Abstract

The gastrointestinal microbiome of ruminants is a complex ecological system. It ferments feed components and protects the body from opportunistic and pathogenic microflora. The interaction between the microbiota and the host organism depends on the diet, which complicates the scientific understanding of their impact on digestive processes, immunity, and yield. The article describes the composition and functional profile of microbiome in the rumen of young Edilbay rams fed with organic additives based on essential microelements. The samples were obtained from seven-month-old Edilbay rams, which received Ioddar-Zn and DAFS-25 feed additives. The study involved four groups of animals: control (no additives), experimental group I (Yoddar-Zn), experimental group II (DAFS-25), and experimental group III (Yoddar-Zn + DAFS-25). The composition and functional profile of the microbiome were studied using the NGS sequencing. The bioinformatics data analysis involved Qiime2 ver. 2020.8 and standard statistical methods. The feed additives had a positive effect on the growth and development of the rams. The highest live weight indicators belonged to experimental group III, which received Yoddar-Zn and DAFS-25. The ratio of Firmicutes and Bacteroidetes phylum changed, indicating a potential shift in metabolic processes towards an increase in the ratio of volatile fatty acids (acetate / propionate). The greatest changes were observed in animals that consumed the selenium additive DAFS-25, both separately and with Ioddar-Zn. The additives did not increase the count of Proteobacteria, Mycoplasma, and Escherichia-Shigella, which are associated with inflammatory processes. The feed additives affected the functional profile of rumen microbiome in young rams: they improved the carbohydrate and energy metabolism, as well as the synthesis of vitamins and cofactors. In addition, the research revealed some patterns of microbiome modification, which indicated a positive effect of the additives on metabolic processes, resulting in a more efficient digestion of feed ingredients and, eventually, in increased meat yield.

Keywords

Rams, ruminants, diet, feed additives, essential trace elements, microbiome, NGS sequencing

REFERENCES

1. Henchion M, Hayes M, Mullen AM, Fenelon M, Tiwari B. Future protein supply and demand: strategies and factors influencing a sustainable equilibrium. Foods. 2017;6(7):53. https://doi.org/10.3390/foods6070053
2. Hunter MC, Smith RG, Schipanski ME, Atwood LW, Mortensen DA. Agriculture in 2050: recalibrating targets for sustainable intensification. Bioscience. 2017;67(4):386–391. https://doi.org/10.1093/biosci/bix010
3. Gorlov IF. Selenium in cattle feeds and dietary supplements. Moscow: Vestnik of the Russian Agricultural Science, 2005. 189 p. (In Russ.). https://elibrary.ru/QKWTOX
4. Bogolyubova NV, Korotky VP, Zenkin AS, Ryzhov VA, Buryakov NP. Digestion and metabolism indices of sheep when using activated charcoal supplement. OnLine Journal of Biological Sciences. 2017;17(2):121–127. https://doi.org/10.3844/ ojbsci.2017.121.127
5. Newbold CJ, Ramos-Morales E. Review: ruminal microbiome and microbial metabolome: effects of diet and ruminant host. Animal. 2020;14(1):s78–s86. https://doi.org/10.1017/S1751731119003252
6. Henderson G, Cox F, Ganesh S, Jonker A, Young W, Collaborators GRC, et al. Rumen microbial community composition varies with diet and host, but a core microbiome is found across a wide geographical range. Scientific Reports. 2015;5:14567. https://doi.org/10.1038/srep14567
7. Tapio I, Fischer D, Blasco L, Tapio M, Wallace RJ, Bayat AR, et al. Taxon abundance, diversity, co-occurrence and network analysis of the ruminal microbiota in response to dietary changes in dairy cows. PloS One. 2017;12(7):e0180260. https://doi.org/10.1371/journal.pone.0180260
8. Fomichev YuP, Bogolyubova NV, Romanov VN, Kolodina EN. Comparative assessment of natural feed additives for functional effects on the digestive processes in the rumen of sheep (Ovis Aries). Agricultural Biology. 2020;55(4):770–783. (In Russ.). https://doi.org/10.15389/agrobiology.2020.4.770rus; https://elibrary.ru/PVTONG
9. Kobayashi Y, Oh S, Myint H, Koike S. Use of Asian selected agricultural byproducts to modulate rumen microbes and fermentation. Journal of Animal Science and Biotechnology. 2016;7:70. https://doi.org/10.1186/s40104-016-0126-4
10. Hendawy AO, Shirai M, Takeya H, Sugimura S, Miyanari S, Taniguchi S, et al. Effects of 5-aminolevulinic acid supplementation on milk production, iron status, and immune response of dairy cows. Journal of Dairy Science. 2019;102(12): 11009–11015. https://doi.org/10.3168/jds.2018-15982
