Enrofloxacin Shifts Intestinal Microbiota and Metabolic Profiling and Hinders Recovery from <named-content content-type="genus-species">Salmonella enterica</named-content> subsp. <italic toggle="yes">enterica</italic> Serovar Typhimurium Infection in Neonatal Chickens

ABSTRACT Enrofloxacin is an important antibiotic used for prevention and treatment of Salmonella infection in poultry in many countries. However, oral administration of enrofloxacin may lead to the alterations in the microbiota and metabolome in the chicken intestine, thereby reducing colonization r...

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Autores principales: Boheng Ma, Xueran Mei, Changwei Lei, Cui Li, Yufeng Gao, Linghan Kong, Xiwen Zhai, Hongning Wang
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Publicado: American Society for Microbiology 2020
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spelling oai:doaj.org-article:ab09c8ab32ec43f8bd2f375c3c0a6f232021-11-15T15:30:58ZEnrofloxacin Shifts Intestinal Microbiota and Metabolic Profiling and Hinders Recovery from <named-content content-type="genus-species">Salmonella enterica</named-content> subsp. <italic toggle="yes">enterica</italic> Serovar Typhimurium Infection in Neonatal Chickens10.1128/mSphere.00725-202379-5042https://doaj.org/article/ab09c8ab32ec43f8bd2f375c3c0a6f232020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00725-20https://doaj.org/toc/2379-5042ABSTRACT Enrofloxacin is an important antibiotic used for prevention and treatment of Salmonella infection in poultry in many countries. However, oral administration of enrofloxacin may lead to the alterations in the microbiota and metabolome in the chicken intestine, thereby reducing colonization resistance to the Salmonella infection. To study the effect of enrofloxacin on Salmonella in the chicken cecum, we used different concentrations of enrofloxacin to feed 1-day-old chickens, followed by oral challenge with Salmonella enterica subsp. enterica serovar Typhimurium (S. Typhimurium). We then explored the distribution pattern of S. Typhimurium in cecum contents in vivo and analyzed the microbial community structure of cecum contents using microbial 16S amplicon sequencing. Untargeted metabolomics was used to explore the gut metabolome on day 14. Faecalibacterium and Anaerostipes, which are closely related to the chicken intestinal metabolome, were screened using a multi-omics technique. The abundance of S. Typhimurium was significantly higher in the enrofloxacin-treated group than in the untreated group, and S. Typhimurium persisted longer. Moreover, the cecal colony structures of the three groups exhibited different characteristics, with Lactobacillus reaching its highest abundance on day 21. Notably, S. Typhimurium infection is known to affect the fecal metabolome of chickens differently. Thus, our results suggested that enrofloxacin and Salmonella infections completely altered the intestinal microbiota and metabolism of chickens. IMPORTANCE In this study, we examined the effects of S. Typhimurium infection and enrofloxacin treatment on the microbiota and metabolite synthesis in chicken cecum, in order to identify target metabolites that may promote S. Typhimurium colonization and aggravate inflammation and to evaluate the important microbiota that may be associated with these metabolites. Our findings may facilitate the use of antibiotics to prevent S. Typhimurium infection.Boheng MaXueran MeiChangwei LeiCui LiYufeng GaoLinghan KongXiwen ZhaiHongning WangAmerican Society for Microbiologyarticlegut microbiotaenrofloxacinmetabolomechickenSalmonellaMicrobiologyQR1-502ENmSphere, Vol 5, Iss 5 (2020)
institution DOAJ
collection DOAJ
language EN
topic gut microbiota
enrofloxacin
metabolome
chicken
Salmonella
Microbiology
QR1-502
spellingShingle gut microbiota
enrofloxacin
metabolome
chicken
Salmonella
Microbiology
QR1-502
Boheng Ma
Xueran Mei
Changwei Lei
Cui Li
Yufeng Gao
Linghan Kong
Xiwen Zhai
Hongning Wang
Enrofloxacin Shifts Intestinal Microbiota and Metabolic Profiling and Hinders Recovery from <named-content content-type="genus-species">Salmonella enterica</named-content> subsp. <italic toggle="yes">enterica</italic> Serovar Typhimurium Infection in Neonatal Chickens
