Effects of the Inclusion of fermented mulberry leaves and branches in the gestational diet on the performance and gut microbiota of sows and their offspring.
Schroyen, Martine ; Université de Liège - ULiège > Département GxABT > Département GxABT
Everaert, Nadia ; Université de Liège - ULiège > Département GxABT > Ingénierie des productions animales et nutrition
Ma, T
Zhang, HF
Language :
English
Title :
Effects of the Inclusion of fermented mulberry leaves and branches in the gestational diet on the performance and gut microbiota of sows and their offspring.
Publication date :
2021
Journal title :
Microorganisms
eISSN :
2076-2607
Publisher :
Molecular Diversity Preservation International (MDPI), Basel, Switzerland
Huang, S.; Wei, J.; Yu, H.; Hao, X.; Zuo, J.; Tan, C.; Deng, J. Effects of Dietary Fiber Sources during Gestation on Stress Status, Abnormal Behaviors and Reproductive Performance of Sows. Animals 2020, 10, 141. [CrossRef]
Oelke, C.A.; Bernardi, M.L.; Nunes, P.R.; Weber, N.C.; Veit, F.C.; Leal Ribeiro, A.M. Physiological and behavioral response of sows fed with different levels of dietary fiber during gestation. J. Vet. Behav. 2018, 28, 54–57. [CrossRef]
Tan, C.; Wei, H.; Sun, H.; Long, G.; Ao, J.; Jiang, S.; Peng, J. Effects of supplementing sow diets during two gestations with konjac flour and Saccharomyces boulardii on constipation in peripartal period, lactation feed intake and piglet performance. Anim. Feed Sci. Technol. 2015, 210, 254–262. [CrossRef]
Ferguson, E.M.; Slevin, J.; Hunter, M.G.; Edwards, S.A.; Ashworth, C.J. Beneficial effects of a high fibre diet on oocyte maturity and embryo survival in gilts. Reproduction 2007, 133, 433–439. [CrossRef]
Zhuo, Y.; Cao, M.; Gong, Y.; Tang, L.; Jiang, X.; Li, Y.; Yang, M.; Xu, S.; Li, J.; Che, L.; et al. Gut microbial metabolism of dietary fibre protects against high energy feeding induced ovarian follicular atresia in a pig model. Br. J. Nutr. 2021, 125, 38–49. [CrossRef]
Matte, J.J.; Robert, S.; Girard, C.L.; Farmer, C.; Martineau, G.-P. Effect of bulky diets based on wheat bran or oat hulls on reproductive performance of sows during their first two parities1. J. Anim. Sci. 1994, 72, 1754–1760. [CrossRef] [PubMed]
Tan, C.Q.; Sun, H.Q.; Wei, H.K.; Tan, J.J.; Long, G.; Jiang, S.W.; Peng, J. Effects of soluble fiber inclusion in gestation diets with varying fermentation characteristics on lactational feed intake of sows over two successive parities. Animal 2018, 12, 1388–1395. [CrossRef]
Ortiz, R.; López, M.; Pérez, R.E.; Ramírez, P.d.l.P.; Ordaz, G. Effect of the Inclusion of Different Levels of Dietary Cactus (Opuntia ficus-indica) on Gilts’ Biochemical Parameters and Feed Intake during Lactation. Animals 2020, 10, 1881. [CrossRef]
Zhao, J.; Bai, Y.; Tao, S.; Zhang, G.; Wang, J.; Liu, L.; Zhang, S. Fiber-rich foods affected gut bacterial community and short-chain fatty acids production in pig model. J. Funct. Foods 2019, 57, 266–274. [CrossRef]
Che, D.; Adams, S.; Wei, C.; Gui-Xin, Q.; Atiba, E.M.; Hailong, J. Effects of Astragalus membranaceus fiber on growth performance, nutrient digestibility, microbial composition, VFA production, gut pH, and immunity of weaned pigs. Microbiologyopen 2019, 8, e00712. [CrossRef]
