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Item Perceived Stress and Molecular-BV in the NIH Longitudinal Study of Vaginal Flora(Oxford University Press, 2021-05) Turpin, Rodman; Slopen, Natalie; Borgogna, Joanna C.; Yeoman, Carl J.; He, Xin; Miller, Ryan S.; Klebanoff, Mark A.; Ravel, Jacques; Brotman, Rebecca M.Vaginal microbiota provide the first line of defense against urogenital infections primarily through protective actions of Lactobacillus spp. Perceived stress increases susceptibility to infection through several mechanisms, including suppression of immune function. We investigated if stress was associated with deleterious changes to vaginal bacterial composition in a subsample of 572 women in the Longitudinal Study of Vaginal Flora, sampled from 1999 through 2002. Using Cox proportional-hazard models, both unadjusted and adjusted for sociodemographics and sexual behaviors, participants who exhibited a 5 unit-increase in Cohen’s perceived stress scale had greater risk (aHR=1.40, 95% CI 1.13-1.74) of developing molecular bacterial vaginosis (BV), a state with low Lactobacillus abundance and diverse anaerobic bacteria. A 5-unit stress increase was also associated with greater risks for transitioning from the L. iners-dominated community state type (26% higher) to molecular-BV (aHR=1.26, 95% CI 1.01-1.56) or maintaining molecular-BV from baseline (aHR=1.23, 95% CI 1.01-1.47). Inversely, women with baseline molecular-BV reporting a 5-unit stress increase were less likely to transition to microbiota dominated by L. crispatus, L. gasseri, or L. jensenii (aHR=0.81, 95% CI 0.68-0.99). These findings suggest psychosocial stress is associated with vaginal microbiota composition, inviting a more mechanistic exploration of the relationship between psychosocial stress and molecular-BV.Item Biogenic Amines Increase the Odds of Bacterial Vaginosis and Affect the Growth of and Lactic Acid Production by Vaginal Lactobacillus spp.(American Society for Microbiology, 2021-04) Borgogna, Joanna-Lynn C.; Shardell, Michelle D.; Grace, Savannah G.; Santori, Elisa K.; Americus, Benjamin; Li, Zhong; Ulanov, Alexander; Forney, Larry; Nelson, Tiffanie M.; Brotman, Rebecca M.; Ravel, Jacques; Yeoman, Carl J.Bacterial vaginosis (BV) is the most common vaginal disorder of reproductive-aged women, yet its etiology remains enigmatic. One clinical symptom of BV, malodor, is linked to the microbial production of biogenic amines (BA). Using targeted liquid chromatography mass spectrometry, we analyzed 149 longitudinally collected vaginal samples to determine the in vivo concentrations of the most common BAs and then assessed their relationship to BV and effect upon the growth kinetics of axenically cultured vaginal Lactobacillus species. Increases in cadaverine, putrescine, and tyramine were associated with greater odds of women transitioning from L. crispatus-dominated vaginal microbiota to microbiota that have a paucity of Lactobacillus spp. and from Nugent scores of 0 to 3 to Nugent scores of 7 to 10, consistent with BV. Exposure to putrescine lengthened the lag time and/or slowed the growth of all vaginal Lactobacillus spp. except L. jensenii 62G. L. iners AB107’s lag time was lengthened by cadaverine but reduced in the presence of spermidine and spermine. The growth rate of L. crispatus VPI 3199 was slowed by cadaverine and tyramine, and strain-specific responses to spermine and spermidine were observed. BAs were associated with reduced production of d- and l-lactic acid by vaginal Lactobacillus spp., and this effect was independent of their effect upon Lactobacillus species growth. The exceptions were higher levels of d- and l-lactic acid by two strains of L. crispatus when grown in the presence of spermine. Results of this study provide evidence of a direct impact of common biogenic amines on vaginal Lactobacillus spp.Item Relationships among intramammary health, udder and teat characteristics, and productivity of extensively managed ewes(Oxford University Press, 2021-02) Knuth, Ryan M.; Stewart, Whit C.; Taylor, Joshua B.; Bisha, Bledar; Yeoman, Carl J.; Van Emon, Megan L.; Murphy, Thomas W.Mastitis is an economically important disease and its subclinical state is difficult to diagnose, which makes mitigation more challenging. The objectives of this study were to screen clinically healthy ewes in order to 1) identify cultivable microbial species in milk, 2) evaluate somatic cell count (SCC) thresholds associated with intramammary infection, and 3) estimate relationships between udder and teat morphometric traits, SCC, and ewe productivity. Milk was collected from two flocks in early (<5 d) and peak (30 to 45 d) lactation to quantify SCC (n = 530) and numerate cultivable microbial species by culture-based isolation followed by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS; n = 243) identification. Within flock