Natural and artificial feeding management before weaning promote different rumen microbial colonization but not differences in gene expression levels at the rumen epithelium of newborn goats

Leticia Abecia, Elisabeth Jiménez, Gonzalo Martínez-Fernandez, A Ignacio Martín-García, Eva Ramos-Morales, Eric Pinloche, Stuart E Denman, C Jamie Newbold, David R Yáñez-Ruiz

Research output: Contribution to journalArticle

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Abstract

The aim of this work was to evaluate the effect of feeding management during the first month of life (natural with the mother, NAT, or artificial with milk replacer, ART) on the rumen microbial colonization and the host innate immune response. Thirty pregnant goats carrying two fetuses were used. At birth one kid was taken immediately away from the doe and fed milk replacer (ART) while the other remained with the mother (NAT). Kids from groups received colostrum during first 2 days of life. Groups of four kids (from ART and NAT experimental groups) were slaughtered at 1, 3, 7, 14, 21 and 28 days of life. On the sampling day, after slaughtering, the rumen content was sampled and epithelial rumen tissue was collected. Pyrosequencing analyses of the bacterial community structure on samples collected at 3, 7, 14 and 28 days showed that both systems promoted significantly different colonization patterns (P = 0.001). Diversity indices increased with age and were higher in NAT feeding system. Lower mRNA abundance was detected in TLR2, TLR8 and TLR10 in days 3 and 5 compared to the other days (7, 14, 21 and 28). Only TLR5 showed a significantly different level of expression according to the feeding system, presenting higher mRNA abundances in ART kids. PGLYRP1 showed significantly higher abundance levels in days 3, 5 and 7, and then experienced a decline independently of the feeding system. These observations confirmed a highly diverse microbial colonisation from the first day of life in the undeveloped rumen, and show that the colonization pattern substantially differs between pre-ruminants reared under natural or artificial milk feeding systems. However, the rumen epithelial immune development does not differentially respond to distinct microbial colonization patterns.

Original languageEnglish
Article numbere0182235
JournalPLoS ONE
Volume12
Issue number8
Early online date16 Aug 2017
DOIs
Publication statusFirst published - 16 Aug 2017
Externally publishedYes

Fingerprint

Nutritional Support
Rumen
Weaning
Goats
Epithelium
Gene Expression
Milk
Bacterial Structures
Messenger RNA
Colostrum
Ruminants
Innate Immunity
Fetus
Parturition
N-acetyltalosaminuronic acid

Keywords

  • Animal Feed
  • Animals
  • Biodiversity
  • Biomarkers
  • DNA Barcoding, Taxonomic
  • Female
  • Gastric Mucosa/immunology
  • Gastrointestinal Microbiome
  • Gene Expression
  • Goats
  • Immunoglobulin A/blood
  • Immunoglobulin G/blood
  • Metagenome
  • Metagenomics/methods
  • Nutritional Support
  • Pregnancy
  • Rumen/immunology
  • Weaning

Cite this

Abecia, Leticia ; Jiménez, Elisabeth ; Martínez-Fernandez, Gonzalo ; Martín-García, A Ignacio ; Ramos-Morales, Eva ; Pinloche, Eric ; Denman, Stuart E ; Newbold, C Jamie ; Yáñez-Ruiz, David R. / Natural and artificial feeding management before weaning promote different rumen microbial colonization but not differences in gene expression levels at the rumen epithelium of newborn goats. In: PLoS ONE. 2017 ; Vol. 12, No. 8.
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Natural and artificial feeding management before weaning promote different rumen microbial colonization but not differences in gene expression levels at the rumen epithelium of newborn goats. / Abecia, Leticia; Jiménez, Elisabeth; Martínez-Fernandez, Gonzalo; Martín-García, A Ignacio; Ramos-Morales, Eva; Pinloche, Eric; Denman, Stuart E; Newbold, C Jamie; Yáñez-Ruiz, David R.

