Log in

Integrative Analysis of the Microbiome and Metabolome of Broiler Intestine: Insights into the Mechanisms of Probiotic Action as an Antibiotic Substitute

  • Research
  • Published:
Probiotics and Antimicrobial Proteins Aims and scope Submit manuscript

Abstract

Antibiotic substitutes have become a research focus due to restrictions on antibiotic usage. Among the antibiotic substitutes on the market, probiotics have been extensively researched and used. However, the mechanism by which probiotics replace antibiotics remains unclear. In this study, we aimed to investigate this mechanism by comparing the effects of probiotics and antibiotics on broiler growth performance and intestinal microbiota composition. Results shown that both probiotics and antibiotics increased daily weight gain and reduced feed conversion rate in broilers. Analysis of ileum and cecum microorganisms via 16S rRNA gene sequencing revealed that both interventions decreased intestinal microbial diversity. Moreover, the abundance of Bacteroides increased in the mature ileum, while that of Erysipelatoclostridium decreased in the cecum in response to both probiotics and antibiotics. The main metabolites of probiotics and antibiotics in the intestine were found to be organic acids, amino acids, and sugars, which might play comparable roles in growth performance. Furthermore, disaccharides and trisaccharides may be essential components in the ileum that enable probiotics to replace antibiotics. These findings provide important insights into the mechanisms underlying the use of probiotics as antibiotic substitutes in broiler breeding.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data and Model Availability 

None of the data were deposited in an official repository, but are available from the corresponding author upon request.

References

  1. Gao P et al (2017) Feed-additive probiotics accelerate yet antibiotics delay intestinal microbiota maturation in broiler chicken. Microbiome 5(1):91

    Article  PubMed  PubMed Central  Google Scholar 

  2. Mehdi Y et al (2018) Use of antibiotics in broiler production: global impacts and alternatives. Anim Nutr 4(2):170–178

    Article  PubMed  PubMed Central  Google Scholar 

  3. Gadde U et al (2017) Alternatives to antibiotics for maximizing growth performance and feed efficiency in poultry: a review. Anim Health Res Rev 18(1):26–45

    Article  CAS  PubMed  Google Scholar 

  4. Coates ME et al (1963) A comparison of the growth of chicks in the Gustafsson germ-free apparatus and in a conventional environment, with and without dietary supplements of penicillin. Br J Nutr 17:141–150

    Article  CAS  PubMed  Google Scholar 

  5. Hill C et al (2014) Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol 11(8):506–14

  6. Azad MAK et al (2018) Probiotic species in the modulation of gut microbiota: an overview. Biomed Res Int 2018:9478630

    Article  PubMed  PubMed Central  Google Scholar 

  7. Dimidi E et al (2017) Mechanisms of action of probiotics and the gastrointestinal microbiota on gut motility and constipation. Adv Nutr 8(3):484–494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Wieers G et al (2019) How probiotics affect the microbiota. Front Cell Infect Microbiol 9:454

    Article  PubMed  Google Scholar 

  9. Timmerman HM et al (2006) Mortality and growth performance of broilers given drinking water supplemented with chicken-specific probiotics. Poult Sci 85(8):1383–1388

    Article  CAS  PubMed  Google Scholar 

  10. Chapman CM, Gibson GR, Rowland I (2011) Health benefits of probiotics: are mixtures more effective than single strains? Eur J Nutr 50(1):1–17

    Article  CAS  PubMed  Google Scholar 

  11. Wells JM (2011) Immunomodulatory mechanisms of lactobacilli. Microb Cell Fact 10(1):S17

  12. Liu H et al (2023) Integrated multi-omics reveals the beneficial role of chlorogenic acid in improving the growth performance and immune function of immunologically stressed broilers. Anim Nutr 14:383–402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Seo YJ et al (2024) Microbial-transcriptome integrative analysis of heat stress effects on amino acid metabolism and lipid peroxidation in poultry jejunum. Anim Biotechnol 35(1):2331179

    Article  PubMed  Google Scholar 

  14. Haas BJ et al (2011) Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res 21(3):494–504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10(10):996–998

