Supplementation of multi-enzymes alone or combined with inactivated Lactobacillus benefits growth performance and gut microbiota in broilers fed wheat diets.
Gao, Qingtao; Wang, Yanchun; Li, Jiahenget al.
2022 • In Frontiers in Microbiology, 13, p. 927932
[en] The effects of multi-enzymes mixture supplementation or combination with inactivated Lactobacillus on growth performance, intestinal barrier, and cecal microbiota were investigated in broilers at the age of 15-42 days fed a wheat-based diet. A total of 576 broilers (12 broilers/cage; n = 12) were used and divided into four groups and randomly allotted to four experimental diets throughout grower (15-28 days of age) and finisher (29-42 days of age) phases. Diets consisted of a corn-soybean meal-based diet (BD), a wheat-soybean meal-based diet (WD), and WD supplemented multi-enzymes (WED) or combined with inactivated Lactobacillus (WEPD). The results showed that the average daily gain (ADG) and body weight (BW) were reduced in broilers fed WD diet compared with those fed BD diet during the grower period (P < 0.05). Broilers in the WED or WEPD group had higher ADG and BW during the grower period (P < 0.05) and had a lower feed-to-gain ratio (F/G) compared to broilers in the WD group during the grower and overall periods (P < 0.05). Improved expression of intestinal barrier genes (claudin-1, ZO-1, and mucin-2) was observed in WEPD compared to the BD or WD group (P < 0.05). Compared to the BD group, the WD group decreased the abundance of Oscillospira, norank_f__Erysipelotrichaceae, and Peptococcus, which are related to anti-inflammatory function and BW gain. The WD also increased Bifidobacterium and some short-chain fatty acid (SCFA)-producing bacteria (Anaerotruncus, Blautia, and Oscillibacter), and Barnesiella, which were presumed as "harmful microbes" [false discovery rate (FDR) < 0.05]. WED and WEPD groups, respectively, improved Bilophila and Eubacterium_hallii_group compared with those in the WD group (FDR < 0.05). In addition, the Enterococcus abundance was reduced in the WEPD group compared to the WD group (FDR < 0.05). Higher acetate and total SCFA concentrations were observed (P < 0.05) among broilers who received a WD diet. Compared with the WD group, the WED or WEPD group further increased cecal propionate content (P < 0.05) and tended to improve butyrate concentration. These results suggested that supplemental multi-enzymes alone and combined with inactivated Lactobacillus could improve the growth performance based on the wheat-based diet and offer additional protective effects on the intestinal barrier function of broilers.
Disciplines :
Animal production & animal husbandry
Author, co-author :
Gao, Qingtao; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China
Wang, Yanchun; Yunnan Provincial Key Laboratory of Animal Nutrition and Feed Science, College of Animal Science and Technology, Yunnan Agricultural University, Kunming, China
Li, Jiaheng ; Université de Liège - ULiège > TERRA Research Centre ; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China
Bai, Guosong; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China
Liu, Lei; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China
Zhong, Ruqing; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China
Ma, Teng; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China
Pan, Hongbin; Yunnan Provincial Key Laboratory of Animal Nutrition and Feed Science, College of Animal Science and Technology, Yunnan Agricultural University, Kunming, China
Zhang, Hongfu; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China
Language :
English
Title :
Supplementation of multi-enzymes alone or combined with inactivated Lactobacillus benefits growth performance and gut microbiota in broilers fed wheat diets.
This work was supported by the China Agriculture Research System of MOF and MARA (CARS-41) and the State Key Laboratory of Animal Nutrition (2004DA125184G2102).
Adeola O. Cowieson A. J. (2011). Board-invited review: opportunities and challenges in using exogenous enzymes to improve nonruminant animal production. J. Anim. Sci. 89 3189–3218. 10.2527/jas.2010-3715 21512114
Alagawany M. Abd El-Hack M. E. Farag M. R. Sachan S. Karthik K. Dhama K. (2018). The use of probiotics as eco-friendly alternatives for antibiotics in poultry nutrition. Environ. Sci. Pollut. Res. Int. 25 10611–10618. 10.1007/s11356-018-1687-x 29532377
AOAC (2012). Official methods of analysis, 19th ed. Arlington, VA: Association of Official Agricultural Chemists.
