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Inoculation with rumen fluid in early life accelerates the rumen microbial development and favours the weaning process in goats

BACKGROUND: Newborn ruminants possess an underdeveloped rumen which is colonized by microorganisms acquired from adult animals and the surrounding environment. This microbial transfer can be limited in dairy systems in which newborns are separated from their dams at birth. This study explores whethe...

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Autores principales: Palma-Hidalgo, Juan Manuel, Jiménez, Elisabeth, Popova, Milka, Morgavi, Diego Pablo, Martín-García, Antonio Ignacio, Yáñez-Ruiz, David Rafael, Belanche, Alejandro
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7814744/
https://www.ncbi.nlm.nih.gov/pubmed/33499992
http://dx.doi.org/10.1186/s42523-021-00073-9
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author Palma-Hidalgo, Juan Manuel
Jiménez, Elisabeth
Popova, Milka
Morgavi, Diego Pablo
Martín-García, Antonio Ignacio
Yáñez-Ruiz, David Rafael
Belanche, Alejandro
author_facet Palma-Hidalgo, Juan Manuel
Jiménez, Elisabeth
Popova, Milka
Morgavi, Diego Pablo
Martín-García, Antonio Ignacio
Yáñez-Ruiz, David Rafael
Belanche, Alejandro
author_sort Palma-Hidalgo, Juan Manuel
collection PubMed
description BACKGROUND: Newborn ruminants possess an underdeveloped rumen which is colonized by microorganisms acquired from adult animals and the surrounding environment. This microbial transfer can be limited in dairy systems in which newborns are separated from their dams at birth. This study explores whether the direct inoculation of fresh or autoclaved rumen fluid from adult goats to newborn kids has a beneficial effect on rumen microbial development and function. RESULTS: Repetitive inoculation of young kids with fresh rumen fluid from adult goats adapted to forage (RFF) or concentrate diets (RFC) accelerated microbial colonization of the rumen during the pre-weaning period leading to high protozoal numbers, a greater diversity of bacterial (+ 234 OTUs), methanogens (+ 6 OTUs) and protozoal communities (+ 25 OTUs) than observed in control kids (CTL) without inoculation. This inoculation also increased the size of the core bacterial and methanogens community and the abundance of key rumen bacteria (Ruminococcaceae, Fibrobacteres, Veillonellaceae, Rikenellaceae, Tenericutes), methanogens (Methanobrevibacter ruminantium, Methanomicrobium mobile and Group 9), anaerobic fungi (Piromyces and Orpinomyces) and protozoal taxa (Enoploplastron, Diplodinium, Polyplastron, Ophryoscolex, Isotricha and Dasytricha) before weaning whereas CTL kids remained protozoa-free through the study. Most of these taxa were positively correlated with indicators of the rumen microbiological and physiological development (higher forage and concentrate intakes and animal growth during the post-weaning period) favoring the weaning process in RFF and RFC kids in comparison to CTL kids. Some of these microbiological differences tended to decrease during the post-weaning period, although RFF and RFC kids retained a more complex and matured rumen microbial ecosystem than CTL kids. Inoculation with autoclaved rumen fluid promoted lower development of the bacterial and protozoal communities during the pre-weaning period than using fresh inocula, but it favored a more rapid microbial development during the post-weaning than observed for CTL kids. CONCLUSIONS: This study demonstrated that inoculation of young ruminants with fresh rumen fluid from adult animals accelerated the rumen microbial colonization which was associated with an earlier rumen functional development. This strategy facilitated a smoother transition from milk to solid feed favoring the animal performance during post-weaning and minimizing stress. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-021-00073-9.
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spelling pubmed-78147442021-01-19 Inoculation with rumen fluid in early life accelerates the rumen microbial development and favours the weaning process in goats Palma-Hidalgo, Juan Manuel Jiménez, Elisabeth Popova, Milka Morgavi, Diego Pablo Martín-García, Antonio Ignacio Yáñez-Ruiz, David Rafael Belanche, Alejandro Anim Microbiome Research Article BACKGROUND: Newborn ruminants possess an underdeveloped rumen which is colonized by microorganisms acquired from adult animals and the surrounding environment. This microbial transfer can be limited in dairy systems in which newborns are separated from their dams at birth. This study explores whether the direct inoculation of fresh or autoclaved rumen fluid from adult goats to newborn kids has a beneficial effect on rumen microbial development and function. RESULTS: Repetitive inoculation of young kids with fresh rumen fluid from adult goats adapted to forage (RFF) or concentrate diets (RFC) accelerated microbial colonization of the rumen during the pre-weaning period leading to high protozoal numbers, a greater diversity of bacterial (+ 234 OTUs), methanogens (+ 6 OTUs) and protozoal communities (+ 25 OTUs) than observed in control kids (CTL) without inoculation. This inoculation also increased the size of the core bacterial and methanogens community and the abundance of key rumen bacteria (Ruminococcaceae, Fibrobacteres, Veillonellaceae, Rikenellaceae, Tenericutes), methanogens (Methanobrevibacter ruminantium, Methanomicrobium mobile and Group 9), anaerobic fungi (Piromyces and Orpinomyces) and protozoal taxa (Enoploplastron, Diplodinium, Polyplastron, Ophryoscolex, Isotricha and Dasytricha) before weaning whereas CTL kids remained protozoa-free through the study. Most of these taxa were positively correlated with indicators of the rumen microbiological and physiological development (higher forage and concentrate intakes and animal growth during the post-weaning period) favoring the weaning process in RFF and RFC kids in comparison to CTL kids. Some of these microbiological differences tended to decrease during the post-weaning period, although RFF and RFC kids retained a more complex and matured rumen microbial ecosystem than CTL kids. Inoculation with autoclaved rumen fluid promoted lower development of the bacterial and protozoal communities during the pre-weaning period than using fresh inocula, but it favored a more rapid microbial development during the post-weaning than observed for CTL kids. CONCLUSIONS: This study demonstrated that inoculation of young ruminants with fresh rumen fluid from adult animals accelerated the rumen microbial colonization which was associated with an earlier rumen functional development. This strategy facilitated a smoother transition from milk to solid feed favoring the animal performance during post-weaning and minimizing stress. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-021-00073-9. BioMed Central 2021-01-19 /pmc/articles/PMC7814744/ /pubmed/33499992 http://dx.doi.org/10.1186/s42523-021-00073-9 Text en © The Author(s) 2021 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Research Article
Palma-Hidalgo, Juan Manuel
Jiménez, Elisabeth
Popova, Milka
Morgavi, Diego Pablo
Martín-García, Antonio Ignacio
Yáñez-Ruiz, David Rafael
Belanche, Alejandro
Inoculation with rumen fluid in early life accelerates the rumen microbial development and favours the weaning process in goats
title Inoculation with rumen fluid in early life accelerates the rumen microbial development and favours the weaning process in goats
title_full Inoculation with rumen fluid in early life accelerates the rumen microbial development and favours the weaning process in goats
title_fullStr Inoculation with rumen fluid in early life accelerates the rumen microbial development and favours the weaning process in goats
title_full_unstemmed Inoculation with rumen fluid in early life accelerates the rumen microbial development and favours the weaning process in goats
title_short Inoculation with rumen fluid in early life accelerates the rumen microbial development and favours the weaning process in goats
title_sort inoculation with rumen fluid in early life accelerates the rumen microbial development and favours the weaning process in goats
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7814744/
https://www.ncbi.nlm.nih.gov/pubmed/33499992
http://dx.doi.org/10.1186/s42523-021-00073-9
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