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

In the present study, we evaluated whether the nasopharyngeal, ruminal, and vaginal microbiota would diverge (1) in virgin yearling beef heifers (9 months old) due to the maternal restricted gain during the first trimester of gestation; and (2) in pregnant beef heifers in response to the vitamin and mineral (VTM) supplementation during the first 6 months of pregnancy. As a secondary objective, using the microbiota data obtained from these two cohorts of beef heifers managed at the same location and sampled at the same time, we performed a holistic assessment of the microbial ecology residing within the respiratory, gastrointestinal, and reproductive tract of cattle. Our 16S rRNA gene sequencing results revealed that both α and β-diversity of the nasopharyngeal, ruminal and vaginal microbiota did not differ between virgin heifers raised from dams exposed to either a low gain (targeted average daily gain of 0.28 kg/d, n = 22) or a moderate gain treatment (0.79 kg/d, n = 23) during the first 84 days of gestation. Only in the vaginal microbiota were there relatively abundant genera that were affected by maternal rate of gain during early gestation. Whilst there was no significant difference in community structure and diversity in any of the three microbiota between pregnant heifers received no VTM (n = 15) and VTM supplemented (n = 17) diets, the VTM supplementation resulted in subtle compositional alterations in the nasopharyngeal and ruminal microbiota. Although the nasopharyngeal, ruminal, and vaginal microbiota were clearly distinct, a total of 41 OTUs, including methanogenic archaea, were identified as core taxa shared across the respiratory, gastrointestinal, and reproductive tracts of both virgin and pregnant heifers.

Bovine Animal Model for Studying the Maternal Microbiome, in utero Microbial Colonization and Their Role in Offspring Development and Fetal Programming

“…Additionally, longitudinal monitoring of the maternal gut microbiota before and during pregnancy, and direct comparison of the maternal gut microbiota changes in pregnant vs. non-pregnant cohort females is also feasible in cattle, which is critical to uncover how the maternal gut microbiota changes in response to pregnancy. Additionally, ruminal fluid samples can be collected from pregnant cattle over the course of pregnancy using a relatively non-invasive ruminal tubing method (Paz et al, 2016;Amat et al, 2021b). Ruminal sampling via tube was performed on heifers during the 2nd and 6th months of pregnancy and had minimal adverse effect on the heifers (Amat et al, 2021b).…”

“…Additionally, ruminal fluid samples can be collected from pregnant cattle over the course of pregnancy using a relatively non-invasive ruminal tubing method (Paz et al, 2016;Amat et al, 2021b). Ruminal sampling via tube was performed on heifers during the 2nd and 6th months of pregnancy and had minimal adverse effect on the heifers (Amat et al, 2021b). Longitudinal sampling of ruminal fluid and feces collected via rectal grab sampling (Fredin et al, 2014) will provide more comprehensive characterization of the gut microbiota changes during pregnancy.…”

“…A longitudinal survey of bovine reproductive microbiota at the time of breeding and during pregnancy can provide important information that can be translated into human maternal practices. Vaginal swab (Amat et al, 2021b), cervical swab (Wang et al, 2018), uterine swab (Jeon et al, 2021), and endometrial brush (Pascottini et al, 2020) sampling from pregnant cattle allow monitoring of the changes in microbiota residing in each of the anatomical sites along the reproductive tract. Applying targeted alterations of vaginal and uterine microbiota during early or late gestation with probiotics or antibiotics will allow for studying the impact of maternal microbiota on pregnancy and health of the dams, and on fetal programming and offspring development.…”

“…An additional paradigm to consider is the feasibility of surveying multigenerational impacts of maternal reproductive microbiota alterations during pregnancy on offspring reproductive microbiome development and reproductive efficiency. Though studies to investigate the multigenerational impact of maternal nutrition during early gestation on offspring development and health have been conducted in beef cattle (McLean et al, 2017;Amat et al, 2021b;Diniz et al, 2021b;Menezes et al, 2021), whether multigenerational impacts exist on microbiota remains to be elucidated. With the common application of sexed semen in cattle production (Hohenboken, 1999), the sex of the fetus can be controlled, which allows the selective production of female or male offspring when studying the reproductive microbiota and its multigeneration impact.…”

“…The pie chart represents the most relatively abundant bacterial phyla. The relative abundance of these phyla present in pie charts was adapted from McMullen et al (2020a) (respiratory tract),Mao et al (2015), and Holman and Gzyl (2019) (gastrointestinal tract), reproductive tract(Amat et al, 2021b; vagina;Wang et al, 2018; Cervix;Quereda et al, 2020; Uterine).…”