11. Nabi F, Arain MA, Hassan F, Umar M, Rajput N, Alagawany M, et al. Nutraceutical role of selenium nanoparticles in poultry nutrition: A review. World’s Poultry Science Journal. 2020;76(3):459–471. https://doi.org/10.1080/00439339. 2020.1789535
12. Hendawy AO, Sugimura S, Sato K, Mansour MM, Abd El-Aziz AH, Samir H, et al. Effects of selenium supplementation on rumen microbiota, rumen fermentation, and apparent nutrient digestibility of ruminant animals: a review. Fermentation. 2022;8(1):4. https://doi.org/10.3390/fermentation8010004
13. Liu C, Li XH, Chen YX, Cheng ZH, Duan QH, Meng QH, et al. Age-related response of rumen microbiota to mineral salt and effects of their interactions on enteric methane emissions in cattle. Microbial Ecology. 2017;73:590–601. https://doi.org/10.1007/s00248-016-0888-4
14. Váradyová Z, Mravčáková D, Holodová M, Grešáková Ľ, Pisarčíková J, Barszcz M, et al. Modulation of ruminal and intestinal fermentation by medicinal plants and zinc from different sources. Journal of Animal Physiology and Animal Nutrition. 2018;102(5):1131–1145. https://doi.org/10.1111/jpn.12940
15. Vigh A, Criste A, Gragnic K, Moquet L, Gerard C. Ruminal solubility and bioavailability of inorganic trace mineral sources and effects on fermentation activity measured in vitro. Agriculture. 2023;13(4):879. https://doi.org/10.3390/agri- culture13040879
16. Cui X, Wang Z, Tan Y, Chang S, Zheng H, Wang H, et al. Selenium Yeast Dietary Supplement Affects Rumen Bacterial Population Dynamics and Fermentation Parameters of Tibetan Sheep (Ovis aries) in Alpine Meadow. Frontiers in Microbiology. 2021;12:663945. https://doi.org/10.3389/fmicb.2021.663945
17. Zhang ZD, Wang C, Du HS, Liu Q, Guo G, Huo WJ, et al. Effects of sodium selenite and coated sodium selenite on lactation performance, total tract nutrient digestion and rumen fermentation in Holstein dairy cows. Animal. 2020;14(10):2091–2099. https://doi.org/10.1017/S1751731120000804
18. Naderi M, Puar P, Zonouzi-Marand M, Chivers DP, Niyogi S, Kwong RWM. A comprehensive review on the neuropathophysiology of selenium. Science of The Total Environment. 2021;767:144329. https://doi.org/10.1016/j.scitotenv. 2020.144329
19. Ishaq SL, Johnson SP, Miller ZJ, Lehnhoff EA, Olivo S, Yeoman CJ, et al. Impact of cropping systems, soil inoculum, and plant species identity on soil bacterial community structure. Microbial Ecology. 2017;73:417–434. https:// doi.org/10.1007/s00248-016-0861-2
20. Koloskova EM, Ezerskiy VA, Ostrenko KS, Ovcharova AN, Belova NV. Studies of the sheep rumen microbiome using molecular genetic methods: a review. Problems of Productive Animal Biology. 2020;(4):5–26. (In Russ.). https://doi. org/10.25687/1996-6733.prodanimbiol.2020.4.5-26; https://elibrary.ru/VXFFAO
21. Grabez V, Coll-Brasas E, Fulladosa E, Hallenstvedt E, Håseth TT, Øverland M, et al. Seaweed inclusion in finishing lamb diet promotes changes in micronutrient content and flavour-related compounds of raw meat and dry-cured leg (Fenalår). Foods. 2022;11(7):1043. https://doi.org/10.3390/foods11071043
22. Paulíková I, Kovác G, Bíris J, Paulík S, Seidel H, Nagy O. Iodine toxicity in ruminants. Veterinární medicína. 2002;47(12):343–350. https://doi.org/10.17221/5845-VETMED
23. Huszenicza GY, Kulcsar M, Rudas P. Clinical endocrinology of thyroid gland function in ruminants. Veterinární medicína. 2002;47(7):199–210. https://doi.org/10.17221/5824-VETMED
24. Makkar HPS, Tran G, Hauzé V, Giger-Reverdin S, Lessire M, Lebas F, et al. Seaweeds for livestock diets: A review. Animal Feed Science and Technology. 2016;212:1–17. https://doi.org/10.1016/j.anifeedsci.2015.09.018
25. Antaya NT, Ghelichkhan M, Pereira ABD, Soder KJ, Brito AF. Production, milk iodine, and nutrient utilization in Jersey cows supplemented with the brown seaweed Ascophyllum nodosum (kelp meal) during the grazing season. Journal of Dairy Science. 2019;102(9):8040–8058. https://doi.org/10.3168/jds.2019-16478
26. Silva LHP, Reis SF, Melo ATO, Jackson BP, Brito AF Supplementation of Ascophyllum nodosum meal and mo- nensin: Effects on diversity and relative abundance of ruminal bacterial taxa and the metabolism of iodine and arsenic in lactating dairy cows. Journal of Dairy Science. 2022;105(5):4083–4098. https://doi.org/10.3168/jds.2021-21107
27. MacDonald RS. The role of zinc in growth and cell proliferation. The Journal of Nutrition. 2000;130(5):1500S–1508S. https://doi.org/10.1093/jn/130.5.1500S
28. Engle TE. Effects Of Mineral Nutrition of Immune Function and Factors That Affect Trace Mineral Requirements of Beef Cattle. Wyoming: University of Nebraska; 2001. 87 p.
