Abstract
In recent years, whole-plant corn silage has been widely used in China. Roughage is an important source of nutrition for ruminants and has an important effect on rumen microbiota, which plays an important role in animal growth performance and feed digestion. To better understand the effects of different silages on rumen microbiota, the effects of whole-plant corn silage or corn straw silage on growth performance, rumen fermentation products, and rumen microbiota of Simmental hybrid cattle were studied. Sixty healthy Simmental hybrid cattle were randomly divided into 2 groups with 6 replicates in each group and 5 cattle in each replicate. They were fed with whole-plant corn silage (WS) diet and corn straw silage (CS) diet respectively. Compared with corn straw silage, whole-plant corn silage significantly increased daily gain and decreased the feed intake-to-weight gain ratio (F/G) of beef cattle. Whole-plant corn silage also decreased the acetic acid in the rumen and the acetate-to-propionate ratio (A/P) compared with corn straw silage. On the genus level, the relative abundance of Prevotella_1 was significantly increased while the relative abundance of Succinivibrionaceae_UCG-002 was decreased in cattle fed whole-plant corn silage compared with those fed corn straw silage. Prevotella_1 was positively correlated with acetic acid and A/P. Succinivibrionaceae_UCG-002 was positively correlated with propionic acid and butyric acid, and negatively correlated with pH. Feeding whole-plant corn silage improved amino acid metabolism, nucleotide metabolism, and carbohydrate metabolism. Correlation analysis between rumen microbiota and metabolic pathways showed that Succinivibrionaceae_UCG-002 was negatively correlated with glycan biosynthesis and metabolism, metabolism of co-factors and vitamins, nucleotide metabolism, and translation while Prevotellaceae_UCG-003 was positively correlated with amino acid metabolism, carbohydrate metabolism, energy metabolism, genetic information processing, lipid metabolism, membrane transport, metabolism of cofactors and vitamins, nucleotide metabolism, replication and repair, and translation. Ruminococcus_2 was positively correlated with amino acid metabolism and carbohydrate metabolism. Feeding whole-plant corn silage can improve the growth performance and rumen fermentation of beef cattle by altering rumen microbiota and regulating the metabolism of amino acids, carbohydrates, and nucleotides.
Key points
• Feeding whole-plant corn silage could decrease the F/G of beef cattle
• Feeding whole-plant corn silage improves rumen fermentation in beef cattle
• Growth performance of beef cattle is related to rumen microbiota and metabolism
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The authors declare that data supporting the findings of this study are available within the article.
References
Anantasook N, Wanapat M, Cherdthong A, Gunun P (2013) Changes of microbial population in the rumen of dairy steers as influenced by plant containing tannins and saponins and roughage to concentrate ratio. Asian-Australasian J Anim Sci 26:1583–1591. https://doi.org/10.5713/ajas.2013.13182
Aschenbach JR, Kristensen NB, Donkin SS, Hammon HM, Penner GB (2010) Gluconeogenesis in dairy cows: the secret of making sweet milk from sour dough. IUBMB Life 62(12):869–877. https://doi.org/10.1002/iub.400
Bergman EN (1990) Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiol Rev 70:567–590. https://doi.org/10.1152/physrev.1990.70.2.567
Broderick GA (1996) Altering ruminal nitrogen metabolism to improve protein utilization. Introduction J Nutr 126:1324S-S1325. https://doi.org/10.1093/jn/126.suppl_4.1324S
Carberry CA, Kenny DA, Han S, McCabe MS, Waters SM (2012) Effect of phenotypic residual feed intake and dietary forage content on the rumen microbial community of beef cattle. Appl Environ Microbiol 78. https://doi.org/10.1128/AEM.07759-11
Chen D, Chen Y, Zhen H, Xiao K, Tang J, Tang Q, Rahman MAU (2019) Effects of replacing whole-plant corn silage with whole-plant rice silage and rice straw on growth performance, apparent digestibility and plasma parameters in growing Angus cross bred beef cattle. IJAB 22(5):1116–1122
Den Besten G, van Eunen K, Groen AK, Venema K, Reijngoud D-J, Bakker BM (2013) The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J Lipid Res 54:2325–2340. https://doi.org/10.1194/jlr.R036012