    Article  CAS  PubMed  Google Scholar 

  16. Quast C et al (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41(Database issue):D590–6

  17. Team RC (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

  18. Caporaso JG et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. van der Wagt I et al (2020) A review on yolk sac utilization in poultry. Poult Sci 99(4):2162–2175

    Article  PubMed  PubMed Central  Google Scholar 

  20. Miles RD et al (2006) Effect of antibiotic growth promoters on broiler performance, intestinal growth parameters, and quantitative morphology. Poult Sci 85(3):476–485

    Article  CAS  PubMed  Google Scholar 

  21. Awad WA et al (2009) Effects of dietary inclusion of probiotic and synbiotic on growth performance, organ weights, and intestinal histomorphology of broiler chickens. Poult Sci 88(1):49–56

    Article  CAS  PubMed  Google Scholar 

  22. El-Moneim A et al (2020) Assessment of in ovo administration of bifidobacterium bifidum and bifidobacterium longum on performance, ileal histomorphometry, blood hematological, and biochemical parameters of broilers. Probiotics Antimicrob Proteins 12(2):439–450

    Article  CAS  PubMed  Google Scholar 

  23. Olnood CG et al (2015) Novel probiotics: their effects on growth performance, gut development, microbial community and activity of broiler chickens. Anim Nutr 1(3):184–191

    Article  PubMed  PubMed Central  Google Scholar 

  24. Choi JH et al (2018) Influence of dietary avilamycin on ileal and cecal microbiota in broiler chickens. Poult Sci 97(3):970–979

    Article  CAS  PubMed  Google Scholar 

  25. Elokil AA et al (2020) Investigation of the impacts of antibiotic exposure on the diversity of the gut microbiota in chicks. Animals (Basel) 10(5)

  26. Amit-Romach E, Sklan D, Uni Z (2004) Microflora ecology of the chicken intestine using 16S ribosomal DNA primers. Poult Sci 83(7):1093–1098

    Article  CAS  PubMed  Google Scholar 

  27. de Oliveira JE et al (2014) In ovo inoculation of chicken embryos with probiotic bacteria and its effect on posthatch Salmonella susceptibility. Poult Sci 93(4):818–829

    Article  PubMed  Google Scholar 

  28. Richards P et al (2019) Development of the caecal microbiota in three broiler breeds. Front Vet Sci 6:201

    Article  PubMed  PubMed Central  Google Scholar 

  29. Ocejo M, Oporto B, Hurtado A (2019) 16S rRNA amplicon sequencing characterization of caecal microbiome composition of broilers and free-range slow-growing chickens throughout their productive lifespan. Sci Rep 9(1):2506

    Article  PubMed  PubMed Central  Google Scholar 

  30. Kluch M et al (2020) The role of disaccharidases in the digestion - diagnosis and significance of their deficiency in children and adults. Pol Merkur Lekarski 49(286):275–278

    PubMed  Google Scholar 

  31. Hayafune M et al (2014) Chitin-induced activation of immune signaling by the rice receptor CEBiP relies on a unique sandwich-type dimerization. Proc Natl Acad Sci USA 111(3):E404–E413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Kim YW et al (2005) Anti-diabetic activity of beta-glucans and their enzymatically hydrolyzed oligosaccharides from Agaricus blazei. Biotechnol Lett 27(7):483–487

    Article  CAS  PubMed  Google Scholar 

  33. Samli HE et al (2007) Effects of Enterococcus faecium and dried whey on broiler performance, gut histomorphology and intestinal microbiota. Arch Anim Nutr 61(1):42–49

    Article  PubMed  Google Scholar 

  34. Tellez G et al (1993) Effect of dietary lactose on cecal morphology, pH, organic acids, and Salmonella enteritidis organ invasion in Leghorn chicks. Poult Sci 72(4):636–642

    Article  CAS  PubMed  Google Scholar 

  35. Hinton A Jr et al (1991) Comparison of the efficacy of cultures of cecal anaerobes as inocula to reduce Salmonella typhimurium colonization in chicks with or without dietary lactose. Poult Sci 70(1):67–73