29. López-Alonso M. Trace minerals and livestock: not too much not too little. International Scholarly Research Notices. 2012;2012(1):704825. https://doi.org/10.5402/2012/704825
30. Spears JW. Trace mineral bioavailability in ruminants. The Journal of Nutrition. 2003;133(5):1506S–1509S. https:// doi.org/10.1093/jn/133.5.1506S
31. Cao J, Henry PR, Guo R, Holwerda RA, Toth JP, Littell RC, et al. Chemical characteristics and relative bioavailability of supplemental organic zinc sources for poultry and ruminants. Journal of Animal Science. 2000;78(8):2039–2054. https:// doi.org/10.2527/2000.7882039x
32. Gunter SA, Malcolm-Callis KJ, Duff GC, Kegley EB. Performance of steers supplemented with zinc during grazing and receiving at the feedlot. The Professional Animal Scientist. 2001;17(4):280–286. https://doi.org/10.15232/S1080- 7446(15)31641-7
33. Froetschel MA, Martin AC, Amos HE, Evans JJ. Effects of zinc sulfate concentration and feeding frequency on ruminal protozoal numbers, fermentation patterns and amino acid passage in steers. Journal of Animal Science. 1990;68(9):2874–2884. https://doi.org/10.2527/1990.6892874x
34. Krasnoslobodtseva AS, Shulaev GM. Efficiency of application of preparations “Iodis-Concentrate” in complex with “DAFS-25” in diets of heifers. Tambov University Reports. Series: Natural and Technical Sciences. 2009;14(1):125–127. (In Russ.). https://elibrary.ru/KXFWIV
35. Berestov DS, Merzlyakova EA, Troshin EI. Antioxidant effect of DAFS-25 on fattening bulls and preventing the effects of radiation exposure. Russian Journal of Veterinary Pathology. 2007;(1):188–192. (In Russ.). https://elibrary.ru/OFNABB
36. Hofstee P, McKeating DR, Bartho LA, Anderson ST, Perkins AV, Cuffe JSM. Maternal selenium deficiency in mice alters offspring glucose metabolism and thyroid status in a sexually dimorphic manner. Nutrients. 2020;12(1):267. https://doi.org/10.3390/nu12010267
37. Zhang F, Teng Z, Wang L, Wang L, Huang T, Zhang X. Dietary selenium deficiency and excess accelerate ubi- quitin-mediated protein degradation in the muscle of rainbow trout (Oncorhynchus mykiss) via Akt/FoxO3a and NF-κB signaling pathways. Biological Trace Element Research. 2021;200:1361–1375. https://doi.org/10.1007/s12011-021-02726-x
38. Xu J, Wang L, Tang J, Jia G, Liu G, Chen X, Cai J, et al. Pancreatic atrophy caused by dietary selenium deficiency induces hypoinsulinemic hyperglycemia via global down-regulation of selenoprotein encoding genes in broilers. PLoS ONE. 2017;12(8):e0182079. https://doi.org/10.1371/journal.pone.0182079
39. Arshad MA, Ebeid HM, Hassan FU. Revisiting the effects of different dietary sources of selenium on the health and performance of dairy animals: A review. Biological Trace Element Research. 2021;199:3319–3337. https://doi.org/10.1007/ s12011-020-02480-6
40. Hadrup N, Ravn-Haren G. Absorption, distribution, metabolism and excretion (ADME) of oral selenium from organic and inorganic sources: A review. Journal of Trace Elements in Medicine and Biology. 2021;67:126801. https://doi.org/ 10.1016/j.jtemb.2021.126801
