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Cited by 136Ruminant Nutrition and Digestive PhysiologyAnimal Nutrition and PhysiologyGut microbiota and health

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Weaning age influences the severity of gastrointestinal microbiome shifts in dairy calves

Open access
Meale, S. J., Li, S. C., Azevedo, P., Derakhshani, H., DeVries, T. J., Plaizier, J. C., Steele, M. A., Khafipour, E.·2017·Scientific Reports
DOI 10.1038/s41598-017-00223-7PMC PMC5428063
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Abstract

Ruminants microbial consortium is responsible for ruminal fermentation, a process which converts fibrous feeds unsuitable for human consumption into desirable dairy and meat products, begins to establish soon after birth. However, it undergoes a significant transition when digestion shifts from the lower intestine to ruminal fermentation. We hypothesised that delaying the transition from a high milk diet to an exclusively solid food diet (weaning) would lessen the severity of changes in the gastrointestinal microbiome during this transition. β-diversity of ruminal and faecal microbiota shifted rapidly in early-weaned calves (6 weeks), whereas, a more gradual shift was observed in late-weaned calves (8 weeks) up to weaning. Bacteroidetes and Firmicutes were the most abundant ruminal phyla in pre- and post-weaned calves, respectively. Yet, the relative abundance of these phyla remained stable in faeces (P ≥ 0.391). Inferred gene families assigned to KEGG pathways revealed an increase in ruminal carbohydrate metabolism (P ≤ 0.009) at 9, compared to 5 weeks. Conversely, carbohydrate metabolism in faeces declined (P ≤ 0.002) following a change in weaning status (i.e., the shift from pre- to post-weaning). Our results indicate weaning later facilitates a more gradual shift in microbiota and could potentially explain the negative effects of early-weaning associated with feeding a high-plane of pre-weaning nutrition.

