Animal Bioscience

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
권호 표지
DOI QR코드

DOI QR Code

Rumen fermentation and microbial diversity of sheep fed a high-concentrate diet supplemented with hydroethanolic extract of walnut green husks

  • Huan Wei (Laboratory of Nutrition for Meat & Dairy Herbivore, College of Animal Science, Xinjiang Agricultural University) ;
  • Jiancheng Liu (Laboratory of Nutrition for Meat & Dairy Herbivore, College of Animal Science, Xinjiang Agricultural University) ;
  • Mengjian Liu (Laboratory of Nutrition for Meat & Dairy Herbivore, College of Animal Science, Xinjiang Agricultural University) ;
  • Huiling Zhang (Laboratory of Nutrition for Meat & Dairy Herbivore, College of Animal Science, Xinjiang Agricultural University) ;
  • Yong Chen (Laboratory of Nutrition for Meat & Dairy Herbivore, College of Animal Science, Xinjiang Agricultural University)
  • Received : 2023.06.10
  • Accepted : 2023.10.20
  • Published : 2024.04.01
Download PDF
⟨ Previous Next ⟩

Abstract

Objective: This study aimed to assess the impact of a hydroethanolic extract of walnut green husks (WGH) on rumen fermentation and the diversity of bacteria, methanogenic archaea, and fungi in sheep fed a high-concentrate diet. Methods: Five healthy small-tailed Han ewes with permanent rumen fistula were selected and housed in individual pens. This study adopted a self-controlled and crossover design with a control period and an experimental period. During the control period, the animals were fed a basal diet (with a ratio of concentrate to roughage of 65:35), while during the treatment period, the animals were fed the basal diet supplemented with 0.5% hydroethanolic extract of WGH. Fermentation parameters, digestive enzyme activities, and microbial diversity in rumen fluid were analyzed. Results: Supplementation of hydroethanolic extract of WGH had no significant effect on feed intake, concentrations of total volatile fatty acids, isovalerate, ammonia nitrogen, and microbial protein (p>0.05). However, the ruminal pH, concentrations of acetate, butyrate and isobutyrate, the ratio of acetate to propionate, protozoa count, and the activities of filter paper cellulase and cellobiase were significantly increased (p<0.05), while concentrations of propionate and valerate were significantly decreased (p<0.05). Moreover, 16S rRNA gene sequencing revealed that the relative abundance of rumen bacteria Christensenellaceae R7 group, Saccharofermentans, and Ruminococcaceae NK4A214 group were significantly increased, while Ruminococcus gauvreauii group, Prevotella 7 were significantly decreased (p<0.05). The relative abundance of the fungus Pseudomonas significantly increased, while Basidiomycota, Fusarium, and Alternaria significantly decreased (p<0.05). However, there was no significant change in the community structure of methanogenic archaea. Conclusion: Supplementation of hydroethanolic extract of WGH to a high-concentrate diet improved the ruminal fermentation, altered the structure of ruminal bacterial and fungal communities, and exhibited beneficial effects in alleviating subacute rumen acidosis of sheep.

Keywords

Acknowledgement

This research was supported by the Open Project of Key Laboratory of Xinjiang (2020D04005) and the Special Project of the Central Government Guidance on Local Science and Technology Development (ZYYD2023B09).

