ORIGINAL PAPER
Dietary supplementation with fermented Broussonetia papyrifera enhances tissue mineral deposition and intestinal microbiome in finishing pigs
More details
Hide details
1
Hunan Open University, Department of Applied Technology, Changsha, 410004, China
2
Tianjin Institute of Industrial Biotechnology, Chinese Academy of Sciences, Tianjin, 300000, China
3
Institute of Biological Resources, Jiangxi Academy of Sciences, Nanchang, 330096, China
These authors had equal contribution to this work
Publication date: 2024-11-15
Corresponding author
Y. Peng
Hunan Open University, Department of Applied Technology, Changsha, 410004, China
KEYWORDS
TOPICS
ABSTRACT
The objective of this study was to investigate the dietary effects
of fermented Broussonetia papyrifera (FBP) on serum biochemistry, mineral
deposition, and intestinal microbiota in finishing pigs. Thirty-six grower pigs
(18 males and 18 females, with an initial body weight of 12.25 ± 0.15 kg) were
selected and randomly assigned to two dietary treatment groups: CON group fed
a basal diet, and treatment group fed an isonitrogenous and isocaloric FBP diet
(20% FBP). Each treatment included 6 replicates with 3 pigs in each replicate, and
the feeding trial lasted 6 months. The results showed that dietary FBP significantly
reduced ammonia, alanine aminotransferase, aspartate aminotransferase and
urea nitrogen in the serum of finishing pigs. In addition, the FBP diet significantly
reduced the concentration of iron, calcium, magnesium, zinc, and manganese in
serum, as well as magnesium and manganese levels in faeces, while significantly
increasing selenium, copper, and iron concentrations in the liver and iron and
selenium in muscles. Dietary FBP raised the abundance of Terrisporobacter,
Clostridium butyricum, Akkermansia, and Turicibacter, while decreasing the
abundance of Lactobacillus in the colon. The abundance of Unclassified_k_
norank_d_Bacteria was closely related to iron and magnesium concentrations.
In conclusion, these results suggest that the dietary effect of FBP on absorption,
metabolism and deposition of minerals could be attributed to an altered microbial
community in the colon. We recommend further studies to unravel the underlying
mechanisms by which gut microbes modulate mineral deposition.
ACKNOWLEDGEMENTS
The study was supported by the Provincial
Natural Science Foundation of Hunan (Science and
education joint project, 2021JJ60037). All authors
would like to thank Jiangxi Fujia agricultural technology
Co., Ltd (Yichun, Jiangxi, China) for its assistance
during pig breeding and preparation of the
fermented Broussonetia papyrifera diet.
CONFLICT OF INTEREST
The Authors declare that there is no conflict
of interest.
REFERENCES (40)
1.
An X., Zhang S., Li T., Chen N., Wang X., Zhang B., Ma Y., 2021. Transcriptomics analysis reveals the effect of Broussonetia papyrifera L. fermented feed on meat quality traits in fattening lamb. PeerJ 9, e11295,
https://doi.org/10.7717/peerj.....
2.
Beaumont M., Portune K.J., Steuer N. et al., 2017. Quantity and source of dietary protein influence metabolite production by gut microbiota and rectal mucosa gene expression: a randomized, parallel, double-blind trial in overweight humans. Am. J. Clin. Nutr. 106, 1005–1019,
https://doi.org/10.3945/ajcn.1....
3.
Burrow K., Young W., McConnell M., Carne A., Barr D., Reid M., Bekhit A.E.-D., 2020. The effect of sheep and cow milk supplementation of a low calcium diet on the distribution of macro and trace minerals in the organs of weanling rats. Nutrients 12, 594,
https://doi.org/10.3390/nu1203....
4.
Cabrera M.C., Saadoun A., 2014. An overview of the nutritional value of beef and lamb meat from South America. Meat Sci. 98, 435–444,
https://doi.org/10.1016/j.meat....
5.
Cassir N., Benamar S., La Scola B., 2016. Clostridium butyricum: from beneficial to a new emerging pathogen. Clin. Micro. Inf. 22, 37–45,
https://doi.org/10.1016/j.cmi.....
6.
Chao J., Yin Z., Ye W., Zhao S., 2006. Chemical constituents from branch of Broussonetia papyrifera. China J. Chin. Materia Med. 31, 1078–1080.
7.
Dominguez M.T., Madejon P., Maranon T., Murillo J.M., 2010. Afforestation of a trace-element polluted area in SW Spain: woody plant performance and trace element accumulation. Eur. J. Forest Res. 129, 47–59,
https://doi.org/10.1007/s10342....
8.
Duan G., Song B., Chen X., Zheng C., Zheng J., Zhang S., Guo Q., Li F., Duan Y., Yin Y., 2022. Effects of low-protein diet supplemented with fermented Broussonetia papyrifera feed on fat deposition and gut microbiota composition of finishing pigs. Chin. J. Anim. Nutr. 34, 2186-2195,
https://kns.cnki.net/kcms/deta....