41. Fakhrolmobasheri M, Nasr-Esfahany Z, Khanahmad H, Zeinalian M. Selenium supplementation can relieve the clinical complications of COVID-19 and other similar viral infections. International Journal for Vitamin and Nutrition Research. 2021;91(3-4):197–199. https://doi.org/10.1024/0300-9831/a000663
42. Jin Z, Du X, Xu Y, Deng Y, Liu M, Zhao Y, et al. Structure of Mpro from SARS-CoV-2 and discovery of its inhibitors. Nature. 2020;582:289–293. https://doi.org/10.1038/s41586-020-2223-y
43. Lee MRF, Fleming HR, Cogan T, Hodgson C, Davies DR. Assessing the ability of silage lactic acid bacteria to incorporate and transform inorganic selenium within laboratory scale silos. Animal Feed Science and Technology. 2019;253:125–134. https://doi.org/10.1016/j.anifeedsci.2019.05.011
44. He L, Zhao J, Wang L, Liu Q, Fan Y, Li B, et al. Using nano-selenium to combat Coronavirus Disease 2019 (COVID-19)? Nano Today. 2021;36:101037. https://doi.org/10.1016/j.nantod.2020.101037
45. Arce-Cordero JA, Monteiro HF, Lelis AL, Lima LR, Restelatto R, Brandao VLN, et al. Copper sulfate and sodium selenite lipid-microencapsulation modifies ruminal microbial fermentation in a dual-flow continuous-culture system. Journal of Dairy Science. 2020;103(8):7068–7080. https://doi.org/10.3168/jds.2019-17913
46. Galbraith ML, Vorachek WR, Estill CT, Whanger PD, Bobe G, Davis TZ, et al. Rumen microorganisms decrease bioavailability of inorganic selenium supplements. Biological Trace Element Research. 2016;171:338–343. https://doi.org/ 10.1007/s12011-015-0560-8
47. Zhang R, Zhu W, Zhu W, Liu J, Mao S. Effect of dietary forage sources on rumen microbiota, rumen fermentation and biogenic amines in dairy cows. Journal of the Science of Food and Agriculture. 2014;94(9):1886–1895. https://doi.org/ 10.1002/jsfa.6508
48. Liu K, Zhang Y, Yu Z, Xu Q, Zheng N, Zhao S, et al. Ruminal microbiota–host interaction and its effect on nutrient metabolism. Animal Nutrition. 2021;7(1):49–55. https://doi.org/10.1016/j.aninu.2020.12.001
49. Söllinger A, Tveit AT, Poulsen M, Noel SJ, Bengtsson M, Bernhardt J, et al. Holistic assessment of rumen microbiome dynamics through quantitative metatranscriptomics reveals multifunctional redundancy during key steps of anaerobic feed degradation. Msystems. 2018;3(4):e00038-18. https://doi.org/10.1128/msystems.00038-18
50. Wu S, Cui Z, Chen X, Zheng L, Ren H, Wang D, et al. Diet-ruminal microbiome-host crosstalk contributes to differential effects of calf starter and alfalfa hay on rumen epithelial development and pancreatic α-amylase activity in yak calves. Journal of Dairy Science. 2021;104(4):4326–4340. https://doi.org/10.3168/jds.2020-18736
51. Ryan SM, Fitzgerald GF, van Sinderen D. Screening for and identification of Starch-, Amylopectin-, and Pullulan- Degrading activities in bifidobacterial strains. Applied and Environmental Microbiology. 2006;72(8):5289–5296. https:// doi.org/10.1128/AEM.00257-06
52. Pokusaeva K, Fitzgerald GF, van Sinderen D. Carbohydrate metabolism in Bifidobacteria. Genes Nutrition. 2011;6: 285–306. https://doi.org/10.1007/s12263-010-0206-6
53. Hernández R, De Mares MC, Jimenez H, Reyes A, Caro-Quintero A. Functional and phylogenetic characterization of bacteria in bovine rumen using fractionation of ruminal fluid. Frontiers in Microbiology. 2022;13:813002. https://doi.org/ 10.3389/fmicb.2022.813002
