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Bacillus amyloliquefaciens and Saccharomyces cerevisiae feed supplements improve growth performance and gut mucosal architecture with modulations on cecal microbiota in red-feathered native chickens

  • Lee, Tzu-Tai (Department of Animal Science, National Chung Hsing University) ;
  • Chou, Chung-Hsi (Department of Veterinary Medicine, School of Veterinary Medicine, National Taiwan University) ;
  • Wang, Chinling (Department of Basic Sciences, College of Veterinary Medicine, Mississippi State University) ;
  • Lu, Hsuan-Ying (Department of Veterinary Medicine, School of Veterinary Medicine, National Taiwan University) ;
  • Yang, Wen-Yuan (Department of Veterinary Medicine, School of Veterinary Medicine, National Taiwan University)
  • Received : 2021.07.15
  • Accepted : 2021.11.06
  • Published : 2022.06.01

Abstract

Objective: The aim of study was to investigate the effects of in-feed supplementation of Bacillus amyloliquefaciens (BA) and Saccharomyces cerevisiae (SC) on growth performance, gut integrity, and microbiota modulations in red-feathered native chickens (RFCs). Methods: A total of 18,000 RFCs in a commercial farm were evenly assigned into two dietary treatments (control diet; 0.05% BA and 0.05% SC) by randomization and raised for 11 weeks in two separate houses. Fifty RFCs in each group were randomly selected and raised in the original house with the partition for performance evaluations at the age of 9 and 11 weeks. Six non-partitioned RFCs per group were randomly selected for analyses of intestinal architecture and 16S rRNA metagenomics. Results: Feeding BA and SC increased the body weight and body weight gain, significantly at the age of 11 weeks (p<0.05). The villus height/crypt ratio in the small intestines and Firmicutes to Bacteroidetes ratio were also notably increased (p<0.05). The supplementation did not disturb the microbial community structure but promote the featured microbial shifts characterized by the significant increments of Bernesiella, Prevotellaceae_NK3B31_group, and Butyrucimonas, following remarkable decrements of Bacteroides, Rikenellaceae_RC9_gut_group, and Succinatimonas in RFCs with growth benefits. Besides, functional pathways of peptidoglycan biosynthesis, nucleotide excision repair, glycolysis/gluconeogenesis, and aminoacyl transfer ribonucleic acid (tRNA) biosynthesis were significantly promoted (p<0.05). Conclusion: In-feed supplementation of BA and SC enhanced the growth performance, improved mucosal architectures in small intestines, and modulated the cecal microbiota and metabolic pathways in RFCs.

Keywords

Acknowledgement

The authors appreciate the support from the Department of Animal Science, National Chung Hsing University and Department of Veterinary Medicine, School of Veterinary Medicine, National Taiwan University.

