Dataset Information

Unravelling the interaction between the phageome and bacteriome in the rumen and its role in influencing metabolome dynamics in dairy cows at different lactation stages

ABSTRACT:

Background: Although the roles of rumen microbiome in milk yield and milk protein synthesis have been widely recognized, knowledge on how ruminal microbiome dynamic changes affect these two traits during the whole lactation is lacking. Phages have been shown to affect the microbiota, but little is known about the shift patterns of ruminal phages and if they may modulate rumen microbiome during lactation. Herein, a longitudinal study was performed to identify the potential roles of ruminal phageome and bacteriome interactions, and metabolic function shift in affecting milk yield and protein content using metagenomic and metabolomic profiling of rumen microbiome from the peak, early and later mid-lactation stages.

Results: A total of 780 ruminal bacterial phages were identified, which exhibited two primary shifting patterns: 1) decreasing then increasing; 2) decreasing then stabilizing through the lactation. Bacteriome also showed first increasing then stabilizing or continuously decline besides exhibiting two similar shifting patterns to those of phages. By associating the differentially abundant phages with their host bacteria, we observed that significantly increased Lactococcus phage BM13, Corynebacterium phage P1201 and Campylobacter phage CJIE4-5 in peak lactation, along with Lactobacillus phage Lv-1 in early and later mid-lactation, and they were positively correlated with the relative abundance of their hosts. However, significantly increased Bacillus phage BCU4 and the Enterococcus phage phiNASRA1 in early mid-lactation were negatively related to their host abundance. In terms of bacteria, such as Ruminococcus flavefaciens and Faecalibacterium sp. CAG 74 had the highest abundance in peak lactation, whereas most Prevotella species were more abundant in early and later mid-lactation. Notably, ruminal carbohydrate and amino acid metabolism functions were enhanced in early mid-lactation. Further structural equation model and network analysis revealed that abundant Bacillus phage BCU4 and Enterococcus phage phiNASRA1 in early mid-lactation were associated with increased relative abundance of Prevotella species, possibly due to a reduction in Bacillus cereus and Enterococcus faecalis. Additionally, these Prevotella species exhibited positive relationships with rumen metabolites, such as L-phenylalanine, phenylacetylglycine, N-acetyl-D-phenylalanine, as well as propionate content, which contributed to the improved milk protein yield.

Conclusions: This study revealed the bacteriome and phageome interactions at different lactation stages, and the key phages and bacteria regulating the rumen function and metabolism thus contributing to the milk traits of cows. The potential regulatory roles of phages in affecting the rumen bacteriome suggest that they can be powerful targets for future interventions to improve rumen functions.

INSTRUMENT(S): Liquid Chromatography MS - negative - reverse phase, Liquid Chromatography MS - positive - reverse phase

PROVIDER: MTBLS12816 | MetaboLights | 2025-08-11

REPOSITORIES: MetaboLights

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			Action	DRS
	a_MTBLS12816_LC-MS_negative_reverse-phase_metabolite_profiling.txt	Txt
	a_MTBLS12816_LC-MS_positive_reverse-phase_metabolite_profiling.txt	Txt
	i_Investigation.txt	Txt
	m_MTBLS12816_LC-MS_negative_reverse-phase_metabolite_profiling_v2_maf.tsv	Tabular
	m_MTBLS12816_LC-MS_positive_reverse-phase_metabolite_profiling_v2_maf.tsv	Tabular

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Project description:Background: High-yield dairy cows are usually accompanied with lower milk fat (MF) rate, with huge variations in MF contents among individuals. The potential mechanisms of key microorganisms, their genes and metabolites participate in MF synthesis are still not well understood. By selecting 12 high-yielding (HIGH) and 12 low-yielding (LOW) cows from a large cohort of dairy cows, multi-omics technologies were applied to identify the hallmark microorganisms, metabolites, and metabolic pathways involved in MF synthesis.Results: The LOW and HIGH cows under the same feeding and management conditions exhibited considerable phenotypic, microbial, functional, and metabolomic differences. The LOW and HIGH cows underwent acetic and propionic ruminal fermentation, respectively, with greater molar proportion of acetate and butyrate in the LOW cows, providing greater precursors for short-chain fatty acids (FAs) synthesis in mammary gland. The HIGH cows had greater molar proportion of propionate in rumen and contents of long-chain FAs and odd-chain FAs (OCFAs) in milk. Metagenomic analysis revealed that the HIGH and LOW cows possessed Prevotella- and Ruminococcus-driven enterotypes, respectively, associated with significantly lower abundances of Methanobacteriota and Methanobrevibacter_A in HIGH than that of the LOW cows. Moreover, 13 carbohydrate and 3 lipid metabolism pathways were greatly enhanced in HIGH cows, accompanied with greater abundances of CAZymes encoding genes and critical enzymes involved in fiber degradation and propionate synthetization. Metabolomic analysis revealed that the free FAs, glycerophospholipids and oxidized lipids in ruminal fluid, and bile acids, glycerides, and glycerophospholipids in serum were greater in HIGH cows; however, the contents of carnitines, being ubiquitously detected in ruminal fluid, serum, and milk, were consistently greater in LOW cows, suggesting the capability of being used as biomarkers for predicting the lactation potentiality.Conclusions: The yield and MF composition between HIGH and LOW cows are microbiome-dependent, specifically greatly depend on the Prevotella- and Ruminococcus-driven enterotypes, respectively. The former enterotype is associated with higher milk efficiency and greater milk contents of OCFAs, which is more environmentally friend and healthier to human; whereas the later enterotype is characterized with greater methanogens and carnitines, which indicates a greater dietary energy loss and a poorer energy status of dairy cows.

Project description:Production of milk is a key characteristic of mammals, but the features of lactation vary greatly between monotreme, marsupial and eutherian mammals. Marsupials have a short gestation followed by a long lactation period, and the milk constituents vary greatly across lactation to meet the changing needs of the developing young. Marsupials are born immunologically naïve and rely on their mother’s milk for immunological protection. The koala is an iconic Australian species and many are increasingly threatened by disease. Here we use a mammary transcriptome, two milk proteomes and the koala genome to comprehensively characterise the protein components of the milk of the koala, with a key focus on the immune constituents during early and late lactation. We have characterised the most abundant peptides present in milk, examined key differences between early and late lactation, and determined differences between the koala and other marsupial species. The most abundant proteins were well characterised mammalian and marsupial-specific milk proteins including β-lactoglobulin, lactotransferrin, caseins and early lactation protein. We have generated a list of 851 immune compounds identified in the mammary transcriptome and examined a range of immune proteins that were highly abundant in the milk proteomes. These include immunoglobulins, complement components and immune receptors. A host of antimicrobial peptides were identified including cathelicidins, lysozyme, WAP four-disulfide core domain protein 2, Mucin-1 and Peptidoglycan recognition protein. We discovered that the previously described marsupial milk protein Very Early Lactation Protein is an ortholog of the eutherian gene Glycam1 (PP3) and likely has an antimicrobial role in milk. We also identified highly abundant koala endogenous retrovirus sequences in the mammary and milk transcriptome and proteomes, identifying a potential route for retroviral transmission from mother to young. Identifying and characterising the immune components of milk is key to understanding how marsupial young are protected throughout lactation and the novel immune compounds identified may have applications in clinical research.

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Unravelling the interaction between the phageome and bacteriome in the rumen and its role in influencing metabolome dynamics in dairy cows at different lactation stages

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