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Linking growth performance and carcass traits with enterotypes in Muscovy ducks

  • Qian Fan (College of Animal Sciences & Technology, Zhejiang A & F University) ;
  • Yini Xu (College of Animal Sciences & Technology, Zhejiang A & F University) ;
  • Yingping Xiao (State Key Laboratory of Hazard Factors and Risk Prevention and Control of Agricultural Product Quality and Safety, Institute of Agro-product Safety and Nutrition, Zhejiang Academy of Agricultural Science) ;
  • Caimei Yang (College of Animal Sciences & Technology, Zhejiang A & F University) ;
  • Wentao Lyu (State Key Laboratory of Hazard Factors and Risk Prevention and Control of Agricultural Product Quality and Safety, Institute of Agro-product Safety and Nutrition, Zhejiang Academy of Agricultural Science) ;
  • Hua Yang (State Key Laboratory of Hazard Factors and Risk Prevention and Control of Agricultural Product Quality and Safety, Institute of Agro-product Safety and Nutrition, Zhejiang Academy of Agricultural Science)
  • Received : 2023.11.11
  • Accepted : 2024.03.20
  • Published : 2024.07.01

Abstract

Objective: Enterotypes (ETs) are the clustering of gut microbial community structures, which could serve as indicators of growth performance and carcass traits. However, ETs have been sparsely investigated in waterfowl. The objective of this study was to identify the ileal ETs and explore the correlation of the ETs with growth performance and carcass traits in Muscovy ducks. Methods: A total of 200 Muscovy ducks were randomly selected from a population of 5,000 ducks at 70-day old, weighed and slaughtered. The growth performance and carcass traits, including body weight, dressed weight and evidenced weight, dressed percentage, percentage of apparent yield, breast muscle weight, leg muscle weight, percentage of leg muscle and percentage of breast muscle, were determined. The contents of ileum were collected for the isolation of DNA and 16S rRNA gene sequencing. The ETs were identified based on the 16S rRNA gene sequencing data and the correlation of the ETs with growth performance and carcass traits was performed by Spearman correlation analysis. Results: Three ETs (ET1, ET2, and ET3) were observed in the ileal microbiota of Muscovy ducks with significant differences in number of features and α-diversity among these ETs (p<0.05). Streptococcus, Candida Arthritis, and Bacteroidetes were the presentative genus in ET1 to ET3, respectively. Correlation analysis revealed that Lactococcus and Bradyrhizobium were significantly correlated with percentage of eviscerated yield and leg muscle weight (p<0.05) while ETs were found to have a close association with percentage of eviscerated yield, leg muscle weight, and percentage of leg muscle in Muscovy ducks. However, the growth performance of ducks with different ETs did not show significant difference (p>0.05). Lactococcus were found to be significantly correlated with leg muscle weight, dressed weight, and percentage of eviscerated yield. Conclusion: Our findings revealed a substantial variation in carcass traits associated with ETs in Muscovy ducks. It is implied that ETs might have the potential to serve as a valuable biomarker for assessing duck carcass traits. It would provide novel insights into the interaction of gut microbiota with growth performance and carcass traits of ducks.

Keywords

Acknowledgement

This work was supported by the National Natural Science Foundation of China (32202704) and China Agriculture Research System of MOF and MARA (CARS-42-27).