54. Zhang K. Research Gi Development and Rumen Microbiome From 0 to 56-day-ole at Cashmere Goat. 2017.
55. Sun L, Jia H, Li J, Yu M, Yang Y, Tian D, et al. Cecal gut microbiota and metabolites might contribute to the severity of acute myocardial ischemia by impacting the intestinal permeability, oxidative stress, and energy metabolism. Frontiers in Microbiology 2019;10:1745. https://doi.org/10.3389/fmicb.2019.01745
56. Zened A, Combes S, Cauquil L, Mariette J, Klopp C, Bouchez O, et al. Microbial ecology of the rumen evaluated by 454 GS FLX pyrosequencing is affected by starch and oil supplementation of diets. FEMS Microbiology Ecology. 2013; 83(2):504–514. https://doi.org/10.1111/1574-6941.12011
57. Qiu X, Qin X, Chen L, Chen Z, Hao R, Zhang S, et al. Serum biochemical parameters, rumen fermentation, and rumen bacterial communities are partly driven by the breed and sex of cattle when fed high-grain diet. Microorganisms. 2022; 10(2):323. https://doi.org/10.3390/microorganisms10020323
58. Liu YJ, Wang C, Liu Q, Guo G, Huo WJ, Zhang YL, et al. Effects of sodium selenite addition on ruminal fermentation, microflora and urinary excretion of purine derivatives in Holstein dairy bulls. Journal of Animal Physiology and Animal Nutrition. 2019;103(6):1719–1726. https://doi.org/10.1111/jpn.13193
59. Mao SY, Huo WJ, Zhu WY. Microbiome-metabolome analysis reveals unhealthy alterations in the composition and metabolism of ruminal microbiota with increasing dietary grain in a goat model. Environmental Microbiology. 2016;18(2):525–541. https://doi.org/10.1111/1462-2920.12724
60. Purushe J, Fouts DE, Morrison M, White BA, Mackie RI, Coutinho PM, et al. Comparative genome analysis of Prevotella ruminicola and Prevotella bryantii: insights into their environmental niche. Microbial Ecology. 2010;60:721–729. https://doi.org/10.1007/s00248-010-9692-8
61. Rubino F, Carberry C, Waters SM, Kenny D, Mccabe MS, Creevey CJ. Divergent functional isoforms drive niche specialisation for nutrient acquisition and use in rumen microbiome. International Society for Microbial Ecology Journal. 2017;11(4):932–944. https://doi.org/10.1038/ismej.2017.34
62. Deusch S, Camarinha-Silva A, Conrad J, Beifuss U, Rodehutscord M, Seifert J. A structural and functional elucidation of the rumen microbiome influenced by various diets and microenvironments. Frontiers in Microbiology. 2017;8:1605. https:// doi.org/10.3389/fmicb.2017.01605
63. He Z, Ma Y, Chen X, Liu S, Xiao J, Wang Y, et al. Protective effects of intestinal gallic acid in neonatal dairy calves against extended-spectrum β-lactamase producing enteroaggregative Escherichia coli infection: modulating intestinal homeostasis and colitis. Frontiers in Nutrition. 2022;9:864080. https://doi.org/10.3389/fnut.2022.864080
64. Goodrich JK, Waters JL, Poole AC, Sutter JL, Koren O, Blekhman R, et al. Human genetics shape the gut microbiome. Cell. 2014;159(4):789–799. https://doi.org/10.1016/j.cell.2014.09.053
65. Morotomi M, Nagai F, Watanabe Y. Description of Christensenella minuta gen. nov., sp. nov., isolated from human faeces, which forms a distinct branch in the order Clostridiales, and proposal of Christensenellaceae fam. nov. International Journal of Systematic and Evolutionary Microbiology. 2012;62(1):144–149. https://doi.org/10.1099/ijs.0.026989-0
66. David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505:559–563. https://doi.org/10.1038/nature12820
67. Manor O, Zubair N, Conomos MP, Xu X, Rohwer JE, Krafft CE, et al. A Multi-omic Association Study of Trimethylamine N-Oxide. Cell reports. 2018;24(4):935–946. https://doi.org/10.1016/j.celrep.2018.06.096
68. Huang C, Ge F, Yao X, Guo X, Bao P, et al. Microbiome and Metabolomics Reveal the Effects of Different Feeding Systems on the Growth and Ruminal Development of Yaks. Frontiers in Microbiology. 2021;12:682989. https://doi.org/10.3389/ fmicb.2021.682989
69. Kittelmann S, Seedorf H, Walters WA, Clemente JC, Knight R, Gordon JI, et al. Simultaneous amplicon sequencing to explore co-occurrence patterns of bacterial, archaeal and eukaryotic microorganisms in rumen microbial communities. PLoS One. 2013;8(2):e47879. https://doi.org/10.1371/journal.pone.0047879
