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Illumina MiSeq Phylogenetic Amplicon Sequencing Shows a Large Reduction of an Uncharacterised Succinivibrionaceae and an Increase of the Methanobrevibacter gottschalkii Clade in Feed Restricted Cattle.

McCabe MS, Cormican P, Keogh K, O'Connor A, O'Hara E, Palladino RA, Kenny DA, Waters SM - PLoS ONE (2015)

Bottom Line: Illumina Miseq Phylogenetic marker amplicon sequencing of DNA extracted from rumen contents of 55 bulls showed that restriction of feed (70% concentrate, 30% grass silage) for 125 days, to levels that caused a 60% reduction of growth rate, resulted in a large increase of relative abundance of Methanobrevibacter gottschalkii clade (designated as OTU-M7), and a large reduction of an uncharacterised Succinivibrionaceae species (designated as OTU-S3004).Reduced A:P ratios in the rumen are associated with increased feed efficiency and reduced production of methane which has a global warming potential (GWP 100 years) of 28.Succinivibrionaceae growth in the rumen was previously suggested to reduce methane emissions as some members of this family utilise hydrogen, which is also utilised by methanogens for methanogenesis, to generate succinate which is converted to propionate.

View Article: PubMed Central - PubMed

Affiliation: Animal and Bioscience Research Department, Animal and Grassland Research and Innovation Centre, Teagasc, Grange, Dunsany, County Meath, Ireland.

ABSTRACT
Periodic feed restriction is used in cattle production to reduce feed costs. When normal feed levels are resumed, cattle catch up to a normal weight by an acceleration of normal growth rate, known as compensatory growth, which is not yet fully understood. Illumina Miseq Phylogenetic marker amplicon sequencing of DNA extracted from rumen contents of 55 bulls showed that restriction of feed (70% concentrate, 30% grass silage) for 125 days, to levels that caused a 60% reduction of growth rate, resulted in a large increase of relative abundance of Methanobrevibacter gottschalkii clade (designated as OTU-M7), and a large reduction of an uncharacterised Succinivibrionaceae species (designated as OTU-S3004). There was a strong negative Spearman correlation (ρ = -0.72, P = <1x10(-20)) between relative abundances of OTU-3004 and OTU-M7 in the liquid rumen fraction. There was also a significant increase in acetate:propionate ratio (A:P) in feed restricted animals that showed a negative Spearman correlation (ρ = -0.69, P = <1x10(-20)) with the relative abundance of OTU-S3004 in the rumen liquid fraction but not the solid fraction, and a strong positive Spearman correlation with OTU-M7 in the rumen liquid (ρ = 0.74, P = <1x10(-20)) and solid (ρ = 0.69, P = <1x10(-20)) fractions. Reduced A:P ratios in the rumen are associated with increased feed efficiency and reduced production of methane which has a global warming potential (GWP 100 years) of 28. Succinivibrionaceae growth in the rumen was previously suggested to reduce methane emissions as some members of this family utilise hydrogen, which is also utilised by methanogens for methanogenesis, to generate succinate which is converted to propionate. Relative abundance of OTU-S3004 showed a positive Spearman correlation with propionate (ρ = 0.41, P = <0.01) but not acetate in the liquid rumen fraction.

No MeSH data available.


Related in: MedlinePlus

Differences in relative abundance of succinate and propionate producers between treatment groups.Box and whisker plots showing median, quartiles, maximum and minimum values, and outliers (asterisks) for the sum of relative abundances within each rumen sample of OTUs assigned to taxonomic groups (apart from Succinivibrionaceae) which are, or have members which are, succinate and propionate (S and P) producers. ‘Total S and P’ box and whisker plot shows sum of relative abundances of all OTUs assigned to S and P taxonomic groups excluding OTU-S3004 (white boxes-) and including OTU-S3004 (grey boxes +). LR = Liquid Restricted (n = 14), SR = Solid Restricted (n = 14), LA = Liquid Ad lib (n = 13), SA = Solid Ad lib (n = 13), LRA = Liquid Restricted/Ad lib (n = 15), SRA = Solid Restricted/Ad lib (n = 15), LAA = Liquid Ad lib/Ad lib (n = 13), SAA = Solid Ad lib/Ad lib (n = 13).
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pone.0133234.g008: Differences in relative abundance of succinate and propionate producers between treatment groups.Box and whisker plots showing median, quartiles, maximum and minimum values, and outliers (asterisks) for the sum of relative abundances within each rumen sample of OTUs assigned to taxonomic groups (apart from Succinivibrionaceae) which are, or have members which are, succinate and propionate (S and P) producers. ‘Total S and P’ box and whisker plot shows sum of relative abundances of all OTUs assigned to S and P taxonomic groups excluding OTU-S3004 (white boxes-) and including OTU-S3004 (grey boxes +). LR = Liquid Restricted (n = 14), SR = Solid Restricted (n = 14), LA = Liquid Ad lib (n = 13), SA = Solid Ad lib (n = 13), LRA = Liquid Restricted/Ad lib (n = 15), SRA = Solid Restricted/Ad lib (n = 15), LAA = Liquid Ad lib/Ad lib (n = 13), SAA = Solid Ad lib/Ad lib (n = 13).