References

  1. Roan SW, Fang WB, Hu CL, Wang BY. Carcase composition of taiwan simulated native chickens. Trop Anim Health Prod 1999;31:245-57. https://doi.org/10.1023/a:1005271211738
  2. Diaz Carrasco JM, Casanova NA, Fernandez Miyakawa ME. Microbiota, gut health and chicken productivity: What is the connection? Microorganisms 2019;7:374. https://doi.org/10.3390/microorganisms7100374
  3. Jha R, Das R, Oak S, Mishra P. Probiotics (direct-fed microbials) in poultry nutrition and their effects on nutrient utilization, growth and laying performance, and gut health: A systematic review. Animals (Basel) 2020;10:1863. https://doi.org/10.3390/ani10101863
  4. Abd El-Hack ME, El-Saadony MT, Shafi ME, et al. Probiotics in poultry feed: A comprehensive review. J Anim Physiol Anim Nutr (Berl) 2020;104:1835-50. https://doi.org/10.1111/jpn.13454
  5. Cao GT, Zhan XA, Zhang LL, Zeng XF, Chen AG, Yang CM. Modulation of broilers' caecal microflora and metabolites in response to a potential probiotic bacillus amyloliquefaciens. J Anim Physiol Anim Nutr (Berl) 2018;102:e909-e17. https://doi.org/10.1111/jpn.12856
  6. Hong Y, Cheng Y, Li Y, et al. Preliminary study on the effect of bacillus amyloliquefaciens tl on cecal bacterial community structure of broiler chickens. Biomed Res Int 2019;2019: Article ID 5431354. https://doi.org/10.1155/2019/5431354
  7. Li Y, Zhang H, Chen YP, et al. Bacillus amyloliquefaciens supplementation alleviates immunological stress in lipopolysaccharide-challenged broilers at early age. Poult Sci 2015;94:1504-11. https://doi.org/10.3382/ps/pev124
  8. Hong Y, Cheng Y, Li Y, et al. Preliminary study on the effect of bacillus amyloliquefaciens tl on cecal bacterial community structure of broiler chickens. Biomed Res Int 2019;2019:5431354. https://doi.org/10.1155/2019/5431354
  9. Jerzsele A, Szeker K, Csizinszky R, et al. Efficacy of protected sodium butyrate, a protected blend of essential oils, their combination, and bacillus amyloliquefaciens spore suspension against artificially induced necrotic enteritis in broilers. Poult Sci 2012;91:837-43. https://doi.org/10.3382/ps.2011-01853
  10. Ezema C, Ugwu CC. Yeast (saccharomyces cerevisiae) as a probiotic of choice for broiler production. In: Liong M-T, editor. Beneficial microorganisms in agriculture, aquaculture and other areas. Cham, Switzerland: Springer International Publishing; 2015. p. 59-79.
  11. Yang Y, Iji PA, Kocher A, Mikkelsen LL, Choct M. Effects of dietary mannanoligosaccharide on growth performance, nutrient digestibility and gut development of broilers given different cereal-based diets. J Anim Physiol Anim Nutr (Berl) 2008;92:650-9. https://doi.org/10.1111/j.1439-0396.2007.00761.x
  12. Froebel LK, Jalukar S, Lavergne TA, Lee JT, Duong T. Administration of dietary prebiotics improves growth performance and reduces pathogen colonization in broiler chickens. Poult Sci 2019;98:6668-76. https://doi.org/10.3382/ps/pez537
  13. Agus A, Planchais J, Sokol H. Gut microbiota regulation of tryptophan metabolism in health and disease. Cell Host Microbe 2018;23:716-24. https://doi.org/10.1016/j.chom.2018.05.003
  14. Yeoman CJ, Chia N, Jeraldo P, Sipos M, Goldenfeld ND, White BA. The microbiome of the chicken gastrointestinal tract. Anim Health Res Rev 2012;13:89-99. https://doi.org/10.1017/s1466252312000138
  15. Timmerman HM, Koning CJM, Mulder L, Rombouts FM, Beynen AC. Monostrain, multistrain and multispecies probiotics--a comparison of functionality and efficacy. Int J Food Microbiol 2004;96:219-33. https://doi.org/10.1016/j.ijfoodmicro.2004.05.012
  16. Lei X, Piao X, Ru Y, Zhang H, Peron A, Zhang H. Effect of bacillus amyloliquefaciens-based direct-fed microbial on performance, nutrient utilization, intestinal morphology and cecal microflora in broiler chickens. Asian-Australas J Anim Sci 2015;28:239-46. https://doi.org/10.5713/ajas.14.0330
