Hostname: page-component-77f85d65b8-pztms Total loading time: 0 Render date: 2026-03-26T14:55:38.471Z Has data issue: false hasContentIssue false
  • English
  • Français

Effects of Dietary Palygorskite Supplementation on Cecal Microbial Community Structure and the Abundance of Antibiotic-Resistant Genes in Broiler Chickens Fed With Chlortetracycline

Published online by Cambridge University Press:  01 January 2024

Rui Jin ,
Yueping Chen ,
Yuru Kang ,
Yunfeng Gu ,
Chao Wen ,
Aiqin Wang  and
Yanmin Zhou
Rui Jin
Affiliation:
College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, P.R. 210095, China
Yueping Chen
Affiliation:
College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, P.R. 210095, China
Yuru Kang
Affiliation:
Center of Eco-material and Green Chemistry, Lanzhou Institute of Chemical Physics, Chinese Academy of Sciences, 730000, Lanzhou, P.R., China R&D Center of Xuyi Palygorskite Applied Technology, Lanzhou Institute of Chemical Physics, Chinese Academy of Sciences, 211700, Xuyi, P.R., China
Yunfeng Gu
Affiliation:
College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, P.R. 210095, China
Chao Wen
Affiliation:
College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, P.R. 210095, China
Aiqin Wang
Affiliation:
Center of Eco-material and Green Chemistry, Lanzhou Institute of Chemical Physics, Chinese Academy of Sciences, 730000, Lanzhou, P.R., China R&D Center of Xuyi Palygorskite Applied Technology, Lanzhou Institute of Chemical Physics, Chinese Academy of Sciences, 211700, Xuyi, P.R., China
Yanmin Zhou*
Affiliation:
College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, P.R. 210095, China
*
*E-mail address of corresponding author: zhouym6308@163.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Antibiotic-resistant genes (ARGs) have been regarded as emerging contaminants that threaten public health worldwide. Poultry excreta, often used as a fertilizer in agriculture, are a major route for the proliferation and dissemination of ARGs in the environment. The aim of the present study was to assess the potential of dietary palygorskite (Plg) supplementation as nutritional manipulation for the modulation of microbial community structure and the attenuation of ARGs in the cecal contents of broilers fed with chlortetracycline (CTC). In total, 256 one-day-old, mixed-sex, broiler chicks were allocated randomly into a 2 × 2 factorial design of four treatments, which consisted of two levels of CTC (0 or 50 mg/kg) and Plg (0 or 10 g/kg). By employing in vivo feeding and slaughter experiments, after collecting the cecal contents and extracting the total genomic DNA, 16S rRNA V3-V4 hypervariable amplicon pyrosequencing and quantitative PCR-based approaches were used to address the impact of Plg on microbiota and the abundance of ARGs in broilers. The results showed that broilers given a diet supplemented with Plg had greater α-diversity indices including Chao1, phylogenetic diversity tree, and observed-species index calculations, when compared with those without Plg supplementation. Birds given a diet supplemented with Plg had fewer Firmicutes at the phylum level, but a greater abundance of Alistipes at the bacterial genus level. Dietary Plg counteracted the CTC-induced increased abundance of ARGs, among which tet(K) had a pronounced decrease, along with a similar decreased tendency for other measured ARGs and intI1. Overall, the results indicated that Plg supplementation caused pronounced changes in cecal microbial diversity and microbiota community composition of broilers, and effectively reduced ARGs, indicating that Plg supplementation is a potential alternative measure for the attenuation of ARGs in the cecal contents of broilers.