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10(10):996–998. https://doi.org/10.1038/NMETH.2604
Gharechahi J, Salekdeh GH (2018) A metagenomic analysis of the camel rumen’s microbiome identifies the major microbes responsible for lignocellulose degradation and fermentation. Biotechnol Biofuels 11. https://doi.org/10.1186/s13068-018-1214-9
Griswold KE (1999) Diversity of extracellular proteolytic activities among prevotella species from the rumen. Curr Microbiol 39:187–194. https://doi.org/10.1007/s002849900443
Guarner F, Malagelada JR (2003) Gut flora in health and disease. Lancet 361:512–519. https://doi.org/10.1016/S0140-6736(03)12489-0
Hameleers A (1998) The effects of the inclusion of either maize silage, fermented whole crop wheat or ure-treated whole crop wheat in a diet based on a high-quality grass silage on the performance of dairy cows. Grass Forage Sci 53:157–163. https://doi.org/10.1046/j.1365-2494.1998.5320157.x
Hanage WP (2014) Microbiology: microbiome science needs a healthy dose of scepticism. Nature 512:247–248. https://doi.org/10.1038/512247a
Henderson G, Cox F, Ganesh S, Jonker A, Young W, Janssen PH (2016) Erratum: Rumen microbial community composition varies with diet and host, but a core microbiome is found across a wide geographical range. Sci Rep 6:19175. https://doi.org/10.1038/srep19175
Holman DB, Gzyl KE (2019) A meta-analysis of the bovine gastrointestinal tract microbiota. FEMS Microbiol Ecol 95. https://doi.org/10.1093/femsec/fiz072
Huws SA, Creevey CJ, Oyama LB, Mizrahi I, Denman SE, Popova M, Muñoz-Tamayo R, Forano E, Waters SM, Hess M, Tapio I, Smidt H, Krizsan SJ, Yáñez-Ruiz DR, Belanche A, Guan L, Gruninger RJ, McAllister TA, Newbold CJ, Roehe R, Dewhurst RJ, Snelling TJ, Watson M, Suen G, Hart EH, Kingston-Smith AH, Scollan ND, do Prado RM, Pilau EJ, Mantovani HC, Attwood GT, Edwards JE, McEwan NR, Morrisson S, Mayorga OL, Elliott C, Morgavi DP (2018) Addressing global ruminant agricultural challenges through understanding the rumen microbiome: past, present, and future. Front Microbiol 9:2161- .https://doi.org/10.3389/fmicb.2018.02161
Iannaccone M, Ianni A, Contaldi F, Esposito S, Martino C, Bennato F, De Angelis E, Grotta L, Pomilio F, Giansante D, Martino G (2019) Whole blood transcriptome analysis in ewes fed with hemp seed supplemented diet. Sci Rep 9:16192. https://doi.org/10.1038/s41598-019-52712-6
Jami E, Mizrahi I (2012) Composition and similarity of bovine rumen microbiota across individual animals. PLoS ONE 7:e33306. https://doi.org/10.1371/journal.pone.0033306
Jami E, White BA, Mizrahi I (2014) Potential role of the bovine rumen microbiome in modulating milk composition and feed efficiency. PLoS ONE 9:e85423. https://doi.org/10.1371/journal.pone.0085423
Jeon S, Jeong S, Lee M, Seo J, Kam DK, Kim JH, Park J, Seo S (2019) Effects of reducing inclusion rate of roughages by changing roughage sources and concentrate types on intake, growth, rumen fermentation characteristics, and blood parameters of Hanwoo growing cattle (Bos taurus coreanae). Asian-Australas J Anim Sci 32(11):1705–1714. https://doi.org/10.5713/ajas.19.0269
Jiang XT, Peng X, Deng GH, Sheng HF, Wang Y, Zhou HW, Tam NFY (2013) Illumina sequencing of 16S rRNA tag revealed spatial variations of bacterial communities in a mangrove wetland. Microb Ecol 66:96–104. https://doi.org/10.1007/s00248-013-0238-8
Kaufmann W, Rohr K (1966) Results of gas chromatographic determinations of volatile fatty acids in the rumen of cows on various diets. Z Tierphysiol Tierernahr Futtermittelkd 22(1):1–8
King TM, Bondurant RG, Jolly-Breithaupt ML, Gramkow JL, Klopfenstein TJ, MacDonald JC (2017) Effect of corn residue harvest method with ruminally undegradable protein supplementation on performance of growing calves and fiber digestibility. J Anim Sci 95:5290–5300. https://doi.org/10.2527/jas2017.1926
Khaing KT, Loh TC, Ghizan S, Halim RA, Samsudin AA (2015) Feed intake, growth performance and digestibility in goats fed whole corn plant silage and Napier grass. Mal J Anim Sci 18(1):87–97
Kolver ES, de Veth MJ (2002) Prediction of ruminal pH from pasture-based diets. J Dairy Sci 85:1255–1266. https://doi.org/10.3168/jds.S0022-0302(02)74190-8
