The nasopharyngeal, ruminal, and vaginal microbiota and the core taxa shared across these microbiomes in virgin yearling heifers exposed to divergent in utero nutrition during their first trimester of gestation and in pregnant beef heifers in response to mineral supplementation

Abstract

Emerging evidence has indicated that microbial transmission from the bovine dam to her fetus may take place before birth, and that the maternal microbiota during pregnancy modulates programming of fetal metabolic and nervous system development, highlighting the potential and extended role of the maternal microbiome in calf health and development. In the present study, we characterized the nasopharyngeal, ruminal and vaginal microbiota from two cohorts of beef heifers managed at the same location: 1) virgin yearling heifers (9 months old) born from dams received gestational diets which resulted in low (LG, n = 22) or medium (MG, n = 23) weight gain during the first 84 days of gestation; and 2) pregnant replacement heifers that received a vitamin and mineral supplement (VTM, n = 17) or not (Control, n = 15) during the first 6 months of gestation. Nasopharyngeal and vaginal swabs as well as ruminal fluid were collected from both cohorts and the microbiota of each sample was assessed using 16S rRNA gene sequencing. In addition to the comparison between treatment groups within each cohort, the similarity of the microbiota of the three sample types were evaluated, and shared taxa amongst these communities were identified. The bacterial genera present in the rumen and vagina that can influence methanogenic archaeal genera were predicted using a stepwise-selected generalized linear mixed model. No significant difference was observed in the alpha and beta diversity in any of the nasopharyngeal, ruminal and vaginal microbiota between LG and MG offspring virgin heifers, or between the control and VTM pregnant heifers (p > 0.05). Subtle compositional changes in the vaginal microbiota in yearling heifers, and in the nasopharyngeal and ruminal microbiota of pregnant heifers were detected in response to treatments. Forty-one archaeal and bacterial OTUs were shared by over 60% of all samples from both virgin and pregnant heifers. Two taxa within the Methanobrevibacter genus were identified as core taxa and this genus was more relatively abundant in pregnant heifers compared to virgin heifers. Among the 25 top genera, Prevotella and Prevotella UCG-003 (negative) and Christensenellaceae R-7 group (positive) were predicted to have a significant effect on ruminal Methanobrevibacter spp. The results of this study indicate that there is little impact of divergent gestational nutrition during the first trimester on the calf microbiome at 9 months postnatal, and that VTM supplementation during pregnancy may not alter the maternal microbiome. This study provides evidence that there are several microbial taxa, including methanogenic archaea, that are shared across the respiratory, gastrointestinal, and reproductive tracts, suggesting the need for a holistic evaluation of the bovine microbiota when considering potential maternal sources for seeding calves with pioneer microbiota.

Late Gestation Maternal Feed Restriction Decreases Microbial Diversity of the Placenta While Mineral Supplementation Improves Richness of the Fetal Gut Microbiome in Cattle

“…Individual mineral intake may not have been consistent, as mineral was provided ad libitum during group feeding. However, previous findings indicate that mineral supplementation during gestation fails to impact the vaginal microbiome [63], which this data confirm. Maternal mineral supplementation has been indicated to promote offspring health and performance [64], but it does not appear to do so by enhancing the vaginal microbiome.…”

“…Both the meconium and the rumen fluid of S-pregnancies had a greater degree of similarities between the microbial communities than the vaginal microbiome displayed at all timepoints (q ≤ 0.03). Although mineral supplementation had no effect on the vaginal or placental microbiomes, these data indicate that in utero supplementation may improve the richness of the fetal gut microbiome, which may later influence calf performance [63]. These interactions remain unexplored but may be established up to 60 days prepartum.…”

Characterization of the Microbiota Associated With 12-Week-Old Bovine Fetuses Exposed to Divergent in utero Nutrition

“…The dominant bacterial phyla observed in the 83-day-old fetuses in the present study were also the predominant phyla in these mid and full-term calf fetuses and in the calves postnatally. These phyla are key members of the bovine respiratory ( Timsit et al, 2020 ), gastrointestinal ( Holman and Gzyl, 2019 ) and reproductive tract ( Amat et al, 2021 ), as well as the mammary gland microbiota ( Khafipour et al, 2016 ; Derakhshani et al, 2018 ). Thus, the bacterial community profile in the 83-day-old fetuses resembles that of the fetus during mid- or late-gestation and after birth at the phylum level.…”

Whole-body Microbiota of Newborn Calves and Their Response to Prenatal Vitamin and Mineral Supplementation

“…DNA extraction of the ruminal fluid was performed using the Qiagen DNeasy PowerLyzer PowerSoil kit (Qiagen Inc., Germantown, MD, USA) following the manufacturer's instructions with modifications previously described (42). DNA was extracted from tissue samples including ruminal tissue, liver tissue, and lung tissue using the Qiagen DNeasy Blood and Tissue Kit (Qiagen Inc., Germantown, MD, USA) with an added bead beating step.…”