Keywords

Antibiotic-resistant genesBroilersChlortetracyclineMicrobial community structurePalygorskite

Information

Type
Article
Information
Clays and Clay Minerals , Volume 69 , Issue 2 , April 2021 , pp. 205 - 216
Copyright
Copyright © Clay Minerals Society 2021

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Aminov, R. I., Garrigues-Jeanjean, N., & Mackie, R. I. (2001). Molecular ecology of tetracycline resistance: Development and validation of primers for detection of tetracycline resistance genes encoding ribosomal protection proteins. Applied and Environmental Microbiology, 67, 22–32.CrossRefGoogle ScholarPubMed
Baquero, F., Martinez, J. L., & Canton, R. (2008). Antibiotics and antibiotic resistance in water environments. Current Opinion in Biotechnology, 19, 260–265.CrossRefGoogle ScholarPubMed
Barr, M. (1957) Adsorption studies on clays II. The adsorption of bacteria by activated attapulgite, halloysite, and kaolin. Journal of the American Pharmaceutical Association, 46(8), 490–492.CrossRefGoogle ScholarPubMed
Berendonk, T. U., Manaia, C. M., Merlin, C., Fatta-Kassinos, D., Cytryn, E., Walsh, F., Burgmann, H., Sorum, H., Norstrom, M., Pons, M. N., Kreuzinger, N., Huovinen, P., Stefani, S., Schwartz, T., Kisand, V., Baquero, F., & Martinez, J. L. (2015). Tackling antibiotic resistance: The environmental framework. Nature Reviews Microbiology, 13, 310–317.CrossRefGoogle ScholarPubMed
Bergaya, F., & Lagaly, G. (2013). Handbook of Clay Science. 2nd edition. Developments in Clay Science, 5, 243–345.Google Scholar
Cai, X., Zhang, J. L., Ouyang, Y., Ma, D., Tan, S. Z., & Peng, Y. L. (2013). Bacteria-adsorbed palygorskite stabilizes the quaternary phosphonium salt with specific-targeting capability, long-term antibacterial activity, and lower cytotoxicity. Langmuir, 29, 5279–5285.CrossRefGoogle ScholarPubMed
Cambray, G., Guerout, A. M., & Mazel, D. (2010). Integrons. Annual Review of Genetics, 44, 141–166.CrossRefGoogle ScholarPubMed
Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., Fierer, N., Pena, A. G., Goodrich, J. K., Gordon, J. I., Huttley, G. A., Kelley, S. T., Knights, D., Koenig, J. E., Ley, R. E., Lozupone, C. A., McDonald, D., Muegge, B. D., Pirrung, M., & Knight, R. (2010). QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 7, 335–336.CrossRefGoogle ScholarPubMed
Castillo, M., Martin-Orue, S. M., Roca, M., Manzanilla, E. G., Badiola, I., Perez, J. F., & Gasa, J. (2006). The response of gastrointestinal microbiota to avilamycin, butyrate, and plant extracts in early-weaned pigs. Journal of Animal Science, 84, 2725–2734.CrossRefGoogle ScholarPubMed
Chalvatzi, S., Kalamaki, M. S., Arsenos, G., & Fortomaris, P. (2016). Dietary supplementation with the clay mineral palygorskite affects performance and beneficially modulates caecal microbiota in laying pullets. Journal of Applied Microbiology, 120, 1033–1040.CrossRefGoogle ScholarPubMed
Chang, P. H., Li, Z. H., Yu, T. L., Munkhbayer, S., Kuo, T. H., Hung, Y. C., Jean, J. S., & Lin, K. H. (2009). Sorptive removal of tetracycline from water by palygorskite. Journal of Hazardous Materials, 165, 148–155.CrossRefGoogle ScholarPubMed
Chee-Sanford, J. C., Mackie, R. I., Koike, S., Krapac, I. G., Lin, Y. F., Yannarell, A. C., Maxwell, S., & Aminov, R. I. (2009). Fate and transport of antibiotic residues and antibiotic resistance genes following land application of manure waste. Journal of Environmental Quality, 38, 1086–1108.CrossRefGoogle ScholarPubMed
Chen, J. F., Peng, C. Y., Qu, X. Y., & Ji, F. (2017). Effects of montmorillonite on performance and cecal microfora of laying hens. Chinese Journal of Animal Nutrition, 29, 4026–4035.Google Scholar