9.
Gerritsen J., Fuentes S., Grievink W., Niftrik L., Tindall B.J., Timmerman H.M., Rijkers G.T., Smidt H., 2014. Characterization of Romboutsia ilealis gen. nov., sp. nov.,nisolated from the gastro-intestinal tract of a rat, and proposal for the reclassification of five closely related members of the genus Clostridium into the genera Romboutsia gen. nov., Intestinibacter gen. nov., Terrisporobacter gen. nov. and Asaccharospora gen. nov. Int. J. Syst. Evol. Micro. 64, 1600–1616,
https://doi.org/10.1099/ijs.0.....
10.
Han H., Zhang L., Shang Y., Wang M., Phillips C.J.C., Wang Y., Su C., Lian H., Fu T., Gao T., 2022. Replacement of maize silage and soyabean meal with Mulberry Silage in the diet of hu lambs on growth, gastrointestinal tissue morphology, rumen fermentation parameters and microbial diversity. Animals 12, 1406,
https://doi.org/10.3390/ani121....
11.
Hanting Z., Xiaoqiang Z., Mingkui W., 2011. Chemical constituents from the Bark of Broussonetia papyrifera L. Vent. Nat. Prod. Sci. 23, 661–663.
12.
Hao Y., Huang S., Si J., et al., 2020. Effects of paper mulberry silage on the milk production, apparent digestibility, antioxidant capacity, and fecal bacteria composition in Holstein dairy cows. Animals 10, 1152,
https://doi.org/10.3390/ani100....
13.
Krga I., Glibetic M. 2022. Gut microbiota in health and diseases In: M. Glibetic (Editor). Comprehensive Gut Microbionta. Elselvier Inc. Amsterdam (Netherlands), pp. 182–198,
https://doi.org/10.1016/B978-0....
14.
Krupa-Kozak U., Drabińska N. 2022. Gut microbiota and a gluten-free diet, In: M. Glibetic (Editor). Comprehensive Gut Microbionta. Elselvier Inc. Amsterdam (Netherlands), pp. 243–255,
https://doi.org/10.1016/B978-0....
15.
Michalak I., Chojnacka K., Korniewicz D., 2015. New feed supplement from macroalgae as the dietary source of microelements for pigs. Open Chem. 13, 1341–1352,
https://doi.org/10.1515/chem-2....
16.
Nakashima T., Fujii K., Seki T., Aoyama M., Azuma A., Kawasome H., 2022. Novel gut microbiota modulator, which markedly increases Akkermansia muciniphila occupancy, ameliorates experimental colitis in rats. Digest. Dis. Sci. 67, 2899–2911,
https://doi.org/10.1007/s10620....
17.
Niu K., Khosravic S., Wang Y., Zhai Z., Wang R., Liu J., Cai L., Deng L., Wu X., 2022. Multi-omics-based functional characterization of hybrid fermented Broussonetia papyrifera: A preliminary study on gut health of laying hens. Fermentation 8, 547,
https://doi.org/10.3390/fermen....
18.
Nwanna L.C., Eisenreich R., Schwarz F.J., 2007. Effect of wet-incubation of dietary plant feedstuffs with phytases on growth and mineral digestibility by common carp (Cyprinus carpio L). Aquaculture 271, 461–468,
https://doi.org/10.1016/j.aqua....
19.
Olukosi O.A., Kuijk S., Han Y., 2018. Copper and zinc sources and levels of zinc inclusion influence growth performance, tissue trace mineral content, and carcass yield of broiler chickens. Poult. Sci. 97, 3891–3898,
https://doi.org/10.3382/ps/pey....
20.
Paganini D., Zimmermann M.B., 2017. The effects of iron fortification and supplementation on the gut microbiome and diarrhea in infants and children: a review. Am. J. Clin. Nutr. 106, 1688S–1693S,
https://doi.org/10.3945/ajcn.1....
21.
Pajarillo E.A.B., Lee E., Kang D.K., 2021. Trace metals and animal health: Interplay of the gut microbiota with iron, manganese, zinc, and copper. Anim. Nutr. 7, 750–761,
https://doi.org/10.1016/j.anin....
22.
Roager H.M., Hansen L.B.S., Bahl M.I. et al., 2016. Colonic transit time is related to bacterial metabolism and mucosal turnover in the gut. Nat. Microbiol. 1, 16093,
https://doi.org/10.1038/nmicro....
23.
Sheng P., He L., Ji S., Huang J., Zhang Z., Wang D., Liu J., Zhang H., 2021. Effect of Broussonetia papyrifera L. (paper mulberry) on growth performance, carcase traits, meat quality and immune performance in Hu ram lambs. Ital. J. Anim. Sci. 20, 691–697,
https://doi.org/10.1080/182805....
24.