Kovatcheva-Datchary P, Nilsson A, Akrami R, Lee YS, De Vadder F, Arora T, Hallen A, Martens E, Björck I, Bäckhed F (2015) Dietary fiber-induced improvement in glucose metabolism is associated with increased abundance of Prevotella. Cell Metab 22:971–982. https://doi.org/10.1016/j.cmet.2015.10.001
Krieg NR, Staley JT, Brown DR, Hedlund BP, Paster BJ, Ward NL, Ludwig W, Whitman WB (2010) Bergey’s Manual® of Systematic Bacteriology: Volume Four The Bacteroidetes, Spirochaetes, Tenericutes (Mollicutes), Acidobacteria, Fibrobacteres, Fusobacteria, Dictyoglomi, Gemmatimonadetes, Lentisphaerae, Verrucomicrobia, Chlamydiae, and Planctomycetes. Springer, New York. https://doi.org/10.1007/978-0-387-68572-4
Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega TRL, Knight R, Beiko RG, Huttenhower C (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814–821. https://doi.org/10.1038/nbt.2676
Lechartier C, Peyraud J-L (2011) The effects of starch and rapidly degradable dry matter from concentrate on ruminal digestion in dairy cows fed corn silage-based diets with fixed forage proportion. J Dairy Sci 94:2440–2454. https://doi.org/10.3168/jds.2010-3285
Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, Schlegel ML, Tucker TA, Schrenzel MD, Knight R, Gordon JI (2008) Evolution of mammals and their gut microbes. Science 80(320):1647–1651. https://doi.org/10.1126/science.1155725
Li Z, Wright ADG, Liu H, Bao K, Zhang T, Wang K, Cui X, Yang F, Zhang Z, Li G (2015) Bacterial community composition and fermentation patterns in the rumen of sika deer (Cervus nippon) fed three different diets. Microb Ecol 69(2):307–318. https://doi.org/10.1007/s00248-014-0497-z
Liu C, Wu H, Liu S, Chai S, Meng Q, Zhou Z (2019) Dynamic alterations in Yak rumen bacteria community and metabolome characteristics in response to feed type. Front Microbiol 10:1116. https://doi.org/10.3389/fmicb.2019.01116
Liu L, Lin Y, Liu L, Wang L, Bian Y, Gao X, Li Q (2016) Regulation of peroxisome proliferator-activated receptor gamma on milk fat synthesis in dairy cow mammary epithelial cells. In Vitro Cell Dev Biol Anim 52(10):1044–1059. https://doi.org/10.1007/s11626-016-0059-4
Lozupone C, Lladser ME, Knights D, Stombaugh J, Knight R (2011) UniFrac: an effective distance metric for microbial community comparison. ISME J 5:169–172. https://doi.org/10.1038/ismej.2010.133
Luo Y, Pfister P, Leisinger T, Wasserfallen A (2001) The genome of archaeal prophage ΨM100 encodes the lytic enzyme responsible for autolysis of Methanothermobacter wolfeii. J Bacteriol 183:5788–5792. https://doi.org/10.1128/JB.183.19.5788-5792.2001
Macfarlane S, Macfarlane GT (2003) Regulation of short-chain fatty acid production. Proc Nutr Soc 62. https://doi.org/10.1079/pns2002207
Mertens DR (1997) Creating a system for meeting the fiber requirements of dairy cows. J Dairy Sci 80. https://doi.org/10.3168/jds.S0022-0302(97)76075-2
Moloney AP, Drennan MJ (2013) Characteristics of fat and muscle from beef heifers offered a grass silage or concentrate-based finishing ration. Livest Sci 152:147–153. https://doi.org/10.1016/j.livsci.2012.12.001
Mu C, Yang Y, Su Y, Zoetendal EG, Zhu W (2017) Differences in microbiota membership along the gastrointestinal tract of piglets and their differential alterations following an early-life antibiotic intervention. Front Microbiol 8:797. https://doi.org/10.3389/fmicb.2017.00797
Nocek JE (1997) Bovine acidosis: implications on laminitis. J Dairy Sci 80:1005–1028. https://doi.org/10.3168/jds.S0022-0302(97)76026-0
O’Mara F, Fitzgerald J, Murphy J, Rath M (1998) The effect on milk production of replacing grass silage with maize silage in the diet of dairy cows. Livest Prod Sci 55:79–87. https://doi.org/10.1016/S0301-6226(98)00115-8
Penner GB, Beauchemin KA, Mutsvangwa T (2007) Severity of ruminal acidosis in primiparous Holstein cows during the periparturient period. J Dairy Sci 90:365–375. https://doi.org/10.3168/jds.S0022-0302(07)72638-3
Purushe J, Fouts DE, Morrison M, White BA, Mackie RI, Coutinho PM, Henrissat B, Nelson KE (2010) Comparative genome analysis of Prevotella ruminicola and Prevotella bryantii: insights into their environmental niche. Microb Ecol 60:721–729. https://doi.org/10.1007/s00248-010-9692-8
