Effects of Dietary Antimicrobial Growth Promoters on Performance Parameters and Abundance and Diversity of Broiler Chicken Gut Microbiome and Selection of Antibiotic Resistance Genes
Antimicrobial growth promoters (AGPs) are commonly used in broiler production. There is a huge societal concern around their use and their contribution to the proliferation of antimicrobial resistance (AMR) in food-producing animals and dissemination to humans or the environment. However, there is a...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-06-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2022.905050/full |
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| author | Shyam Sundar Paul Savaram Venkata Rama Rao Nagendra Hegde Nicola J. Williams Rudra Nath Chatterjee Mantena Venkata Lakshmi Narasimha Raju Godumagadda Narender Reddy Vikas Kumar Prakki Santosh Phani Kumar Sathi Mallick Madhuranjana Gargi |
| author_facet | Shyam Sundar Paul Savaram Venkata Rama Rao Nagendra Hegde Nicola J. Williams Rudra Nath Chatterjee Mantena Venkata Lakshmi Narasimha Raju Godumagadda Narender Reddy Vikas Kumar Prakki Santosh Phani Kumar Sathi Mallick Madhuranjana Gargi |
| author_sort | Shyam Sundar Paul |
| collection | DOAJ |
| description | Antimicrobial growth promoters (AGPs) are commonly used in broiler production. There is a huge societal concern around their use and their contribution to the proliferation of antimicrobial resistance (AMR) in food-producing animals and dissemination to humans or the environment. However, there is a paucity of comprehensive experimental data on their impact on poultry production and the AMR resistome. Here, we investigated the effect of five antimicrobial growth promoters (virginiamycin, chlortetracycline, bacitracin methyl disalicylate, lincomycin, and tylosin) used in the commercial broiler production in the Indian subcontinent and in the different parts of the world for three consecutive production cycles on performance variables and also the impact on gut bacteria, bacteriophage, and resistome profile using culture-independent approaches. There was no significant effect of AGPs on the cumulative growth or feed efficiency parameters at the end of the production cycles and cumulative mortality rates were also similar across groups. Many antibiotic resistance genes (ARGs) were ubiquitous in the chicken gut irrespective of AGP supplementation. In total, 62 ARGs from 15 antimicrobial classes were detected. Supplementation of AGPs influenced the selection of several classes of ARGs; however, this was not correlated necessarily with genes relevant to the AGP drug class; some AGPs favored the selection of ARGs related to antimicrobials not structurally related to the AGP. AGPs did not impact the gut bacterial community structure, including alpha or beta diversity significantly, with only 16–20 operational taxonomic units (OTUs) of bacteria being altered significantly. However, several AGPs significantly reduced the population density of some of the potential pathogenic genera of bacteria, such as Escherichia coli. Chlortetracycline increased the abundance of Escherichia phage, whereas other AGPs did not influence the abundance of bacteriophage significantly. Considering the evidence that AGPs used in poultry production can select for resistance to more than one class of antimicrobial resistance, and the fact that their effect on performance is not significant, their use needs to be reduced and there is a need to monitor the spread of ARGs in broiler chicken farms. |
| first_indexed | 2024-04-13T18:05:43Z |
| format | Article |
| id | doaj.art-ba751f3e994d4ab6b1ece1b3754f6854 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-04-13T18:05:43Z |
| publishDate | 2022-06-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-ba751f3e994d4ab6b1ece1b3754f68542022-12-22T02:36:05ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-06-011310.3389/fmicb.2022.905050905050Effects of Dietary Antimicrobial Growth Promoters on Performance Parameters and Abundance and Diversity of Broiler Chicken Gut Microbiome and Selection of Antibiotic Resistance GenesShyam Sundar Paul0Savaram Venkata Rama Rao1Nagendra Hegde2Nicola J. Williams3Rudra Nath Chatterjee4Mantena Venkata Lakshmi Narasimha Raju5Godumagadda Narender Reddy6Vikas Kumar7Prakki Santosh Phani Kumar8Sathi Mallick9Madhuranjana Gargi10Poultry Nutrition Lab, ICAR-Directorate of Poultry Research, Poultry Nutrition, Indian Council of Agricultural Research, Hyderabad, IndiaPoultry Nutrition Lab, ICAR-Directorate of Poultry Research, Poultry Nutrition, Indian Council of Agricultural Research, Hyderabad, IndiaNational Institute of Animal Biotechnology, Hyderabad, IndiaDepartment of Livestock and One Health, Institute of Infection, Veterinary and Ecological Sciences, University of Liverpool, Liverpool, United KingdomDirector’s Lab, ICAR-Directorate of Poultry Research, Poultry Nutrition, Indian Council of Agricultural Research, Hyderabad, IndiaPoultry Nutrition Lab, ICAR-Directorate of Poultry Research, Poultry Nutrition, Indian Council of