70. Haas KN, Blanchard JL Kineothrix alysoides, gen. nov., sp. nov., a saccharolytic butyrate-producer within the family Lachnospiraceae. International Journal of Systematic and Evolutionary Microbiology. 2017;67(2):402–410. https:// doi.org/10.1099/ijsem.0.001643
71. Xu H, Collins JF, Bai L, Kiela PR, Lynch RM, Ghishan FK. Epidermal growth factor regulation of rat NHE2 gene expression. American Journal of Physiology-Cell Physiology. 2001;281(2):C504–C513. https://doi.org/10.1152/ajpcell. 2001.281.2.C504
72. Bekele AZ, Koike S, Kobayashi Y. Phylogenetic diversity and dietary association of rumen Treponema revealed using group-specific 16S rRNA gene-based analysis. FEMS Microbiology Letters. 2011;316(1):51–60. https://doi.org/10.1111/j.1574- 6968.2010.02191.x
73. Nyonyo T, Shinkai T, Mitsumori M. Improved culturability of cellulolytic rumen bacteria and phylogenetic diversity of culturable cellulolytic and xylanolytic bacteria newly isolated from the bovine rumen. FEMS Microbiology Ecology. 2014;88(3):528–537. https://doi.org/10.1111/1574-6941.12318
74. Zhao C, Li Y, Chen Q, Guo Y, Sun B, Liu D. Effect of organic acids on fermentation quality and microbiota of horseshoe residue and corn protein powder. AMB Express. 2024;14:58. https://doi.org/10.1186/s13568-024-01686-4
75. Ransom-Jones E, Jones DL, Mccarthy AJ, Mcdonald JE. The Fibrobacteres: an important phylum of cellulosedegrading bacteria. Microbiology Ecology. 2012;63:267–281. https://doi.org/10.1007/s00248-011-9998-1
76. Béra-Maillet C, Mosoni P, Kwasiborski A, Suau F, Ribot Y, Forano E. Development of a RT-qPCR method for the quantification of Fibrobacter succinogenes S85 glycoside hydrolase transcripts in the rumen content of gnotobiotic and conventional sheep. Journal of Microbiological Methods. 2009;77(1):8–16. https://doi.org/10.1016/j.mimet.2008.11.009
77. Karami A, Sarshar M, Ranjbar R, Zanjani RS. The Phylum Spirochaetaceae. In: Rosenberg E, editor. The Prokaryotes: Other Major Lineages of Bacteria and The Archaea. Germany: Springer Berlin Heidelberg. 2014. pp. 915–929.
78. Savin KW, PJ Moate, Williams SRO, Bath C, Hemsworth J, Wang J, et al. Dietary wheat and reduced methane yield are linked to rumen microbiome changes in dairy cows. PLoS One. 2022;17(5):e0268157. https://doi.org/10.1371/ journal.pone.0268157
79. Kamke J, Kittelmann S, Soni P, Li Y, Tavendale M, Ganesh S, et al. Rumen metagenome and metatranscriptome analyses of low methane yield sheep reveals a Sharpea-enriched microbiome characterised by lactic acid formation and utilisation. Microbiome. 2016;4:56. https://doi.org/10.1186/s40168-016-0201-2
80. Yi S, Dai D, Wu H, Chai S, Liu S, Meng Q, et al. Dietary Concentrate-to-Forage Ratio Affects Rumen Bacterial Community Composition and Metabolome of Yaks. Frontiers in Nutrition. 2022;9:927206. https://doi.org/10.3389/fnut.2022.927206
81. Wang C, Xu Y, Han L, Liu Q, Guo G, Huo W, et al. Effects of zinc sulfate and coated zinc sulfate on lactation performance, nutrient digestion and rumen fermentation in Holstein dairy cows. Livestock Science. 2021;251:104673. https:// doi.org/10.1016/j.livsci.2021.104673
82. Ishaq SL, Page CM, Yeoman CJ, Murphy TW, Van Emon ML, Stewart WC. Zinc AA supplementation alters yearling ram rumen bacterial communities but zinc sulfate supplementation does not. Journal of Animal Science. 2019;97(2):687–697. https://doi.org/10.1093/jas/sky456
83. Du HS, Wang C, Wu ZZ, Zhang GW, Liu Q, Guo G, et al. Effects of rumen-protected folic acid and rumen-protected sodium selenite supplementation on lactation performance, nutrient digestion, ruminal fermentation and blood metabolites in dairy cows. Journal of the Science of Food and Agriculture. 2019;99(13):5826–5833. https://doi.org/10.1002/jsfa.9853
84. Liu H, Xu T, Xu S, Ma L, Han X, Wang X, et al. Effect of dietary concentrate to forage ratio on growth performance, rumen fermentation and bacterial diversity of Tibetan sheep under barn feeding on the Qinghai-Tibetan plateau. Peer Journal. 2019;7:e7462. https://doi.org/10.7717/peerj.7462
