Animal Bioscience

  • 제37권2호
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  • Pages.240-252
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  • 2024
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  • 2765-0189(pISSN)
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  • 2765-0235(eISSN)
아세아태평양축산학회 (Asian Australasian Association of Animal Production Societies)
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Nicotinic acid changes rumen fermentation and apparent nutrient digestibility by regulating rumen microbiota in Xiangzhong black cattle

  • Zhuqing Yang (College of Animal Science and Technology, Jiangxi Agricultural University) ;
  • Linbin Bao (Animal Husbandry and Veterinary Bureau of Guangchang County) ;
  • Wanming Song (College of Animal Science and Technology, Jiangxi Agricultural University) ;
  • Xianghui Zhao (Jiangxi Provincial Key Laboratory for Animal Nutrition/Engineering Research Center of Feed Development, Jiangxi Agricultural University) ;
  • Huan Liang (Jiangxi Provincial Key Laboratory for Animal Nutrition/Engineering Research Center of Feed Development, Jiangxi Agricultural University) ;
  • Mingjin Yu (College of Animal Science and Technology, Jiangxi Agricultural University) ;
  • Mingren Qu (Jiangxi Provincial Key Laboratory for Animal Nutrition/Engineering Research Center of Feed Development, Jiangxi Agricultural University)
  • 투고 : 2023.04.23
  • 심사 : 2023.09.06
  • 발행 : 2024.02.01
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초록

Objective: The aim of this study was to investigate the impact of dietary nicotinic acid (NA) on apparent nutrient digestibility, rumen fermentation, and rumen microbiota in uncastrated Xiangzhong black cattle. Methods: Twenty-one uncastrated Xiangzhong black cattle (385.08±15.20 kg) aged 1.5 years were randomly assigned to the control group (CL, 0 mg/kg NA in concentrate diet), NA1 group (800 mg/kg NA in concentrate diet) and NA2 group (1,200 mg/kg NA in concentrate diet). All animals were fed a 60% concentrate diet and 40% dried rice straw for a 120-day feeding experiment. Results: Supplemental NA not only enhanced the apparent nutrient digestibility of acid detergent fiber (p<0.01), but also elevated the rumen acetate and total volatile fatty acid concentrations (p<0.05). 16S rRNA gene sequencing analysis of rumen microbiota revealed that dietary NA changed the diversity of rumen microbiota (p<0.05) and the abundance of bacterial taxa in the rumen. The relative abundances of eight Erysipelotrichales taxa, five Ruminococcaceae taxa, and five Sphaerochaetales taxa were decreased by dietary NA (p<0.05). However, the relative abundances of two taxa belonging to Roseburia faecis were increased by supplemental 800 mg/kg NA, and the abundances of seven Prevotella taxa, three Paraprevotellaceae taxa, three Bifidobacteriaceae taxa, and two operational taxonomic units annotated to Fibrobacter succinogenes were increased by 1,200 mg/kg NA in diets. Furthermore, the correlation analysis found significant correlations between the concentrations of volatile fatty acids in the rumen and the abundances of bacterial taxa, especially Prevotella. Conclusion: The results from this study suggest that dietary NA plays an important role in regulating apparent digestibility of acid detergent fiber, acetate, total volatile fatty acid concentrations, and the composition of rumen microbiota.

키워드

과제정보

This project was financially supported by the Natural Science Foundation of China (32260921), the Jiangxi province natural science foundation of China (2020BAB205003), the Jiangxi province focuses on research and development plan (20171BBF60008), and the China Agriculture Research System of MOF and MARA (CARS-37).