Liu, P.; Zhao, J.; Wang, W.; Guo, P.; Lu, W.; Wang, C.; Liu, L.; Johnston, L.J.; Zhao, Y.; Wu, X.; et al. Dietary Corn Bran Altered the Diversity of Microbial Communities and Cytokine Production in Weaned Pigs. Front. Microbiol. 2018, 9. [CrossRef]
Parada Venegas, D.; De la Fuente, M.K.; Landskron, G.; González, M.J.; Quera, R.; Dijkstra, G.; Harmsen, H.J.M.; Faber, K.N.; Hermoso, M.A. Short Chain Fatty Acids (SCFAs)-Mediated Gut Epithelial and Immune Regulation and Its Relevance for Inflammatory Bowel Diseases. Front. Immunol. 2019, 10. [CrossRef]
Agyekum, A.K.; Columbus, D.A.; Farmer, C.; Beaulieu, A.D. Effects of supplementing processed straw during late gestation on sow physiology, lactation feed intake, and offspring body weight and carcass quality1. J. Anim. Sci. 2019, 97, 3958–3971. [CrossRef]
Li, Y.; Liu, H.; Zhang, L.; Yang, Y.; Lin, Y.; Zhuo, Y.; Fang, Z.; Che, L.; Feng, B.; Xu, S.; et al. Maternal Dietary Fiber Composition during Gestation Induces Changes in Offspring Antioxidative Capacity, Inflammatory Response, and Gut Microbiota in a Sow Model. Int. J. Mol. Sci. 2020, 21, 31. [CrossRef]
Kwawukume, A. The Gut and Vaginal Microbiome Profiles of Pregnant Sows and Their Contribution to Neonatal Piglet Gut Microbiome Development. Available online: http://hdl.handle.net/1993/32262 (accessed on 6 June 2017).
Leblois, J.; Massart, S.; Li, B.; Wavreille, J.; Bindelle, J.; Everaert, N. Modulation of piglets’ microbiota: Differential effects by a high wheat bran maternal diet during gestation and lactation. Sci. Rep. 2017, 7, 7426. [CrossRef]
Zhu, Z.; Jiang, J.J.; Jie, Y.; Mao, X.B.; Bing, Y.; Chen, D.W. Effect of dietary supplementation with mulberry (Morus alba L.) leaves on the growth performance, meat quality and antioxidative capacity of finishing pigs. J. Integr. Agric. 2019, 18, 143–151. [CrossRef]
Liu, S.X.; Hua, J.L.; Wang, B. Hypoglycemic function of mulberry leaf polysaccharide and 1-deoxynojirimycin (DNJ). Adv. Mater. Res. 2011, 361, 808–812. [CrossRef]
Ann, J.-Y.; Eo, H.; Lim, Y. Mulberry leaves (Morus alba L.) ameliorate obesity-induced hepatic lipogenesis, fibrosis, and oxidative stress in high-fat diet-fed mice. Genes Nutr. 2015, 10, 46. [CrossRef]
Zhao, X.; Li, L.; Luo, Q.; Ye, M.; Luo, G.; Kuang, Z.J.L.S. Effects of mulberry (Morus alba L.) leaf polysaccharides on growth performance, diarrhea, blood parameters, and gut microbiota of early-weanling pigs. Livest. Sci. 2015, 177, 88–94. [CrossRef]
Council, N.R. Nutrient requirements of swine. In National Research Council. Nutrient Requirements of Swine; Eleventh, R., Ed.; National Academies Press: Washington, DC, USA, 2012; ISBN 978-0-309-22423-9.
Van Soest, P.J.; Robertson, J.B.; Lewis, B.A. Methods for Dietary Fiber, Neutral Detergent Fiber, and Nonstarch Polysaccharides in Relation to Animal Nutrition. J. Dairy Sci. 1991, 74, 3583–3597. [CrossRef]
Adeola, O.; Lewis, A.J.; Southern, L.L. Digestion and Balance Techniques in Pigs; CRC Press: Washington, DC, USA, 2001; Volume 2, p. 903, Swine nutrition.