References

  1. Jaramillo-Lopez E, Itza-Ortiz MF, Peraz a-Mercado G, Carrera-Chavez JM. Ruminal acidosis: strategies for its control. Austral J Vet Sci 2017;49:139-48. https://doi.org/10.4067/S0719-81322017000300139
  2. Ahmed MG, Al-Sagheer AA, El-Zarkouny SZ, Elwakeel EA. Potential of selected plant extracts to control severe subacute ruminal acidosis in vitro as compared with monensin. BMC Vet Res 2022;18:356. https://doi.org/10.1186/s12917-022-03457-4
  3. Vieira V, Pereira C, Abreu RMV, et al. Hydroethanolic extract of Juglans regia L. green husks: A source of bioactive phytochemicals. Food Chem Toxicol 2020;137:111189. https://doi.org/10.1016/j.fct.2020.111189
  4. Fernandez-Agullo A, Pereira E, Freire MS, et al. Influence of solvent on the antioxidant and antimicrobial properties of walnut (Juglans regia L.) green husk extracts. Ind Crops Prod 2013;42:126-132. https://doi.org/10.1016/j.indcrop.2012.05.021
  5. Chen W, Chen BL, Yang DL, Zhang X, Chen Y. Effects of walnut green husk extract on ruminal fermentation of sheep with subacute ruminal acidosis. Chin J Anim Nutr 2022;34: 3824-34. https://doi.org/10.3969/j.issn.1006-267x.2022.06.042
  6. Makkar HP, Blummel M, Borowy NK, Becker K. Gravimetric determination of tannins and their correlations with chemical and protein precipitation methods. J Sci Food Agric 1993;61:161-5. https://doi.org/10.1002/jsfa.2740610205
  7. Zarina Z, Tan SY. Determination of flavonoids in Citrus grandis (pomelo) peels and their inhibition activity on lipid peroxidation in fish tissue. Int Food Res J 2013;20:313-7.
  8. More GK, Makola RT. In-vitro analysis of free radical scavenging activities and suppression of LPS-induced ROS production in macrophage cells by Solanum sisymbriifolium extracts. Sci Rep 2020;10:6493. https://doi.org/10.1038/s41598-020-63491-w
  9. Mu LQ, Liu LP, Ma DI. Optimal ultrasonic extraction condition and determination of polysaccharides in Tilia amurensis flowers. J For Res 2010;21:77-80. https://doi.org/10.1007/s11676-010-0013-3
  10. AOAC International. Official methods of analysis, 18th Ed., Washington, DC, USA: Academy Press; 2005.
  11. van Soest PJ, Robertson JB, Lewis BA. Methods of dietary fibre, neutral detergent fibre and non-starch monosaccharides in relation to animal nutrition. J Dairy Sci 1991;74:3583-97. https://doi.org/10.3168/jds.S0022-0302(91)78551-2
  12. Chaney AL, Marbach EP. Modified reagents for determination of urea and ammonia. Clin Chem 1962;8:130-2. https://doi.org/10.1093/clinchem/8.2.130
  13. Wei H, Li XY, Yu QP, Chen Y. Effects of five plant phenolics on in vitro ruminal fermentation and methane production of a high concentrate-based substrate. Acta Prataculturae Sinica 2018;27:192-9. https://doi.org/10.11686/cyxb2018023
  14. Makkar HP, Sharma OP, Dawra RK, Negi SS. Simple determination of microbial protein in rumen liquor. J Dairy Sci 1982;65:2170-3. https://doi.org/10.3168/jds.S0022-0302(82)82477-6
  15. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976;72: 248-54. https://doi.org/10.1016/0003-2697(76)90527-3
  16. Dehority BA. Evaluation of subsampling and fixation procedures used for counting rumen protozoa. Appl Environ Microbiol 1984;48:182-5. https://doi.org/10.1128/aem.48.1.182-185.1984
  17. Yu C, Luo Q, Chen Y, Liu S, Zang C. Impact of docusate and fauna-free on feed intake, ruminal flora and digestive enzyme activities of sheep. J Anim Physiol Anim Nutr 2020;104:1043-51. https://doi.org/10.1111/jpn.13382
  18. Sharma R, Jacob John S, Damgaard DM, McAllister TA. Extraction of PCR-quality plant and microbial DNA from total rumen contents. Biotechniques 2003;34:92-7. https://doi.org/10.2144/03341st06
  19. Bashir Y, Rather IA, Konwar BK. Rapid and simple DNA extraction protocol from goat rumen digesta for metagenomic analysis. Pak J Pharm Sci 2015;28:2305-9.
  20. Kongmun P, Wanapat M, Pakdee P, Navanukraw C, Yu Z. Manipulation of rumen fermentation and ecology of swamp buffalo by coconut oil and garlic powder supplementation. Livest Sci 2011;135:84-92. https://doi.org/10.1016/j.livsci.2010.06.131
  21. Sucu E. Effects of microalgae species on in vitro rumen fermentation pattern and methane production. Ann Anim Sci 2020;20:207-18. https://doi.org/10.2478/aoas-2019-0061
  22. Broudiscou LP, Papon Y, Broudiscou AF. Effects of dry plant extracts on feed degradation and the production of rumen microbial biomass in a dual outflow fermenter. Anim Feed Sci Technol 2002;101:183-9. https://doi.org/10.1016/S0377-8401(02)00221-3
  23. Quast C, Pruesse E, Yilmaz P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucl Acids Res 2013;41:D590-6. https://doi.org/10.1093/nar/gks1219
  24. Bolyen E, Rideout JR, Dillon MR, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 2019;37:852-7. https://doi.org/10.1038/s41587-019-0209-9
  25. Koljalg U, Nilsson HR, Schigel D, et al. The taxon hypothesis paradigm-on the unambiguous detection and communication of taxa. Microorganisms 2020;8:1910. https://doi.org/10.3390/microorganisms8121910
  26. Segata N, Izard J, Waldron L, et al. Metagenomic biomarker discovery and explanation. Genome Biol 2011;12:R60. https://doi.org/10.1186/gb-2011-12-6-r60