Mentions: To try and determine the extent to which OTU-S3004 might influence rumen A:P ratio, we also looked at the abundance of OTUs which were assigned to 7 taxons (Veillonellaceae Megasphaera, Ruminococcus flavefaciens, Prevotella, Selenomonas ruminantium, Veillonellaceae Succiniclasticum, Fibrobacter succinogenes, Spirochaetaceae Treponema) that are, or contain members which are, known succinate and/or propionate (S and P) producers [54, 55] (Fig 8). The overall sum of the relative abundances of these S and P producers was reduced in group R, mainly due to decreases in Prevotella, R. flavefaciens and Megasphaera. Several of these taxonomic groups were clearly more associated with either the solid (e.g. Treponema, R. flavefaciens), or liquid (e.g. Prevotella) fraction. Addition of the relative abundance values for OTU-S3004 results in a large increase in overall abundance of S and P producers in the liquid fraction (Fig 8). Selenomonas ruminantium, which is thought to be one of the main rumen bacterial species that converts succinate to propionate and can account for up to 51% of the total viable bacterial count in the rumen [56, 57], but is undetectable under certain feeding regimes [58], was only detected as <1% in most animals in our study.


Illumina MiSeq Phylogenetic Amplicon Sequencing Shows a Large Reduction of an Uncharacterised Succinivibrionaceae and an Increase of the Methanobrevibacter gottschalkii Clade in Feed Restricted Cattle.

McCabe MS, Cormican P, Keogh K, O'Connor A, O'Hara E, Palladino RA, Kenny DA, Waters SM - PLoS ONE (2015)

Differences in relative abundance of succinate and propionate producers between treatment groups.Box and whisker plots showing median, quartiles, maximum and minimum values, and outliers (asterisks) for the sum of relative abundances within each rumen sample of OTUs assigned to taxonomic groups (apart from Succinivibrionaceae) which are, or have members which are, succinate and propionate (S and P) producers. ‘Total S and P’ box and whisker plot shows sum of relative abundances of all OTUs assigned to S and P taxonomic groups excluding OTU-S3004 (white boxes-) and including OTU-S3004 (grey boxes +). LR = Liquid Restricted (n = 14), SR = Solid Restricted (n = 14), LA = Liquid Ad lib (n = 13), SA = Solid Ad lib (n = 13), LRA = Liquid Restricted/Ad lib (n = 15), SRA = Solid Restricted/Ad lib (n = 15), LAA = Liquid Ad lib/Ad lib (n = 13), SAA = Solid Ad lib/Ad lib (n = 13).
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4520551&req=5