description ABSTRACT Enrofloxacin is an important antibiotic used for prevention and treatment of Salmonella infection in poultry in many countries. However, oral administration of enrofloxacin may lead to the alterations in the microbiota and metabolome in the chicken intestine, thereby reducing colonization resistance to the Salmonella infection. To study the effect of enrofloxacin on Salmonella in the chicken cecum, we used different concentrations of enrofloxacin to feed 1-day-old chickens, followed by oral challenge with Salmonella enterica subsp. enterica serovar Typhimurium (S. Typhimurium). We then explored the distribution pattern of S. Typhimurium in cecum contents in vivo and analyzed the microbial community structure of cecum contents using microbial 16S amplicon sequencing. Untargeted metabolomics was used to explore the gut metabolome on day 14. Faecalibacterium and Anaerostipes, which are closely related to the chicken intestinal metabolome, were screened using a multi-omics technique. The abundance of S. Typhimurium was significantly higher in the enrofloxacin-treated group than in the untreated group, and S. Typhimurium persisted longer. Moreover, the cecal colony structures of the three groups exhibited different characteristics, with Lactobacillus reaching its highest abundance on day 21. Notably, S. Typhimurium infection is known to affect the fecal metabolome of chickens differently. Thus, our results suggested that enrofloxacin and Salmonella infections completely altered the intestinal microbiota and metabolism of chickens. IMPORTANCE In this study, we examined the effects of S. Typhimurium infection and enrofloxacin treatment on the microbiota and metabolite synthesis in chicken cecum, in order to identify target metabolites that may promote S. Typhimurium colonization and aggravate inflammation and to evaluate the important microbiota that may be associated with these metabolites. Our findings may facilitate the use of antibiotics to prevent S. Typhimurium infection.
format article
author Boheng Ma
Xueran Mei
Changwei Lei
Cui Li
Yufeng Gao
Linghan Kong
Xiwen Zhai
Hongning Wang
author_facet Boheng Ma
Xueran Mei
Changwei Lei
Cui Li
Yufeng Gao
Linghan Kong
Xiwen Zhai
Hongning Wang
author_sort Boheng Ma
title Enrofloxacin Shifts Intestinal Microbiota and Metabolic Profiling and Hinders Recovery from <named-content content-type="genus-species">Salmonella enterica</named-content> subsp. <italic toggle="yes">enterica</italic> Serovar Typhimurium Infection in Neonatal Chickens
title_short Enrofloxacin Shifts Intestinal Microbiota and Metabolic Profiling and Hinders Recovery from <named-content content-type="genus-species">Salmonella enterica</named-content> subsp. <italic toggle="yes">enterica</italic> Serovar Typhimurium Infection in Neonatal Chickens
title_full Enrofloxacin Shifts Intestinal Microbiota and Metabolic Profiling and Hinders Recovery from <named-content content-type="genus-species">Salmonella enterica</named-content> subsp. <italic toggle="yes">enterica</italic> Serovar Typhimurium Infection in Neonatal Chickens
title_fullStr Enrofloxacin Shifts Intestinal Microbiota and Metabolic Profiling and Hinders Recovery from <named-content content-type="genus-species">Salmonella enterica</named-content> subsp. <italic toggle="yes">enterica</italic> Serovar Typhimurium Infection in Neonatal Chickens
title_full_unstemmed Enrofloxacin Shifts Intestinal Microbiota and Metabolic Profiling and Hinders Recovery from <named-content content-type="genus-species">Salmonella enterica</named-content> subsp. <italic toggle="yes">enterica</italic> Serovar Typhimurium Infection in Neonatal Chickens
title_sort enrofloxacin shifts intestinal microbiota and metabolic profiling and hinders recovery from <named-content content-type="genus-species">salmonella enterica</named-content> subsp. <italic toggle="yes">enterica</italic> serovar typhimurium infection in neonatal chickens
publisher American Society for Microbiology
publishDate 2020
url https://doaj.org/article/ab09c8ab32ec43f8bd2f375c3c0a6f23
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