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Differential Impact of Subtherapeutic Antibiotics and Ionophores on Intestinal Microbiota of Broilers
Antimicrobial growth promoters (AGPs) are commonly used in the livestock industry at subtherapeutic levels to improve production efficiency, which is achieved mainly through modulation of the intestinal microbiota. However, how different classes of AGPs, particularly ionophores, regulate the gut mic...
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Published in: | Microorganisms (Basel) 2019-08, Vol.7 (9), p.282 |
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description | Antimicrobial growth promoters (AGPs) are commonly used in the livestock industry at subtherapeutic levels to improve production efficiency, which is achieved mainly through modulation of the intestinal microbiota. However, how different classes of AGPs, particularly ionophores, regulate the gut microbiota remains unclear. In this study, male Cobb broiler chickens were supplemented for 14 days with or without one of five commonly used AGPs including three classical antibiotics (bacitracin methylene disalicylate, tylosin, and virginiamycin) and two ionophores (monensin and salinomycin) that differ in antimicrobial spectrum and mechanisms. Deep sequencing of the V3-V4 region of the bacterial 16S rRNA gene revealed that two ionophores drastically reduced a number of rare bacteria resulting in a significant decrease in richness and a concomitant increase in evenness of the cecal microbiota, whereas three antibiotics had no obvious impact. Although each AGP modulated the gut microbiota differently, the closer the antibacterial spectrum of AGPs, the more similarly the microbiota was regulated. Importantly, all AGPs had a strong tendency to enrich butyrate- and lactic acid-producing bacteria, while reducing bile salt hydrolase-producing bacteria, suggestive of enhanced metabolism and utilization of dietary carbohydrates and lipids and improved energy harvest, which may collectively be responsible for the growth-promoting effect of AGPs. |
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However, how different classes of AGPs, particularly ionophores, regulate the gut microbiota remains unclear. In this study, male Cobb broiler chickens were supplemented for 14 days with or without one of five commonly used AGPs including three classical antibiotics (bacitracin methylene disalicylate, tylosin, and virginiamycin) and two ionophores (monensin and salinomycin) that differ in antimicrobial spectrum and mechanisms. Deep sequencing of the V3-V4 region of the bacterial 16S rRNA gene revealed that two ionophores drastically reduced a number of rare bacteria resulting in a significant decrease in richness and a concomitant increase in evenness of the cecal microbiota, whereas three antibiotics had no obvious impact. Although each AGP modulated the gut microbiota differently, the closer the antibacterial spectrum of AGPs, the more similarly the microbiota was regulated. Importantly, all AGPs had a strong tendency to enrich butyrate- and lactic acid-producing bacteria, while reducing bile salt hydrolase-producing bacteria, suggestive of enhanced metabolism and utilization of dietary carbohydrates and lipids and improved energy harvest, which may collectively be responsible for the growth-promoting effect of AGPs.</description><identifier>ISSN: 2076-2607</identifier><identifier>EISSN: 2076-2607</identifier><identifier>DOI: 10.3390/microorganisms7090282</identifier><identifier>PMID: 31443457</identifier><language>eng</language><publisher>Switzerland: MDPI AG</publisher><subject>Animals ; antibacterial properties ; Antibiotics ; Antiinfectives and antibacterials ; antimicrobial growth promoters ; Bacitracin ; Bacteria ; bile salts ; broiler chickens ; butyrates ; Carbohydrates ; Cecum ; chickens ; Diet ; dietary carbohydrate ; Digestive system ; energy ; Energy harvesting ; Feeds ; Gastrointestinal tract ; genes ; Gram-positive bacteria ; growth promotion ; high-throughput nucleotide sequencing ; Hydrolase ; Intestinal microflora ; intestinal microorganisms ; Intestine ; Ionophores ; Lactic acid ; Lipid metabolism ; Lipids ; Livestock ; livestock and meat industry ; Livestock industry ; males ; metabolism ; Microbiota ; Monensin ; Poultry ; ribosomal RNA ; rRNA 16S ; Salinomycin ; Tylosin ; Virginiamycin</subject><ispartof>Microorganisms (Basel), 2019-08, Vol.7 (9), p.282</ispartof><rights>2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2019 by the authors. 