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

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

doi:10.1128/mBio.02171-19

mBio (Oct 2019)

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

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

Affiliations

Tonya L. Ward: Department of Veterinary and Biomedical Sciences, University of Minnesota, Saint Paul, Minnesota, USA
Bonnie P. Weber: Department of Veterinary and Biomedical Sciences, University of Minnesota, Saint Paul, Minnesota, USA
Kristelle M. Mendoza: Department of Veterinary and Biomedical Sciences, University of Minnesota, Saint Paul, Minnesota, USA
Jessica L. Danzeisen: Department of Veterinary and Biomedical Sciences, University of Minnesota, Saint Paul, Minnesota, USA
Katharine Llop: Department of Veterinary and Biomedical Sciences, University of Minnesota, Saint Paul, Minnesota, USA
Kevin Lang: Department of Veterinary and Biomedical Sciences, University of Minnesota, Saint Paul, Minnesota, USA
Jonathan B. Clayton: Department of Veterinary and Biomedical Sciences, University of Minnesota, Saint Paul, Minnesota, USA
Elicia Grace: Department of Veterinary and Biomedical Sciences, University of Minnesota, Saint Paul, Minnesota, USA
Jeanine Brannon: Department of Animal Science, University of Minnesota, Saint Paul, Minnesota, USA
Igor Radovic: Department of Animal Science, University of Minnesota, Saint Paul, Minnesota, USA
Mai Beauclaire: Department of Computer Science and Engineering, University of Minnesota, Minneapolis, Minnesota, USA
Timothy J. Heisel: Department of Pediatrics, University of Minnesota, Minneapolis, Minnesota, USA
Dan Knights: Department of Computer Science and Engineering, University of Minnesota, Minneapolis, Minnesota, USA
Carol Cardona: Department of Veterinary and Biomedical Sciences, University of Minnesota, Saint Paul, Minnesota, USA
Mike Kogut: Agricultural Research Service, United States Department of Agriculture, College Station, Texas, USA
Casey Johnson: Department of Animal and Food Sciences, University of Delaware, Newark, Delaware, USA
Sally L. Noll: Department of Animal Science, University of Minnesota, Saint Paul, Minnesota, USA
Ryan Arsenault: Department of Animal and Food Sciences, University of Delaware, Newark, Delaware, USA
Kent M. Reed: Department of Veterinary and Biomedical Sciences, University of Minnesota, Saint Paul, Minnesota, USA
Timothy J. Johnson: Department of Veterinary and Biomedical Sciences, University of Minnesota, Saint Paul, Minnesota, USA

DOI: https://doi.org/10.1128/mBio.02171-19
Journal volume & issue: Vol. 10, no. 5

Abstract

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ABSTRACT 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. IMPORTANCE 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.

Published in mBio

ISSN: 2161-2129 (Print); 2150-7511 (Online)
Publisher: American Society for Microbiology
Country of publisher: United States
LCC subjects: Science: Microbiology
Website: https://journals.asm.org/journal/mbio

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