  17. Zhang AW, Lee BD, Lee SK, et al. Effects of yeast (saccharomyces cerevisiae) cell components on growth performance, meat quality, and ileal mucosa development of broiler chicks. Poult Sci 2005;84:1015-21. https://doi.org/10.1093/ps/84.7.1015
  18. Markowiak P, Slizewska K, Nowak A, et al. Probiotic microorganisms detoxify ochratoxin a in both a chicken liver cell line and chickens. J Sci Food Agric 2019;99:4309-18. https://doi.org/10.1002/jsfa.9664
  19. Chen KL, Kho WL, You SH, Yeh RH, Tang SW, Hsieh CW. Effects of bacillus subtilis var. Natto and saccharomyces cerevisiae mixed fermented feed on the enhanced growth performance of broilers. Poult Sci 2009;88:309-15. https:// doi.org/10.3382/ps.2008-00224
  20. Wilson FD, Cummings TS, Barbosa TM, Williams CJ, Gerard PD, Peebles ED. Comparison of two methods for determination of intestinal villus to crypt ratios and documentation of early age-associated ratio changes in broiler chickens. Poult Sci 2018;97:1757-61. https://doi.org/10.3382/ps/pex349
  21. Aliakbarpour HR, Chamani M, Rahimi G, Sadeghi AA, Qujeq D. The bacillus subtilis and lactic acid bacteria probiotics influences intestinal mucin gene expression, histomorphology and growth performance in broilers. Asian-Australas J Anim Sci 2012;25:1285-93. https://doi.org/10.5713/ajas.2012.12110
  22. Caspary WF. Physiology and pathophysiology of intestinal absorption. Am J Clin Nutr 1992;55:299s-308s. https://doi.org/10.1093/ajcn/55.1.299s
  23. Langhout DJ, Schutte JB, Van Leeuwen P, Wiebenga J, Tamminga S. Effect of dietary high- and low-methylated citrus pectin on the activity of the ileal microflora and morphology of the small intestinal wall of broiler chicks. Br Poult Sci 1999;40:340-7. https://doi.org/10.1080/00071669987421
  24. Prakatur I, Miskulin M, Pavic M, et al. Intestinal morphology in broiler chickens supplemented with propolis and bee pollen. Animals (Basel) 2019;9:301. https://doi.org/10.3390/ani9060301
  25. Oakley BB, Lillehoj HS, Kogut MH, et al. The chicken gastrointestinal microbiome. FEMS Microbiol Lett 2014;360:100-12. https://doi.org/10.1111/1574-6968.12608
  26. Mancabelli L, Ferrario C, Milani C, et al. Insights into the biodiversity of the gut microbiota of broiler chickens. Environ Microbiol 2016;18:4727-38. https://doi.org/10.1111/1462-2920.13363
  27. Abdallah Ismail N, Ragab SH, Abd Elbaky A, Shoeib ARS, Alhosary Y, Fekry D. Frequency of firmicutes and bacteroidetes in gut microbiota in obese and normal weight egyptian children and adults. Arch Med Sci 2011;7:501-7. https://doi.org/10.5114/aoms.2011.23418
  28. Salaheen S, Kim SW, Haley BJ, Van Kessel JAS, Biswas D. Alternative growth promoters modulate broiler gut microbiome and enhance body weight gain. Front Microbiol 2017;8:2088. https://doi.org/10.3389/fmicb.2017.02088
  29. Manichanh C, Rigottier-Gois L, Bonnaud E, et al. Reduced diversity of faecal microbiota in crohn's disease revealed by a metagenomic approach. Gut 2006;55:205-11. https://doi.org/10.1136/gut.2005.073817
  30. Jayaraman S, Thangavel G, Kurian H, Mani R, Mukkalil R, Chirakkal H. Bacillus subtilis pb6 improves intestinal health of broiler chickens challenged with clostridium perfringensinduced necrotic enteritis. Poult Sci 2013;92:370-4. https://doi.org/10.3382/ps.2012-02528
  31. Ubeda C, Bucci V, Caballero S, et al. Intestinal microbiota containing barnesiella species cures vancomycin-resistant enterococcus faecium colonization. Infect Immun 2013;81:965-73. https://doi.org/10.1128/iai.01197-12
  32. Presley LL, Wei B, Braun J, Borneman J. Bacteria associated with immunoregulatory cells in mice. Appl Environ Microbiol 2010;76:936-41. https://doi.org/10.1128/aem.01561-09
  33. Weiss GA, Chassard C, Hennet T. Selective proliferation of intestinal barnesiella under fucosyllactose supplementation in mice. Br J Nutr 2014;111:1602-10. https://doi.org/10.1017/s0007114513004200
  34. Zhang L, Wu W, Lee YK, Xie J, Zhang H. Spatial heterogeneity and co-occurrence of mucosal and luminal microbiome across swine intestinal tract. Front Microbiol 2018;9:48. https://doi.org/10.3389/fmicb.2018.00048