Chen, X., Zhang, W. Q., Yin, J. J., Zhang, N., Geng, S. Z., Zhou, X. H., Wang, Y. H., Gao, S., & Jiao, X. N. (2014). Escherichia coli isolates from sick chickens in China: Changes in antimicrobial resistance between 1993 and 2013. Veterinary Journal, 202, 112–115.Google ScholarPubMed
Chen, Y. P., Cheng, Y. F., Li, X. H., Zhang, H., Yang, W. L., Wen, C., & Zhou, Y. M. (2016). Dietary palygorskite supplementation improves immunity, oxidative status, intestinal integrity, and barrier function of broilers at early age. Animal Feed Science and Technology, 219, 200–209.CrossRefGoogle Scholar
Chopra, I. (2001). Glycylcyclines: Third-generation tetracycline antibiotics. Current Opinion in Pharmacology, 1, 464–469.CrossRefGoogle ScholarPubMed
Chopra, I., & Roberts, M. (2001). Tetracycline antibiotics: Mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiology and Molecular Biology Reviews, 65, 232–260.CrossRefGoogle ScholarPubMed
Depaola, A., & Roberts, M. C. (1995). Class-D and class-E tetracycline resistance determinants in gram-negative bacteria from catfsh ponds. Molecular and Cellular Probes, 9, 311–313.CrossRefGoogle Scholar
Duan, W. S., Niu, Q. G., Xu, X. G., Li, W., & Fu, D. F. (2017). Influence of attapulgite addition on the biological performance and microbial communities of submerged dynamic membrane bioreactor. Journal of Water Reuse and Desalination, 7, 488–501.CrossRefGoogle Scholar
Feighner, S. D., & Dashkevicz, M. P. (1987). Subtherapeutic levels of antibiotics in poultry feeds and their effects on weight gain, feed efficiency, and bacterial cholyltaurine hydrolase activity. Applied and Environmental Microbiology, 53, 331–336.CrossRefGoogle ScholarPubMed
Gao, P., Munir, M., & Xagoraraki, I. (2012). Correlation of tetracycline and sulfonamide antibiotics with corresponding resistance genes and resistant bacteria in a conventional municipal wastewater treatment plant. Science of the Total Environment, 421, 173–183.CrossRefGoogle Scholar
Ghosh, T. S., Sen Gupta, S., Bhattacharya, T., Yadav, D., Barik, A., Chowdhury, A., Das, B., Mande, S. S., & Nair, G. B. (2014). Gut microbiomes of Indian children of varying nutritional status. PLoS ONE, 9, e95547.CrossRefGoogle ScholarPubMed
Gillings, M., Boucher, Y., Labbate, M., Holmes, A., Krishnan, S., Holley, M., & Stokes, H. W. (2008). The evolution of class 1 integrons and the rise of antibiotic resistance. Journal of Bacteriology, 190, 5095–5100.CrossRefGoogle ScholarPubMed
Gillings, M. R., Gaze, W. H., Pruden, A., Smalla, K., Tiedje, J. M., & Zhu, Y. G. (2015). Using the class 1 integronintegrase gene as a proxy for anthropogenic pollution. The ISME Journal, 9, 1269–1279.CrossRefGoogle ScholarPubMed
Hall, R. M., & Collis, C. M. (1995). Mobile gene cassettes and integrons - capture and spread of genes by site-specifc recombination. Molecular Microbiology, 15, 593–600.CrossRefGoogle Scholar
Harvey, R., Funk, J., Wittum, T. E., & Hoet, A. E. (2009). A metagenomic approach for determining prevalence of tetracycline resistance genes in the fecal flora of conventionally raised feedlot steers and feedlot steers raised without antimicrobials. American Journal of Veterinary Research, 70, 198–202.CrossRefGoogle ScholarPubMed
He, J. Z., Shen, J. P., Zhang, L. M., Zhu, Y. G., Zheng, Y. M., Xu, M. G., & Di, H. J. (2007). Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices. Environmental Microbiology, 9, 2364–2374.CrossRefGoogle ScholarPubMed
Henao, L., & Mazeau, K. (2008). The molecular basis of the adsorption of bacterial exopolysaccharides on montmorillonite mineral surface. Molecular Simulation, 34, 1185–1195.CrossRefGoogle Scholar