Si B., Tao H., Zhang X., Guo J., Cui K., Tu Y., Diao Q., 2018. Effect of Broussonetia papyrifera L. (paper mulberry) silage on dry matter intake, milk composition, antioxidant capacity and milk fatty acid profile in dairy cows. Asian-Australas. J. Anim. Sci. 31, 1259–1266,
https://doi.org/10.5713/ajas.1....
25.
Song B., Zheng C., Zhong Y. et al., 2020. Effects of low-protein diet supplemented with fermented broussonetia papyrifera on growth performance,carcass traits and meat quality of finishing pigs. Chin. J. Anim. Nutr. 32, 4841–4851,
https://kns.cnki.net/kcms/deta....
26.
Tan B., Yin Y., 2017. Environmental sustainability analysis and nutritional strategies of animal production in China. Annu. Rev. Anim. Biosci. 5, 171–184,
https://doi.org/10.1146/annure....
27.
Tang M., Frank D.N., Hendricks A.E., Ir D., Esamai F., Liechty E., Hambidge M.K., Krebs N.F., 2017. Iron in micronutrient powder promotes an unfavorable gut microbiota in Kenyan infants. Nutrients 9, 776,
https://doi.org/10.3390/nu9070....
28.
Wang G., Liu L., Wang Z., Pei X., Tao W., Xiao Z., Liu B., Wang M., Lin G., Ao T., 2019. Comparison of inorganic and organically bound trace minerals on tissue mineral deposition and fecal excretion in broiler breeders. Biol. Trace Elem. Res. 189, 224–232,
https://doi.org/10.1007/s12011....
29.
Wang X., Shang Y., Wei Q. et al., 2022. Comparative analyses of the gut microbiome of two fox species, the red fox (Vulpes Vulpes) and corsac fox (Vulpes Corsac), that occupy different ecological niches. Microb. Ecol. 83, 753–765,
https://doi.org/10.1007/s00248....
30.
Waters J.L., Ley R.E., 2019. The human gut bacteria Christensenellaceae are widespread, heritable, and associated with health. BMC Biol. 17, 83,
https://doi.org/10.1186/s12915....
32.
Wen Z., Chen Y., Wu L., Tian H., Zhu N., Guo Y., Deng M., Liu J., Sun B., 2022. Effects of Broussonetia papyrifera silage on rumen fermentation parameters and microbes of Holstein heifers. AMB Express 12, 62,
https://doi.org/10.1186/s13568....
33.
Wu Q., Wang X., Ding Y., Hu Y., Nie Y., Wei W., Ma S., Yan L., Zhu L., Wei F., 2017. Seasonal variation in nutrient utilization shapes gut microbiome structure and function in wild giant pandas. Proc. R. Soc. B 284, 20170955,
https://doi.org/10.1098/rspb.2....
34.
Wu X., Jiang X., Sheng S. et al., 2019. Dynamics of nirK type denitrifying bacterial community in static aerobic high temperature composting. Microbiol. China. 46, 986-996,
https://doi.org/10.13344/j.mic....
35.
Xiong Y., Guo C., Wang L., Chen F., Dong X., Li X., Ni K., Yang F., 2021. Effects of paper mulberry silage on the growth performance, rumen microbiota and muscle fatty acid composition in Hu lambs. Fermentation 7, 286,
https://doi.org/10.3390/fermen....
36.
Yang Q., Chen S., Liu Y., 2014. The Effect of Broussonetia papyrifera leaf on the production performance, meat quality and apparent digestibility of fatting pigs. J. Hen. Agric Sci. 43, 133-137.
37.
Yin D., Zhai F., Lu W., Moss A.F., Kuang Y., Li F., Zhu Y., Zhang R., Zhang Y., Zhang S., 2022. Comparison of coated and uncoated trace minerals on growth performance, tissue mineral deposition, and intestinal microbiota in ducks. Front. Microbiol. 13, 831945,
https://doi.org/10.3389/fmicb.....
38.
Zhang J.P., Wei Q.X., Li Q.L., Liu R.F., Tang L.Q., Song Y.X., Luo J., Liu S.M., Wang P., 2022. Effects of hybrid Broussonetia papyrifera silage on growth performance, visceral organs, blood biochemical indices, antioxidant indices, and carcass traits in dairy goats. Anim. Feed Sci. Tech. 292, 115435,
https://doi.org/10.1016/j.anif....
39.
Zhang X., Zhu S., Yang Q., Su Z., Tan H., Liu C., Wu M., Duan Y., Yin Y., 2019. Effects of Broussonetia papyrifera fermented diet on growth performance,carcass quality and meat quality of Xiangsha pigs commercial line of commercial pigs. Chin. J. Anim. Nutr. 31, 5760–5771
40.
Zhou X., Zhang N., Zhang J., Gu Q., Zheng Y., Ma Y., Zou C., 2022. Effects of mixed silage of sugarcane top or sugarcane and Broussonetia papyrifera leaf on its fermentation quality. Chin. J. Anim. Nutr. 34, 516–532,
https://kns.cnki.net/kcms/deta....