Koh, H.; Lee, M.J.; Kim, M.J.; Shin, J.I.; Chung, K.S. Simple diagnostic approach to childhood fecal retention using the Leech score and Bristol stool form scale in medical practice. J. Gastroenterol. Hepatol. 2010, 25, 334–338. [CrossRef] [PubMed]
Liu, P.; Piao, X.; Thacker, P.; Zeng, Z.; Li, P.; Wang, D.; Kim, S. Chito-oligosaccharide reduces diarrhea incidence and attenuates the immune response of weaned pigs challenged with Escherichia coli K88. J. Anim. Sci. 2010, 88, 3871–3879. [CrossRef]
McParland, S.; Berry, D.P. The potential of Fourier transform infrared spectroscopy of milk samples to predict energy intake and efficiency in dairy cows. J. Dairy. Sci. 2016, 99, 4056–4070. [CrossRef] [PubMed]
Edgar, R.C. UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 2013, 10, 996–998. [CrossRef] [PubMed]
Wang, Q.; Garrity, G.M.; Tiedje, J.M.; Cole, J.R. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 2007, 73, 5261–5267. [CrossRef]
Love, M.I.; Huber, W.; Anders, S.J.G.B. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014, 15, 1–21. [CrossRef]
Benjamini, Y.; Hochberg, Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B Methodol. 1995, 57, 289–300. [CrossRef]
Cheng, C.; Wei, H.; Xu, C.; Xie, X.; Jiang, S.; Peng, J. Maternal Soluble Fiber Diet during Pregnancy Changes the Intestinal Microbiota, Improves Growth Performance, and Reduces Intestinal Permeability in Piglets. Appl. Environ. Microbiol. 2018, 84, e01047-18. [CrossRef]
Tan, C.; Wei, H.; Ao, J.; Long, G.; Peng, J. Inclusion of Konjac Flour in the Gestation Diet Changes the Gut Microbiota, Alleviates Oxidative Stress, and Improves Insulin Sensitivity in Sows. Appl. Environ. Microbiol. 2016, 82, 5899. [CrossRef]
Zhuo, Y.; Feng, B.; Xuan, Y.; Che, L.; Fang, Z.; Lin, Y.; Xu, S.; Li, J.; Feng, B.; Wu, D. Inclusion of purified dietary fiber during gestation improved the reproductive performance of sows. J. Anim. Sci. Biotechnol. 2020, 11, 1–17. [CrossRef] [PubMed]
Tian, M.; Chen, J.; Liu, J.; Chen, F.; Guan, W.; Zhang, S. Dietary fiber and microbiota interaction regulates sow metabolism and reproductive performance. Anim. Nutr. 2020. [CrossRef] [PubMed]
Jha, R.; Fouhse, J.M.; Tiwari, U.P.; Li, L.; Willing, B.P. Dietary Fiber and Intestinal Health of Monogastric Animals. Front. Vet. Sci. 2019, 6, 48. [CrossRef] [PubMed]
Xu, C.; Cheng, C.; Zhang, X.; Peng, J. Inclusion of soluble fiber in the gestation diet changes the gut microbiota, affects plasma propionate and odd-chain fatty acids levels, and improves insulin sensitivity in sows. Int. J. Mol. Sci. 2020, 21, 635. [CrossRef] [PubMed]
Shang, Q.; Liu, H.; Liu, S.; He, T.; Piao, X. Effects of dietary fiber sources during late gestation and lactation on sow performance, milk quality, and intestinal health in piglets1. J. Anim. Sci. 2019, 97, 4922–4933. [CrossRef]