Huang, J. H., Liu, Y. F., Jin, Q. Z., Wang, X. G., & Yang, J. (2007). Adsorption studies of a water soluble dye, reactive red MF-3B, using sonication-surfactant-modified attapulgite clay. Journal of Hazardous Materials, 143, 541–548.CrossRefGoogle ScholarPubMed
Huyghebaert, G., Ducatelle, R., & Van Immerseel, F. (2011). An update on alternatives to antimicrobial growth promoters for broilers. The Veterinary Journal, 187, 182–188.CrossRefGoogle ScholarPubMed
Henriques, I. S., Fonseca, F., Alves, A., Saavedra, M. J., & Correia, A. (2006). Occurrence and diversity of integrons and β-lactamase genes among ampicillin-resistant isolates from estuarine waters. Research in Microbiology, 157, 938–947.CrossRefGoogle ScholarPubMed
La-Ongkhum, O., Pungsungvorn, N., Amornthewaphat, N., & Nitisinprasert, S. (2011). Effect of the antibiotic avilamycin on the structure of the microbial community in the jejunal intestinal tract of broiler chickens. Poultry Science, 90, 1532–1538.CrossRefGoogle ScholarPubMed
Lai, X. L., Wu, P. X., Ruan, B., Liu, J., Liu, Z. H., Zhu, N. W., & Dang, Z. (2019). Inhibition effect of kaolinite on the development of antibiotic resistance genes in Escherichia coli induced by sublethal ampicillin and its molecular mechanism. Environmental Chemistry, 16, 347–359.CrossRefGoogle Scholar
Levy, S. B., McMurry, L. M., Barbosa, T. M., Burdett, V., Courvalin, P., Hillen, W., Roberts, M. C., Rood, J. I., & Taylor, D. E. (1999). Nomenclature for new tetracycline resistance determinants. Antimicrobial Agents and Chemotherapy, 43, 1523–1524.CrossRefGoogle ScholarPubMed
Luo, Y., Mao, D., Rysz, M., Zhou, Q., Zhang, H., Xu, L., & Alvarez, P. J. J. (2010). Trends in antibiotic resistance genes occurrence in the Haihe river, China. Environmental Science & Technology, 44, 7220–7225.CrossRefGoogle ScholarPubMed
Mamber, S. W., & Katz, S. E. (1985). Effects of antimicrobial agents fed to chickens on some gram-negative enteric bacilli. Applied and Environmental Microbiology, 50, 638–648.CrossRefGoogle ScholarPubMed
Marshall, B. M., & Levy, S. B. (2011). Food animals and antimicrobials: Impacts on human health. Clinical Microbiology Reviews, 24, 718–733.CrossRefGoogle ScholarPubMed
Mazel, D. (2006). Integrons: Agents of bacterial evolution. Nature Reviews Microbiology, 4, 608–620.CrossRefGoogle ScholarPubMed
Mead, G. C. (1997). Bacteria in the gastrointestinal tract of birds. Gastrointestinal Microbiology, 2, 216–240.CrossRefGoogle Scholar
Mendes, R. E., Castanheira, M., Toleman, M. A., Sader, H. S., Jones, R. N., & Walsh, T. R. (2007). Characterization of an integron carrying blaIMP-1 and a new aminoglycoside resistance gene, aac(6')-31, and its dissemination among genetically unrelated clinical isolates in a brazilian hospital. Antimicrobial Agents and Chemotherapy, 51, 2611–2614.CrossRefGoogle Scholar
Moghadam, M.M., Amiri, M., & Riabi, H.R.A. (2016). Evaluation of antibiotic residues in pasteurized and raw milk distributed in the south of Khorasan-e Razavi province, Iran. Journal of Clinical and Diagnostic Research, 10, FC31-FC35.Google ScholarPubMed
National Research Council. (1994). Nutrient Requirements of Poultry: Ninth edition (revised). National Academies Press, USA.Google Scholar
Ng, L. K., Martin, I., Alfa, M., & Mulvey, M. (2001). Multiplex PCR for the detection of tetracycline resistant genes. Molecular and Cellular Probes, 15, 209–215.CrossRefGoogle ScholarPubMed
Oakley, B. B., & Kogut, M. H. (2016). Spatial and temporal changes in the broiler chicken cecal and fecal microbiomes and correlations of bacterial taxa with cytokine gene expression. Frontiers in Veterinary Science, 3, 11.CrossRefGoogle ScholarPubMed
