Cargando…

Antibiotics and Host-Tailored Probiotics Similarly Modulate Effects on the Developing Avian Microbiome, Mycobiome, and Host Gene Expression

The microbiome is important to all animals, including poultry, playing a critical role in health and performance. Low-dose antibiotics have historically been used to modulate food production animals and their microbiome. Identifying alternatives to antibiotics conferring similar modulatory propertie...

Descripción completa

Detalles Bibliográficos
Autores principales: Ward, Tonya L., Weber, Bonnie P., Mendoza, Kristelle M., Danzeisen, Jessica L., Llop, Katharine, Lang, Kevin, Clayton, Jonathan B., Grace, Elicia, Brannon, Jeanine, Radovic, Igor, Beauclaire, Mai, Heisel, Timothy J., Knights, Dan, Cardona, Carol, Kogut, Mike, Johnson, Casey, Noll, Sally L., Arsenault, Ryan, Reed, Kent M., Johnson, Timothy J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6794479/
https://www.ncbi.nlm.nih.gov/pubmed/31615957
http://dx.doi.org/10.1128/mBio.02171-19
_version_ 1783459303612481536
author Ward, Tonya L.
Weber, Bonnie P.
Mendoza, Kristelle M.
Danzeisen, Jessica L.
Llop, Katharine
Lang, Kevin
Clayton, Jonathan B.
Grace, Elicia
Brannon, Jeanine
Radovic, Igor
Beauclaire, Mai
Heisel, Timothy J.
Knights, Dan
Cardona, Carol
Kogut, Mike
Johnson, Casey
Noll, Sally L.
Arsenault, Ryan
Reed, Kent M.
Johnson, Timothy J.
author_facet Ward, Tonya L.
Weber, Bonnie P.
Mendoza, Kristelle M.
Danzeisen, Jessica L.
Llop, Katharine
Lang, Kevin
Clayton, Jonathan B.
Grace, Elicia
Brannon, Jeanine
Radovic, Igor
Beauclaire, Mai
Heisel, Timothy J.
Knights, Dan
Cardona, Carol
Kogut, Mike
Johnson, Casey
Noll, Sally L.
Arsenault, Ryan
Reed, Kent M.
Johnson, Timothy J.
author_sort Ward, Tonya L.
collection PubMed
description The microbiome is important to all animals, including poultry, playing a critical role in health and performance. Low-dose antibiotics have historically been used to modulate food production animals and their microbiome. Identifying alternatives to antibiotics conferring similar modulatory properties has been elusive. The purpose of this study was to determine if a host-tailored probiotic could recapitulate effects of a low-dose antibiotic on host response and the developing microbiome. Over 13 days of life, turkey poults were supplemented continuously with a low-dose antibiotic or oral supplementation of a prebiotic with or without two different probiotics (8 cage units, n = 80 per group). Gastrointestinal bacterial and fungal communities of poults were characterized by 16S rRNA gene and ITS2 amplicon sequencing. Localized and systemic host gene expression was assessed using transcriptome sequencing (RNA-Seq), kinase activity was assessed by avian-specific kinome peptide arrays, and performance parameters were assessed. We found that development of the early-life microbiome of turkey poults was tightly ordered in a tissue- and time-specific manner. Low-dose antibiotic and turkey-tailored probiotic supplementation, but not nontailored probiotic supplementation, elicited similar shifts in overall microbiome composition during development compared to controls. Treatment-induced bacterial changes were accompanied by parallel shifts in the fungal community and host gene expression and enhanced performance metrics. These results were validated in pen trials that identified further additive effects of the turkey-tailored probiotic combined with different prebiotics. Alternative approaches to low-dose antibiotic use in poultry are feasible and can be optimized utilizing the indigenous poultry microbiome. Similar approaches may also be beneficial for humans.
format Online
Article
Text
id pubmed-6794479
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher American Society for Microbiology
record_format MEDLINE/PubMed
spelling pubmed-67944792019-10-21 Antibiotics and Host-Tailored Probiotics Similarly Modulate Effects on the Developing Avian Microbiome, Mycobiome, and Host Gene Expression Ward, Tonya L. Weber, Bonnie P. Mendoza, Kristelle M. Danzeisen, Jessica L. Llop, Katharine Lang, Kevin Clayton, Jonathan B. Grace, Elicia Brannon, Jeanine Radovic, Igor Beauclaire, Mai Heisel, Timothy J. Knights, Dan Cardona, Carol Kogut, Mike Johnson, Casey Noll, Sally L. Arsenault, Ryan Reed, Kent M. Johnson, Timothy J. mBio Research Article The microbiome is important to all animals, including poultry, playing a critical role in health and performance. Low-dose antibiotics have historically been used to modulate food production animals and their microbiome. Identifying alternatives to antibiotics conferring similar modulatory properties has been elusive. The purpose of this study was to determine if a host-tailored probiotic could recapitulate effects of a low-dose antibiotic on host response and the developing microbiome. Over 13 days of life, turkey poults were supplemented continuously with a low-dose antibiotic or oral supplementation of a prebiotic with or without two different probiotics (8 cage units, n = 80 per group). Gastrointestinal bacterial and fungal communities of poults were characterized by 16S rRNA gene and ITS2 amplicon sequencing. Localized and systemic host gene expression was assessed using transcriptome sequencing (RNA-Seq), kinase activity was assessed by avian-specific kinome peptide arrays, and performance parameters were