pone.0133234.g008: Differences in relative abundance of succinate and propionate producers between treatment groups.Box and whisker plots showing median, quartiles, maximum and minimum values, and outliers (asterisks) for the sum of relative abundances within each rumen sample of OTUs assigned to taxonomic groups (apart from Succinivibrionaceae) which are, or have members which are, succinate and propionate (S and P) producers. ‘Total S and P’ box and whisker plot shows sum of relative abundances of all OTUs assigned to S and P taxonomic groups excluding OTU-S3004 (white boxes-) and including OTU-S3004 (grey boxes +). LR = Liquid Restricted (n = 14), SR = Solid Restricted (n = 14), LA = Liquid Ad lib (n = 13), SA = Solid Ad lib (n = 13), LRA = Liquid Restricted/Ad lib (n = 15), SRA = Solid Restricted/Ad lib (n = 15), LAA = Liquid Ad lib/Ad lib (n = 13), SAA = Solid Ad lib/Ad lib (n = 13).
Mentions: To try and determine the extent to which OTU-S3004 might influence rumen A:P ratio, we also looked at the abundance of OTUs which were assigned to 7 taxons (Veillonellaceae Megasphaera, Ruminococcus flavefaciens, Prevotella, Selenomonas ruminantium, Veillonellaceae Succiniclasticum, Fibrobacter succinogenes, Spirochaetaceae Treponema) that are, or contain members which are, known succinate and/or propionate (S and P) producers [54, 55] (Fig 8). The overall sum of the relative abundances of these S and P producers was reduced in group R, mainly due to decreases in Prevotella, R. flavefaciens and Megasphaera. Several of these taxonomic groups were clearly more associated with either the solid (e.g. Treponema, R. flavefaciens), or liquid (e.g. Prevotella) fraction. Addition of the relative abundance values for OTU-S3004 results in a large increase in overall abundance of S and P producers in the liquid fraction (Fig 8). Selenomonas ruminantium, which is thought to be one of the main rumen bacterial species that converts succinate to propionate and can account for up to 51% of the total viable bacterial count in the rumen [56, 57], but is undetectable under certain feeding regimes [58], was only detected as <1% in most animals in our study.

Bottom Line: Illumina Miseq Phylogenetic marker amplicon sequencing of DNA extracted from rumen contents of 55 bulls showed that restriction of feed (70% concentrate, 30% grass silage) for 125 days, to levels that caused a 60% reduction of growth rate, resulted in a large increase of relative abundance of Methanobrevibacter gottschalkii clade (designated as OTU-M7), and a large reduction of an uncharacterised Succinivibrionaceae species (designated as OTU-S3004).Reduced A:P ratios in the rumen are associated with increased feed efficiency and reduced production of methane which has a global warming potential (GWP 100 years) of 28.Succinivibrionaceae growth in the rumen was previously suggested to reduce methane emissions as some members of this family utilise hydrogen, which is also utilised by methanogens for methanogenesis, to generate succinate which is converted to propionate.

View Article: PubMed Central - PubMed

Affiliation: Animal and Bioscience Research Department, Animal and Grassland Research and Innovation Centre, Teagasc, Grange, Dunsany, County Meath, Ireland.

ABSTRACT
Periodic feed restriction is used in cattle production to reduce feed costs. When normal feed levels are resumed, cattle catch up to a normal weight by an acceleration of normal growth rate, known as compensatory growth, which is not yet fully understood. Illumina Miseq Phylogenetic marker amplicon sequencing of DNA extracted from rumen contents of 55 bulls showed that restriction of feed (70% concentrate, 30% grass silage) for 125 days, to levels that caused a 60% reduction of growth rate, resulted in a large increase of relative abundance of Methanobrevibacter gottschalkii clade (designated as OTU-M7), and a large reduction of an uncharacterised Succinivibrionaceae species (designated as OTU-S3004). There was a strong negative Spearman correlation (ρ = -0.72, P = <1x10(-20)) between relative abundances of OTU-3004 and OTU-M7 in the liquid rumen fraction. There was also a significant increase in acetate:propionate ratio (A:P) in feed restricted animals that showed a negative Spearman correlation (ρ = -0.69, P = <1x10(-20)) with the relative abundance of OTU-S3004 in the rumen liquid fraction but not the solid fraction, and a strong positive Spearman correlation with OTU-M7 in the rumen liquid (ρ = 0.74, P = <1x10(-20)) and solid (ρ = 0.69, P = <1x10(-20)) fractions. Reduced A:P ratios in the rumen are associated with increased feed efficiency and reduced production of methane which has a global warming potential (GWP 100 years) of 28. Succinivibrionaceae growth in the rumen was previously suggested to reduce methane emissions as some members of this family utilise hydrogen, which is also utilised by methanogens for methanogenesis, to generate succinate which is converted to propionate. Relative abundance of OTU-S3004 showed a positive Spearman correlation with propionate (ρ = 0.41, P = <0.01) but not acetate in the liquid rumen fraction.

No MeSH data available.


Related in: MedlinePlus