Ochman, H., Lawrence, J. G., & Groisman, E. A. (2000). Lateral gene transfer and the nature of bacterial innovation. Nature, 405, 299–304.CrossRefGoogle ScholarPubMed
Pfaf, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research, 29, e45.Google Scholar
Pruden, A., Pei, R. T., Storteboom, H., & Carlson, K. H. (2006). Antibiotic resistance genes as emerging contaminants: Studies in northern Colorado. Environmental Science & Technology, 40, 7445–7450.CrossRefGoogle ScholarPubMed
Qian, X., Sun, W., Gu, J., Wang, X. J., Zhang, Y. J., Duan, M. L., Li, H. C., & Zhang, R. R. (2016). Reducing antibiotic resistance genes, integrons, and pathogens in dairy manure by continuous thermophilic composting. Bioresource Technology, 220, 425–432.CrossRefGoogle ScholarPubMed
Qu, H. M., Cheng, Y. F., Chen, Y. P., Li, J., Zhao, Y. R., & Zhou, Y. M. (2019). Effects of dietary zeolite supplementation as an antibiotic alternative on growth performance, intestinal integrity, and cecal antibiotic resistance genes abundance of broilers. Animals, 9, 909.CrossRefGoogle Scholar
Roberts, M. C. (2003). Tetracycline therapy: Update. Clinical Infectious Diseases, 36, 462–467.CrossRefGoogle ScholarPubMed
Slamova, R., Trckova, M., Vondruskova, H., Zraly, Z., & Pavlik, I. (2011). Clay minerals in animal nutrition. Applied Clay Science, 51, 395–398.CrossRefGoogle Scholar
Speer, B. S., Bedzyk, L., & Salyers, A. A. (1991). Evidence that a novel tetracycline resistance gene found on 2 Bacteroides transposons encodes an NADP-requiring oxidoreductase. Journal of Bacteriology, 173, 176–183.CrossRefGoogle Scholar
Stanley, D., Hughes, R. J., & Moore, R. J. (2014). Microbiota of the chicken gastrointestinal tract: influence on health, productivity and disease. Applied Microbiology and Biotechnology, 98, 4301–4310.CrossRefGoogle ScholarPubMed
Wang, F. H., Qiao, M., Lv, Z. E., Guo, G. X., Jia, Y., Su, Y. H., & Zhu, Y. G. (2014). Impact of reclaimed water irrigation on antibiotic resistance in public parks, Beijing, China. Environmental Pollution, 184, 247–253.CrossRefGoogle ScholarPubMed
Zaid, M. R. B., Hasan, M., & Khan, A. A. (1995). Attapulgite in the treatment of acute diarrhoea: A double-blind placebo-controlled study. Journal of Diarrhoeal Diseases Research, 13, 44–46.Google ScholarPubMed
Zhang, J. M., Lv, Y. F., Tang, C. H., & Wang, X. Q. (2013). Effects of dietary supplementation with palygorskite on intestinal integrity in weaned piglets. Applied Clay Science, 86, 185–189.CrossRefGoogle Scholar
Zhang, J. Y., Chen, M. X., Sui, Q. W., Tong, J., Jiang, C., Lu, X. T., Zhang, Y. X., & Wei, Y. S. (2016a). Impacts of addition of natural zeolite or a nitrification inhibitor on antibiotic resistance genes during sludge composting. Water Research, 91, 339–349.CrossRefGoogle Scholar
Zhang, J. Y., Chen, M. X., Sui, Q. W., Wang, R., Tong, J., & Wei, Y. S. (2016b). Fate of antibiotic resistance genes and its drivers during anaerobic co-digestion of food waste and sewage sludge based on microwave pretreatment. Bioresource Technology, 217, 28–36.CrossRefGoogle Scholar
Zhang, Y. J., Li, H. C., Gu, J., Qian, X., Yin, Y. N., Li, Y., Zhang, R. R., & Wang, X. J. (2016c). Effects of adding different surfactants on antibiotic resistance genes and IntI1 during chicken manure composting. Bioresource Technology, 219, 545–551.CrossRefGoogle Scholar
Zhao, L., Dong, Y. H., & Wang, H. (2010). Residues of veterinary antibiotics in manures from feedlot livestock in eight provinces of China. Science of the Total Environment, 408, 1069–1075.CrossRefGoogle ScholarPubMed
Zhou, C. H., Zhao, L. Z., Wang, A. Q., Chen, T. H., & He, H. P. (2016). Current fundamental and applied research into clay minerals in China. Applied Clay Science, 119, 3–7.CrossRefGoogle Scholar