참고문헌

  1. Flachowsky G. Niacin in dairy and beef cattle nutrition. Archiv fur Tierernahrung 1993;43:195-213. https://doi.org/10.1080/17450399309386036 
  2. Chilliard Y. Dietary fat and adipose tissue metabolism in ruminants, pigs, and rodents: a review. J Dairy Sci 1993;76:3897-931. https://doi.org/10.3168/jds.S0022-0302(93)77730-9 
  3. Kristensen NB, Harmon DL. Splanchnic metabolism of volatile fatty acids absorbed from the washed reticulorumen of steers. J Anim Sci 2004;82:2033-42. https://doi.org/10.2527/2004.8272033x 
  4. Pescara JB, Pires JAA, Grummer RR. Antilipolytic and lipolytic effects of administering free or ruminally protected nicotinic acid to feed-restricted Holstein cows. J Dairy Sci 2010;93:5385-96. https://doi.org/10.3168/jds.2010-3402 
  5. Titgemeyer EC, Spivey KS, Mamedova LK, Bradford BJ. Effects of pharmacological amounts of nicotinic acid on lipolysis and feed intake in cattle. Int J Dairy Sci 2011;6:134-41. https://doi.org/10.3923/ijds.2011.134.141 
  6. Luo D, Gao YF, Lu YY, et al. Niacin supplementation improves growth performance and nutrient utilisation in Chinese Jinjiang cattle. Italian J Anim Sci 2019;18:57-62. https://doi.org/10.1080/1828051X.2018.1480426 
  7. Luo D, Gao Y, Lu Y, et al. Niacin alters the ruminal microbial composition of cattle under high-concentrate condition. Anim Nutr 2017;3:180-5. https://doi.org/10.1016/j.aninu.2017.04.005 
  8. Doreau M, Ottou JF. Influence of niacin supplementation on in vivo digestibility and ruminal digestion in dairy cows. J Dairy Sci 1996;79:2247-54. https://doi.org/10.3168/jds.S0022-0302(96)76601-8 
  9. Horner JL, Coppock CE, Moya JR, et al. Effects of niacin and whole cottonseed on ruminal fermentation, protein degradability, and nutrient digestibility. J Dairy Sci 1988;71:1239-47. https://doi.org/10.3168/jds.S0022-0302(88)79679-4 
  10. Erickson PS, Trusk AM, Murphy MR. Effects of niacin source on epinephrine stimulation of plasma nonesterified fatty acid and glucose concentrations, on diet digestibility and on rumen protozoal numbers in lactating dairy cows. J Nutr 1990;120:1648-53. https://doi.org/10.1093/jn/120.12.1648 
  11. Shah AM, Wang Z, Ma J, et al. Effects of uni and bilateral castration on growth performance and lipid metabolism in yellow cattle. Anim Biotechnol 2023;34:77-84. https://doi.org/10.1080/10495398.2021.1936540 
  12. Cotta MA. Interaction of ruminal bacteria in the production and utilization of maltooligosaccharides from starch. Appl Environ Microbiol 1992;58:48-54. https://doi.org/10.1128/aem.58.1.48-54.1992 
  13. Yang ZQ, Bao LB, Zhao XH, et al. Effects of nicotinic acid on growth performance, meat quality and serum biochemical parameters of uncastrated xiangzhong bulls. Chinese J Anim Nutr 2015;27:85-92. https://doi.org/10.3969/j.issn.1006-267x.2015.01.012 
  14. Parada AE, Needham DM, Fuhrman JA. Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ Microbiol 2016;18:1403-14. https://doi.org/10.1111/1462-2920.13023 
  15. Magoc T, Salzberg SL. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 2011;27:2957-63. https://doi.org/10.1093/bioinformatics/btr507 
  16. Edgar R. Taxonomy annotation and guide tree errors in 16S rRNA databases. PeerJ 2018;6:e5030. https://doi.org/10.7717/peerj.5030 
  17. Schloss PD. Reintroducing mothur: 10 years later. Appl Environ Microbiol 2020;86:e02343-19. https://doi.org/10.1128/AEM.02343-19 
  18. Werner JJ, Zhou D, Caporaso JG, Knight R, Angenent LT. Comparison of Illumina paired-end and single-direction sequencing for microbial 16S rRNA gene amplicon surveys. ISME J 2012;6:1273-6. https://doi.org/10.1038/ismej.2011.186 
