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Repeated inoculation with fresh rumen fluid before or during weaning modulates the microbiota composition and co-occurrence of the rumen and colon of lambs.

ABSTRACT: BACKGROUND:Many recent studies have gravitated towards manipulating the gastrointestinal (GI) microbiome of livestock to improve host nutrition and health using dietary interventions. Few studies, however, have evaluated if inoculation with rumen fluid could effectively reprogram the development of GI microbiota. We hypothesized that inoculation with rumen fluid at an early age could modulate the development of GI microbiota because of its low colonization resistance. RESULTS:In this study, we tested the above hypothesis using young lambs as a model. Young lambs were orally inoculated repeatedly (four times before or twice during gradual weaning) with the rumen fluid collected from adult sheep. The oral inoculation did not significantly affect starter intake, growth performance, or ruminal fermentation. Based on sequencing analysis of 16S rRNA gene amplicons, however, the inoculation (both before and during weaning) affected the assemblage of the rumen microbiota, increasing or enabling some bacterial taxa to colonize the rumen. These included operational taxonomic units (OTUs) belonging to Moryella, Acetitomaculum, Tyzzerella 4, Succiniclasticum, Prevotella 1, Lachnospiraceae, Christensenellaceae R-7 group, Family XIII AD3011, and Bacteroidales S24-7 corresponding to inoculation before weaning; and OTUs belonging to Succiniclasticum, Prevotellaceae UCG-003, Erysipelotrichaceae UCG-004, Prevotella 1, Bacteroidales S24-7 gut group uncultured bacterium, and candidate Family XIII AD3011 corresponding to inoculation during weaning. Compared to the inoculation during weaning, the inoculation before weaning resulted in more co-occurrences of OTUs that were exclusively predominant in the inoculum. However, inoculation during weaning appeared to have more impacts on the colonic microbiota than the inoculation before weaning. Considerable successions in the microbial colonization of the GI tracts accompanied the transition from liquid feed to solid feed during weaning. CONCLUSIONS:Repeated rumen fluid inoculation during early life can modulate the establishment of the microbiota in both the rumen and the colon and co-occurrence of some bacteria. Oral inoculation with rumen microbiota may be a useful approach to redirect the development of the microbiota in both the rumen and colon.

SUBMITTER: Yu S

PROVIDER: S-EPMC7006167 | biostudies-literature | 2020 Feb

REPOSITORIES: biostudies-literature

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Repeated inoculation with fresh rumen fluid before or during weaning modulates the microbiota composition and co-occurrence of the rumen and colon of lambs.

Yu Shaobo S Zhang Guangyu G Liu Zhibo Z Wu Peng P Yu Zhongtang Z Wang Jiakun J

BMC microbiology 20200207 1

<h4>Background</h4>Many recent studies have gravitated towards manipulating the gastrointestinal (GI) microbiome of livestock to improve host nutrition and health using dietary interventions. Few studies, however, have evaluated if inoculation with rumen fluid could effectively reprogram the development of GI microbiota. We hypothesized that inoculation with rumen fluid at an early age could modulate the development of GI microbiota because of its low colonization resistance.<h4>Results</h4>In t ...[more]

