Dataset Information

Toxic tall fescue grazing increases susceptibility of the Angus steer fecal microbiota and plasma/urine metabolome to environmental effects.

ABSTRACT: Impaired thermoregulation and lowered average daily gains (ADG) result when livestock graze toxic endophyte (Epichloë coenophialum)-infected tall fescue (E+) and are hallmark signs of fescue toxicosis (FT), a disease exacerbated by increased temperature and humidity (+temperature-humidity index; +THI). We previously reported FT is associated with metabolic and microbiota perturbations under thermoneutral conditions; here, we assessed the influence of E+ grazing and +THI on the microbiota:metabolome interactions. Using high-resolution metabolomics and 16S rRNA gene sequencing, plasma/urine metabolomes and the fecal microbiota of Angus steers grazing non-toxic or E+ tall fescue were evaluated in the context of +THI. E+ grazing affected the fecal microbiota profile; +THI conditions modulated the microbiota only in E+ steers. E+ also perturbed many metabolic pathways, namely amino acid and inflammation-related metabolism; +THI affected these pathways only in E+ steers. Integrative analyses revealed the E+ microbiota correlated and co-varied with the metabolomes in a THI-dependent manner. Operational taxonomic units in the families Peptococcaceae, Clostridiaceae, and Ruminococcaceae correlated with production parameters (e.g., ADG) and with multiple plasma/urine metabolic features, providing putative FT biomarkers and/or targets for the development of FT therapeutics. Overall, this study suggests that E+ grazing increases Angus steer susceptibility to +THI, and offers possible targets for FT interventions.

SUBMITTER: Mote RS

PROVIDER: S-EPMC7016188 | biostudies-literature | 2020 Feb

REPOSITORIES: biostudies-literature

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Toxic tall fescue grazing increases susceptibility of the Angus steer fecal microbiota and plasma/urine metabolome to environmental effects.

Mote Ryan S RS Hill Nicholas S NS Skarlupka Joseph H JH Tran ViLinh T VT Walker Douglas I DI Turner Zachary B ZB Sanders Zachary P ZP Jones Dean P DP Suen Garret G Filipov Nikolay M NM

Scientific reports 20200212 1

Impaired thermoregulation and lowered average daily gains (ADG) result when livestock graze toxic endophyte (Epichloë coenophialum)-infected tall fescue (E+) and are hallmark signs of fescue toxicosis (FT), a disease exacerbated by increased temperature and humidity (+temperature-humidity index; +THI). We previously reported FT is associated with metabolic and microbiota perturbations under thermoneutral conditions; here, we assessed the influence of E+ grazing and +THI on the microbiota:metabol ...[more]

PMID: 32051515

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Project description:Tall fescue, the predominant southeastern United States cool-season forage grass, frequently becomes infected with an ergot alkaloid-producing toxic endophyte, Epichloë coenophialum Consumption of endophyte-infected fescue results in fescue toxicosis (FT), a condition that lowers beef cow productivity. Limited data on the influence of ergot alkaloids on rumen fermentation profiles or ruminal bacteria that could degrade the ergot alkaloids are available, but how FT influences the grazing bovine fecal microbiota or what role fecal microbiota might play in FT etiology and associated production losses has yet to be investigated. Here, we used 16S rRNA gene sequencing of fecal samples from weaned Angus steers grazing toxic endophyte-infected (E+; n = 6) or nontoxic (Max-Q; n = 6) tall fescue before and 1, 2, 14, and 28 days after pasture assignment. Bacteria in the Firmicutes and Bacteroidetes phyla comprised 90% of the Max-Q and E+ steer fecal microbiota throughout the trial. Early decreases in the Erysipelotrichaceae family and delayed increases of the Ruminococcaceae and Lachnospiraceae families were among the major effects of E+ grazing. E+ also increased abundances within the Planctomycetes, Chloroflexi, and Proteobacteria phyla and the Clostridiaceae family. Multiple operational taxonomic units classified as Ruminococcaceae and Lachnospiraceae were correlated negatively with weight gains (lower in E+) and positively with respiration rates (increased by E+). These data provide insights into how E+ grazing alters the Angus steer microbiota and the relationship of fecal microbiota dynamics with FT.IMPORTANCE Consumption of E+ tall fescue has an estimated annual $1 billion negative impact on the U.S. beef industry, with one driver of these costs being lowered weight gains. As global agricultural demand continues to grow, mitigating production losses resulting from grazing the predominant southeastern United States forage grass is of great value. Our investigation of the effects of E+ grazing on the fecal microbiota furthers our understanding of bovine fescue toxicosis in a real-world grazing production setting and provides a starting point for identifying easy-to-access fecal bacteria that could serve as potential biomarkers of animal productivity and/or FT severity for tall fescue-grazing livestock.