    Article  PubMed  Google Scholar 

  36. Zhu X, Liu J, Yang G (2021) Effects of soybean oligosaccharide, stachyose, and raffinose on growth performance and cecal microbiota in broiler chickens. Anim Sci J 92(1):e13668

    Article  CAS  PubMed  Google Scholar 

  37. Xu Y et al (2016) High-throughput sequencing technology to reveal the composition and function of cecal microbiota in Dagu chicken. BMC Microbiol 16(1):259

    Article  PubMed  PubMed Central  Google Scholar 

  38. Pagliassotti MJ et al (2017) Trehalose supplementation reduces hepatic endoplasmic reticulum stress and inflammatory signaling in old mice. J Nutr Biochem 45:15–23

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Sinha P, Verma B, Ganesh S (2021) Trehalose ameliorates seizure susceptibility in Lafora disease mouse models by suppressing neuroinflammation and endoplasmic reticulum stress. Mol Neurobiol 58(3):1088–1101

    Article  CAS  PubMed  Google Scholar 

  40. Sergin I et al (2017) Exploiting macrophage autophagy-lysosomal biogenesis as a therapy for atherosclerosis. Nat Commun 8:15750

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Oku T, Nakamura S (2000) Estimation of intestinal trehalase activity from a laxative threshold of trehalose and lactulose on healthy female subjects. Eur J Clin Nutr 54(10):783–788

    Article  CAS  PubMed  Google Scholar 

  42. Wu YT et al (2020) Modulations of growth performance, gut microbiota, and inflammatory cytokines by trehalose on Salmonella typhimurium-challenged broilers. Poult Sci 99(8):4034–4043

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was supported by the Collaborative Innovation Center of GDAAS (No. XTXM 202205), Special Fund for Rural Revitalization Strategy of Guangdong Province (No. Jiangke[2021]183), Scientific Research Project of Guangdong Laboratory for Lingnan Modern Agriculture Heyuan Sub-center (No. DT20220038), the Open Competition Program of Top Nine Critical Priorities of Agricultural Science, Technology Innovation for the 14th Five-Year Plan of Guangdong Province (2023SDZG09), Natural Science Foundation of Guangdong Province (2023A1515011088), Young Talent Support Project of Guangzhou Association for Science and Technology (QT20230101087), and 2022 Provincial Agricultural Science and Technology Development and Resource Environment Protect Management Projects (2022KJ158).

Author information

Authors and Affiliations

Authors

Contributions

Yang Li: Conceptualization, Methodology, Investigation, Writing—Original Draft; Jian-Ling Zhang: Investigation, Resources, Data Curation; Jun-** Deng, Wang Jia-Qi and Jia-Zhou Li: Methodology, Writing—Review & Editing; **g Liu and Shi Liu: Methodology, Writing—Review & Editing; Wen-Jie Wang and Dong Ruan: Investigation, Formal Analysis; Jun-** Deng, Zhuang Chen and Zhi-Lin Wang: Supervision.

Corresponding authors

Correspondence to Jun-** Deng or Zhi-Lin Wang.

Ethics declarations

Ethics Statement

The animal study was reviewed and approved by Animal Experimental Ethical Inspection Form of Agro-biological Gene Research Center, Guangdong Academy of Agricultural Sciences No. 201912.

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Implications

As the most potent antibiotic substitute in poultry breeding, the mechanism by which probiotics replace antibiotics remains unclear. The study aimed to investigate this mechanism by comparing the effects of probiotics and antibiotics on broilers. Results showed that Bacteroides in the ileum and Erysipelatoclostridium in the cecum might be important. Additionally, a central role was played by the disaccharides and trisaccharides in the ileum.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 1149 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, Y., Zhang, JL., Chen, JQ. et al. Integrative Analysis of the Microbiome and Metabolome of Broiler Intestine: Insights into the Mechanisms of Probiotic Action as an Antibiotic Substitute. Probiotics & Antimicro. Prot. (2024). https://doi.org/10.1007/s12602-024-10304-5

Download citation

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12602-024-10304-5

Keywords

Navigation