Shang, Q.; Liu, S.; Liu, H.; Mahfuz, S.; Piao, X. Impact of sugar beet pulp and wheat bran on serum biochemical profile, inflammatory responses and gut microbiota in sows during late gestation and lactation. Res. Sq. 2020. [CrossRef]
Weng, R.C. Dietary supplementation with different types of fiber in gestation and lactation: Effects on sow serum biochemical values and performance. Asian-Australas. J. Anim. Sci. 2020, 33, 1323–1331. [CrossRef]
Mroz, Z.; Partridge, I.G.; Mitchell, G.; Keal, H.D. The effect of oat hulls, added to the basal ration for pregnant sows, on reproductive performance, apparent digestibility, rate of passage and plasma parameters. Sci. Food Agric. 1986, 37, 239–247. [CrossRef]
Leblois, J.; Zhang, Y.; Wavreille, J.; Uerlings, J.; Schroyen, M.; Sureda, E.A.; Soyeurt, H.; Dehareng, F.; Grelet, C.; Oswald, I.P.J.A. Effects of Wheat Bran Applied to Maternal Diet on the Intestinal Architecture and Immune Gene Expression in Suckling Piglets. Animals 2020, 10, 2051. [CrossRef]
Hu, L.; Che, L.; Wu, C.; Curtasu, M.V.; Wu, F.; Fang, Z.; Lin, Y.; Xu, S.; Feng, B.; Li, J. Metabolomic profiling reveals the difference on reproductive performance between high and low lactational weight loss sows. Metabolites 2019, 9, 295. [CrossRef] [PubMed]
Jiang, X.; Lu, N.; Xue, Y.; Liu, S.; Lei, H.; Tu, W.; Lu, Y.; Xia, D. Crude fiber modulates the fecal microbiome and steroid hormones in pregnant Meishan sows. Gen. Comp. Endocrinol. 2019, 277, 141–147. [CrossRef] [PubMed]
Duncan, S.H.; Barcenilla, A.; Stewart, C.S.; Pryde, S.E.; Flint, H.J. Acetate utilization and butyryl coenzyme A (CoA): Acetate-CoA transferase in butyrate-producing bacteria from the human large intestine. Gen. Comp. Endocrinol. 2002, 68, 5186–5190. [CrossRef]
Duncan, S.H.; Louis, P.; Flint, H.J. Lactate-utilizing bacteria, isolated from human feces, that produce butyrate as a major fermentation product. Appl. Environ. Microbiol. 2004, 70, 5810–5817. [CrossRef]
Loisel, F.; Farmer, C.; Ramaekers, P.; Quesnel, H. Effects of high fiber intake during late pregnancy on sow physiology, colostrum production, and piglet performance1. J. Anim. Sci. 2013, 91, 5269–5279. [CrossRef]
Wang, J.; Qin, C.; He, T.; Qiu, K.; Sun, W.; Zhang, X.; Jiao, N.; Zhu, W.; Yin, J. Alfalfa-containing diets alter luminal microbiota structure and short chain fatty acid sensing in the caecal mucosa of pigs. J. Anim. Sci. Biotechnol. 2018, 9, 11. [CrossRef] [PubMed]
Pu, G.; Li, P.; Du, T.; Niu, Q.; Fan, L.; Wang, H.; Liu, H.; Li, K.; Niu, P.; Wu, C.; et al. Adding Appropriate Fiber in Diet Increases Diversity and Metabolic Capacity of Distal Gut Microbiota Without Altering Fiber Digestibility and Growth Rate of Finishing Pig. Front. Microbiol. 2020, 11. [CrossRef]
Agyekum, A.K.; Nyachoti, C.M. Nutritional and metabolic consequences of feeding high-fiber diets to swine: A review. Engineering 2017, 3, 716–725. [CrossRef]
