Microbial inoculum effects on the rumen epithelial transcriptome and rumen epimural metatranscriptome in calves

Authors: FREGULIA, PRISCILA - Oak Ridge Institute For Science And Education (ORISE); PARK, TANSOL - Oak Ridge Institute For Science And Education (ORISE); CERSOSIMO, LAURA - Oak Ridge Institute For Science And Education (ORISE); Zanton, Geoffrey; Li, Wenli

Submitted to: Scientific Reports
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/23/2024
Publication Date: N/A
Citation: N/A

Interpretive Summary: The rumen of dairy cattle contains microbiota from all domains of life that play a prominent role in digestion and may also affect animal health, production, and efficiency. To evaluate the effects of directed rumen microbial establishment on the gene expression of the rumen tissue and epimural (rumen wall-associated) microbiota, we dosed the rumen of pre-weaned dairy bull calves with either bacteria- or protozoa-enriched inoculum. This is the first study to show that inoculation with different microbial treatments can alter the expression of genes on the rumen wall and its associated microbiota. These findings could provide the foundation to develop methods to improve production efficiency and host health through manipulation of the rumen microbiota.

Technical Abstract: Manipulation of the rumen microbial ecosystem in early life may affect ruminal fermentation and enhance the productive performance of dairy cows. The objective of this study was to evaluate the effects of dosing three different types of microbial inoculum on the rumen epithelium tissue (RE) transcriptome and the rumen epimural metatranscriptome (REM) in dairy calves. Fifteen Holstein bull calves were enrolled in the study at birth and assigned to three different intraruminal inoculum treatments dosed orally once weekly from three to six weeks of age. The inoculum treatments were prepared from rumen contents collected from rumen fistulated lactating cows and were either autoclaved (control; ARF), processed by differential centrifugation to create bacterial-enriched inoculum (BE), or through gravimetric separation to create protozoal-enriched inoculum (PE). Calves were fed 2.5 L/feeding pasteurized waste milk thrice daily from zero to seven weeks of age and texturized starter until euthanasia at nine weeks of age, when the RE tissues were collected for transcriptome and microbial metatranscriptome analyses. The different types of inoculum altered the RE transcriptome and REM. Compared to ARF, nine genes were upregulated in the RE of BE and 92 in PE, whereas between BE and PE there were 13 genes upregulated in BE and 114 in PE. Gene ontology analysis identified the enrichment of differentially expressed genes in cellular components for the comparison between BE and ARF, with no enrichment in PE. The RE functional signature showed different KEGG pathways related to BE and ARF, and no specific RE KEGG pathway for PE. We observed a reduction in alpha diversity indices for RE microbiome in ARF (observed genera and Chao1 (P < 0.05)). The abundance changes of five microbial genera showed a significant correlation with the changes in host gene expression: Roseburia (26 genes), Entamoeba (two genes); Anaerosinus, Lachnospira, and Succiniclasticum were each related to one gene. Sparse Partial Least Squares Discriminant Analysis (sPLS-DA) showed that the microbial communities differ among the treatments, although the taxonomic and functional microbial profiles show different distributions. Co-expression Differential Network Analysis indicated that both BE and PE had an impact on the abundance of microbial KEGG modules related to acyl-CoA synthesis, type VI secretion, and methanogenesis, while PE had a significant impact on KEGGs related to ectoine biosynthesis and D-xylose transport. Our study indicates that artificial dosing with different microbial inocula in early life alters not only the RE transcriptome, but also affects the REM and its functions.