assessed. We found that development of the early-life microbiome of turkey poults was tightly ordered in a tissue- and time-specific manner. Low-dose antibiotic and turkey-tailored probiotic supplementation, but not nontailored probiotic supplementation, elicited similar shifts in overall microbiome composition during development compared to controls. Treatment-induced bacterial changes were accompanied by parallel shifts in the fungal community and host gene expression and enhanced performance metrics. These results were validated in pen trials that identified further additive effects of the turkey-tailored probiotic combined with different prebiotics. Alternative approaches to low-dose antibiotic use in poultry are feasible and can be optimized utilizing the indigenous poultry microbiome. Similar approaches may also be beneficial for humans. American Society for Microbiology 2019-10-15 /pmc/articles/PMC6794479/ /pubmed/31615957 http://dx.doi.org/10.1128/mBio.02171-19 Text en Copyright © 2019 Ward et al. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Ward, Tonya L.
Weber, Bonnie P.
Mendoza, Kristelle M.
Danzeisen, Jessica L.
Llop, Katharine
Lang, Kevin
Clayton, Jonathan B.
Grace, Elicia
Brannon, Jeanine
Radovic, Igor
Beauclaire, Mai
Heisel, Timothy J.
Knights, Dan
Cardona, Carol
Kogut, Mike
Johnson, Casey
Noll, Sally L.
Arsenault, Ryan
Reed, Kent M.
Johnson, Timothy J.
Antibiotics and Host-Tailored Probiotics Similarly Modulate Effects on the Developing Avian Microbiome, Mycobiome, and Host Gene Expression
title Antibiotics and Host-Tailored Probiotics Similarly Modulate Effects on the Developing Avian Microbiome, Mycobiome, and Host Gene Expression
title_full Antibiotics and Host-Tailored Probiotics Similarly Modulate Effects on the Developing Avian Microbiome, Mycobiome, and Host Gene Expression
title_fullStr Antibiotics and Host-Tailored Probiotics Similarly Modulate Effects on the Developing Avian Microbiome, Mycobiome, and Host Gene Expression
title_full_unstemmed Antibiotics and Host-Tailored Probiotics Similarly Modulate Effects on the Developing Avian Microbiome, Mycobiome, and Host Gene Expression
title_short Antibiotics and Host-Tailored Probiotics Similarly Modulate Effects on the Developing Avian Microbiome, Mycobiome, and Host Gene Expression
title_sort antibiotics and host-tailored probiotics similarly modulate effects on the developing avian microbiome, mycobiome, and host gene expression
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6794479/
https://www.ncbi.nlm.nih.gov/pubmed/31615957
http://dx.doi.org/10.1128/mBio.02171-19
work_keys_str_mv AT wardtonyal antibioticsandhosttailoredprobioticssimilarlymodulateeffectsonthedevelopingavianmicrobiomemycobiomeandhostgeneexpression
AT weberbonniep antibioticsandhosttailoredprobioticssimilarlymodulateeffectsonthedevelopingavianmicrobiomemycobiomeandhostgeneexpression
AT mendozakristellem antibioticsandhosttailoredprobioticssimilarlymodulateeffectsonthedevelopingavianmicrobiomemycobiomeandhostgeneexpression
AT danzeisenjessical antibioticsandhosttailoredprobioticssimilarlymodulateeffectsonthedevelopingavianmicrobiomemycobiomeandhostgeneexpression
AT llopkatharine antibioticsandhosttailoredprobioticssimilarlymodulateeffectsonthedevelopingavianmicrobiomemycobiomeandhostgeneexpression
AT langkevin antibioticsandhosttailoredprobioticssimilarlymodulateeffectsonthedevelopingavianmicrobiomemycobiomeandhostgeneexpression
AT claytonjonathanb antibioticsandhosttailoredprobioticssimilarlymodulateeffectsonthedevelopingavianmicrobiomemycobiomeandhostgeneexpression
AT graceelicia antibioticsandhosttailoredprobioticssimilarlymodulateeffectsonthedevelopingavianmicrobiomemycobiomeandhostgeneexpression
AT brannonjeanine antibioticsandhosttailoredprobioticssimilarlymodulateeffectsonthedevelopingavianmicrobiomemycobiomeandhostgeneexpression
AT radovicigor antibioticsandhosttailoredprobioticssimilarlymodulateeffectsonthedevelopingavianmicrobiomemycobiomeandhostgeneexpression
AT beauclairemai antibioticsandhosttailoredprobioticssimilarlymodulateeffectsonthedevelopingavianmicrobiomemycobiomeandhostgeneexpression
AT heiseltimothyj antibioticsandhosttailoredprobioticssimilarlymodulateeffectsonthedevelopingavianmicrobiomemycobiomeandhostgeneexpression
AT knightsdan antibioticsandhosttailoredprobioticssimilarlymodulateeffectsonthedevelopingavianmicrobiomemycobiomeandhostgeneexpression
AT cardonacarol antibioticsandhosttailoredprobioticssimilarlymodulateeffectsonthedevelopingavianmicrobiomemycobiomeandhostgeneexpression
AT kogutmike antibioticsandhosttailoredprobioticssimilarlymodulateeffectsonthedevelopingavianmicrobiomemycobiomeandhostgeneexpression
AT johnsoncasey antibioticsandhosttailoredprobioticssimilarlymodulateeffectsonthedevelopingavianmicrobiomemycobiomeandhostgeneexpression
AT nollsallyl antibioticsandhosttailoredprobioticssimilarlymodulateeffectsonthedevelopingavianmicrobiomemycobiomeandhostgeneexpression
AT arsenaultryan antibioticsandhosttailoredprobioticssimilarlymodulateeffectsonthedevelopingavianmicrobiomemycobiomeandhostgeneexpression
AT reedkentm antibioticsandhosttailoredprobioticssimilarlymodulateeffectsonthedevelopingavianmicrobiomemycobiomeandhostgeneexpression
AT johnsontimothyj antibioticsandhosttailoredprobioticssimilarlymodulateeffectsonthedevelopingavianmicrobiomemycobiomeandhostgeneexpression