Effect of tannin-degrading bacteria isolated from the rumen of some ruminants on the in vitro digestibility and gas production of fruits residues silage

Document Type : Original Article

Authors

1 Environmental Technologies Research Center, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran

2 Department of Animal Science, Faculty of Agriculture, University of Birjand, Birjand, Iran

3 Research Group of Environmental Stress in Animal Science, Faculty of Agriculture, University of Birjand, Birjand, Iran

4 Department of Aquaculture, Faculty of Natural Resources, Behbahan Khatam Alanbia University of Technology, Behbahan, Iran

5 Department of Environmental Science, Faculty of Environmental and Natural Resources, University of Birjand, Birjand, Iran

6 Department of Biology, Faculty of Science, Shahid Chamran University of Ahvaz, Ahvaz, Iran

7 Biotechnology and Biological Science Research Center, Shahid Chamran University of Ahvaz, Ahvaz, Iran

Abstract
While severe shortage of feed has presented livestock industry with a major challenge, millions of tons of fruit by-products (FBPs) are discarded annually, as valuable sources of energy and numerous nutrients. However, some of FBPs contain high tannins that must be treated for use in animal feeding. This study was investigated the effect of tannin-degrading bacteria isolated from the rumen of some ruminants on the in vitro digestibility and gas production of FBPs silage. The FBPs, including pomegranate peel (PP), and the pulps of lemon (LP), grape (GP), and orange (OP) were ensilaged with tannin-degrading bacteria (enzyme activity: 10.46 - 8.60 U mL-1) isolated from the rumen of male goat (Escherichia coli GHMGHE41), deer (Escherichia fergusonii GHMGHE44), ram (E. fergusonii GHMGHE30), and camel (Klebsiella aerogenes GHMGHE38). After anaerobic incubation (30 days; 39.00 ˚C), PP + camel strain silage showed the highest dry matter, and the lowest natural acid detergent fiber and pH. The camel strain increased crude protein content of LP silage to the highest level, and decreased acid detergent fiber of GP silage to the lowest level. The highest digestibility was observed for LP + goat strain silage (50.37%) compared to the uninoculated OP silage (42.73%). The maximum ammonia (N-NH3) and minimum level of pH were recorded for the silages of LP + goat strain and PP + CR strain, respectively. Overall, the current results showed that tannin-degrading E. coli GHMGHE41 and K. aerogenes GHMGHE38 were able to improve the digestibility of LP and PP silages as ingredients in ruminants’ diets.