  19. Douglas GM, Maffei VJ, Zaneveld JR, et al. PICRUSt2 for prediction of metagenome functions. Nat Biotechnol 2020;38:685-8. https://doi.org/10.1038/s41587-020-0548-6 
  20. Van Soest PJ, Robertson JB, Lewis BA. Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. J Dairy Sci 1991;74:3583-97. https://doi.org/10.3168/jds.S0022-0302(91)78551-2 
  21. Samanta AK, Kewalramani N, Kaur H. Effect of niacin supplementation on VFA production and microbial protein synthesis in cattle. Indian J Dairy Sci 2000;53:150-3. 
  22. Ghosh NR, Kewalramani N, Kaur H. Comparative efficacy of niacin vs nicotinamide on rumen fermentation in buffaloes fed straw hased diets. Buffalo J 2003;19:249-59. 
  23. Yang ZQ, Bao LB, Zhao XH, et al. Nicotinic acid supplementation in diet favored intramuscular fat deposition and lipid metabolism in finishing steers. Exp Biol Med (Maywood) 2016;241:1195-201. https://doi.org/10.1177/1535370216639395 
  24. Harmon BG, Becker DE, Jensen AH, Baker DH. Nicotinic acid--tryptophan relationship in the nutrition of the weanling pig. J Anim Sci 1969;28:848-52. https://doi.org/10.2527/jas1969.286848x 
  25. Aschemann M, Lebzien P, Huther L, Doll S, Sudekum KH, Danicke S. Effect of niacin supplementation on digestibility, nitrogen utilisation and milk and blood variables in lactating dairy cows fed a diet with a negative rumen nitrogen balance. Arch Anim Nutr 2012;66:200-14. https://doi.org/10.1080/1745039x.2012.676813 
  26. Uebanso T, Shimohata T, Mawatari K, Takahashi A. Functional roles of B-vitamins in the gut and gut microbiome. Mol Nutr Food Res 2020;64:2000426. https://doi.org/10.1002/mnfr.202000426 
  27. Zhong W, Li Q, Zhang W, Sun Q, Sun X, Zhou Z. Modulation of intestinal barrier and bacterial endotoxin production contributes to the beneficial effect of nicotinic acid on alcohol-induced endotoxemia and hepatic inflammation in rats. Biomolecules 2015;5:2643-58. https://doi.org/10.3390/biom5042643 
  28. Fangmann D, Theismann E, Turk K, et al. Targeted Microbiome intervention by microencapsulated delayed-release niacin beneficially affects insulin sensitivity in humans. Diabetes Care 2018;41:398-405. https://doi.org/10.2337/dc17-1967 
  29. Chen C, Fang S, Wei H, et al. Prevotella copri increases fat accumulation in pigs fed with formula diets. Microbiome 2021;9:175. https://doi.org/10.1186/s40168-021-01110-0 
  30. Huws SA, Kim EJ, Lee MRF, et al. As yet uncultured bacteria phylogenetically classified as Prevotella, Lachnospiraceae incertae sedis and unclassified Bacteroidales, Clostridiales and Ruminococcaceae may play a predominant role in ruminal biohydrogenation. Environ Microbiol 2011;13:1500-12. https://doi.org/10.1111/j.1462-2920.2011.02452.x 
  31. Kabel MA, Yeoman CJ, Han Y, et al. Biochemical characterization and relative expression levels of multiple carbohydrate esterases of the xylanolytic rumen bacterium Prevotella ruminicola 23 grown on an ester-enriched substrate. Appl Environ Microbiol 2011;77:5671-81. https://doi.org/10.1128/AEM.05321-11 
  32. Betancur-Murillo CL, Aguilar-Marin SB, Jovel J. Prevotella: A key player in ruminal metabolism. Microorganisms 2022;11:1. https://doi.org/10.3390/microorganisms11010001 
  33. Gardner RG, Wells JE, Russell JB, et al. The cellular location of Prevotella ruminicola beta-1,4-D-endoglucanase and its occurrence in other strains of ruminal bacteria. Appl Environ Microbiol 1995;61:3288-92. https://doi.org/10.1128/aem.61.9.3288-3292.1995 
  34. Krause DO, Denman SE, Mackie RI, et al. Opportunities to improve fiber degradation in the rumen: microbiology, ecology, and genomics. FEMS Microbiol Rev 2003;27:663-93. https://doi.org/10.1016/S0168-6445(03)00072-X 