  27. Arowolo MA, He J. Use of probiotics and botanical extracts to improve ruminant production in the tropics: a review. Anim Nutr 2018;4:241-9. https://doi.org/10.1016/j.aninu.2018.04.010
  28. Wanapat M, Viennasay B, Matra M, et al. Supplementation of fruit peel pellet containing phytonutrients to manipulate rumen pH, fermentation efficiency, nutrient digestibility and microbial protein synthesis. J Sci Food Agric 2021;101:4543-50. https://doi.org/10.1002/jsfa.11096
  29. Barekat S, Nasirpour A, Keramat J, et al. Phytochemical composition, antimicrobial, anticancer properties, and antioxidant potential of green husk from several walnut varieties (Juglans regia L.). Antioxidants 2023;12:52. https://doi.org/10.3390/antiox12010052
  30. Oskoueian E, Abdullah N, Oskoueian A. Effects of flavonoids on rumen fermentation activity, methane production, and microbial population. BioMed Res Int 2013;2013:349129. https://doi.org/10.1155/2013/349129
  31. Lowry J, Kennedy P. Fermentation of flavonols by rumen organisms. Proc Aust Soc Anim Prod I996;21:366.
  32. McSweeney CS, Mackie RI. Gastrointestinal detoxification and digestive disorders in ruminant animals. In: Mackie RI, White BA, editors. Gastrointestinal microbiology. Chapman & Hall Microbiology Series. Boston, MA, USA: Springer; 1997. pp. 583-634. https://doi.org/10.1007/978-1-4615-4111-0_15
  33. Jayanegara A, Goel G, Makkar HP, Becker K. Divergence between purified hydrolysable and condensed tannin effects on methane emission, rumen fermentation and microbial population in vitro. Anim Feed Sci Technol 2015;209:60-8. https://doi.org/10.1016/j.anifeedsci.2015.08.002
  34. Field JA, Kortekaas S, Lettinga G. The tannin theory of methanogenic toxicity. Biol Wastes 1989;29:241-62. https://doi.org/10.1016/0269-7483(89)90016-5
  35. Patra AK, Saxena J. Dietary phytochemicals as rumen modifiers: a review of the effects on microbial populations. Antonie van Leeuwenhoek 2009;96:363-75. https://doi.org/10.1007/s10482-009-9364-1
  36. Vyas D, Alemu AW, McGinn SM, Duval SM, Kindermann M, Beauchemin KA. The combined effects of supplementing monensin and 3-nitrooxypropanol on methane emissions, growth rate, and feed conversion efficiency in beef cattle fed high-forage and high-grain diets. J Anim Sci 2018;96:2923-38. https://doi.org/10.1093/jas/sky174
  37. Bamberger C, Rossmeier A, Lechner K, et al. A walnut-enriched diet affects gut microbiome in healthy caucasian subjects: A randomized, controlled trial. Nutrients 2018;10:244. https://doi.org/10.3390/nu10020244
  38. Byerley LO, Samuelson D, Blanchard E, et al. Changes in the gut microbial communities following addition of walnuts to the diet. J Nutr Biochem 2017;48:94-102. https://doi.org/10.1016/j.jnutbio.2017.07.001
  39. Fang Q, Li X, Wang M, et al. Walnut green husk ethanol extract improves gut microbiota and their metabolites associated with NLRP3 in non-alcoholic steatohepatitis. Food Funct 2022;13:6387-403. https://doi.org/10.1039/d2fo00012a
  40. Waters JL, Ley RE. The human gut bacteria Christensenellaceae are widespread, heritable, and associated with health. BMC Biol 2019;17:83. https://doi.org/10.1186/s12915-019-0699-4
  41. Ma Y, Deng X, Yang X, et al. Characteristics of bacterial microbiota in different intestinal segments of aohan finewool sheep. Front Microbiol 2022;13:874536. https://doi.org/10.3389/fmicb.2022.874536
  42. Chen S. Saccharofermentans. In: Trujillo ME, Dedysh S, DeVos P, et al, editors. Bergey's manual of systematics of archaea and bacteria. New York, USA: John Wiley & Sons, Inc.; 2017. p. 1-5. https://doi.org/10.1002/9781118960608.gbm01450
  43. Duda-Chodak A. The inhibitory effect of polyphenols on human gut microbiota. J Physiol Pharmacol 2012;63:497-503.
  44. Tett A, Pasolli E, Masetti G, Ercolini D, Segata N. Prevotella diversity, niches and interactions with the human host. Nat Rev Microbiol 2021;19:585-99. https://doi.org/10.1038/s41579-021-00559-y
  45. Zhao Y, Zhang Y, Khas E, Ao C, Bai C. Effects of Allium mongolicum Regel ethanol extract on three flavor-related rumen branched-chain fatty acids, rumen fermentation and rumen bacteria in lambs. Front Microbiol 2022;13:978057. https://doi.org/10.3389/fmicb.2022.978057
  46. Chiquette J, Allison MJ, Rasmussen M. Use of Prevotella bryantii 25A and a commercial probiotic during subacute acidosis challenge in midlactation dairy cows. J Dairy Sci 2012;95:5985-95. https://doi.org/10.3168/jds.2012-5511
  47. Nagaraja TG, Titgemeyer EC. Ruminal acidosis in beef cattle: the current microbiological and nutritional outlook. J Dairy Sci 2007;90 (Suppl 1):E17-38. https://doi.org/10.3168/jds.2006-478
  48. Song J, Jin YJ, Kim M. Diversity census of fungi in the ruminal microbiome: a meta-analysis. J Korea Acad Ind Coop Soc 2017;18:466-72. https://doi.org/10.5762/KAIS.2017.18.12.466
  49. Xing BS, Han Y, Wang XC, et al, Yuan H. Persistent action of cow rumen microorganisms in enhancing biodegradation of wheat straw by rumen fermentation. Sci Total Environ 2020;715:136529. https://doi.org/10.1016/j.scitotenv.2020.136529