and lactation stage, 11% to 74% (mean = 36%) of samples were culture positive. More than 50 unique identifications were classified by MALDI-TOF MS analysis, and Bacillus licheniformis (18% to 27%), Micrococcus flavus (25%), Bacillus amyloliquefaciens (7% to 18%), and Staphylococcus epidermidis (26%) were among the most common within flock and across lactation stage. Optimum SCC thresholds to identify culture-positive samples ranged from 175 × 103 to 1,675 × 103 cells/mL. Ewe productivity was assessed as total 120-d adjusted litter weight (LW120) and analyzed within flock with breed, parity, year, and the linear covariate of log10 SCC (LSCC) at early or peak lactation. Although dependent on lactation stage and year, each 1-unit increase in LSCC (e.g., an increase in SCC from 100 × 103 to 1,000 × 103 cells/mL) was predicted to decrease LW120 between 9.5 and 16.1 kg when significant. Udder and teat traits included udder circumference, teat length, teat placement, and degree of separation of the udder halves. Correlations between traits were generally low to moderate within and across lactation stage and most were not consistently predictive of ewe LSCC. Overall, the frequencies of bacteria-positive milk samples indicated that subclinical mastitis (SCM) is common in these flocks and can impact ewe productivity. Therefore, future research is warranted to investigate pathways and timing of microbial invasion, genomic regions associated with susceptibility, and husbandry to mitigate the impact of SCM in extensively managed ewes.Item In Vivo Competitions between Fibrobacter succinogenes, Ruminococcus flavefaciens, and Ruminoccus albus in a Gnotobiotic Sheep Model Revealed by Multi-Omic Analyses(American Society for Microbiology, 2021-04) Yeoman, Carl J.; Fields, Christopher J.; Lepercq, Pascale; Ruiz, Philippe; Forano, Evelyne; White, Bryan A.; Mosoni, PascaleRuminant animals, including cattle and sheep, depend on their rumen microbiota to digest plant biomass and convert it into absorbable energy. Considering that the extent of meat and milk production depends on the efficiency of the microbiota to deconstruct plant cell walls, the functionality of predominant rumen cellulolytic bacteria, Fibrobacter succinogenes , Ruminococcus albus , and Ruminococcus flavefaciens , has been extensively studied in vitro to obtain a better knowledge of how they operate to hydrolyze polysaccharides and ultimately find ways to enhance animal production.Item Dryland Cropping Systems, Weed Communities, and Disease Status Modulate the Effect of Climate Conditions on Wheat Soil Bacterial Communities(2020-08) Ishaq, Suzanne L.; Seipel, Tim F.; Yeoman, Carl J.; Menalled, Fabian D.Little knowledge exists on how soil bacteria in agricultural settings are impacted by management practices and environmental conditions in current and predicted climate scenarios. We assessed the impact of soil moisture, soil temperature, weed communities, and disease status on soil bacterial communities in three cropping systems: (i) conventional no-till (CNT) systems utilizing synthetic pesticides and herbicides, (ii) USDA-certified tilled organic (OT) systems, and (iii) USDA-certified organic systems with sheep grazing (OG). Sampling date within the growing season and associated soil temperature and moisture exerted the greatest effect on bacterial communities, followed by cropping system, Wheat streak mosaic virus (WSMV) infection status, and weed community. Soil temperature was negatively correlated with bacterial richness and evenness, while soil moisture was positively correlated with bacterial richness and evenness. Soil temperature and soil moisture independently altered soil bacterial community similarity between treatments. Inoculation of wheat with WSMV altered the associated soil bacteria, and there were interactions between disease status and cropping system, sampling date, and climate conditions, indicating the effect of multiple stressors on bacterial communities in soil. In May and July, cropping system altered the effect of climate change on the bacterial community composition in hotter conditions and in hotter and drier conditions compared to ambient conditions, in samples not treated with WSMV. Overall, this study indicates that predicted climate modifications as well as biological stressors play a fundamental role in the impact of cropping systems on soil bacterial communities.Item Plasticity in the Human Gut Microbiome Defies Evolutionary Constraints(2019-07-19) Gomez, Andres; Sharma, Ashok Kumar; Mallott, Elizabeth K.; Petrzelkova, Klara J.; Jost Robinson, Carolyn A.; Yeoman, Carl J.; Carbonero, Franck; Pafco, Barbora; Rothman, Jessica M.; Ulanov, Alexander; Vlckova, Klara; Amato, Katherine R.; Schnorr, Stephanie L.; Dominy, Nathaniel J.; Modry, David; Todd, Angelique F.; Torralba, Manolito; Nelson, Karen E.; Burns, Michael