Ball M. E. Owens B. McCracken K. J. (2013). The effect of variety and growing conditions on the chemical composition and nutritive value of wheat for broilers. Asian-Australas. J. Anim. Sci. 26 378–385. 10.5713/ajas.2012.12180 25049800
Banerjee S. Sindberg G. Wang F. Meng J. Sharma U. Zhang L. et al. (2016). Opioid-induced gut microbial disruption and bile dysregulation leads to gut barrier compromise and sustained systemic inflammation. Mucosal. Immunol. 9 1418–1428. 10.1038/mi.2016.9 26906406
Bhogoju S. Khwatenge C. N. Taylor-Bowden T. Akerele G. Kimathi B. M. Donkor J. et al. (2021). Effects of Lactobacillus reuteri and Streptomyces coelicolor on growth performance of broiler chickens. Microorganisms 9 1314–1325. 10.3390/microorganisms9061341 34205811
Bunesova V. Lacroix C. Schwab C. (2018). Mucin cross-feeding of infant Bifidobacteria and Eubacterium hallii. Microb. Ecol. 75 228–238. 10.1007/s00248-017-1037-4 28721502
Choct M. Hughes R. J. Trimble R. P. Angkanaporn K. Annison G. (1995). Non-starch polysaccharide-degrading enzymes increase the performance of broiler chickens fed wheat of low apparent metabolizable energy. J. Nutr. 125 485–492. 10.1093/jn/125.3.485 7876924
Choct M. Kocher A. Waters D. L. E. Petterson D. Ross G. (2004). A comparison of three xylanases on the nutritive value of two wheats for broiler chickens. Br. J. Nutr. 92 53–61. 10.1079/BJN20041166 15230987
Crisol-Martínez E. Stanley D. Geier M. S. Hughes R. J. Moore R. J. (2017). Sorghum and wheat differentially affect caecal microbiota and associated performance characteristics of meat chickens. PeerJ. 5:e3071. 10.7717/peerj.3071 28286717
De Maesschalck C. Eeckhaut V. Maertens L. De Lange L. Marchal L. Nezer C. et al. (2015). Effects of xylo-oligosaccharides on broiler chicken performance and microbiota. Appl. Environ. Microbiol. 81 5880–5888. 10.1128/AEM.01616-15 26092452
Díaz Carrasco J. M. Redondo E. A. Pin Viso N. D. Redondo L. M. Farber M. D. Fernández Miyakawa M. E. (2018). Tannins and bacitracin differentially modulate gut microbiota of broiler chickens. Biomed. Res. Int. 2018:1879168. 10.1155/2018/1879168 29682522
Engevik M. A. Luck B. Visuthranukul C. Ihekweazu F. D. Engevik A. C. Shi Z. et al. (2021). Human-derived Bifidobacterium dentium modulates the mammalian serotonergic system and gut-brain axis. Cell Mol. Gastroenterol. Hepatol. 11 221–248. 10.1016/j.jcmgh.2020.08.002 32795610
Fraumene C. Manghina V. Cadoni E. Marongiu F. Abbondio M. Serra M. et al. (2018). Caloric restriction promotes rapid expansion and long-lasting increase of Lactobacillus in the rat fecal microbiota. Gut Microbes 9 104–114. 10.1080/19490976.2017.1371894 28891744
Gonzalez-Ortiz G. Sola-Oriol D. Martinez-Mora M. Perez J. F. Bedford M. R. (2017). Response of broiler chickens fed wheat-based diets to xylanase supplementation. Poult. Sci. 96 2776–2785. 10.3382/ps/pex092 28431146
Han H. Zhong R. Zhou Y. Xiong B. Chen L. Jiang Y. et al. (2021). Hydroxytyrosol benefits boar semen quality via improving gut microbiota and blood metabolome. Front. Nutr. 8:815922. 10.3389/fnut.2021.815922 35111800
Hu S. Xu Y. Gao X. Li S. Jiang W. Liu Y. et al. (2019). Long-chain bases from sea cucumber alleviate obesity by modulating gut microbiota. Mar. Drugs. 17:455. 10.3390/md17080455 31374958
Huang P. Zhang Y. Xiao K. Jiang F. Wang H. Tang D. et al. (2018). The chicken gut metagenome and the modulatory effects of plant-derived benzylisoquinoline alkaloids. Microbiome 6:211. 10.1186/s40168-018-0590-5 30482240