  35. Jacobs DM, Gaudier E, van Duynhoven J, et al. Non-digestible food ingredients, colonic microbiota and the impact on gut health and immunity: a role for metabolomics. Curr Drug Metab 2009;10:41-54. https://doi.org/10.2174/138920009787048383 
  36. Milani C, Turroni F, Duranti S, et al. Genomics of the genus bifidobacterium reveals species-specific adaptation to the glycan-rich gut environment. Appl Environ Microbiol 2016;82:980-91. https://doi.org/10.1128/AEM.03500-15 
  37. Burnet MC, Dohnalkova AC, Neumann AP, et al. Evaluating models of cellulose degradation by fibrobacter succinogenes S85. PLoS One 2015;10:e0143809. https://doi.org/10.1371/journal.pone.0143809 
  38. Simunek J, Jr., Killer J, Sechovcova H, et al. Characterization of a xylanolytic bacterial strain C10 isolated from the rumen of a red deer (Cervus elaphus) closely related of the recently described species Actinomyces succiniciruminis, A. glycerinitolerans, and A. ruminicola. Folia Microbiol (Praha) 2018;63:391-9. https://doi.org/10.1007/s12223-017-0577-9 
  39. Paz HA, Hales KE, Wells JE, et al. Rumen bacterial community structure impacts feed efficiency in beef cattle. J Anim Sci 2018;96:1045-58. https://doi.org/10.1093/jas/skx081 
  40. Boutard M, Cerisy T, Nogue PY, et al. Functional diversity of carbohydrate-active enzymes enabling a bacterium to ferment plant biomass. PLoS Genet 2014;10:e1004773. https://doi.org/10.1371/journal.pgen.1004773 
  41. Aurilia V, Martin JC, McCrae SI, Scott KP, Rincon MT, Flint HJ. Three multidomain esterases from the cellulolytic rumen anaerobe Ruminococcus flavefaciens 17 that carry divergent dockerin sequences. Microbiology 2000;146(Pt 6):1391-7. https://doi.org/10.1099/00221287-146-6-1391 
  42. Giraud I, Besle J, Fonty G. Hydrolysis and degradation of esterified phenolic acids from the maize cell wall by rumen microbial species. Reprod Nutr Dev 1997;37(Suppl 1):52-3. https://doi.org/10.1051/rnd:19970733 
  43. Xie J, Li LF, Dai TY, et al. Short-chain fatty acids produced by ruminococcaceae mediate alpha-linolenic acid promote intestinal stem cells proliferation. Mol Nutr Food Res 2022;66:e2100408. https://doi.org/10.1002/mnfr.202100408 
  44. Ritalahti KM, Justicia-Leon SD, Cusick KD, et al. Sphaerochaeta globosa gen. nov., sp. nov. and Sphaerochaeta pleomorpha sp. nov., free-living, spherical spirochaetes. Int J Syst Evol Microbiol 2012;62:210-6. https://doi.org/10.1099/ijs.0.023986-0 
  45. Kaakoush NO. Insights into the role of erysipelotrichaceae in the human host. Front Cell Infection Microbiol 2015;5:84. https://doi.org/10.3389/fcimb.2015.00084 
  46. Fleissner CK, Huebel N, Abd El-Bary MM, Loh G, Klaus S, Blaut M. Absence of intestinal microbiota does not protect mice from diet-induced obesity. Br J Nutr 2010;104:919-29. https://doi.org/10.1017/S0007114510001303 
  47. Spencer MD, Hamp TJ, Reid RW, Fischer LM, Zeisel SH, Fodor AA. Association between composition of the human gastrointestinal microbiome and development of fatty liver with choline deficiency. Gastroenterology 2011;140:976-86. https://doi.org/10.1053/j.gastro.2010.11.049 
  48. Turnbaugh PJ, Backhed F, Fulton L, Gordon JI. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 2008;3:213-23. https://doi.org/10.1016/j.chom.2008.02.015 
  49. Martinez I, Wallace G, Zhang C, et al. Diet-induced metabolic improvements in a hamster model of hypercholesterolemia are strongly linked to alterations of the gut microbiota. Appl Environ Microbiol 2009;75:4175-84. https://doi.org/10.1128/AEM.00380-09