Evidence for the amnion-fetal gut-microbial axis in late gestation beef calves1

Hummel, Gwendolynn L; Woodruff, Kelly L; Austin, Kathy J.; Smith, Travis; Cunningham-Hollinger, Hannah C

doi:10.1093/tas/txaa138

Cited by 7 publications

(7 citation statements)

References 19 publications

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“…The meconium has been considered the best sampling method due to the importance of gastrointestinal microbes to host physiology, higher biomass compared to other body systems, and ease of collection (Stinson et al, 2018). Additionally, the meconium is formed in the neonate in utero, so there should be little influence of early environmental microbe exposure post-delivery (Stinson et al, 2018;Woodruff et al, 2020). Previously, the method of delivery of the neonate has been thought to be the first exposure to microbes.…”

Section: Placental Bacterial Communities and Fetal Colonization In Uteromentioning

confidence: 99%

“…One of the first studies to identify a placental microbiome was conducted in humans and found a placental microbiome that was similar to the oral microbiome (Aagaard et al, 2014). Hummel et al (2020) utilized cattle to compare bacterial communities of the maternal vagina, amnion fluid, calf rumen fluid, and meconium. The bacterial communities of the amnion fluid and calf meconium were the most similar, while the vaginal samples were the most different (Hummel et al, 2020).…”

Section: Placental Bacterial Communities and Fetal Colonization In Uteromentioning

confidence: 99%

“…Hummel et al (2020) utilized cattle to compare bacterial communities of the maternal vagina, amnion fluid, calf rumen fluid, and meconium. The bacterial communities of the amnion fluid and calf meconium were the most similar, while the vaginal samples were the most different (Hummel et al, 2020). A study was conducted performing a cesarean delivery of all calves to collect amnion fluid before the rupture of membranes and decrease contamination (Husso et al, 2021).…”

Section: Placental Bacterial Communities and Fetal Colonization In Uteromentioning

confidence: 99%

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Importance of the female reproductive tract microbiome and its relationship with the uterine environment for health and productivity in cattle: A review

et al. 2023

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Once thought to be sterile, the reproductive tract microbiome has been characterized due to the transition from culture-dependent identification of bacteria to culture-independent sequencing methods. The urogenital microbiome was first identified in women through the Human Microbiome Project, which led to research in other species such as the bovine. Previous research focused on uterine bacteria associated with postpartum disease, but next generation sequencing methods identified a normal, healthy bacterial community of the reproductive tract of cows and heifers. Bacterial communities are now understood to differ between the uterus and vagina, and throughout the estrous cycle with changes in hormone dominance. In a healthy state, the bacterial communities largely interact with the uterine environment by assisting in maintaining the proper pH, providing and utilizing nutrients and metabolites, and influencing the immunological responses of the reproductive tract. If the bacterial communities become unbalanced due to an increase in potentially pathogenic bacteria, the health and fertility of the host may be affected. Although the presence of a reproductive tract microbiome has become widely accepted, the existence of a placental microbiome and in utero colonization of the fetus is still a popular debate due to conflicting study results. Currently, researchers are evaluating methods to manipulate the reproductive bacterial communities, such as diet changes and utilizing probiotics, to improve reproductive outcomes. The following review discusses the current understanding of the reproductive tract microbiome, how it differs between humans and cattle, and its relationship with the uterine environment.

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Section: Placental Bacterial Communities and Fetal Colonization In Uteromentioning

confidence: 99%

Section: Placental Bacterial Communities and Fetal Colonization In Uteromentioning

confidence: 99%

Section: Placental Bacterial Communities and Fetal Colonization In Uteromentioning

confidence: 99%

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Importance of the female reproductive tract microbiome and its relationship with the uterine environment for health and productivity in cattle: A review

et al. 2023

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“…The human gut microbiome is also altered by FR in adulthood [ 27 , 28 ], and differences between appropriate and excessive gestational weight gain illustrate that the placental microbiome may reflect the maternal gut microbiome [ 29 ], offering an avenue by which maternal diet may influence fetal gut inoculation [ 23 , 30 ]. While excessive gestational weight gain has been shown to cause aberrations to the placental microbiome in humans, the effects of insufficient gestational weight gain remain to be explored.…”

Section: Introductionmentioning

confidence: 99%

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

Hummel

Woodruff

Austin

et al. 2021

Animals

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Feed intake restriction impacts both humans and ruminants in late gestation, although it is unknown whether this adverse maternal environment influences the microbiome of the reproductive tract, and through it, the colonization of the fetal gut. A 2 × 2 factorial design including a 70% feed intake restriction (feed restricted ‘FR’ or control diets ‘CON’) and mineral supplementation (unsupplemented ‘S−’ or supplemented ‘S+’) was used to analyze these effects in multiparous cows (n = 27). Vaginal swabs were obtained 60, 30, and 10 days prior to the estimated calving date, along with neonatal rumen fluid and meconium. Placental tissues and efficiency measurements were collected. Microbial DNA was extracted for 16S sequencing of the V4 region. Feed restriction decreased the diversity of the placental microbiome, but not the vagina, while mineral supplementation had little impact on these microbial communities. Mineral supplementation did improve the richness and diversity of the fetal gut microbiomes in relation to reproductive microbes. These differences within the placental microbiome may influence individual health and performance. Adequate maternal nutrition and supplementation yielded the greatest placental efficiency, which may aid in the establishment of a healthy placental microbiome and fetal microbial colonization.