References

  1. Qian Y, Song K, Hu T, Ying T. Environmental status of livestock and poultry sectors in China under current transformation stage. Sci Total Environ 2018;622-3:702-9. https://doi.org/10.1016/j.scitotenv.2017.12.045
  2. Deng MT, Zhu F, Yang YZ, et al. Genome-wide association study reveals novel loci associated with body size and carcass yields in Pekin ducks. BMC Genomics 2019;20:1 https://doi.org/10.1186/s12864-018-5379-1
  3. Fu Z, Yang H, Xiao Y, et al. Ileal microbiota alters the immunity statues to affect body weight in muscovy ducks. Front Immunol 2022;13:844102. https://doi.org/10.3389/fimmu.2022.844102
  4. Khajeh Bami M, Afsharmanesh M, Ebrahimnejad H. Effect of dietary bacillus coagulans and different forms of zinc on performance intestinal microbiota carcass and meat quality of broiler chickens. Probiotics Antimicrob Proteins 2020;12:461-72. https://doi.org/10.1007/s12602-019-09558-1
  5. Janssen AWF, Kersten S. The role of the gut microbiota in metabolic health. FASEB J 2015;29:3111-23. https://doi.org/10.1096/fj.14-269514
  6. Wei RX, Ye FJ, He F, et al. Comparison of overfeeding effects on gut physiology and microbiota in two goose breeds. Poult Sci 2021;100:100960. https://doi.org/10.1016/j.psj.2020.12.057
  7. Wang S, Chen L, He M, et al. Different rearing conditions alter gut microbiota composition and host physiology in Shaoxing ducks. Sci Rep 2018;8:7387 https://doi.org/10.1038/s41598-018-25760-7
  8. Ma L, Lyu W, Zeng T, et al. Duck gut metagenome reveals the microbiome signatures linked to intestinal regional, temporal development, and rearing condition. iMeta 2024;e198. https://doi.org/10.1002/imt2.198
  9. Lyu W, Yang H, Li N, et al. Molecular characterization, developmental expression, and modulation of occludin by early intervention with Clostridium butyricum in Muscovy ducks. Poult Sci 2021;100:101271. https://doi.org/10.1016/j.psj.2021.101271
  10. Arumugam M, Raes J, Pelletier E, et al. Enterotypes of the human gut microbiome. Nature 2011;473:174-80. https://doi.org/10.1038/nature09944
  11. Wu GD, Chen J, Hoffmann C, et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 2011;334:105-8. https://doi.org/10.1126/science.1208344
  12. Li JP, Wu QF, Ma SC, et al. Effect of feed restriction on the intestinal microbial community structure of growing ducks. Arch Microbiol 2022;204:85. https://doi.org/10.1007/s00203-021-02636-5
  13. Yatsunenko T, Rey FE, Manary MJ, et al. Human gut microbiome viewed across age and geography. Nature 2012;486:222-7. https://doi.org/10.1038/nature11053
  14. Cheng M, Ning K. Stereotypes about enterotype: the old and new ideas. Genomics Proteomics Bioinformatics 2019;17:4-12. https://doi.org/10.1016/j.gpb.2018.02.004
  15. Moeller AH, Degnan PH, Pusey AE, Wilson ML, Hahn BH, Ochman H. Chimpanzees and humans harbour compositionally similar gut enterotypes. Nat Commun 2012;3:1179. https://doi.org/10.1038/ncomms2159
  16. Fan C, Zhang L, Fu H, et al. Enterotypes of the gut microbial community and their response to plant secondary compounds in plateau pikas. Microorganisms 2020;8:1311. https://doi.org/10.3390/microorganisms8091311
  17. Guo N, Wu Q, Shi F, et al. Seasonal dynamics of diet-gut microbiota interaction in adaptation of yaks to life at high altitude. NPJ Biofilms Microbiomes 2021;7:38. https://doi.org/10.1038/s41522-021-00207-6
  18. Christensen L, Roager HM, Astrup A, Hjorth MF. Microbial enterotypes in personalized nutrition and obesity management. Am J Clin Nutr 2018;108:645-51. https://doi.org/10.1093/ajcn/nqy175
  19. Lyu W, Liu X, Lu L, et al. Cecal microbiota modulates fat deposition in muscovy ducks. Front Vet Sci 2021;8:609348. https://doi.org/10.3389/fvets.2021.609348
  20. Ministry of Agriculture and Rural Development. Poultry production performance nomenclature and statistical methods of measurement. Beijing, China: Ministry of Agriculture and Rural Development; 2020. NY/T 823-2020.
  21. Xiao Y, Kong F, Xiang Y, et al. Comparative biogeography of the gut microbiome between Jinhua and Landrace pigs. Sci Rep 2018;8:5985. https://doi.org/10.1038/s41598-018-24289-z
  22. Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 2007;73:5261-7. https://doi.org/10.1128/AEM.00062-07
  23. Kruskal WH, Wallis WA. Use of ranks in one-criterion variance analysis. J Am Stat Assoc 1952;47:583-621. https://doi.org/10.1080/01621459.1952.10483441
  24. Best DJ, Roberts DE. The upper tail probabilities of spearman's rho. J R Stat Soc Ser C Appl Stat 2018;24:377-9. https://doi.org/10.2307/2347111
  25. Chang F, He S, Dang C. Assisted selection of biomarkers by linear discriminant analysis effect size (LEfSe) in microbiome data. J Vis Exp 2022;183:e61715. https://doi.org/10.3791/61715