PMID: 32028889

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Project description:BackgroundNewborn ruminants possess an underdeveloped rumen which is colonized by microorganisms acquired from adult animals and the surrounding environment. This microbial transfer can be limited in dairy systems in which newborns are separated from their dams at birth. This study explores whether the direct inoculation of fresh or autoclaved rumen fluid from adult goats to newborn kids has a beneficial effect on rumen microbial development and function.ResultsRepetitive inoculation of young kids with fresh rumen fluid from adult goats adapted to forage (RFF) or concentrate diets (RFC) accelerated microbial colonization of the rumen during the pre-weaning period leading to high protozoal numbers, a greater diversity of bacterial (+ 234 OTUs), methanogens (+ 6 OTUs) and protozoal communities (+ 25 OTUs) than observed in control kids (CTL) without inoculation. This inoculation also increased the size of the core bacterial and methanogens community and the abundance of key rumen bacteria (Ruminococcaceae, Fibrobacteres, Veillonellaceae, Rikenellaceae, Tenericutes), methanogens (Methanobrevibacter ruminantium, Methanomicrobium mobile and Group 9), anaerobic fungi (Piromyces and Orpinomyces) and protozoal taxa (Enoploplastron, Diplodinium, Polyplastron, Ophryoscolex, Isotricha and Dasytricha) before weaning whereas CTL kids remained protozoa-free through the study. Most of these taxa were positively correlated with indicators of the rumen microbiological and physiological development (higher forage and concentrate intakes and animal growth during the post-weaning period) favoring the weaning process in RFF and RFC kids in comparison to CTL kids. Some of these microbiological differences tended to decrease during the post-weaning period, although RFF and RFC kids retained a more complex and matured rumen microbial ecosystem than CTL kids. Inoculation with autoclaved rumen fluid promoted lower development of the bacterial and protozoal communities during the pre-weaning period than using fresh inocula, but it favored a more rapid microbial development during the post-weaning than observed for CTL kids.ConclusionsThis study demonstrated that inoculation of young ruminants with fresh rumen fluid from adult animals accelerated the rumen microbial colonization which was associated with an earlier rumen functional development. This strategy facilitated a smoother transition from milk to solid feed favoring the animal performance during post-weaning and minimizing stress.

Project description:The complex rumen microbiota exhibits some degree of host specificity. The undeveloped simple rumen microbiota is hypothetically more amendable. The objective of this study was to investigate if the rumen prokaryotic microbial assemblage of young calves can be reprogrammed by oral inoculation with rumen microbiota of adult cows. Twenty newborn male calves were randomly assigned to four groups (n = 5 per group), with two groups being orally inoculated with rumen microbiota (fresh rumen fluid) collected from two lactating dairy cows, while the other two groups receiving autoclaved rumen fluid collected from another two donor cows. Each calf was orally drenched with 100, 200, 300, 400, and 500 mL of the rumen fluid at d3, d7, d21, d42, and d50, respectively, after birth. The inoculation with rumen microbiota did not affect (P > 0.05) feed intake, average daily gain (ADG), heart girth, or feed conversion ratio but significantly (P < 0.01) lowered instance of diarrhea. At the age of 77 days (27 days post-weaning), all the calves were slaughtered for the sampling of rumen content and determination of empty rumen weight. Rumen fermentation characteristics were not affected (P > 0.05) by the inoculation. Rumen prokaryotic microbiota analysis using metataxonomics (targeting the V4 region of the 16S rRNA genes) showed that the calf rumen prokaryotic microbiota differed from that of the donors. Two Succinivibrionaceae OTUs, two Prevotella OTUs, and one Succiniclasticum OTU were predominant (relative abundance > 2%) in the donors, but only one Succinivibrionaceae OTU was found in the calves. On the other hand, five other Prevotella OTUs were predominant (>3%) in the calves, but none of them was a major OTU in the donors. No correlation was observed in relative abundance of major OTUs or genera between the donor and the calves. Principal coordinates analysis (PCoA) based on weighted UniFrac distance showed no significant (P > 0.05) difference in the overall rumen prokaryotic microbiota profiles among the four calf groups, and principal component analysis (PCA) based on Bray-Curtis dissimilarity showed no significant (P > 0.05) difference in functional features predicted from the detected taxa. Nor the calf rumen microbiota showed any clustering with their donor's. Repeated oral inoculation with rumen microbiota probably has a limited effect on the development of rumen microbiota, and the rumen microbiota seems to develop following a program determined by the host and other factors.

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Repeated inoculation with fresh rumen fluid before or during weaning modulates the microbiota composition and co-occurrence of the rumen and colon of lambs.

Publications

Repeated inoculation with fresh rumen fluid before or during weaning modulates the microbiota composition and co-occurrence of the rumen and colon of lambs.

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