B.; Blekhman, Ran; Remis, Melissa; Stumpf, Rebecca M.; Wilson, Brenda A.; Gaskins, H. Rex; Garber, Paul A.; White, Bryan A.; Leigh, Steven R.The gut microbiome of primates, including humans, is reported to closely follow host evolutionary history, with gut microbiome composition being specific to the genetic background of its primate host. However, the comparative models used to date have mainly included a limited set of closely related primates. To further understand the forces that shape the primate gut microbiome, with reference to human populations, we expanded the comparative analysis of variation among gut microbiome compositions and their primate hosts, including 9 different primate species and 4 human groups characterized by a diverse set of subsistence patterns (n = 448 samples). The results show that the taxonomic composition of the human gut microbiome, at the genus level, exhibits increased compositional plasticity. Specifically, we show unexpected similarities between African Old World monkeys that rely on eclectic foraging and human populations engaging in nonindustrial subsistence patterns; these similarities transcend host phylogenetic constraints. Thus, instead of following evolutionary trends that would make their microbiomes more similar to that of conspecifics or more phylogenetically similar apes, gut microbiome composition in humans from nonindustrial populations resembles that of generalist cercopithecine monkeys. We also document that wild cercopithecine monkeys with eclectic diets and humans following nonindustrial subsistence patterns harbor high gut microbiome diversity that is not only higher than that seen in humans engaging in industrialized lifestyles but also higher compared to wild primates that typically consume fiber-rich diets.Item Pelleted-hay alfalfa feed increases sheep wether weight gain and rumen bacterial richness over loose-hay alfalfa feed(2019-06) Ishaq, Suzanne L.; Lachman, Medora M.; Wenner, Benjamin A.; Baeza, Amy; Butler, Molly; Gates, Emily; Olivo, Sarah; Geddes, Julie Buono; Hatfield, Patrick G.; Yeoman, Carl J.Diet composed of smaller particles can improve feed intake, digestibility, and animal growth or health, but in ruminant species can reduce rumination and buffering – the loss of which may inhibit fermentation and digestibility. However, the explicit effect of particle size on the rumen microbiota remains untested, despite their crucial role in digestion. We evaluated the effects of reduced particle size on rumen microbiota by feeding long-stem (loose) alfalfa hay compared to a ground and pelleted version of the same alfalfa in yearling sheep wethers. In situ digestibility of the pelleted diet was greater at 48 h compared with loose hay; however, distribution of residual fecal particle sizes in sheep did not differ between the dietary treatments at any time point. Both average daily gain and feed efficiency were greater for the wethers consuming the pelleted diet. Observed bacterial richness was very low at the end of the adaptation period and increased over the course of the study, suggesting the rumen bacterial community was still in flux after two weeks of adaptation. The pelleted-hay diet group had a greater increase in bacterial richness, including common fibrolytic rumen inhabitants. The pelleted diet was positively associated with several Succiniclasticum, a Prevotella, and uncultured taxa in the Ruminococcaceae and Rickenellaceae families and Bacteroidales order. Pelleting an alfalfa hay diet for sheep does shift the rumen microbiome, though the interplay of diet particle size, retention and GI transit time, microbial fermentative and hydrolytic activity, and host growth or health is still largely unexplored.Item Ground Juniperus pinchotii and urea in supplements fed to Rambouillet ewe lambs Part 2: Ewe lamb rumen microbial communities(2018-12) Ishaq, Suzanne L.; Yeoman, Carl J.; Whitney, T. R.This study evaluated effects of ground redberry juniper (Juniperus pinchotii) and urea in dried distillers grains with solubles-based supplements fed to Rambouillet ewe lambs (n = 48) on rumen physiological parameters and bacterial diversity. In a randomized study (40 d), individually-penned lambs were fed ad libitum ground sorghum-sudangrass hay and of 1 of 8 supplements (6 lambs/treatment; 533 g/d; as-fed basis) in a 4 x 2 factorial design with 4 concentrations of ground juniper (15%, 30%, 45%, or 60% of DM) and 2 levels of urea (1% or 3% of DM). Increasing juniper resulted in minor changes in microbial β-diversity (PERMANOVA, pseudo F = 1.33, P = 0.04); however, concentrations of urea did not show detectable broad-scale differences at phylum, family, or genus levels according to ANOSIM (P > 0.05), AMOVA (P > 0.10), and PERMANOVA (P > 0.05). Linear discriminant analysis indicated some genera were specific to certain dietary treatments (P < 0.05), though none of