  35. Du CT, Gao W, Ma K, et al. Microrna-146a deficiency protects against listeria monocytogenes infection by modulating the gut microbiota. Int J Mol Sci 2018;19:993. https://doi.org/10.3390/ijms19040993
  36. Jiang X, Lu N, Zhao H, Yuan H, Xia D, Lei H. The microbiomemetabolome response in the colon of piglets under the status of weaning stress. Front Microbiol 2020;11:2055. https://doi.org/10.3389/fmicb.2020.02055
  37. Xiong X, Zhou J, Liu H, Tang Y, Tan B, Yin Y. Dietary lysozyme supplementation contributes to enhanced intestinal functions and gut microflora of piglets. Food Funct 2019;10:1696-706. https://doi.org/10.1039/c8fo02335b
  38. Wang W, Wang Y, Hao X, et al. Dietary fermented soybean meal replacement alleviates diarrhea in weaned piglets challenged with enterotoxigenic escherichia coli k88 by modulating inflammatory cytokine levels and cecal microbiota composition. BMC Vet Res 2020;16:245. https://doi.org/10.1186/s12917-020-02466-5
  39. Fu X, Liu Z, Zhu C, Mou H, Kong Q. Nondigestible carbohydrates, butyrate, and butyrate-producing bacteria. Crit Rev Food Sci Nutr 2019;59:S130-52. https://doi.org/10.1080/10408398.2018.1542587
  40. Lee H, Lee Y, Kim J, et al. Modulation of the gut microbiota by metformin improves metabolic profiles in aged obese mice. Gut Microbes 2018;9:155-65. https://doi.org/10.1080/19490976.2017.1405209
  41. Hooper LV, Midtvedt T, Gordon JI. How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu Rev Nutr 2002;22:283-307. https://doi.org/10.1146/annurev.nutr.22.011602.092259
  42. Niu J, Zhang J, Wei L, Ma X, Zhang W, Nie C. Cottonseed meal fermented by candida tropical reduces the fat deposition in white-feather broilers through cecum bacteria-host metabolic cross-talk. Appl Microbiol Biotechnol 2020;104:4345-57. https://doi.org/10.1007/s00253-020-10538-7
  43. Gao X, Chang S, Liu S, et al. Correlations between α-linolenic acid-improved multitissue homeostasis and gut microbiota in mice fed a high-fat diet. mSystems 2020;5:e00391-20. https://doi.org/10.1128/mSystems.00391-20
  44. Hippe H, Hagelstein A, Kramer I, Swiderski J, Stackebrandt E. Phylogenetic analysis of formivibrio citricus, propionivibrio dicarboxylicus, anaerobiospirillum thomasii, succinimonas amylolytica and succinivibrio dextrinosolvens and proposal of succinivibrionaceae fam. Nov. Int J Syst Bacteriol 1999;49:779-82. https://doi.org/10.1099/00207713-49-2-779
  45. Morotomi M, Nagai F, Watanabe Y, Tanaka R. Succinatimonas hippei gen. Nov., sp. Nov., isolated from human faeces. Int J Syst Evol Microbiol 2010;60:1788-93. https://doi.org/10.1099/ijs.0.015958-0
  46. Li M, Wang B, Zhang M, et al. Symbiotic gut microbes modulate human metabolic phenotypes. Proc Natl Acad Sci USA 2008;105:2117-22. https://doi.org/10.1073/pnas.0712038105
  47. Martinez B, Rodriguez A, Kulakauskas S, Chapot-Chartier MP. Cell wall homeostasis in lactic acid bacteria: Threats and defences. FEMS Microbiol Rev 2020;44:538-64. https://doi.org/10.1093/femsre/fuaa021
  48. van Baarlen P, Wells JM, Kleerebezem M. Regulation of intestinal homeostasis and immunity with probiotic lactobacilli. Trends Immunol 2013;34:208-15. https://doi.org/10.1016/j.it.2013.01.005
  49. RajBhandary UL, Soll D. Aminoacyl-trnas, the bacterial cell envelope, and antibiotics. Proc Natl Acad Sci USA 2008;105:5285-6. https://doi.org/10.1073/pnas.0801193105
  50. Shepherd J, Ibba M. Lipid ii-independent trans editing of mischarged trnas by the penicillin resistance factor murm. J Biol Chem 2013;288:25915-23. https://doi.org/10.1074/jbc.M113.479824
  51. Jager M, Blokzijl F, Kuijk E, et al. Deficiency of nucleotide excision repair is associated with mutational signature observed in cancer. Genome Res 2019;29:1067-77. https://doi.org/10.1101/gr.246223.118
  52. Scharer OD. Nucleotide excision repair in eukaryotes. Cold Spring Harb Perspect Biol 2013;5:a012609. https://doi.org/10.1101/cshperspect.a012609