2019</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c604t-16325d74ad2d790f67bd84c3ca426a90511d8503d91eb6738b30e7de060117ec3</citedby><cites>FETCH-LOGICAL-c604t-16325d74ad2d790f67bd84c3ca426a90511d8503d91eb6738b30e7de060117ec3</cites><orcidid>0000-0003-4781-5816</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/2548915522/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2548915522?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,25733,27903,27904,36991,36992,44569,53769,53771,74872</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31443457$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Robinson, Kelsy</creatorcontrib><creatorcontrib>Becker, Sage</creatorcontrib><creatorcontrib>Xiao, Yingping</creatorcontrib><creatorcontrib>Lyu, Wentao</creatorcontrib><creatorcontrib>Yang, Qing</creatorcontrib><creatorcontrib>Zhu, Huiling</creatorcontrib><creatorcontrib>Yang, Hua</creatorcontrib><creatorcontrib>Zhao, Jiangchao</creatorcontrib><creatorcontrib>Zhang, Guolong</creatorcontrib><title>Differential Impact of Subtherapeutic Antibiotics and Ionophores on Intestinal Microbiota of Broilers</title><title>Microorganisms (Basel)</title><addtitle>Microorganisms</addtitle><description>Antimicrobial growth promoters (AGPs) are commonly used in the livestock industry at subtherapeutic levels to improve production efficiency, which is achieved mainly through modulation of the intestinal microbiota. However, how different classes of AGPs, particularly ionophores, regulate the gut microbiota remains unclear. In this study, male Cobb broiler chickens were supplemented for 14 days with or without one of five commonly used AGPs including three classical antibiotics (bacitracin methylene disalicylate, tylosin, and virginiamycin) and two ionophores (monensin and salinomycin) that differ in antimicrobial spectrum and mechanisms. Deep sequencing of the V3-V4 region of the bacterial 16S rRNA gene revealed that two ionophores drastically reduced a number of rare bacteria resulting in a significant decrease in richness and a concomitant increase in evenness of the cecal microbiota, whereas three antibiotics had no obvious impact. Although each AGP modulated the gut microbiota differently, the closer the antibacterial spectrum of AGPs, the more similarly the microbiota was regulated. Importantly, all AGPs had a strong tendency to enrich butyrate- and lactic acid-producing bacteria, while reducing bile salt hydrolase-producing bacteria, suggestive of enhanced metabolism and utilization of dietary carbohydrates and lipids and improved energy harvest, which may collectively be responsible for the growth-promoting effect of AGPs.</description><subject>Animals</subject><subject>antibacterial properties</subject><subject>Antibiotics</subject><subject>Antiinfectives and antibacterials</subject><subject>antimicrobial growth promoters</subject><subject>Bacitracin</subject><subject>Bacteria</subject><subject>bile salts</subject><subject>broiler chickens</subject><subject>butyrates</subject><subject>Carbohydrates</subject><subject>Cecum</subject><subject>chickens</subject><subject>Diet</subject><subject>dietary carbohydrate</subject><subject>Digestive system</subject><subject>energy</subject><subject>Energy harvesting</subject><subject>Feeds</subject><subject>Gastrointestinal tract</subject><subject>genes</subject><subject>Gram-positive bacteria</subject><subject>growth promotion</subject><subject>high-throughput nucleotide