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Figure 1 Similarities of ruminal and faecal microbiota compared across weaning age [early-weaned (Wk 6) vs. late-weaned (Wk 8)] and calf age (Wk 5, Wk 7 and Wk 9). Distance between the samples, based on similarity in OTU composition (OTU similarity ≥97%) calculated using weighted UniFrac distance in the a) rumen, and b) faeces, were visualised in principal coordinates analysis (PCoA) plots. A greater distance between two points infers a lower similarity. The impact of weaning age × calf age on the clustering pattern of microbial communities was tested using PERMANOVA (implemented in PRIMER-6 software; significance was declared when P < 0.05). Within the rumen, weaning age × calf age differed (P = 0.035) across all ages and groups, with the exception (P > 0.05) of early- versus late-weaned calves at 9 weeks of age, which were similar. Weaning age × calf age also differed (P = 0.004) in the faeces, with the exception (P > 0.05) of early- versus late-weaned calves at 5 and 9 weeks of age, and in early-weaned calves aged 7, compared to 9 weeks of age.
Figure 1 Similarities of ruminal and faecal microbiota compared across weaning age [early-weaned (Wk 6) vs. late-weaned (Wk 8)] and calf age (Wk 5, Wk 7 and Wk 9). Distance between the samples, based on similarity in OTU composition (OTU similarity ≥97%) calculated using weighted UniFrac distance in the a) rumen, and b) faeces, were visualised in principal coordinates analysis (PCoA) plots. A greater distance between two points infers a lower similarity. The impact of weaning age × calf age on the clustering pattern of microbial communities was tested using PERMANOVA (implemented in PRIMER-6 software; significance was declared when P < 0.05). Within the rumen, weaning age × calf age differed (P = 0.035) across all ages and groups, with the exception (P > 0.05) of early- versus late-weaned calves at 9 weeks of age, which were similar. Weaning age × calf age also differed (P = 0.004) in the faeces, with the exception (P > 0.05) of early- versus late-weaned calves at 5 and 9 weeks of age, and in early-weaned calves aged 7, compared to 9 weeks of age.CC BY · PubMed Central
Figure 2 Phylum level composition. Bar plots showing average relative abundance of bacterial phyla (%) in (a) rumen and (b) faeces of early- (week 6) and late-weaned (week 8) calves for each weaning age.
Figure 2 Phylum level composition. Bar plots showing average relative abundance of bacterial phyla (%) in (a) rumen and (b) faeces of early- (week 6) and late-weaned (week 8) calves for each weaning age.CC BY · PubMed Central
Figure 3 Correlation between ruminal microbiota and calf age and weaning strategy. The heatmap shows bacterial abundance in rumen varied with calf age (5, 7 and 9 weeks) and weaning age (6 vs. 8 weeks for early- and late-weaning, respectively). Data represent taxa present at greater than 1% of community that were significantly different (P < 0.05) between at least two ages or between treatment groups (weaning age). See Table S1 for additional data. The OTU count data was subjected to variance stabilizing transformation and summarised to calculate genus abundant data. Hierarchically clustering was then performed based on complete linkage of Euclidean distances matrix and visualized over heatmap using the heatmap.2 function of the “gplots” R package.
Figure 3 Correlation between ruminal microbiota and calf age and weaning strategy. The heatmap shows bacterial abundance in rumen varied with calf age (5, 7 and 9 weeks) and weaning age (6 vs. 8 weeks for early- and late-weaning, respectively). Data represent taxa present at greater than 1% of community that were significantly different (P < 0.05) between at least two ages or between treatment groups (weaning age). See Table S1 for additional data. The OTU count data was subjected to variance stabilizing transformation and summarised to calculate genus abundant data. Hierarchically clustering was then performed based on complete linkage of Euclidean distances matrix and visualized over heatmap using the heatmap.2 function of the “gplots” R package.CC BY · PubMed Central
Figure 4 Correlation between faecal microbiota and calf age and weaning strategy. The heatmap shows bacterial abundance in faeces varied with calf age (5, 7 and 9 weeks) and weaning age (6 vs. 8 weeks for early- and late-weaning, respectively). Data presented represent taxa present at greater than 1% of community that were significantly different (P < 0.05) between at least two ages or between treatment groups (weaning age). See Table S2 for additional data. The OTU count data was subjected to variance stabilising transformation and summarised to calculate genus abundant data. Hierarchically clustering was then performed based on complete linkage of Euclidean distances matrix and visualised over heatmap using the heatmap.2 function of the “gplots” R package.
Figure 4 Correlation between faecal microbiota and calf age and weaning strategy. The heatmap shows bacterial abundance in faeces varied with calf age (5, 7 and 9 weeks) and weaning age (6 vs. 8 weeks for early- and late-weaning, respectively). Data presented represent taxa present at greater than 1% of community that were significantly different (P < 0.05) between at least two ages or between treatment groups (weaning age). See Table S2 for additional data. The OTU count data was subjected to variance stabilising transformation and summarised to calculate genus abundant data. Hierarchically clustering was then performed based on complete linkage of Euclidean distances matrix and visualised over heatmap using the heatmap.2 function of the “gplots” R package.CC BY · PubMed Central
Figure 5 Correlations between production variables and relative taxa abundance. Spearman non-parametric rank correlation matrix of the dominant bacterial genera across (a) rumen and (b) faecal samples. The genera were included in the matrix if they were in at least 50% of calves and represented at least 0.1% of the bacterial community in at least one calf. All correlations presented were statistically significant (P < 0.05), with strong correlations indicated by large circles and weaker correlations indicated by small circles. The scale colours denote whether the correlation is positive (closer to 1, blue circles) or negative (closer to −1, red circles) between the taxa and production variables. The OTU count data was subjected to variance stabilising transformation then pairwise Spearman correlations between bacterial genus and biological parameters at corresponding ages were analysed. P-values were adjusted for multiple comparisons.
Figure 5 Correlations between production variables and relative taxa abundance. Spearman non-parametric rank correlation matrix of the dominant bacterial genera across (a) rumen and (b) faecal samples. The genera were included in the matrix if they were in at least 50% of calves and represented at least 0.1% of the bacterial community in at least one calf. All correlations presented were statistically significant (P < 0.05), with strong correlations indicated by large circles and weaker correlations indicated by small circles. The scale colours denote whether the correlation is positive (closer to 1, blue circles) or negative (closer to −1, red circles) between the taxa and production variables. The OTU count data was subjected to variance stabilising transformation then pairwise Spearman correlations between bacterial genus and biological parameters at corresponding ages were analysed. P-values were adjusted for multiple comparisons.CC BY · PubMed Central
Figure 6 PICRUSt predicted summary of COG categories from 16S amplicon sequencing of (a) ruminal and (b) faecal microbiomes. Relative abundances of Level 2 KEGG pathways are depicted by calf age within treatment group (weaning age) in circular barplots. Relative abundances of the three most abundant L3 KEGG pathways involved in Carbohydrate Metabolism (Fructose and Mannose Metabolism, Glycose/gluconeogenesis and, Amino sugar and nucleotide sugar Metabolism) at different ages (5, 7, or 9) subjected to weaning at either 6 weeks (Early) or 8 weeks (Late) of age are also presented within the boxes. *P < 0.05 for the shown comparisons of L3 pathways (See Supplementary Tables 3–6 for complete KEGG data).
Figure 6 PICRUSt predicted summary of COG categories from 16S amplicon sequencing of (a) ruminal and (b) faecal microbiomes. Relative abundances of Level 2 KEGG pathways are depicted by calf age within treatment group (weaning age) in circular barplots. Relative abundances of the three most abundant L3 KEGG pathways involved in Carbohydrate Metabolism (Fructose and Mannose Metabolism, Glycose/gluconeogenesis and, Amino sugar and nucleotide sugar Metabolism) at different ages (5, 7, or 9) subjected to weaning at either 6 weeks (Early) or 8 weeks (Late) of age are also presented within the boxes. *P < 0.05 for the shown comparisons of L3 pathways (See Supplementary Tables 3–6 for complete KEGG data).CC BY · PubMed Central

