): 468-479.
26. Highley TL (1991) Processes of wood decay and deterioration. Biodeterior Res 4: 227-230.
27. Gao Z, Mori T, Kondo R (2012) The pretreatment of corn stover with Gloeophyllum trabeum KU-41 for enzymatic hydrolysis. Biotechnol Biofuels 5: 1-11.
28. Kleman-Leyer K, Agosin E, Conner AH, Kirk TK (1992) Changes in molecular size distribution of cellulose during attack by white rot and brown rot fungi. Appl Environ Microbiol 58(4): 1266-1270.
29. Grant RJ, Ferraretto LF (2018) Silage review: Silage feeding management: Silage characteristics and dairy cow feeding behavior. J Dairy Sci 101(5): 4111-4121.
30. Sattler SE, Funnell-Harris DL, Pedersen JF (2010) Brown midrib mutations and their importance to the utilization of maize, sorghum, and pearl millet lignocellulosic tissues. Plant Sci 178(3): 229-238.
31. Jung HG, Mertens DR, Phillips RL (2011) Effect of reduced ferulate-mediated lignin/arabinoxylan cross-linking in corn silage on feed intake, digestibility, and milk production. J Dairy Sci 94(10): 5124-5137.
32. Furukawa K, Ichikawa S, Nigorikawa M, Sonoki T, Ito Y (2014) Enhanced production of reducing sugars from transgenic rice expressing exo-glucanase under the control of a senescence-inducible promoter. Transgenic Res 23: 531-537.
33. Brunecky R, Selig MJ, Vinzant TB, Himmel ME, Lee D, et al. (2011) In planta expression of A. cellulolyticus Cel5A endocellulase reduces cell wall recalcitrance in tobacco and maize. Biotechnol Biofuels 4: 1-11.