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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

Relative abundance of individual methanogen and Succinivibrionaceae OTUs in group R and group A.Relative abundance of OTUs identified as family Succinivibrionaceae, kingdom Archaea or class Thermoplasmata (recently reclassified as members of the order Methanomassiliicoccales) in individual liquid (L) and solid (S) rumen samples from groups R and A are shown. Different colours represent different OTU numbers. Taxonomic assignments for all OTU numbers are given in S1 Table.
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pone.0133234.g004: Relative abundance of individual methanogen and Succinivibrionaceae OTUs in group R and group A.Relative abundance of OTUs identified as family Succinivibrionaceae, kingdom Archaea or class Thermoplasmata (recently reclassified as members of the order Methanomassiliicoccales) in individual liquid (L) and solid (S) rumen samples from groups R and A are shown. Different colours represent different OTU numbers. Taxonomic assignments for all OTU numbers are given in S1 Table.

Mentions: By far the largest significant change (FDR<0.05) in both solid and liquid fractions was a decrease in group R, relative to the three ad libitum groups, of the relative abundance of OTU-S3004 which QIIME identified only as far as the family Succinivibrionaceae. Compared to group A, this single OTU accounted for an 8.7% (relative to all other OTUs) decrease in the group R liquid fraction and a 3.4% (relative to all other OTUs) decrease in the group R solid fraction. The relative abundance of OTU-S3004, while barely detectable in all group R animals, was detected as being high, particularly in the liquid fraction (30% in one of the liquid samples from group RA), in most of the animals in the ad libitum groups (Figs 4, 5 and 6). PCA showed that the rumen prokaryotic composition of ad libitum animals that had low levels of OTU-S3004 was more similar to group R (Fig 2) than group A. 96% of the 16S V4 sequences within this OTU were 100% identical suggesting that this is either mostly a single species or a group of very closely related bacteria. So it appears that there was an abundant population of an uncharacterised putative Succinivibrionaceae, mostly associated with the liquid fraction, that was dramatically reduced (88 fold in liquid and 425 fold in the solid fraction) by feed restriction in group R and then recovered to high levels upon return to an ad libitum diet in most of the group RA animals (Figs 4, 5 and 6). However, we do not know how many copies of the 16S rRNA gene are in the genome of this putative species so the relative abundance could be an overestimation of absolute abundance of the bacterial cells. The closest relatives to Succininvibrionaceae on the rrnDB 16S copy number data base [36] are members of the order Aeromonadales which have up to ten 16S rRNA gene copies per genome, although closely related species of bacteria can have different copy numbers of 16S genes in their genomes.


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)

Relative abundance of individual methanogen and Succinivibrionaceae OTUs in group R and group A.Relative abundance of OTUs identified as family Succinivibrionaceae, kingdom Archaea or class Thermoplasmata (recently reclassified as members of the order Methanomassiliicoccales) in individual liquid (L) and solid (S) rumen samples from groups R and A are shown. Different colours represent different OTU numbers. Taxonomic assignments for all OTU numbers are given in S1 Table.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4520551&req=5

pone.0133234.g004: Relative abundance of individual methanogen and Succinivibrionaceae OTUs in group R and group A.Relative abundance of OTUs identified as family Succinivibrionaceae, kingdom Archaea or class Thermoplasmata (recently reclassified as members of the order Methanomassiliicoccales) in individual liquid (L) and solid (S) rumen samples from groups R and A are shown. Different colours represent different OTU numbers. Taxonomic assignments for all OTU numbers are given in S1 Table.
Mentions: By far the largest significant change (FDR<0.05) in both solid and liquid fractions was a decrease in group R, relative to the three ad libitum groups, of the relative abundance of OTU-S3004 which QIIME identified only as far as the family Succinivibrionaceae. Compared to group A, this single OTU accounted for an 8.7% (relative to all other OTUs) decrease in the group R liquid fraction and a 3.4% (relative to all other OTUs) decrease in the group R solid fraction. The relative abundance of OTU-S3004, while barely detectable in all group R animals, was detected as being high, particularly in the liquid fraction (30% in one of the liquid samples from group RA), in most of the animals in the ad libitum groups (Figs 4, 5 and 6). PCA showed that the rumen prokaryotic composition of ad libitum animals that had low levels of OTU-S3004 was more similar to group R (Fig 2) than group A. 96% of the 16S V4 sequences within this OTU were 100% identical suggesting that this is either mostly a single species or a group of very closely related bacteria. So it appears that there was an abundant population of an uncharacterised putative Succinivibrionaceae, mostly associated with the liquid fraction, that was dramatically reduced (88 fold in liquid and 425 fold in the solid fraction) by feed restriction in group R and then recovered to high levels upon return to an ad libitum diet in most of the group RA animals (Figs 4, 5 and 6). However, we do not know how many copies of the 16S rRNA gene are in the genome of this putative species so the relative abundance could be an overestimation of absolute abundance of the bacterial cells. The closest relatives to Succininvibrionaceae on the rrnDB 16S copy number data base [36] are members of the order Aeromonadales which have up to ten 16S rRNA gene copies per genome, although closely related species of bacteria can have different copy numbers of 16S genes in their genomes.

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