Response of Beef Cattle Fecal Microbiota to Grazing on Toxic Tall Fescue

Abstract

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 (Eϩ; n ϭ 6) or nontoxic (Max-Q; n ϭ 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 Eϩ 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 Eϩ grazing. Eϩ 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 Eϩ) and positively with respiration rates (increased by Eϩ). These data provide insights into how Eϩ grazing alters the Angus steer microbiota and the relationship of fecal microbiota dynamics with FT. IMPORTANCE Consumption of Eϩ 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 Eϩ grazing on the fecal microbiota furthers our understanding of bovine fescue toxicosis in a realworld grazing production setting and provides a starting point for identifying easyto-access fecal bacteria that could serve as potential biomarkers of animal productivity and/or FT severity for tall fescue-grazing livestock.KEYWORDS Epichloë coenophialum, fescue toxicosis, beef cattle, ergot alkaloids, microbiome, tall fescue C ulture-independent next-generation sequencing (NGS)-based microbiota studies (e.g., 16S rRNA gene) in food-producing animals, like ruminants, are on the rise. The influence of the bovine microbiota on host energy status and metabolism has been studied (1-4), and recent NGS studies have linked enteric microbiota shifts to animal Citation Mote RS, Hill NS, Skarlupka JH, Turner ZB, Sanders ZP, Jones DP, Suen G, Filipov NM. 2019. Response of beef cattle fecal microbiota to grazing on toxic tall fescue. Appl Environ

Beef cattle that respond differently to fescue toxicosis have distinct gastrointestinal tract microbiota

“…However, the knowledge about a possible involvement of GI tract microbial communities, especially fungal communities, in FT is still highly limited. Recently, Mote et al found in animals fed toxic fescue, relative abundances of the bacterial families Ruminoccocaceae and Lachnospiraceae were significantly increased [17]. Our study predominantly found consistent changes in the fungal OTUs and only detected a single significantly different bacterial OTU (OTU3, Acinetobacter ) within the 50 most abundant OTUs between the tolerance groups, and this OTU was not related to either of the aforementioned families (Fig.…”

“…In general, our knowledge about FT has significantly advanced during recent years [1, 2, 4, 17, 31–35]. However, the knowledge about a possible involvement of GI tract microbial communities, especially fungal communities, in FT is still highly limited.…”

“…2). It should be noted that the study by Mote et al, used Angus steers, not cows, and was performed at a different location (in Georgia, USA) [17]. Thus, the comparability of these two studies might be limited.…”

“…The current literature published on the effect of toxic tall fescue effects on gastrointestinal (GI) microbiota is still limited. Most recently, Mote et al, 2019 [17] surveyed fecal bacterial communities of beef cattle during a FT challenge, and described possible connections between the abundance of certain bacterial phylotypes and the host response to FT. Other studies have suggested microbial communities within the cow rumen [18, 19], earthworm’s intestine [20], and soil [21] are able to degrade ergovaline. It is thus conceivable that the GI tract microbiota may be able to alleviate some of the impact of FT symptoms.…”

Use of Integrative Interactomics for Improvement of Farm Animal Health and Welfare: An Example with Fescue Toxicosis

“…New data from our lab [ 67 , 68 , 69 ], among other recent reports [ 38 , 70 , 71 ], indicate that developing integrative interactomics-based approaches to complement other, more traditional methods for evaluating the livestock integrome could increase our understanding about the development and adaptive versus pathophysiological responses to one of the costliest diseases to the United States beef industry, fescue toxicosis. The rest of this review will focus on introducing what we currently know about fescue toxicosis development and pathophysiology and how newly generated ‘omics data could be integrated to help fill crucial knowledge gaps related to this disease.…”