sequencing</subject><subject>Hydrolase</subject><subject>Intestinal microflora</subject><subject>intestinal microorganisms</subject><subject>Intestine</subject><subject>Ionophores</subject><subject>Lactic acid</subject><subject>Lipid metabolism</subject><subject>Lipids</subject><subject>Livestock</subject><subject>livestock and meat industry</subject><subject>Livestock industry</subject><subject>males</subject><subject>metabolism</subject><subject>Microbiota</subject><subject>Monensin</subject><subject>Poultry</subject><subject>ribosomal RNA</subject><subject>rRNA 16S</subject><subject>Salinomycin</subject><subject>Tylosin</subject><subject>Virginiamycin</subject><issn>2076-2607</issn><issn>2076-2607</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNqFUstu1TAQtRCIVqWfAIrEhs2F8TvZIJXyilTEAlhbjj3p9VUSBztB4u9xuKVqERLeeOQ5c3zmzBDylMJLzht4NQaXYkzXdgp5zBoaYDV7QE4ZaLVjCvTDO_EJOc_5AOU0lNeSPiYnnArBhdSnBN-GvseE0xLsULXjbN1Sxb76snbLHpOdcV2Cqy5KvguxhLmyk6_aOMV5HxPmKk5VOy2YlzAVhk-bsg1pN5Y3KYYBU35CHvV2yHh-c5-Rb-_ffb38uLv6_KG9vLjaOQVi2VHFmfRaWM-8bqBXuvO1cNxZwZRtQFLqawncNxQ7pXndcUDtERRQqtHxM9IeeX20BzOnMNr000QbzO-H4pixqTQxoIG6951z3DPrhPPcAnLalI9dLYsGVrheH7nmtRvRu2JRssM90vuZKezNdfxhlK5BKigEL24IUvy-FoPMGLLDYbATxjUbJgCE1mUm_4dySpXUiukCff4X9BDXVKwvKCnqhkrJNvHyiCrTyDlhf6ubgtlWyPxzhUrds7tN31b9WRj-CwUtx4E</recordid><startdate>20190822</startdate><enddate>20190822</enddate><creator>Robinson, Kelsy</creator><creator>Becker, Sage</creator><creator>Xiao, Yingping</creator><creator>Lyu, Wentao</creator><creator>Yang, Qing</creator><creator>Zhu, Huiling</creator><creator>Yang, Hua</creator><creator>Zhao, Jiangchao</creator><creator>Zhang, Guolong</creator><general>MDPI AG</general><general>MDPI</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7T7</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>LK8</scope><scope>M7P</scope><scope>P64</scope><scope>PATMY</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PYCSY</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0003-4781-5816</orcidid></search><sort><creationdate>20190822</creationdate><title>Differential Impact of Subtherapeutic Antibiotics and Ionophores on Intestinal Microbiota of Broilers</title><author>Robinson, Kelsy ; 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However, how different classes of AGPs, particularly ionophores, regulate the gut microbiota remains unclear. In this study, male Cobb broiler chickens were supplemented for 14 days with or without one of five commonly used AGPs including three classical antibiotics (bacitracin methylene disalicylate, tylosin, and virginiamycin) and two ionophores (monensin and salinomycin) that differ in antimicrobial spectrum and mechanisms. Deep sequencing of the V3-V4 region of the bacterial 16S rRNA gene revealed that two ionophores drastically reduced a number of rare bacteria resulting in a significant decrease in richness and a concomitant increase in evenness of the cecal microbiota, whereas three antibiotics had no obvious impact. Although each AGP modulated the gut microbiota differently, the closer the antibacterial spectrum of AGPs, the more similarly the microbiota was regulated. 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subjects | Animals antibacterial properties Antibiotics Antiinfectives and antibacterials antimicrobial growth promoters Bacitracin Bacteria bile salts broiler chickens butyrates Carbohydrates Cecum chickens Diet dietary carbohydrate Digestive system energy Energy harvesting Feeds Gastrointestinal tract genes Gram-positive bacteria growth promotion high-throughput nucleotide sequencing Hydrolase Intestinal microflora intestinal microorganisms Intestine Ionophores Lactic acid Lipid metabolism Lipids Livestock livestock and meat industry Livestock industry males metabolism Microbiota Monensin Poultry ribosomal RNA rRNA 16S Salinomycin Tylosin Virginiamycin |
title | Differential Impact of Subtherapeutic Antibiotics and Ionophores on Intestinal Microbiota of Broilers |
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