Keywords

Subjects


  1. Wanapat M, Suriyapha C, Dagaew G, et al. The recycling of tropical fruit peel waste-products applied in feed additive for ruminants: food manufacturing industries, phytonutrient properties, mechanisms, and future applications. J Agric Food Res 2024; 17(2-3): 101234. doi:10.1016/j.jafr.2024.101234.
  2. Besharati M, Palangi V, Salem AZM, et al. Substitution of raw lucerne with raw citrus lemon by-product in silage: in vitro apparent digestibility and gas production. Front Vet Sci 2022; 9: 1006581. doi: 10.3389/fvets.2022.1006581.
  3. Li BY, Xia ZY, Gou M, et al. Production of volatile fatty acid from fruit waste by anaerobic digestion at high organic loading rates: performance and microbial community characteristics. Bioresour Technol 2022; 346: 126648. doi: 10.1016/j.biortech.2021.126648.
  4. Plazzotta S, Cottes M, Simeoni P, et al. Evaluating the environmental and economic impact of fruit and vegetable waste valorisation: the lettuce waste study-case. J Clean Prod 2020; 262: 121435. doi: 10.1016/ j.jclepro.2020.121435.
  5. Taghizadeh-Alisaraei A, Hosseini SH, Ghobadian B, et al. Biofuel production from citrus wastes: a feasibility study in Iran. Renew Sustain Energy Rev 2017; 69: 1100-1112.
  6. Zhao C, Wang L, Ma G, et al. Cellulase interacts with lactic acid bacteria to affect fermentation quality, microbial community, and ruminal degradability in mixed silage of soybean residue and corn stover. Animals (Basel) 2021; 11(2): 334. doi: 10.3390/ ani11020334.
  7. El Barnossi A, Moussaid F, Iraqi Housseini A. Tangerine, banana and pomegranate peels valorisation for sustainable environment: a review. Biotechnol Rep (Amst) 2021; 29: e00574. doi: 10.1016/j.btre.2020. e00574.
  8. Chen C, Xin Y, Li X, et al. Effects of Acremonium cellulase and heat-resistant lactic acid bacteria on lignocellulose degradation, fermentation quality, and microbial community structure of hybrid elephant grass silage in humid and hot areas. Front Microbiol 2022; 13: 1066753. doi: 10.3389/fmicb.2022. 1066753.
  9. Tedesco DEA, Conti C, Lovarelli D, et al. Bioconversion of fruit and vegetable waste into earthworms as a new protein source: the environmental impact of earthworm meal production. Sci Total Environ 2019; 683: 690-698.
  10. De Bellis P, Maggiolino A, Albano C, et al. Ensiling grape pomace with and without addition of a Lactiplanti-bacillus plantarum strain: effect on polyphenols and microbiological characteristics, in vitro nutrient apparent digestibility, and gas emission. Front Vet Sci 2022; 9: 808293. doi: 10.3389/fvets.2022.808293.
  11. Dawood MA, Habotta OA, Elsabagh M, et al. Fruit processing by‐products in the aquafeed industry: a feasible strategy for aquaculture sustainability. Rev Aquac 2022; 14(8): 1-21.
  12. Kolla MC, Laya A, Bayang JP, et al. Effect of different drying methods and storage conditions on physical, nutritional, bioactive compounds and antioxidant properties of doum (Hyphaene thebaica) fruits. Heliyon 2021; 7(4): e06678. doi: 10.1016/j.heliyon. 2021.e06678.
  13. Motamedi H, Azizi A, Ahmadi M. Nutritive value of treated Quercus infectoria and Quercus libani leaves with the tannin‐degrading bacterium Klebsiella pneumoniae for ruminant feeding in vitro. J Appl Microbiol 2019; 127(5): 1339-1348.
  14. Mudhita IK, Putra RA, Rahman MM, et al. The silage quality of Pennisetum purpureum cultivar gamma umami mixed with Calliandra calothyrsus and Lactiplantibacillus plantarum. Trop J Anim Sci 2024; 47(1): 112-124.
  15. Besharati M, Palangı V, Nekoo M, et al. Effects of Lactobacillus buchneri inoculation and fresh whey addition on alfalfa silage quality and fermentation properties. KSÜ Tarım ve Doğa Dergisi 2021: 24(3): 671-678.
  16. Gheibipour M, Ghiasi SE, Bashtani M, et al. The potential of tannin degrading bacteria isolated from rumen of Iranian Urial ram as silage additives. Bioresour Technol Rep 2022; 18(8): 101024. doi:10.1016/j.biteb.2022.101024.
  17. Gheibipour M, Ghiasi SE, Bashtani M, et al. Tannase-producing bacteria isolated from the rumen of Fallow deer (Dama dama): livestock potential feed additives. J Microb Biol 2023; 12(48): 27-40.
  18. Gheibipour M, Ghiasi SE, Bashtani M, et al. Screening the rumen of Balochi camel (Camelus dromedarius) and Cashmere goat (Capra hircus) to isolate enzyme-producing bacteria as potential additives for animal feed. Indian J Microbiol 2024; 64(2): 572-582.
  19. Gheibipour M, Ghiasi SE, Bashtani M, et al. The effect of probiotic tannase bacterial additive on diarrhea score in weaning lambs fed with pomegranate peel. In Proceedings: The First International and The Sixth National Conference on Biodiversity and Its Impact on Agriculture and Environment. Urmia, Iran 2024; 238-251.
  20. Official Methods of Analysis of AOAC International, 16th ed. AOAC International: Washington DC, USA, 2005.
  21. Van Soest PJ, Robertson JB, Lewis BA. Methods for dietary fiber, neutral detergent fiber, and non-starch polysaccharides in relation to animal nutrition. J Dairy Sci 1991; 74(10): 3583-3597.
  22. Gheibipour M, Ghiasi SE, Bashtani M, et al. The effect of tannase-producing supplementation with probiotic potential on ruminal fermentation of diets containing pomegranate peel in vitro. In Proceedings: The First International and The Sixth National Conference on Biodiversity and Its Impact on Agriculture and Environment. Urmia, Iran 2024; 224-238.
  23. Kumar S, Stecher G, Li M, et al. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 2018; 35(6): 1547-1549.
