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

Alternative approaches are greatly needed to reduce the need for antibiotic use in food animal production. This study utilized a pipeline for the development of a host-tailored probiotic to enhance performance in commercial turkeys and modulate their microbiota, similar to the effects of low-dose an...

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Main Authors: Tonya L. Ward, Bonnie P. Weber, Kristelle M. Mendoza, Jessica L. Danzeisen, Katharine Llop, Kevin Lang, Jonathan B. Clayton, Elicia Grace, Jeanine Brannon, Igor Radovic, Mai Beauclaire, Timothy J. Heisel, Dan Knights, Carol Cardona, Mike Kogut, Casey Johnson, Sally L. Noll, Ryan Arsenault, Kent M. Reed, Timothy J. Johnson
Format: Article
Language:English
Published: American Society for Microbiology 2019-10-01
Series:mBio
Subjects:
Online Access:https://doi.org/10.1128/mBio.02171-19
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spelling doaj-5e4fec16f9aa40ad93cd87a5a45517b02021-07-02T10:17:24ZengAmerican Society for MicrobiologymBio2150-75112019-10-01105e02171-1910.1128/mBio.02171-19Antibiotics and Host-Tailored Probiotics Similarly Modulate Effects on the Developing Avian Microbiome, Mycobiome, and Host Gene ExpressionTonya L. WardBonnie P. WeberKristelle M. MendozaJessica L. DanzeisenKatharine LlopKevin LangJonathan B. ClaytonElicia GraceJeanine BrannonIgor RadovicMai BeauclaireTimothy J. HeiselDan KnightsCarol CardonaMike KogutCasey JohnsonSally L. NollRyan ArsenaultKent M. ReedTimothy J. JohnsonAlternative approaches are greatly needed to reduce the need for antibiotic use in food animal production. This study utilized a pipeline for the development of a host-tailored probiotic to enhance performance in commercial turkeys and modulate their microbiota, similar to the effects of low-dose antibiotic administration. We determined that a host-tailored probiotic, developed in the context of the commercial turkey gut microbiome, was more effective at modulating these parameters than a nontailored probiotic cocktail. Furthermore, the host-tailored probiotic mimicked many of the effects of a low-dose antibiotic growth promoter. Surprisingly, the effects of the antibiotic growth promoter and host-tailored probiotic were observed across kingdoms, illustrating the coordinated interkingdom effects of these approaches. This work suggests that tailored approaches to probiotic development hold promise for modulating the avian host and its microbiota.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.https://doi.org/10.1128/mBio.02171-19antibioticbacteriafungihostmicrobiotapoultryprobiotics
collection DOAJ
language English
format Article
sources DOAJ
author Tonya L. Ward
Bonnie P. Weber
Kristelle M. Mendoza
Jessica L. Danzeisen
Katharine Llop
Kevin Lang
Jonathan B. Clayton
Elicia Grace
Jeanine Brannon
Igor Radovic
Mai Beauclaire
Timothy J. Heisel
Dan Knights
Carol Cardona
Mike Kogut
Casey Johnson
Sally L. Noll
Ryan Arsenault
Kent M. Reed
Timothy J. Johnson
spellingShingle Tonya L. Ward
Bonnie P. Weber
Kristelle M. Mendoza
Jessica L. Danzeisen
Katharine Llop
Kevin Lang
Jonathan B. Clayton
Elicia Grace
Jeanine Brannon
Igor Radovic
Mai Beauclaire
Timothy J. Heisel
Dan Knights
Carol Cardona
Mike Kogut
Casey Johnson
Sally L. Noll
Ryan Arsenault
Kent M. Reed
Timothy J. Johnson
Antibiotics and Host-Tailored Probiotics Similarly Modulate Effects on the Developing Avian Microbiome, Mycobiome, and Host Gene Expression
mBio
antibiotic
bacteria
fungi
host
microbiota
poultry
probiotics
author_facet Tonya L. Ward
Bonnie P. Weber
Kristelle M. Mendoza
Jessica L. Danzeisen
Katharine Llop
Kevin Lang
Jonathan B. Clayton
Elicia Grace
Jeanine Brannon
Igor Radovic
Mai Beauclaire
Timothy J. Heisel
Dan Knights
Carol Cardona
Mike Kogut
Casey Johnson
Sally L. Noll
Ryan Arsenault
Kent M. Reed
Timothy J. Johnson
author_sort Tonya L. Ward
title 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_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_sort antibiotics and host-tailored probiotics similarly modulate effects on the developing avian microbiome, mycobiome, and host gene expression
publisher American Society for Microbiology
series mBio
issn 2150-7511
publishDate 2019-10-01
description Alternative approaches are greatly needed to reduce the need for antibiotic use in food animal production. This study utilized a pipeline for the development of a host-tailored probiotic to enhance performance in commercial turkeys and modulate their microbiota, similar to the effects of low-dose antibiotic administration. We determined that a host-tailored probiotic, developed in the context of the commercial turkey gut microbiome, was more effective at modulating these parameters than a nontailored probiotic cocktail. Furthermore, the host-tailored probiotic mimicked many of the effects of a low-dose antibiotic growth promoter. Surprisingly, the effects of the antibiotic growth promoter and host-tailored probiotic were observed across kingdoms, illustrating the coordinated interkingdom effects of these approaches. This work suggests that tailored approaches to probiotic development hold promise for modulating the avian host and its microbiota.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.
topic antibiotic
bacteria
fungi
host
microbiota
poultry
probiotics
url https://doi.org/10.1128/mBio.02171-19
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