Incharoen T. Charoensook R. Onoda S. Tatrakoon W. Numthuam S. Pechkong T. (2019). The effects of heat-killed Lactobacillus plantarum L-137 supplementation on growth performance, intestinal morphology, and immune-related gene expression in broiler chickens. 257:114272. 10.1016/j.anifeedsci.2019.114272
Kareem K. Y. Loh T. C. Foo H. L. Asmara S. A. Akit H. (2017). Influence of postbiotic RG14 and inulin combination on cecal microbiota, organic acid concentration, and cytokine expression in broiler chickens. Poult. Sci. 96 966–975. 10.3382/ps/pew362 28339522
Khonyoung D. Yamauchi K.-E. (2019). Improved growth performance due to hypertrophied intestinal absorptive epithelial cells by heat-killed Lactobacillus sakei HS-1 in broiler chickens1. J. Anim. Sci. 97 2066–2075. 10.1093/jas/skz075 30788512
Kiarie E. Romero L. F. Ravindran V. (2014). Growth performance, nutrient utilization, and digesta characteristics in broiler chickens fed corn or wheat diets without or with supplemental xylanase. Poult. Sci. 93 1186–1196. 10.3382/ps.2013-03715 24795311
Kim H. J. Kim D. Kim K. W. Lee S. H. Jang A. (2021). Comparative analysis of the gut microbiota of mice fed a diet supplemented with raw and cooked beef loin powder. Sci. Rep. 11 11489–11489. 10.1038/s41598-021-90461-7 34075086
Knudsen K. E. B. (2014). Fiber and nonstarch polysaccharide content and variation in common crops used in broiler diets. Poult. Sci. 93 2380–2393. 10.3382/ps.2014-03902 25012855
Liang Y. N. Yu J. G. Zhang D. B. Zhang Z. Ren L. L. Li L. H. et al. (2019). Indigo naturalis ameliorates dextran sulfate sodium-induced colitis in mice by modulating the intestinal microbiota community. Molecules 24:4086. 10.3390/molecules24224086 31726738
Livak K. J. Schmittgen T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25 402–408. 10.1006/meth.2001.1262 11846609
Masey-O’Neill H. V. Singh M. Cowieson A. J. (2014). Effects of exogenous xylanase on performance, nutrient digestibility, volatile fatty acid production and digestive tract thermal profiles of broilers fed on wheat- or maize-based diet. Br. Poult. Sci. 55 351–359. 10.1080/00071668.2014.898836 24579789
McCafferty K. W. Bedford M. R. Kerr B. J. Dozier W. A. (2019b). Effects of cereal grain source and supplemental xylanase concentrations on broiler growth performance and cecal volatile fatty acid concentrations from 1 to 40 d of age. Poult. Sci. 98 2866–2879. 10.3382/ps/pez032 30805626
McCafferty K. W. Bedford M. R. Kerr B. J. Dozier W. A. (2019a). Effects of age and supplemental xylanase in corn- and wheat-based diets on cecal volatile fatty acid concentrations of broilers1. Poult. Sci. 98 4787–4800. 10.3382/ps/pez194 31065717
Munyaka P. M. Nandha N. K. Kiarie E. Nyachoti C. M. Khafipour E. (2016). Impact of combined β-glucanase and xylanase enzymes on growth performance, nutrients utilization and gut microbiota in broiler chickens fed corn or wheat-based diets. Poult. Sci. 95 528–540. 10.3382/ps/pev333 26574039
Musigwa S. Cozannet P. Morgan N. Swick R. A. Wu S. B. (2021). Multi-carbohydrase effects on energy utilization depend on soluble non-starch polysaccharides-to-total non-starch polysaccharides in broiler diets. Poult. Sci. 100 788–796. 10.1016/j.psj.2020.10.038 33518133
National Research Council (1994). Nutrient Requirements of Poultry. 9th Edn. Washington, DC: The National Academies Press.