these genera were present in high abundance; high concentrations of juniper were associated with Moraxella and Streptococcus, low concentrations of urea were associated with Fretibacterium, and high concentrations of urea were associated with Oribacterium and Pyramidobacter. Prevotella were decreased by juniper and urea. Ruminococcus, Butyrivibrio, and Succiniclasticum increased with juniper and were positively correlated (Spearman\'s, P < 0.05) with each other but not to rumen factors, suggesting a symbiotic interaction. Overall, there was not a juniper x urea interaction for total VFA, VFA by concentration or percent total, pH, or ammonia (P > 0.29). When considering only percent inclusion of juniper, ruminal pH and proportion of acetic acid linearly increased (P < 0.001) and percentage of butyric acid linearly decreased (P = 0.009). Lamb ADG and G:F were positively correlated with Prevotella (Spearman\'s, P < 0.05) and negatively correlated with Synergistaceae, the BS5 group, and Lentisphaerae. Firmicutes were negatively correlated with serum urea nitrogen, ammonia, total VFA, total acetate, and total propionate. Overall, modest differences in bacterial diversity among treatments occurred in the abundance or evenness of several OTUs, but there was not a significant difference in OTU richness. As diversity was largely unchanged, the reduction in ADG and lowerend BW was likely due to reduced DMI rather than a reduction in microbial fermentative ability.Item Biogeographical Differences in the Influence of Maternal Microbial Sources on the Early Successional Development of the Bovine Neonatal Gastrointestinal tract(2018-02) Yeoman, Carl J.; Ishaq, Suzanne L.; Bichi, Elena; Olivo, Sarah K.; Lowe, James; Aldridge, Brian M.The impact of maternal microbial influences on the early choreography of the neonatal calf microbiome were investigated. Luminal content and mucosal scraping samples were collected from ten locations in the calf gastrointestinal tract (GIT) over the first 21 days of life, along with postpartum maternal colostrum, udder skin, and vaginal scrapings. Microbiota were found to vary by anatomical location, between the lumen and mucosa at each GIT location, and differentially enriched for maternal vaginal, skin, and colostral microbiota. Most calf sample sites exhibited a gradual increase in α-diversity over the 21 days beginning the first few days after birth. The relative abundance of Firmicutes was greater in the proximal GIT, while Bacteroidetes were greater in the distal GIT. Proteobacteria exhibited greater relative abundances in mucosal scrapings relative to luminal content. Forty-six percent of calf luminal microbes and 41% of mucosal microbes were observed in at-least one maternal source, with the majority being shared with microbes on the skin of the udder. The vaginal microbiota were found to harbor and uniquely share many common and well-described fibrolytic rumen bacteria, as well as methanogenic archaea, potentially indicating a role for the vagina in populating the developing rumen and reticulum with microbes important to the nutrition of the adult animal.Item Cigarette smoking is associated with an altered vaginal tract metabolomic profile(2018-01) Nelson, Tiffanie M.; Borgogna, Joanna-Lynn C.; Michalek, R. D.; Roberts, David W.; Rath, J. M.; Glover, E. D.; Ravel, Jacques; Shardell, M. D.; Yeoman, Carl J.; Brotman, Rebecca M.Cigarette smoking has been associated with both the diagnosis of bacterial vaginosis (BV) and a vaginal microbiota lacking protective Lactobacillus spp. As the mechanism linking smoking with vaginal microbiota and BV is unclear, we sought to compare the vaginal metabolomes of smokers and non-smokers (17 smokers/19 non-smokers). Metabolomic profiles were determined by gas and liquid chromatography mass spectrometry in a cross-sectional study. Analysis of the 16S rRNA gene populations revealed samples clustered into three community state types (CSTs) ---- CST-I (L. crispatus-dominated), CST-III (L. iners-dominated) or CST-IV (low-Lactobacillus). We identified 607 metabolites, including 12 that differed significantly (q-value < 0.05) between smokers and non-smokers. Nicotine, and the breakdown metabolites cotinine and hydroxycotinine were substantially higher in smokers, as expected. Among women categorized to CST-IV, biogenic amines, including agmatine, cadaverine, putrescine, tryptamine and tyramine were substantially higher in smokers, while dipeptides were lower in smokers. These biogenic amines are known to affect the virulence of infective pathogens and contribute to vaginal malodor. Our data suggest that cigarette smoking is associated with differences in important vaginal metabolites, and women who smoke, and particularly women who are also depauperate for Lactobacillus spp., may have increased susceptibilities to urogenital infections and increased malodor.