Fecal Microbiota Transplantation in Gestating Sows and Neonatal Offspring Alters Lifetime Intestinal Microbiota and Growth in Offspring

ABSTRACT Previous studies suggest a link between intestinal microbiota and porcine feed efficiency (FE). Therefore, we investigated whether fecal microbiota transplantation (FMT) in sows and/or neonatal offspring, using inocula derived from highly feed-efficient pigs, could improve offspring FE. Pre...

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Autores principales:	Ursula M. McCormack, Tânia Curião, Toby Wilkinson, Barbara U. Metzler-Zebeli, Henry Reyer, Tomas Ryan, Julia A. Calderon-Diaz, Fiona Crispie, Paul D. Cotter, Christopher J. Creevey, Gillian E. Gardiner, Peadar G. Lawlor
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	fecal microbiota transplantation feed efficiency intestinal microbiota pigs Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/3d1e31e4da2f4d15937ff570de44d235
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spelling	oai:doaj.org-article:3d1e31e4da2f4d15937ff570de44d2352021-12-02T19:46:17ZFecal Microbiota Transplantation in Gestating Sows and Neonatal Offspring Alters Lifetime Intestinal Microbiota and Growth in Offspring10.1128/mSystems.00134-172379-5077https://doaj.org/article/3d1e31e4da2f4d15937ff570de44d2352018-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00134-17https://doaj.org/toc/2379-5077ABSTRACT Previous studies suggest a link between intestinal microbiota and porcine feed efficiency (FE). Therefore, we investigated whether fecal microbiota transplantation (FMT) in sows and/or neonatal offspring, using inocula derived from highly feed-efficient pigs, could improve offspring FE. Pregnant sows were assigned to control or FMT treatments and the subsequent offspring to control treatment, FMT once (at birth), or FMT four times (between birth and weaning). FMT altered sow fecal and colostrum microbiota compositions and resulted in lighter offspring body weight at 70 and 155 days of age when administered to sows and/or offspring. This was accompanied by FMT-associated changes within the offspring’s intestinal microbiota, mostly in the ileum. These included transiently higher fecal bacterial diversity and load and numerous compositional differences at the phylum and genus levels (e.g., Spirochaetes and Bacteroidetes at high relative abundances and mostly members of Clostridia, respectively), as well as differences in the abundances of predicted bacterial pathways. In addition, intestinal morphology was negatively impacted, duodenal gene expression altered, and serum protein and cholesterol concentrations reduced due to FMT in sows and/or offspring. Taken together, the results suggest poorer absorptive capacity and intestinal health, most likely explaining the reduced body weight. An additive effect of FMT in sows and offspring also occurred for some parameters. Although these findings have negative implications for the practical use of the FMT regime used here for improving FE in pigs, they nonetheless demonstrate the enormous impact of early-life intestinal microbiota on the host phenotype. IMPORTANCE Here, for the first time, we investigate FMT as a novel strategy to modulate the porcine intestinal microbiota in an attempt to improve FE in pigs. However, reprogramming the maternal and/or offspring microbiome by using fecal transplants derived from highly feed-efficient pigs did not recapitulate the highly efficient phenotype in the offspring and, in fact, had detrimental effects on lifetime growth. Although these findings may not be wholly attributable to microbiota transplantation, as antibiotic and purgative were also part of the regime in sows, similar effects were also seen in offspring, in which these interventions were not used. Nonetheless, additional work is needed to unravel the effects of each component of the FMT regime and to provide additional mechanistic insights. This may lead to the development of an FMT procedure with practical applications for the improvement of FE in pigs, which could in turn improve the profitability of pig production.Ursula M. McCormackTânia CuriãoToby WilkinsonBarbara U. Metzler-ZebeliHenry ReyerTomas RyanJulia A. Calderon-DiazFiona CrispiePaul D. CotterChristopher J. CreeveyGillian E. GardinerPeadar G. LawlorAmerican Society for Microbiologyarticlefecal microbiota transplantationfeed efficiencyintestinal microbiotapigsMicrobiologyQR1-502ENmSystems, Vol 3, Iss 3 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	fecal microbiota transplantation feed efficiency intestinal microbiota pigs Microbiology QR1-502
