Effects of fermented mushroom residue feed on goat growth performance
Previous studies have shown that adding fermented mushroom residue to the diet can improve growth performance of livestock animals. Fazaeli et al. [14] found that adding 20% fermented Agaricus bisporus residue to the diet of fattening sheep significantly increased ADG and ADFI (p < 0.05) and reduced F/G. However, when the additive exceeded 20%, feed intake and digestibility were significantly reduced (p < 0.05). Song et al. [15] fed Berkshire fattening pigs a basic control diet and added 30%, 50%, and 70% fermented Pleurotus ostreatus residue. In the supplemented groups ADFI and feed to gain ratio were significantly elevated (p < 0.05). Addition of 30% fermented Pleurotus ostreatus residue to experimental pigs diets did not significantly affect ADG (p > 0.05), but ADG was significantly higher in the 50% and 70% groups (p < 0.05). Kim et al. [16] added high cellulose-decomposing bacteria to Pleurotus eryngii residue to promote anaerobic fermentation before feeding to Han Yu bulls. Dry matter intake and BW of the experimental group increased by 15% and 12%, respectively, compared with the control group.
In the current study, fermented mushroom residue had significant effects on BW, ADG, ADFI, and F/G of fattening goats. BW, ADG, and ADFI initially increased then decreased, while F/G initially decreased before increasing in line with the amount of dietary fermented mushroom residue. The beneficial effects were greatest with 20% dietary residue, which is generally consistent with previously published studies. The reason for the improvement in growth performance is likely to be that mushroom residue contains a large amount of crude protein and is rich in minerals, amino acids, and other nutrients that promote animal growth [17,18]. Fermentation of mushroom residue degrades cellulose, hemicellulose and other macromolecular substances to sugars, amino acids, vitamins, and other nutrients which are easily digested and absorbed by ruminants, improving the beneficial feed properties of this material [19,20].
Effects of fermented mushroom residue feed on goat rumen microorganisms
Alpha diversity analysis focused on rumen microbial community richness and diversity. Adding fermented mushroom residue to goat diets improved Shannon, Chao1, and ACE indices, but not significantly. Chao1 and ACE indices were highest in group L, indicating that fermented mushroom residue could increase the richness and diversity of the rumen microbial communities. This is not consistent with the results of Jami et al. [21]. This may be because the composition of gastrointestinal flora is influenced by many factors, such as dietary nutrition level, heredity, and stress, which lead to differences in microbial community composition [22]. The beta diversity indexes of groups L and H were also significantly higher than control group C (p < 0.05), which further indicates that the addition of fermented mushroom residue changes the diversity of microbial communities. This is in agreement with the results of Rey et al. [23]. Following the addition of fermented mushroom residue, the rumen flora in the goats gradually tended to a stable state and reached a dynamic balance.
Gastrointestinal microorganisms can promote the ontogenetic process of animals and participate in animal metabolism. Qin et al. [10]and Ley et al. [24] Studies have consistently shown that Firmicutes and Bacteroidetes are the dominant bacterial phyla in ruminants. Firmicutes are mainly involved in the energy absorption process and Bacteroidetes in the carbohydrate metabolism process. When the ratio of Firmicutes to Bacteroidetes (F/B) in the intestinal tract is relatively high it can be easier to promote the absorption and storage of energy by the host. In this study the main microorganisms in the control and experimental groups were Firmicutes and Bacteroidetes but their relative abundance varied between groups. Since the F/B ratio was highest in group L (1.46), it can be speculated that 20% dietary fermented mushroom residue promoted the storage of fat in fattening goats. This result is consistent with that of Kittelmann et al. [25] Firmicutes is the main phylum responsible for fiber decomposition and contains a large number of cellulose-decomposing fungi [26]. This study showed that the relative abundance of Ruminococcaceae (Firmicutes) was highest when 20% fermented mushroom residue was incorporated (group L). Ruminococcaceae is the major family of fiber-decomposing bacteria in the rumen and can degrade cellulose, hemicellulose, and other macromolecules into nutrients which are easily digested and absorbed by the animal, thus promoting growth [27]. In addition, LEfSe analysis showed that Veillonellaceae abundance in group L was significantly higher than in control group C. Veillonellaceae metabolize lactic acid into short chain fatty acids (SCFAs), acetate, and propionate via the methylmalonyl-COA pathway [28]. Scheiman et al. [29] found that lactic acid generated after continuous exercise could be absorbed by Veillonellaceae and converted into SCFAs to improve exercise performance. High propionate content is beneficial to ruminant production, its major role being as the main substrate of gluconeogenesis which improves production performance [30].