In: PLoS ONE, Vol. 12, No. 8, e0182235, 16.08.2017.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Natural and artificial feeding management before weaning promote different rumen microbial colonization but not differences in gene expression levels at the rumen epithelium of newborn goats

AU - Abecia, Leticia

AU - Jiménez, Elisabeth

AU - Martínez-Fernandez, Gonzalo

AU - Martín-García, A Ignacio

AU - Ramos-Morales, Eva

AU - Pinloche, Eric

AU - Denman, Stuart E

AU - Newbold, C Jamie

AU - Yáñez-Ruiz, David R

PY - 2017/8/16

Y1 - 2017/8/16

N2 - The aim of this work was to evaluate the effect of feeding management during the first month of life (natural with the mother, NAT, or artificial with milk replacer, ART) on the rumen microbial colonization and the host innate immune response. Thirty pregnant goats carrying two fetuses were used. At birth one kid was taken immediately away from the doe and fed milk replacer (ART) while the other remained with the mother (NAT). Kids from groups received colostrum during first 2 days of life. Groups of four kids (from ART and NAT experimental groups) were slaughtered at 1, 3, 7, 14, 21 and 28 days of life. On the sampling day, after slaughtering, the rumen content was sampled and epithelial rumen tissue was collected. Pyrosequencing analyses of the bacterial community structure on samples collected at 3, 7, 14 and 28 days showed that both systems promoted significantly different colonization patterns (P = 0.001). Diversity indices increased with age and were higher in NAT feeding system. Lower mRNA abundance was detected in TLR2, TLR8 and TLR10 in days 3 and 5 compared to the other days (7, 14, 21 and 28). Only TLR5 showed a significantly different level of expression according to the feeding system, presenting higher mRNA abundances in ART kids. PGLYRP1 showed significantly higher abundance levels in days 3, 5 and 7, and then experienced a decline independently of the feeding system. These observations confirmed a highly diverse microbial colonisation from the first day of life in the undeveloped rumen, and show that the colonization pattern substantially differs between pre-ruminants reared under natural or artificial milk feeding systems. However, the rumen epithelial immune development does not differentially respond to distinct microbial colonization patterns.

AB - The aim of this work was to evaluate the effect of feeding management during the first month of life (natural with the mother, NAT, or artificial with milk replacer, ART) on the rumen microbial colonization and the host innate immune response. Thirty pregnant goats carrying two fetuses were used. At birth one kid was taken immediately away from the doe and fed milk replacer (ART) while the other remained with the mother (NAT). Kids from groups received colostrum during first 2 days of life. Groups of four kids (from ART and NAT experimental groups) were slaughtered at 1, 3, 7, 14, 21 and 28 days of life. On the sampling day, after slaughtering, the rumen content was sampled and epithelial rumen tissue was collected. Pyrosequencing analyses of the bacterial community structure on samples collected at 3, 7, 14 and 28 days showed that both systems promoted significantly different colonization patterns (P = 0.001). Diversity indices increased with age and were higher in NAT feeding system. Lower mRNA abundance was detected in TLR2, TLR8 and TLR10 in days 3 and 5 compared to the other days (7, 14, 21 and 28). Only TLR5 showed a significantly different level of expression according to the feeding system, presenting higher mRNA abundances in ART kids. PGLYRP1 showed significantly higher abundance levels in days 3, 5 and 7, and then experienced a decline independently of the feeding system. These observations confirmed a highly diverse microbial colonisation from the first day of life in the undeveloped rumen, and show that the colonization pattern substantially differs between pre-ruminants reared under natural or artificial milk feeding systems. However, the rumen epithelial immune development does not differentially respond to distinct microbial colonization patterns.

KW - Animal Feed

KW - Animals

KW - Biodiversity

KW - Biomarkers

KW - DNA Barcoding, Taxonomic

KW - Female

KW - Gastric Mucosa/immunology

KW - Gastrointestinal Microbiome

KW - Gene Expression

KW - Goats

KW - Immunoglobulin A/blood

KW - Immunoglobulin G/blood

KW - Metagenome

KW - Metagenomics/methods

KW - Nutritional Support

KW - Pregnancy

KW - Rumen/immunology

KW - Weaning

U2 - 10.1371/journal.pone.0182235

DO - 10.1371/journal.pone.0182235

M3 - Article

C2 - 28813529

VL - 12

JO - PLoS ONE

JF - PLoS ONE

SN - 1932-6203

IS - 8

M1 - e0182235

ER -