Agricultural Research, Hyderabad, IndiaPoultry Nutrition Lab, ICAR-Directorate of Poultry Research, Poultry Nutrition, Indian Council of Agricultural Research, Hyderabad, IndiaPoultry Nutrition Lab, ICAR-Directorate of Poultry Research, Poultry Nutrition, Indian Council of Agricultural Research, Hyderabad, IndiaPoultry Nutrition Lab, ICAR-Directorate of Poultry Research, Poultry Nutrition, Indian Council of Agricultural Research, Hyderabad, IndiaNational Institute of Animal Biotechnology, Hyderabad, IndiaNational Institute of Animal Biotechnology, Hyderabad, IndiaAntimicrobial growth promoters (AGPs) are commonly used in broiler production. There is a huge societal concern around their use and their contribution to the proliferation of antimicrobial resistance (AMR) in food-producing animals and dissemination to humans or the environment. However, there is a paucity of comprehensive experimental data on their impact on poultry production and the AMR resistome. Here, we investigated the effect of five antimicrobial growth promoters (virginiamycin, chlortetracycline, bacitracin methyl disalicylate, lincomycin, and tylosin) used in the commercial broiler production in the Indian subcontinent and in the different parts of the world for three consecutive production cycles on performance variables and also the impact on gut bacteria, bacteriophage, and resistome profile using culture-independent approaches. There was no significant effect of AGPs on the cumulative growth or feed efficiency parameters at the end of the production cycles and cumulative mortality rates were also similar across groups. Many antibiotic resistance genes (ARGs) were ubiquitous in the chicken gut irrespective of AGP supplementation. In total, 62 ARGs from 15 antimicrobial classes were detected. Supplementation of AGPs influenced the selection of several classes of ARGs; however, this was not correlated necessarily with genes relevant to the AGP drug class; some AGPs favored the selection of ARGs related to antimicrobials not structurally related to the AGP. AGPs did not impact the gut bacterial community structure, including alpha or beta diversity significantly, with only 16–20 operational taxonomic units (OTUs) of bacteria being altered significantly. However, several AGPs significantly reduced the population density of some of the potential pathogenic genera of bacteria, such as Escherichia coli. Chlortetracycline increased the abundance of Escherichia phage, whereas other AGPs did not influence the abundance of bacteriophage significantly. Considering the evidence that AGPs used in poultry production can select for resistance to more than one class of antimicrobial resistance, and the fact that their effect on performance is not significant, their use needs to be reduced and there is a need to monitor the spread of ARGs in broiler chicken farms.https://www.frontiersin.org/articles/10.3389/fmicb.2022.905050/fullamplicon sequencingshotgun sequencingchickensgut microbiomeantimicrobial resistanceantibiotic growth promoter |
| spellingShingle | Shyam Sundar Paul Savaram Venkata Rama Rao Nagendra Hegde Nicola J. Williams Rudra Nath Chatterjee Mantena Venkata Lakshmi Narasimha Raju Godumagadda Narender Reddy Vikas Kumar Prakki Santosh Phani Kumar Sathi Mallick Madhuranjana Gargi Effects of Dietary Antimicrobial Growth Promoters on Performance Parameters and Abundance and Diversity of Broiler Chicken Gut Microbiome and Selection of Antibiotic Resistance Genes Frontiers in Microbiology amplicon sequencing shotgun sequencing chickens gut microbiome antimicrobial resistance antibiotic growth promoter |
| title | Effects of Dietary Antimicrobial Growth Promoters on Performance Parameters and Abundance and Diversity of Broiler Chicken Gut Microbiome and Selection of Antibiotic Resistance Genes |
| title_full | Effects of Dietary Antimicrobial Growth Promoters on Performance Parameters and Abundance and Diversity of Broiler Chicken Gut Microbiome and Selection of Antibiotic Resistance Genes |
| title_fullStr | Effects of Dietary Antimicrobial Growth Promoters on Performance Parameters and Abundance and Diversity of Broiler Chicken Gut Microbiome and Selection of Antibiotic Resistance Genes |
| title_full_unstemmed | Effects of Dietary Antimicrobial Growth Promoters on Performance Parameters and Abundance and Diversity of Broiler Chicken Gut Microbiome and Selection of Antibiotic Resistance Genes |
| title_short | Effects of Dietary Antimicrobial Growth Promoters on Performance Parameters and Abundance and Diversity of Broiler Chicken Gut Microbiome and Selection of Antibiotic Resistance Genes |
| title_sort | effects of dietary antimicrobial growth promoters on performance parameters and abundance and diversity of broiler chicken gut microbiome and selection of antibiotic resistance genes |
| topic | amplicon sequencing shotgun sequencing chickens gut microbiome antimicrobial resistance antibiotic growth promoter |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2022.905050/full |
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