Ramšak A, Peterka M, Tajima K, Martin JC, Wood J, Johnston MEA, Aminov RI, Flint HJ, Avguštin G (2000) Unravelling the genetic diversity of ruminal bacteria belonging to the CFB phylum. FEMS Microbiol Ecol 33. https://doi.org/10.1016/S0168-6496(00)00049-0
Rey M, Enjalbert F, Combes S, Cauquil L, Bouchez O, Monteils V (2014) Establishment of ruminal bacterial community in dairy calves from birth to weaning is sequential. J Appl Microbiol 116. https://doi.org/10.1111/jam.12405
Russell JB (1998) The importance of pH in the regulation of ruminal acetate to propionate ratio and methane production in vitro. J Dairy Sci 81. https://doi.org/10.3168/jds.S0022-0302(98)75886-2
Russell JB, Rychlik JL (2001) Factors that alter rumen microbial ecology. Science (80- ) 292:1119–1122 .https://doi.org/10.1126/science.1058830
Sharma A, Prasad S, Singh Y, Bishisth R (2014) Effect of polyherbal preparation supplementation on immunity and udder health of periparturient Karan-Fries crossbred dairy cows. J Appl Anim Res 42:217–221. https://doi.org/10.1080/09712119.2013.842477
Shen JS, Chai Z, Song LJ, Liu JX, Wu YM (2012) Insertion depth of oral stomach tubes may affect the fermentation parameters of ruminal fluid collected in dairy cows. J Dairy Sci 95:5978–5984. https://doi.org/10.3168/jds.2012-5499
Singh KM, Jisha TK, Reddy B, Parmar N, Patel A, Patel AK, Joshi CG (2015) Microbial profiles of liquid and solid fraction associated biomaterial in buffalo rumen fed green and dry roughage diets by tagged 16S rRNA gene pyrosequencing. Mol Biol Rep 42:95–103. https://doi.org/10.1007/s11033-014-3746-9
Van Gylswyk NO (1995) Succiniclasticum ruminis gen. nov., sp. nov., a ruminal bacterium converting succinate to propionate as the sole energy-yielding mechanism. Int J Syst Bacteriol 45(2): 297–300. https://doi.org/10.1099/00207713-45-2-297.
Van Soest PJ (1965) Symposium on factors influencing the voluntary intake of herbage by ruminants: voluntary intake in relation to chemical composition and digestibility. J Anim Sci 24. https://doi.org/10.2527/jas1965.243834x
Xi YM, Jin ZH, Lin LJ, Han ZY (2014) Effect of phytosterols on rumen fermentation in vitro. Genet Mol Res 13:3869–3875. https://doi.org/10.4238/2014.May.16.12
Xue D, Chen H, Zhao X, Xu S, Hu L, Xu T, Jiang L, Zhan W (2017) Rumen prokaryotic communities of ruminants under different feeding paradigms on the Qinghai-Tibetan Plateau. Syst Appl Microbiol 40:227–236. https://doi.org/10.1016/j.syapm.2017.03.006
Yang C, Liu J, Wu X, Bao P, Long R, Guo X, Ding X, Yan P (2017) The response of gene expression associated with lipid metabolism, fat deposition and fatty acid profile in the longissimus dorsi muscle of Gannan yaks to different energy levels of diets. PLoS ONE 12:e0187604. https://doi.org/10.1371/journal.pone.0187604
Young JW (1977) Gluconeogenesis in cattle: significance and methodology. J Dairy Sci 60(1):1–15. https://doi.org/10.3168/jds.S0022-0302(77)83821-6
Zaralis K, Nørgaard P, Helander C, Murphy M, Weisbjerg MR, Nadeau E (2014) Effects of maize maturity at harvest and dietary proportion of maize silage on intake and performance of growing/finishing bulls. Livest Sci 168:89–93. https://doi.org/10.1016/j.livsci.2014.07.013
Funding
Thanks for the financial support of China Agriculture Research System of MOF and MARA, Science and Technology Innovation Team of Henan Province High Quality Forage and Animal Health (No.22IRTSTHN022), and Outstanding Talents of Henan Agricultural University (No.30500636), Henan Province Science and Technology Research Project (No.222102110007).
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Y. C. and H. L. performed experiments and analyzed data. Z. G., J. X., and B. L. participated in the data collection. M. G., X. Y., J. N., and X. Z. assisted with animal experimentation. S. M. and D. L. provided advice on the design and performance of experiments. Y. C. and H. L. wrote the manuscript draft. Y. S. and Y. H. S. supervised the study. All of us read and approved the final manuscript.
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Cui, Y., Liu, H., Gao, Z. et al. Whole-plant corn silage improves rumen fermentation and growth performance of beef cattle by altering rumen microbiota. Appl Microbiol Biotechnol 106, 4187–4198 (2022). https://doi.org/10.1007/s00253-022-11956-5
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DOI: https://doi.org/10.1007/s00253-022-11956-5