Nguyen H. T. Bedford M. R. Wu S. B. Morgan N. K. (2021). Soluble non-starch polysaccharide modulates broiler gastrointestinal tract environment. Poult. Sci. 100:101183. 10.1016/j.psj.2021.101183 34198096
Ozato N. Saito S. Yamaguchi T. Katashima M. Tokuda I. Sawada K. et al. (2019). Blautia genus associated with visceral fat accumulation in adults 20-76 years of age. NPJ Biofilms Microb. 5:28. 10.1038/s41522-019-0101-x 31602309
Raza A. Bashir S. Tabassum R. (2019). An update on carbohydrases: growth performance and intestinal health of poultry. Heliyon 5:e01437. 10.1016/j.heliyon.2019.e01437 31008387
Rebolé A. Ortiz L. T. Rodríguez M. L. Alzueta C. Treviño J. Velasco S. (2010). Effects of inulin and enzyme complex, individually or in combination, on growth performance, intestinal microflora, cecal fermentation characteristics, and jejunal histomorphology in broiler chickens fed a wheat- and barley-based diet. Poult. Sci. 89 276–286. 10.3382/ps.2009-00336 20075280
Rehman A. Arif M. Sajjad N. Al-Ghadi M. Q. Alagawany M. Abd El-Hack M. E. et al. (2020). Dietary effect of probiotics and prebiotics on broiler performance, carcass, and immunity. Poult. Sci. 99 6946–6953. 10.1016/j.psj.2020.09.043 33248610
Romero L. F. Sands J. S. Indrakumar S. E. Plumstead P. W. Dalsgaard S. Ravindran V. (2014). Contribution of protein, starch, and fat to the apparent ileal digestible energy of corn- and wheat-based broiler diets in response to exogenous xylanase and amylase without or with protease. Poult. Sci. 93 2501–2513. 10.3382/ps.2013-03789 25071229
Salazar N. Gueimonde M. Hernández-Barranco A. M. Ruas-Madiedo P. de los Reyes-Gavilán C. G. (2008). Exopolysaccharides produced by intestinal Bifidobacterium strains act as fermentable substrates for human intestinal bacteria. Appl. Environ. Microbiol. 74 4737–4745. 10.1128/AEM.00325-08 18539803
Santoru M. L. Piras C. Murgia A. Palmas V. Camboni T. Liggi S. et al. (2017). Cross sectional evaluation of the gut-microbiome metabolome axis in an Italian cohort of IBD patients. Sci. Rep. 7 9523–9523. 10.1038/s41598-017-10034-5 28842640
Smeets N. Nuyens F. Van Campenhout L. Delezie E. Niewold T. A. (2018). Interactions between the concentration of non-starch polysaccharides in wheat and the addition of an enzyme mixture in a broiler digestibility and performance trial. Poult. Sci. 97 2064–2070. 10.3382/ps/pey038 29471412
Smeets N. Nuyens F. Van Campenhout L. Niewold T. (2014). Variability in the in vitro degradation of non-starch polysaccharides from wheat by feed enzymes. Anim. Feed Sci. Technol. 187 110–114. 10.1016/j.anifeedsci.2013.10.020
Stanley D. Denman S. E. Hughes R. J. Geier M. S. Crowley T. M. Chen H. et al. (2012). Intestinal microbiota associated with differential feed conversion efficiency in chickens. Appl. Microbiol. Biotechnol. 96 1361–1369. 10.1007/s00253-011-3847-5 22249719
Taciak M. Barszcz M. Tuśnio A. Pastuszewska B. (2015). Interactive effects of indigestible carbohydrates, protein type, and protein level on biomarkers of large intestine health in rats. PLoS One 10:e0142176. 10.1371/journal.pone.0142176 26536028
Tang S. Zhang S. Zhong R. Su D. Xia B. Liu L. et al. (2021a). Time-course alterations of gut microbiota and short-chain fatty acids after short-term lincomycin exposure in young swine. Appl. Microbiol. Biotechnol. 105 8441–8456. 10.1007/s00253-021-11627-x 34651253
Tang S. Zhong R. Yin C. Su D. Xie J. Chen L. et al. (2021b). Exposure to high aerial ammonia causes hindgut dysbiotic microbiota and alterations of microbiota-derived metabolites in growing pigs. Front. Nutr. 8:689818. 10.3389/fnut.2021.689818 34179063
Tiwari U. P. Chen H. Kim S. W. Jha R. (2018). Supplemental effect of xylanase and mannanase on nutrient digestibility and gut health of nursery pigs studied using both in vivo and in vitro models. Anim. Feed Sci. Technol. 245 77–90. 10.1016/j.anifeedsci.2018.07.002