  24. Ghiasi SE, Gheibipour M, Motamedi H, et al. Screening and evaluation of the ruminal cellulolytic bacteria and their potential application as probiotics. Iran J Microbiol 2024; 16(3): 389-400.
  25. Sahu AR, Singh B, Mal G, et al. Isolation, identification and molecular characterization of tannase producing Klebsiella, from the rumen of migratory goats and sheep. Asian J Anim Vet Adv 2015; 10(8): 422-432.
  26. Sawabe Y, Yamano H, Koike S, et al. Isolation and characterization of tannin‐degrading bacteria from the rumen of wild Hokkaido sika deer (Cervus nipponyezoensis). Anim Sci J 2024; 95(1): e13918. doi: 10.1111/asj.13918.
  27. Gheibipour M. Isolation of tannin-degrading bacteria from the gastrointestinal tract of deer and using for improving the nutritional value of tannin rich feeds. M.Sc. thesis, Khuzestan Ramin Agriculture and Natural Resource University, Molasani, Iran: 2017.
  28. Tahmourespour A, Tabatabaee N, Khalkhali H, et al. Study of tannin-degrading bacteria isolated from pistachio soft hulls and feces of goat feeding on it. J Microbiol Biol, 2017; 5(2): 61-69.
  29. Mosleh H, Naghiha A, Naghi Keshtkaran A, et al. Isolation and identification of tannin-degrading bacteria from native sheep and goat feces in Kohgiloye and Boyer-Ahmad province. Int J Adv Biol Biomed Res 2014; 2(1):, 176-180.
  30. Kumar K, Chaudhary LC, Agarwal N, et al. Isolation and characterization of tannin-degrading bacteria from the rumen of goats fed oak (Quercus semicarpifolia) leaves. Agric Res 2014; 3(4): 377-385.
  31. Asadi N, Karimi Alavijeh M, Zilouei H. Biological hydrogen production by Enterobacter aerogenes: structural analysis of treated rice straw and effect of substrate concentration. Int J Hydrogen Energy 2018; 43: 8718-8728.
  32. Miyamoto-Shinohara Y, Sukenobe J, Imaizumi T, et al. Survival of freeze-dried bacteria. J Gen Appl Microbiol 2008; 54(1): 9-24.
  33. Madigan MT, Martinko JM. Brock Biology of micro-organisms. 11th New Jersey, USA: Pearson Prentice Hall 2005; 149-152.
  34. Massaro Junior FL, Bumbieris Junior VH, Zanin E, et al. Effect of storage time and use of additives on the quality of grape pomace silages. J Food Process Preserv 2020; 44(2): e14373. doi:10.1111/jfpp.14373.
  35. Asadnejad B, Pirmohammadi R, Khalilvandi- Behroozyar H. The effect of microwave irradiation at different times on in vitro nutritional value components of red grape pomace [Persian]. J Anim Sci Research (Agric Sci) 2020; 29(4): 35-54.
  36. Fitri A, Obitsu T, Sugino T. Effect of ensiling persimmon peel and grape pomace as tannin‐rich byproduct feeds on their chemical composition and in vitro rumen fermentation. Anim Sci J 2021; 92(1): e13524. doi: 10.1111/asj.13524.
  37. Galla NA, Nampija Z, Lutwama V, et al. Effects of inclusion levels of sweet potato vine silage on feed intake, milk production and profitability of lactating crossbred dairy cows. Open J Anim Sci 2020; 10: 608-617.
  38. Nutrient requirements of dairy cattle. 6th ed. Washington DC, USA: National Research Council, National Academy of Sciences. 1989.
  39. Mangwe MC, Rangubhet KT, Mlambo V, et al. Effects of Lactobacillus formosensis S215T and Lactobacillus buchneri on quality and in vitro ruminal biological activity of condensed tannins in sweet potato vines silage. J Appl Microbiol 2016; 121(5): 1242-1253.
  40. Kaewpila C, Khota W, Gunun P, et al. Characterization of green manure sunn hemp crop silage prepared with additives: aerobic instability, nitrogen value, and in vitro rumen methane production. Fermentation 2022; 8(3): 104. doi: 10.3390/fermentation8030104.
  41. Singh D, Tyagi N, Yadav S, et al. Growth performance, nitrogen balance and blood biochemical parameters on feeding TMR diet containing sugarcane tops silage supplemented with lactic acid bacteria inoculants and exogenous fibrolytic enzymes in crossbred calves. Indian J Anim Res 2022; 56: 1119-1125.
  42. Hatami A, Alipour D, Tabatabaei M, et al. Effect of ensiling pomegranate peels on chemical composition, in vitro gas production kinetics and microbial biomass production [Persian]. Anim Prod Res 2015; 4(1): 79-93.
  43. Khota W, Panyakaew P, Kesorn P, et al. In vitro rumen fermentation of coconut, sugar palm, and durian peel silages, prepared with selected additives. Fermentation 2023; 9(6): 567. doi: 10.3390/fermentation9060567.
  44. Yanti Y, Hadi RF, Riyanto J, et al. Fermentation quality of ratoon rice fermented with fermented juice of epiphytic lactic acid bacteria from tropical grass. In Proceedings: The 4th International Conference on Agriculture and Bio-industry. Banda Aceh, Indonesia 2022; 1-4.
  45. Yu S, Zhao Y, Li L, et al. Flavonoids from citrus peel display potential synergistic effects on inhibiting rumen methanogenesis and ammoniagenesis: a microbiome perspective. Environ Sci Pollut Res Int 2024; 31(14): 21208-21223.
  46. Matra M, Totakul P, Wanapat M. Utilization of dragon fruit waste by-products and non-protein nitrogen source: effects on in vitro rumen fermentation, nutrients degradability and methane production. Livest Sci 2021; 243: 104386. doi:10.1016/j.livsci. 2020.104386.
  47. Pazla R, Jamarun N, Arief A, et al. In vitro evaluation of feed quality of fermented Tithonia diversifolia with Lactobacillus bulgaricus and Persea americana miller leaves as forages for goat. Trop Anim Sci J 2023; 46(1): 43-54.
Volume 16, Issue 8
August 2025
Pages 455-464

  • Receive Date 17 August 2024
  • Revise Date 02 February 2025
  • Accept Date 08 February 2025