Project description:Tall fescue (Schedonorus arundinaceus) is a cool-season perennial grass that is widely used as a forage for many livestock species including sheep. An endophyte (Neotyphodium coenophialum) in tall fescue produces ergot alkaloids that enhance plant survival but produce toxicosis in animals. The objective of this study was to investigate the rumen microbiota from gestation and lactation in ewes grazing tall fescue pastures with high (HA) or moderate (MA) levels of endophyte infection, and their relationship with serum parameters. Data were collected at the beginning of the study (d1), the week before initiation of lambing (d51), and at the end of the trial (d115). The rumen microbiota was evaluated using 16S rRNA gene sequencing. Ewes grazing HA had greater serum non-esterified fatty acid (NEFA) (P = 0.024) levels compared with ewes in MA pasture at d115. Both the number of observed OTUs and Shannon diversity index tended (P = 0.08, P = 0.06) to be greater for HA than for MA on d115. At the genus level, Prevotella relative abundance increased with time in both MA and HA (on d1, d51, and d115: 15.17, 25.59, and 24.78% in MA; 14.17, 18.10, and 19.41% in HA). Taxa unclassified at the genus level including (unclassified) Lachnospiraceae, Coriobacteriaceae, and Veillonellaceae exhibited higher abundances in HA at d51 (3.72, 2.07, and 11.22%) compared with MA (2.06, 1.28, and 7.42%). The predictor microbiota for HA and MA were identified by a random forest classification model. The HA predictors included bacteria associated with unclassified Coriobacteriaceae and Ruminococcaceae. Other OTUs classified as Prevotella and Clostridiales could be microbial predictors for MA. The OTUs classified as Prevotella and Lachnospiraceae were negatively correlated with serum concentration of prolactin. Negative correlations with NEFA were observed in the microbiota such as species affiliated to unclassified Clostridiales and Prevotella. OTUs classified as Bacteroidetes and Coriobacteriaceae exhibited a positive correlation with NEFA. Our study confirmed that the rumen microbiota populations were affected by high levels of toxins in endophyte-infected tall fescue and were associated with host hormone and energy metabolism.

Project description:Consumption of ergot alkaloid-containing tall fescue grass impairs several metabolic, vascular, growth, and reproductive processes in cattle, collectively producing a clinical condition known as "fescue toxicosis." Despite the apparent association between pituitary function and these physiological parameters, including depressed serum prolactin; no reports describe the effect of fescue toxicosis on pituitary genomic expression profiles. To identify candidate regulatory mechanisms, we compared the global and selected targeted mRNA expression patterns of pituitaries collected from beef steers that had been randomly assigned to undergo summer-long grazing (89 to 105 d) of a high-toxic endophyte-infected tall fescue pasture (HE; 0.746 ?g/g ergot alkaloids; 5.7 ha; n = 10; BW = 267 ± 14.5 kg) or a low-toxic endophyte tall fescue-mixed pasture (LE; 0.023 ?g/g ergot alkaloids; 5.7 ha; n = 9; BW = 266 ± 10.9 kg). As previously reported, in the HE steers, serum prolactin and body weights decreased and a potential for hepatic gluconeogenesis from amino acid-derived carbons increased. In this manuscript, we report that the pituitaries of HE steers had 542 differentially expressed genes (P < 0.001, false discovery rate ? 4.8%), and the pattern of altered gene expression was dependent (P < 0.001) on treatment. Integrated Pathway Analysis revealed that canonical pathways central to prolactin production, secretion, or signaling were affected, in addition to those related to corticotropin-releasing hormone signaling, melanocyte development, and pigmentation signaling. Targeted RT-PCR analysis corroborated these findings, including decreased (P < 0.05) expression of DRD2, PRL, POU1F1, GAL, and VIP and that of POMC and PCSK1, respectively. Canonical pathway analysis identified HE-dependent alteration in signaling of additional pituitary-derived hormones, including growth hormone and GnRH. We conclude that consumption of endophyte-infected tall fescue alters the pituitary transcriptome profiles of steers in a manner consistent with their negatively affected physiological parameters.

Dataset Information

Toxic tall fescue grazing increases susceptibility of the Angus steer fecal microbiota and plasma/urine metabolome to environmental effects.

Publications

Toxic tall fescue grazing increases susceptibility of the Angus steer fecal microbiota and plasma/urine metabolome to environmental effects.

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