Regulation of rumen development in neonatal ruminants through microbial metagenomes and host transcriptomes

Abstract

Background In ruminants, early rumen development is vital for efficient fermentation that converts plant materials to human edible food such as milk and meat. Here, we investigate the extent and functional basis of host-microbial interactions regulating rumen development during the first 6 weeks of life. Results The use of microbial metagenomics, together with quantification of volatile fatty acids (VFAs) and qPCR, reveals the colonization of an active bacterial community in the rumen at birth. Colonization of active complex carbohydrate fermenters and archaea with methyl-coenzyme M reductase activity was also observed from the first week of life in the absence of a solid diet. Integrating microbial metagenomics and host transcriptomics reveals only 26.3% of mRNA transcripts, and 46.4% of miRNAs were responsive to VFAs, while others were ontogenic. Among these, one host gene module was positively associated with VFAs, while two other host gene modules and one miRNA module were negatively associated with VFAs. Eight host genes and five miRNAs involved in zinc ion binding-related transcriptional regulation were associated with a rumen bacterial cluster consisting of Prevotella , Bacteroides , and Ruminococcus . Conclusion This three-way interaction suggests a potential role of bacteria-driven transcriptional regulation in early rumen development via miRNAs. Our results reveal a highly active early microbiome that regulates rumen development of neonatal calves at the cellular level, and miRNAs may coordinate these host-microbial interactions. Electronic supplementary material The online version of this article (10.1186/s13059-019-1786-0) contains supplementary material, which is available to authorized users.

Survey of rumen microbiota of domestic grazing yak during different growth stages revealed novel maturation patterns of four key microbial groups and their dynamic interactions

“…Among the four groups, the bacterial community colonized the rumen before day 7, which is similar to studies on dairy calves. For example, previous studies revealed that bacteria were detected in the rumen of dairy calves as early as birth and for the first week (1-7 days) of age [21,33,34], suggesting that rumen bacterial colonization occurs before the intake of solid food. The predominant bacterial phylum, Bacteroidetes, was found across all age groups, and the relative abundance of this phylum reached a maximum at 6 months of age, which is similar to the changes in the rumen of dairy cows from birth to 2 years of age [21].…”

Interactions of Symbiotic Partners Drive the Development of a Complex Biogeography in the Squid-Vibrio Symbiosis

“…Biogeographic patterns that are influenced by interactions with symbionts have also been noted in consortial gut symbioses. A recent study showed that the monogastric gut of a newborn ruminate requires interactions with microbial symbionts to differentiate into the characteristic chambered stomach with the rumen, reticulum, and oma- on November 3, 2020 by guest http://mbio.asm.org/ sum (43). In addition, symbiont colonization of germfree mice leads to changes in the epithelium of the gastrointestinal tract, such as the shortening of the intestine (44) and the generation of adaptive lymphoid tissues (45).…”

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