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“…Gut microbiota is integral to feed digestion, nutrient absorption and metabolism, immune response, and gastrointestinal development ( Morgavi et al, 2015 ), and the colonization of intestinal microbiota during early life could further influence the subsequent microbiota of adult host ( Ben Salem et al, 2005 ). Many studies demonstrated that the intestine of prenatal animals really has microorganism ( Alipour et al, 2018 ; Stinson et al, 2019 ; Hummel et al, 2020 ; Bi et al, 2021 ; Husso et al, 2021 ), and at present, no literature on the differences in intestinal microbiota composition between mutant and wild-type fetuses is found, but for postnatal individuals, there are differences in gut microbiota between mutant and wild-type host, for example, nucleotide-binding oligomerization domain-containing protein 2 (NOD2) mutation caused Crohn’s disease (CD) ( Hampe et al, 2001 ; Ogura et al, 2001 ) and Crohn’s disease individuals had lower bacterial diversity than healthy controls ( Joossens et al, 2011 ). Cystic fibrosis transmembrane conductance regulator (CFTR) mutation resulted in multiorgan defects, and CFTR –/– mice had significantly lower alpha diversity of intestinal bacterial community ( p < 0.05) and had reduced relative abundance of protective species such as Acinetobacter lwoffii and Lactobacilliales members compared with wild-type mice ( Lynch et al, 2013 ).…”

Section: Introductionmentioning

confidence: 99%

Administration of All-Trans Retinoic Acid to Pregnant Sows Alters Gut Bacterial Community of Neonatal Piglets With Different Hoxa1 Genotypes

Zhou

Chen

et al. 2021

Front. Microbiol.

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Administration of all-trans retinoic acid (ATRA) to pregnant sows improves developmental defects of Hoxa1–/– fetal pigs, and this study aimed to explore the influence of maternal ATRA administration during pregnancy on gut microbiota of neonatal piglets. Samples of jejunal and ileal meconium of neonatal piglets before suckling were collected including 5 Hoxa1–/– and 20 non-Hoxa1–/– (Hoxa1+/+ and Hoxa1+/−) neonatal piglets from the control group and 5 Hoxa1–/– and 7 non-Hoxa1–/– neonatal piglets from the experimental group. Results indicated that Hoxa1 mutation shaped the bacterial composition of the jejunum and ileum of neonatal piglets and Hoxa1–/– neonatal piglets had significantly higher diversity and species richness, higher relative abundance of phylum Bacteroidetes, lower relative abundances of phylum Firmicutes and genus Lactobacillus, and lower ratio of Firmicutes to Bacteroidetes than non-Hoxa1–/– neonatal piglets. After maternal ATRA administration, Hoxa1–/– neonatal piglets had significantly higher diversity and species richness, higher relative abundances of two bacterial phyla (Bacteroidetes and Proteobacteria), and lower relative abundances of phylum Firmicutes and genus Lactobacillus in the jejunum than non-Hoxa1–/– neonatal piglets. Hoxa1–/– neonatal piglets delivered by sows with maternal ATRA administration had lower diversity and species richness and higher relative abundance of phylum Firmicutes in the jejunum than Hoxa1–/– neonatal piglets born by sows with no maternal ATRA administration. Non-Hoxa1–/– neonatal piglets delivered by sows with maternal ATRA administration had higher diversity and species richness and significantly lower relative abundances of phyla Firmicutes and Actinobacteria and genus Lactobacillus in the ileum than non-Hoxa1–/– neonatal piglets born by sows with no maternal ATRA administration. Hoxa1 mutation decreased the expression of bacterial genes involved in ABC transporters, purine metabolism, and aminoacyl-tRNA biosynthesis and increased the expression of bacterial genes involved in two-component system, starch and sucrose metabolism, and arginine and proline metabolism. Maternal ATRA administration decreased the expression of bacterial genes involved in arginine and proline metabolism, peptidoglycan biosynthesis, and fatty acid biosynthesis. Hoxa1 mutation resulted in bacterial dysbiosis of the small intestine of Hoaxa1–/– neonatal piglets, and maternal ATRA administration restored the bacterial dysbiosis of Hoxa1–/– neonatal piglets and altered the bacterial composition of the small intestine of non-Hoxa1–/– neonatal piglets.

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Evidence for the amnion-fetal gut-microbial axis in late gestation beef calves1

Cited by 7 publications

References 19 publications

Importance of the female reproductive tract microbiome and its relationship with the uterine environment for health and productivity in cattle: A review

Importance of the female reproductive tract microbiome and its relationship with the uterine environment for health and productivity in cattle: A review

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

Administration of All-Trans Retinoic Acid to Pregnant Sows Alters Gut Bacterial Community of Neonatal Piglets With Different Hoxa1 Genotypes

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