85. Miltko R, Rozbicka-Wieczorek JA, Wiesyk E, Czauderna M. The influence of different chemical forms of selenium added to the diet including carnosic acid, fish oil and rapeseed oil on the formation of volatile fatty acids and methane in the rumen, and fatty acid profiles in the rumen content and muscles of lambs. Acta Veterinaria. 2016;66(3):373–391. https:// doi.org/10.1515/acve-2016-0032
86. Shahid A, Moolchand M, Soomro SA, Giasuddin SM, Kalhoro NH, Kaka A, et al. Influence of dietary selenium yeast supplementation on fermentation pattern, papillae morphology and antioxidant status in rumen of goat. Pakistan Journal of Zoology. 2020;52(2):565–571. https://doi.org/10.17582/journal.pjz/20190205120240
87. Liu YJ, Zhang ZD, Dai SH, Wang Y, Tian XF, Zhao JH, et al. Effects of sodium selenite and coated sodium selenite addition on performance, ruminal fermentation, nutrient digestibility and hepatic gene expression related to lipid metabolism in dairy bulls. Livestock Science. 2020;237:104062. https://doi.org/10.1016/j.livsci.2020.104062
88. Samo SP, Malhi M, Gadahi J, Lei Y, Kaciwal AB, Soomro SA. Effect of organic selenium supplementation in diet on gastrointestinal tract performance and meat quality of goat. Pakistan Journal of Zoology. 2018;50(3):995–1001. https:// doi.org/10.17582/journal.pjz/2018.50.3.995.1003
89. Ye X, Zhou L, Zhang Y, Xue S, Gan QF, Fang S. Effect of host breeds on gut microbiome and serum metabolome in meat rabbits. BMC Veterinary Research. 2021;17:24. https://doi.org/10.1186/s12917-020-02732-6
90. Wu I-W, Lee C-C, Hsu H-J, Sun C-Y, Chen Y-C, Yang K-J, et al. Compositional and functional adaptations of intestinal microbiota and related metabolites in CKD patients receiving dietary protein restriction. Nutrients. 2020;12(9):2799. https://doi.org/10.3390/nu12092799
91. Zhu W, Yan J, Zhi C, Zhou Q, Yuan X. 1,25(OH)2D3 deficiency-induced gut microbial dysbiosis degrades the colonic mucus barrier in Cyp27b1 knockout mouse model. Gut Pathogens. 2019;11:8. https://doi.org/10.1186/s13099-019-0291-z
92. Ricci S, Pacífico C, Castillo-Lopez E, Rivera-Chacon R, Schwartz-Zimmermann HE, Reisinger N, et al. Progressive microbial adaptation of the bovine rumen and hindgut in response to a step-wise increase in dietary starch and the influence of phytogenic supplementation. Frontiers in Microbiology. 2022;13:920427. https://doi.org/10.3389/fmicb.2022.920427
93. Pacífico C, Petri RM, Ricci S, Mickdam E, Wetzels SU, Neubauer V, et al. Unveiling the Bovine Epimural Microbiota Composition and Putative Function. Microorganisms. 2021;9(2):342. https://doi.org/10.3390/microorganisms9020342
94. Hackmann TJ, Firkins JL. Maximizing efficiency of rumen microbial protein production. Frontiers in Microbiology. 2015;6:465. https://doi.org/10.3389/fmicb.2015.00465
95. Tsuchiya Y, Chiba E, Kimura A, Kawashima K, Hasunuma T, Kushibiki S, et al. Predicted functional analysis of rumen microbiota suggested the underlying mechanisms of the postpartum subacute ruminal acidosis in Holstein cows. Journal of Veterinary Science. 2023;24(2):e27. https://doi.org/10.4142/jvs.22246
96. Weiss B. Effect of supplemental biotin on performance of lactating dairy cows. Proceedings DIGAL Conference. Chihuahua Mexico: Delicias; 2001. 7–17.
97. Streit WR, Entcheva P. Biotin in microbes, the genes involved in its biosynthesis, its biochemical role and perspectives for biotechnological production. Applied Microbiology and Biotechnology. 2003;61:21–31. https://doi.org/10.1007/s00253- 002-1186-2
98. Hayashi A, Mikami Y, Miyamoto K, Kamada N, Sato T, Mizuno S, et al. Intestinal dysbiosis and biotin deprivation induce alopecia through overgrowth of Lactobacillus murinus in mice. Cell Reports. 2017;20:1513–1524. https://doi.org/ 10.1016/j.celrep.2017.07.057
99. Colagiorgi A, Turroni F, Mancabelli L, Serafini F, Secchi A, van Sinderen D, et al. Insights into teichoic acid biosynthesis by Bifidobacterium bifidum PRL2010. FEMS Microbiology Letters. 2015;362(17):fnv141. https://doi.org/10.1093/ femsle/fnv141
100. Garcia M, Bradford BJ, Nagaraja TG. Invited review: ruminal microbes, microbial products, and systemic inflammation. The Professional Animal Scientists. 2017;33(6):635–650. https://doi.org/10.15232/pas.2017-01663