spellingShingle	fecal microbiota transplantation feed efficiency intestinal microbiota pigs Microbiology QR1-502 Ursula M. McCormack Tânia Curião Toby Wilkinson Barbara U. Metzler-Zebeli Henry Reyer Tomas Ryan Julia A. Calderon-Diaz Fiona Crispie Paul D. Cotter Christopher J. Creevey Gillian E. Gardiner Peadar G. Lawlor Fecal Microbiota Transplantation in Gestating Sows and Neonatal Offspring Alters Lifetime Intestinal Microbiota and Growth in Offspring
description	ABSTRACT Previous studies suggest a link between intestinal microbiota and porcine feed efficiency (FE). Therefore, we investigated whether fecal microbiota transplantation (FMT) in sows and/or neonatal offspring, using inocula derived from highly feed-efficient pigs, could improve offspring FE. Pregnant sows were assigned to control or FMT treatments and the subsequent offspring to control treatment, FMT once (at birth), or FMT four times (between birth and weaning). FMT altered sow fecal and colostrum microbiota compositions and resulted in lighter offspring body weight at 70 and 155 days of age when administered to sows and/or offspring. This was accompanied by FMT-associated changes within the offspring’s intestinal microbiota, mostly in the ileum. These included transiently higher fecal bacterial diversity and load and numerous compositional differences at the phylum and genus levels (e.g., Spirochaetes and Bacteroidetes at high relative abundances and mostly members of Clostridia, respectively), as well as differences in the abundances of predicted bacterial pathways. In addition, intestinal morphology was negatively impacted, duodenal gene expression altered, and serum protein and cholesterol concentrations reduced due to FMT in sows and/or offspring. Taken together, the results suggest poorer absorptive capacity and intestinal health, most likely explaining the reduced body weight. An additive effect of FMT in sows and offspring also occurred for some parameters. Although these findings have negative implications for the practical use of the FMT regime used here for improving FE in pigs, they nonetheless demonstrate the enormous impact of early-life intestinal microbiota on the host phenotype. IMPORTANCE Here, for the first time, we investigate FMT as a novel strategy to modulate the porcine intestinal microbiota in an attempt to improve FE in pigs. However, reprogramming the maternal and/or offspring microbiome by using fecal transplants derived from highly feed-efficient pigs did not recapitulate the highly efficient phenotype in the offspring and, in fact, had detrimental effects on lifetime growth. Although these findings may not be wholly attributable to microbiota transplantation, as antibiotic and purgative were also part of the regime in sows, similar effects were also seen in offspring, in which these interventions were not used. Nonetheless, additional work is needed to unravel the effects of each component of the FMT regime and to provide additional mechanistic insights. This may lead to the development of an FMT procedure with practical applications for the improvement of FE in pigs, which could in turn improve the profitability of pig production.
format	article
author	Ursula M. McCormack Tânia Curião Toby Wilkinson Barbara U. Metzler-Zebeli Henry Reyer Tomas Ryan Julia A. Calderon-Diaz Fiona Crispie Paul D. Cotter Christopher J. Creevey Gillian E. Gardiner Peadar G. Lawlor
author_facet	Ursula M. McCormack Tânia Curião Toby Wilkinson Barbara U. Metzler-Zebeli Henry Reyer Tomas Ryan Julia A. Calderon-Diaz Fiona Crispie Paul D. Cotter Christopher J. Creevey Gillian E. Gardiner Peadar G. Lawlor
author_sort	Ursula M. McCormack
title	Fecal Microbiota Transplantation in Gestating Sows and Neonatal Offspring Alters Lifetime Intestinal Microbiota and Growth in Offspring
title_short	Fecal Microbiota Transplantation in Gestating Sows and Neonatal Offspring Alters Lifetime Intestinal Microbiota and Growth in Offspring
title_full	Fecal Microbiota Transplantation in Gestating Sows and Neonatal Offspring Alters Lifetime Intestinal Microbiota and Growth in Offspring
title_fullStr	Fecal Microbiota Transplantation in Gestating Sows and Neonatal Offspring Alters Lifetime Intestinal Microbiota and Growth in Offspring
title_full_unstemmed	Fecal Microbiota Transplantation in Gestating Sows and Neonatal Offspring Alters Lifetime Intestinal Microbiota and Growth in Offspring
title_sort	fecal microbiota transplantation in gestating sows and neonatal offspring alters lifetime intestinal microbiota and growth in offspring
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/3d1e31e4da2f4d15937ff570de44d235
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Fecal Microbiota Transplantation in Gestating Sows and Neonatal Offspring Alters Lifetime Intestinal Microbiota and Growth in Offspring

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