Niu, Q.; Li, P.; Hao, S.; Zhang, Y.; Kim, S.W.; Li, H.; Ma, X.; Gao, S.; He, L.; Wu, W. Dynamic distribution of the gut microbiota and the relationship with apparent crude fiber digestibility and growth stages in pigs. Sci. Rep. 2015, 5, 9938. [CrossRef]
Kanengoni, A.T.; Chimonyo, M.; Tasara, T.; Cormican, P.; Chapwanya, A.; Ndimba, B.K.; Dzama, K. A comparison of faecal microbial populations of South African Windsnyer-type indigenous pigs (SAWIPs) and Large White× Landrace (LW × LR) crosses fed diets containing ensiled maize cobs. FEMS. Microbiol. Lett. 2015, 362, fnv100. [CrossRef]
Pajarillo, E.A.B.; Chae, J.P.; Balolong, M.P.; Kim, H.B.; Seo, K.S.; Kang, D.K. Pyrosequencing-based analysis of fecal microbial communities in three purebred pig lines. J. Microbiol. 2014, 52, 646–651. [CrossRef]
Lu, X.-M.; Lu, P.-Z.; Zhang, H. Bacterial communities in manures of piglets and adult pigs bred with different feeds revealed by 16S rDNA 454 pyrosequencing. J. Microbiol. Biotechnol. 2014, 98, 2657–2665. [CrossRef]
Leitzmann, M.F.; Moore, S.C.; Koster, A.; Harris, T.B.; Park, Y.; Hollenbeck, A.; Schatzkin, A. Waist circumference as compared with body-mass index in predicting mortality from specific causes. PLoS ONE 2011, 6, e18582. [CrossRef]
Jewell, K.A.; Scott, J.J.; Adams, S.M.; Suen, G. A phylogenetic analysis of the phylum Fibrobacteres. Syst. Appl. Microbiol. 2013, 36, 376–382. [CrossRef]
Ransom Jones, E.; Jones, D.L.; McCarthy, A.J.; McDonald, J.E. The Fibrobacteres: An important phylum of cellulose-degrading bacteria. Microbial. Ecol. 2012, 63, 267–281. [CrossRef]
Thomas, F.; Hehemann, J.H.; Rebuffet, E.; Czjzek, M.; Michel, G. Environmental and Gut Bacteroidetes: The Food Connection. Front. Microbiol. 2011, 2. [CrossRef] [PubMed]
Hung, D.-Y.; Cheng, Y.H.; Chen, W.J.; Hua, K.F.; Pietruszka, A.; Dybus, A.; Lin, C.-S.; Yu, Y.-H. Bacillus licheniformis-Fermented Products Reduce Diarrhea Incidence and Alter the Fecal Microbiota Community in Weaning Piglets. Animals 2019, 9, 1145. [CrossRef]
Xing, S.C.; Huang, C.B.; Mi, J.D.; Wu, Y.B.; Liao, X.D. Bacillus coagulans R11 maintained intestinal villus health and decreased intestinal injury in lead-exposed mice by regulating the intestinal microbiota and influenced the function of faecal microRNAs. Environ. Pollut. 2019, 255, 113139. [CrossRef]
Wang, T.; Teng, K.; Liu, Y.; Shi, W.; Zhang, J.; Dong, E.; Zhang, X.; Tao, Y.; Zhong, J. Lactobacillus plantarum PFM 105 Promotes Intestinal Development Through Modulation of Gut Microbiota in Weaning Piglets. Front. Microbiol. 2019, 10. [CrossRef]
Jiang, X.; Lu, N.; Zhao, H.; Yuan, H.; Xia, D.; Lei, H. The Microbiome–Metabolome Response in the Colon of Piglets Under the Status of Weaning Stress. Front. Microbiol. 2020, 11. [CrossRef]
Biddle, A.; Stewart, L.; Blanchard, J.; Leschine, S. Untangling the Genetic Basis of Fibrolytic Specialization by Lachnospiraceae and Ruminococcaceae in Diverse Gut Communities. Diversity 2013, 5, 627–640. [CrossRef]