101. Lu X, Ce Q, Jin L, Zheng, J, Sun M, Tang X, et al. Deoiled sunflower seeds ameliorate depression by promoting the production of monoamine neurotransmitters and inhibiting oxidative stress. Food and Function. 2021;12(2):573–586. https://doi.org/10.1039/D0FO01978J
102. Mao SY, Zhang RY, Wang DS, Zhu WY. Impact of subacute ruminal acidosis (SARA) adaptation on rumen microbiota in dairy cattle using pyrosequencing. Anaerobe. 2013;24:12–19. https://doi.org/10.1016/j.anaerobe.2013.08.003
103. Liu Q, Zhang Y, Zhang J, Du Z, He B, Qin J, et al. Organic Iodine Improves the Growth Performance and Gut Health of Fujian Yellow Rabbits. Animals. 2024;14(13):935. https://doi.org/10.3390/ani14131935
104. Mehri A. Trace elements in human nutrition (II)–An update. International Journal of Preventive Medicine. 2020;11:2. https://doi.org/10.4103/ijpvm.IJPVM_48_19
105. Hilal EY, Elkhairey MAE, Osman AOA. The role of zinc, manganse and copper in rumen metabolism and immune function: a review article. Open Journal of Animal Sciences. 2016;6:304–324. https://doi.org/10.4236/ojas.2016.64035
106. Miller WJ. Zinc nutrition of cattle: a review. Journal of Dairy Science. 1970;53(8):1123–1135. https://doi.org/10.3168/ jds.S0022-0302(70)86355-X
107. Ma L, Terwilliger A, Maresso AW. Iron and zinc exploitation during bacterial pathogenesis. Metallomics. 2015;7 (12):1541–1554. https://doi.org/10.1039/c5mt00170f
108. McDevitt CA, Ogunniyi AD, Valkov E, Lawrence MC, Kobe B, McEwan AG, et al. A molecular mechanism for bacterial susceptibility to zinc. PLoS Pathogens. 2011;7(11):e1002357. https://doi.org/10.1371/journal.ppat.1002357
109. Kwak WS, Kim YI, Choi DY, Lee YH. Effect of feeding mixed microbial culture fortified with trace minerals on ruminal fermentation, nutrient digestibility, nitrogen and trace mineral balance in sheep. Journal of Animal Science and Technology. 2016;58:21. https://doi.org/10.1186/s40781-016-0102-8
110. Lee MRF, Fleming HR, Whittington F, Hodgson C, Suraj PT, Davies DR. The potential of silage lactic acid bacteria- derived nano-selenium as a dietary supplement in sheep. Animal Production Science. 2019;59(11):1999–2009. https://doi.org/ 10.1071/AN19258
111. Romero-Pérez A, García-García E, Zavaleta-Mancera A, Ramírez-Bribiesca JE, Revilla-Vázquez A, Hernández- Calva LM, et al. Designing and evaluation of sodium selenite nanoparticles in vitro to improve selenium absorption in ruminants. Veterinary Research Communications. 2010;34:71–79. https://doi.org/10.1007/s11259-009-9335-z
112. Grabez V, Coll-Brasas E, Fulladosa E, Hallenstvedt E, Håseth TT, Øverland M, et al. Seaweed inclusion in finishing lamb diet promotes changes in micronutrient content and flavour-related compounds of raw meat and dry-cured leg (Fenalår). Foods. 2022;11(7):1043. https://doi.org/10.3390/foods11071043
113. Hendawy AO, Khattab MS, Sugimura S, Sato K. Effects of 5-aminolevulinic acid as a supplement on animal performance, iron status, and immune response in farm animals: A review. Animals. 2020;10(8):1352. https://doi.org/10.3390/ ani10081352
114. Li X, Højberg O, Canibe N, Jensen BB. Phylogenetic diversity of cultivable butyrate-producing bacteria from pig gut content and feces. Journal of Animal Science. 2016;94(3):377–381. https://doi.org/10.2527/jas.2015-9868
115. Makkar HPS, Tran G, Hauzé V, Giger-Reverdin S, Lessire M, Lebas F, Ankers P. Seaweeds for livestock diets: A review. Animal Feed Science and Technology. 2016;212:1–17. https://doi.org/10.1016/j.anifeedsci.2015.09.018
116. NRC (National Research Council) Nutrient Requirements of Beef Cattle. 8th Revised Edition. Washington, DC: National Academies Press. 2015.
117. Giro TM, Kulikovsky AV, Giro AV. Effect of Essential Microelements on Proteomic Profile of Lamb Muscle Tissue Protein. Food Processing: Techniques and Technology. 2023;53(2):396–403. (In Russ.). https://doi.org/10.21603/2074- 9414-2023-2-2443
118. Giro TM, Ilina LA, Kulikovsky AV, Ziruk IV, Giro AV. Molecular genetic studies of microbiocenosis and microstructure of jejunum wall in young rams grown on biofortified feed additives. Foods and Raw Materials. 2022;10(2):310–317. https://doi.org/10.21603/2308-4057-2022-2-541