Tornavaca O. Chia M. Dufton N. Almagro L. O. Conway D. E. Randi A. M. et al. (2015). ZO-1 controls endothelial adherens junctions, cell-cell tension, angiogenesis, and barrier formation. J. Cell Biol. 208 821–838. 10.1083/jcb.201404140 25753039
Torok V. A. Hughes R. J. Mikkelsen L. L. Perez-Maldonado R. Balding K. MacAlpine R. et al. (2011). Identification and characterization of potential performance-related gut microbiotas in broiler chickens across various feeding trials. Appl. Environ. Microbiol. 77 5868–5878. 10.1128/AEM.00165-11 21742925
Turnbaugh P. J. Ridaura V. K. Faith J. J. Rey F. E. Knight R. Gordon J. I. (2009). The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci. Transl. Med. 1:6ra14. 10.1126/scitranslmed.3000322 20368178
Umare V. Pradhan V. Nadkar M. Rajadhyaksha A. Patwardhan M. Ghosh K. K. et al. (2014). Effect of proinflammatory cytokines (IL-6, TNF-α, and IL-1β) on clinical manifestations in Indian SLE patients. Mediators Inflamm. 2014:385297. 10.1155/2014/385297 25548434
Wang J. Ji H. Wang S. Liu H. Zhang W. Zhang D. et al. (2018). Probiotic promotes intestinal barrier function by strengthening the epithelium and modulating gut microbiota. Front. Microbiol. 9:1953. 10.3389/fmicb.2018.01953 30197632
Wang Q. Garrity G. M. Tiedje J. M. Cole J. R. (2007). Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73 5261–5267. 10.1128/AEM.00062-07 17586664
Wang T. Yao W. Li J. Shao Y. He Q. Xia J. et al. (2020). Dietary garcinol supplementation improves diarrhea and intestinal barrier function associated with its modulation of gut microbiota in weaned piglets. J. Anim. Sci. Biotechnol. 11 12–24. 10.1186/s40104-020-0426-6 32140225
Wang J. Liu S. Ma J. Piao X. (2021b). Changes in growth performance and ileal microbiota composition by xylanase supplementation in broilers fed wheat-based diets. Front. Microbiol. 12:706396. 10.3389/fmicb.2021.706396 34335542
Wang J. Cao H. Bao C. Liu Y. Dong B. Wang C. et al. (2021a). Effects of xylanase in corn- or wheat-based diets on cecal microbiota of broilers. Front. Microbiol. 12:757066. 10.3389/fmicb.2021.757066 34721363
Wang Y. Heng C. Zhou X. Cao G. Jiang L. Wang J. et al. (2021c). Supplemental DSM 29784 and enzymes, alone or in combination, as alternatives for antibiotics to improve growth performance, digestive enzyme activity, anti-oxidative status, immune response and the intestinal barrier of broiler chickens. Br. J. Nutr. 125 494–507. 10.1017/S0007114520002755 32693847
Ward N. E. (2021). Debranching enzymes in corn-soybean meal-based poultry feeds: a review. Poult. Sci. 100 765–775. 10.1016/j.psj.2020.10.074 33518131
Xiong X. Tan B. Song M. Ji P. Kim K. Yin Y. et al. (2019). Nutritional intervention for the intestinal development and health of weaned pigs. Front. Vet. Sci. 6:46–59. 10.3389/fvets.2019.00046 30847348
Zhang L. Gao L. Chen L. Zhong R. Zhang H. (2017). Optimization of non-starch polysaccharide enzymes of corn-soybean-diets and wheat-soybean diets for growing pig using in vitro method. Chin. J. Anim. Vet. Sci. 48 1468–1480.
Zhang S. Zhong G. Shao D. Wang Q. Hu Y. Wu T. et al. (2021). Dietary supplementation with Bacillus subtilis promotes growth performance of broilers by altering the dominant microbial community. Poult. Sci. 100, 100935–100947. 10.1016/j.psj.2020.12.032 33652528
Zhao W. Sun Z. Wang X. Fu L. Liang H. Zhen Y. (2016). Effect of inactivated Lactobacillus cultures on growth performance, cecal microflora and serum biochemical indexes of broilers. Chin. J. Vet. Sci. 36, 1440–1445. 10.16303/j.cnki.1005-4545.2016.08.33
Zhu C. Gong L. Huang K. Li F. Tong D. Zhang H. (2020). Effect of heat-inactivated compound probiotics on growth performance, plasma biochemical indices, and cecal microbiome in Yellow-Feathered broilers. Front. Microbiol. 11:585623. 10.3389/fmicb.2020.585623 33193234