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Cites

Research works printed but not linked: 3

  1. Church, D. C. Digestive Physiology and Nutrition of Ruminants. 2 edn, Vol. 1 (Corvallis OR: O&B Books, 1976).
  2. Hungate, R. E. (Academic Press, New York, 1966).
  3. Geishauser, T. An instrument for the collection and transfer of ruminal fluid and for the administration of water soluble drugs in adult cattle. Bovine Practice 27, 38–42 (1993).

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Metadata

Authors
Meale, S. J., Li, S. C., Azevedo, P., Derakhshani, H., DeVries, T. J., Plaizier, J. C., Steele, M. A., & Khafipour, E.
Affiliations
  • VetAgro Sup (FR)
  • University of Manitoba (CA)
  • University of Guelph (CA)
  • University of Alberta (CA)
Corresponding author
  • Steele, M. A.
  • Khafipour, E.
ORCID
Venue
Scientific Reports
Publisher
Springer Science and Business Media LLC
Published
2017-03-15
Volume
7
Issue
1
Pages
198-198
ISSN
2045-2322 (ISSN-L)
DOI
10.1038/s41598-017-00223-7
PMC
PMC5428063
OpenAlex
W2594291939
Cited by
133
References
53
Citations by year
2026: 9 · 2025: 10 · 2024: 14 · 2023: 17 · 2022: 22 · 2021: 19 · 2020: 19 · 2019: 10 · 2018: 11 · 2017: 2
FWCI
20.90
Type
journal article
Language
en
Open access
Licence
Locations
  • Scientific Reports (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • HAL (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Ruminant Nutrition and Digestive Physiology
  • Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Nutrition and Physiology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Keywords
weaning age, dairy calves, gastrointestinal microbiome, rumen microbiota, fecal microbiota, rumen fermentation, Bacteroidetes, Firmicutes, carbohydrate metabolism, early weaning, plane of nutrition, microbial diversity
MeSH terms
Bacillota, Gastrointestinal Microbiome, Animals, Cattle, Feces, Phylogeny, Rumen, Weaning, Bacteroidetes, Carbohydrate Metabolism

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