  26. Fouhy F, Ross RP, Fitzgerald GF, Stanton C, Cotter PD. Composition of the early intestinal microbiota: knowledge knowledge gaps and the use of high-throughput sequencing to address these gaps. Gut Microbes 2012;3:203-20. https://doi.org/10.4161/gmic.20169
  27. Yang H, Lyu W, Lu L, et al. Biogeography of microbiome and short-chain fatty acids in the gastrointestinal tract of duck. Poult Sci 2020;99:4016-27. https://doi.org/10.1016/j.psj.2020.03.040
  28. Chen X, Zheng M, Lin F, et al. Impacts of novel duck reovirus infection on the composition of intestinal microbiota of Muscovy ducklings. Microb Pathog 2019;137:103764. https://doi.org/10.1016/j.micpath.2019.103764
  29. Chen X, Zheng M, Huang M, et al. Muscovy duck reovirus infection disrupts the composition of intestinal microbiota in muscovy ducklings. Curr Microbiol 2020;77:769-78. https://doi.org/10.1007/s00284-019-01865-8
  30. Vasai F, Ricaud KB, Bernadet MD, et al. Overfeeding and genetics affect the composition of intestinal microbiota in Anas platyrhynchos (Pekin) and Cairina moschata (Muscovy) ducks. FEMS Microbiol Ecol 2014;87:204-16. https://doi.org/10.1111/1574-6941.12217
  31. Yuan Z, Yan W, Wen C, Zheng J, Yang N, Sun C. Enterotype identification and its influence on regulating the duodenum metabolism in chickens. Poult Sci 2020;99:1515-27. https://doi.org/10.1016/j.psj.2019.10.078
  32. Xu E, Yang H, Ren M, et al. Identification of enterotype and its effects on intestinal butyrate production in pigs. Animals (Basel) 2021;11:730. https://doi.org/10.3390/ani11030730
  33. Hay1 MC, Hinsu AT, Koringa PG, et al. Chicken caecal enterotypes in indigenous Kadaknath and commercial Cobb chicken lines are associated with Campylobacter abundance and influenced by farming practices. Res Sq 2023 Jul 11 [ePub]. https://doi.org/10.21203/rs.3.rs-2381640/v1
  34. Wen C, Gou Q, Gu S, et al. The cecal ecosystem is a great contributor to intramuscular fat deposition in broilers. Poult Sci 2023;102:102568. https://doi.org/10.1016/j.psj.2023.102568
  35. Lu D, Tiezzi F, Schillebeeckx C, et al. Host contributes to longitudinal diversity of fecal microbiota in swine selected for lean growth. Microbiome 2018;6:4. https://doi.org/10.1186/s40168-017-0384-1
  36. Li J, Powell JE, Guo J, et al. Two gut community enterotypes recur in diverse bumblebee species. Curr Biol 2015;25:R652-3. https://doi.org/10.1016/j.cub.2015.06.031
  37. Tang X, Zhang L, Ren S, Zhao Y, Zhang Y. Temporal and geographic distribution of gut microbial enterotypes associated with host thermogenesis characteristics in plateau pikas. Microbiol Spectr 2023;11:e0002023. https://doi.org/10.1128/spectrum.00020-23
  38. Wang X, Tsai T, Deng F, et al. Longitudinal investigation of the swine gut microbiome from birth to market reveals stage and growth performance associated bacteria. Microbiome 2019;7:109. https://doi.org/10.1186/s40168-019-0721-7
  39. Costea PI, Hildebrand F, Arumugam M, et al. Enterotypes in the landscape of gut microbial community composition. Nat Microbiol 2018;3:8-16. https://doi.org/10.1038/s41564-017-0072-8
  40. Danzeisen JL, Calvert AJ, Noll SL, et al. Succession of the turkey gastrointestinal bacterial microbiome related to weight gain. PeerJ 2013;1:e237. https://doi.org/10.7717/peerj.237
  41. Ma L, Tao S, Song T, et al. Clostridium butyricum and carbohydrate active enzymes contribute to the reduced fat deposition in pigs. iMeta 2024;3:e160. https://doi.org/10.1002/imt2.160
  42. Zafar H, Saier MH Jr. Gut bacteroides species in health and disease. Gut Microbes 2021;13:1848158. https://doi.org/10.1080/19490976.2020.1848158
  43. Attwood G, Li D, Pacheco D, Tavendale M. Production of indolic compounds by rumen bacteria isolated from grazing ruminants. J Appl Microbiol 2006;100:1261-71. https://doi.org/10.1111/j.1365-2672.2006.02896.x
  44. Li J, Zhang L, Wu T, Li Y, Zhou X, Ruan Z. Indole-3-propionic acid improved the intestinal barrier by enhancing epithelial barrier and mucus barrier. J Agric Food Chem 2021;69:1487-95. https://doi.org/10.1021/acs.jafc.0c05205
  45. Chen L, Zhang W, Hua J, et al. Dysregulation of intestinal health by environmental pollutants: involvement of the estrogen receptor and aryl hydrocarbon receptor. Environ Sci Technol 2018;52:2323-30. https://doi.org/10.1021/acs.est.7b06322
  46. Huang S, Ji S, Yan H, et al. The day-to-day stability of the ruminal and fecal microbiota in lactating dairy cows. Microbiologyopen 2020;9:e990. https://doi.org/10.1002/mbo3.990
  47. Miyake S, Ngugi DK, Stingl U. Phylogenetic diversity distribution and cophylogeny of giant bacteria (Epulopiscium) with their surgeonfish hosts in the red sea. Front Microbiol 2016;7:285. https://doi.org/10.3389/fmicb.2016.00285
  48. Zhang Q, Kim JH, Kim Y, Kim W. Lactococcus chungangensis CAU 28 alleviates diet-induced obesity and adipose tissue metabolism in vitro and in mice fed a high-fat diet. J Dairy Sci 2020;103:9803-14. https://doi.org/10.3168/jds.2020-18681