Bacteroidetes, as one of the dominant phyla in the gastrointestinal tract of animals, accounts for 10–50% of total rumen microorganisms. It is mainly involved in the degradation of non-fibrous carbohydrates and the metabolism of polysaccharides, and plays an important role in animal growth and health [31,32]. In this study, the abundances of Bacteroides and Prevotellaceae were higher in the experimental groups than control group. The relative abundance of Prevotellaceae increased in line with the amount of dietary fermented mushroom residue, reaching 18.36%. This is consistent with studies in dairy cattle [33], beef cattle [34] and sheep [35]. The high nutrient content of fermented mushroom residue promoted Prevotellaceae growth until it became the dominant bacterial family in the rumen of the goats. Prevotellaceae plays a role in rumen digestion and absorption of carbohydrates through direct and indirect pathways, its abundance in the rumen indirectly reflecting the level of carbohydrate digestion [36,37]. A higher abundance of Prevotellaceae in the rumen can also improve protein degradation and utilization [38,39]. Fraga et al. [40] also found that Prevotellaceae is involved in the synthesis of SCFAs and can ferment sugars and lactate through succinic acid and acrylic acid pathways to produce propionic acid, thus improving the rumen environment.
The comparative analysis of intestinal microbial function showed that KEGG pathways related to metabolism of cofactors and vitamins, lipid metabolism, and xenobiotic biodegradation and metabolism were more abundant in group L (20% mushroom residue). The main participant in metabolism of cofactors, vitamins, and pigments such as porphyrin and chlorophyll, is Bacteroides [41]. Some studies have shown that Ruminococcaceae contribute to lipid metabolism, including synthesis and degradation of ketone bodies. The effect of Ruminococcaceae on the lipid metabolism of the host can be mediated via metabolites (such as SCFAs, secondary bile acids, and trimethylamine) produced by the rumen flora and by pro-inflammatory bacterial-derived factors such as fats and polysaccharides [42].
Forty-nine KEGG pathways were identified that were significantly correlated with ADG. Twenty-six pathways, including protein kinases, propanoate metabolism, and biosynthesis of unsaturated fatty acids, were positively correlated with ADG. Shchemelinin et al. [43] found that protein kinases are involved in various pathological processes including malignant tumors. Protein kinase activities are known to fall in chronic myeloid leukemia, gastrointestinal stromal tumors, and various other sarcomas and cancers, as well as non-malignant diseases. They, therefore, function to maintain intestinal health and enhance disease resistance in animals. Propanoate metabolism mediated by rumen flora activates gastrointestinal gluconeogenesis through the enteroencephalic circuit, which is beneficial to promoting body weight gain and controlling blood glucose metabolism [44]. Many unsaturated fatty acids are hydrogenated by rumen microorganisms to produce stearic acid which, when oxidized, provides an energy source for metabolism and can also improve the composition of fatty acids in ruminant meat [45,46]. Twenty-three KEGG pathways, including pathogenic Escherichia coli infection and shigellosis, were negatively correlated with ADG. Pathogenic Escherichia coli infection can cause diarrhea, acute gastroenteritis, and result in weight loss [47]. Shigella adhere to intestinal epithelial cells, destroying the intestinal mucosa and causing ulceration which can lead to intestinal obstruction and diarrhea, adversely affecting the health and growth of the host [48,49].