Dominant Remodeling of Cattle Rumen Microbiome by Schedonorus arundinaceus (Tall Fescue) KY-31 Carrying a Fungal Endophyte

Abstract

Tall fescue KY-31 feeds ~20% of the beef cattle in the United States. It carries a fungal endophyte that produces ergovaline, which causes toxicosis in cattle, leading to $2 billion revenue loss annually. The MaxQ cultivar of the grass is non-toxic, but less attractive economically. To develop ways of mitigating the toxicity, the rumen microbiome of cattle consuming KY-31 and MaxQ have been analyzed, principally for identifying ergovaline transforming microorganisms and often using fecal microbiome as a surrogate. We have hypothesized that KY-31 not only causes toxicosis, but also impacts rumen metabolism broadly, and tested the hypothesis by analyzing rumen microbiome compositions of cattle that grazed MaxQ with an intervening KY-31 grazing period with 16S rRNA-V4 element as identifier. We found that KY-31 remodeled the cellulolytic and saccharolytic communities substantially. This effect was not evident at whole microbiome levels but in the compositions of sessile and planktonic fractions. A move from MaxQ to KY-31 lowered the Firmicutes abundance in the sessile fraction and increased it in planktonic part and caused an opposite effect for Bacteroidetes, although the total abundances of these dominant rumen organisms remained unchanged. In the sessile fraction, the abundances of Fibrobacter, which degrades less degradable fibers, and certain cellulolytic Firmicutes such as Pseudobutyrivibrio and Butyrivibrio 2, dropped, and these losses were apparently compensated by increased occurrences of Eubacterium and specific Ruminococcaceae and Lachnospiraceae. In planktonic fraction the Tenericutes abundance increased as saccharolytic Bacteroidetes level dropped. Several potential ergovaline degraders were enriched. A return to MaxQ restored the original Firmicutes and Bacteroidetes distributions. However, the Fibrobacter and Butyrivibrio 2 abundances remained low and their substitutes maintained significant presence. The rumen microbiome was influenced minimally by animals fescue toxicosis and was distinct from previously reported fecal microbiomes in composition. In summary, KY-31 and MaxQ cultivars of tall fescue were digested in the cattle rumen with distinct consortia and the KY-31-specific features were dominant. The study highlighted the importance of analyzing sessile and planktonic fractions separately.