Dominant remodelling of cattle rumen microbiome by Schedonorus arundinaceus (tall fescue) KY-31 carrying a fungal endophyte

Abstract

Tall fescue KY-31 is an important primary forage for beef cattle. It carries a fungal endophyte that produces ergovaline, the main cause of tall fescue toxicosis that leads to major revenue loss for livestock producers. The MaxQ, an engineered cultivar, hosts an ergovaline nonproducing strain of the fungus and consequently is nontoxic. However, it is less attractive economically. It is not known how rumen microbiome processes these two forages towards nutrient generation and ergovaline transformation. We have analysed the rumen microbiome compositions of cattle that grazed MaxQ with an intervening KY-31 grazing period using the 16S rRNA-V4 element as an identifier and found that KY-31 remodelled the microbiome substantially, encompassing both cellulolytic and saccharolytic functions. The effect was not evident at the whole microbiome levels but was identified by analysing the sessile and planktonic fractions separately. 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. The abundances of Fibrobacter , which degrades less degradable fibres, and certain cellulolytic Firmicutes such as Pseudobutyrivibrio and Butyrivibrio 2, dropped in the sessile fraction, and these losses were apparently compensated by increased occurrences of Eubacterium and specific Ruminococcaceae and Lachnospiraceae . A return to MaxQ restored the original Firmicutes and Bacteroidetes distributions. However, several KY-31 induced changes, such as the low abundance of Fibrobacter and Butyrivibrio two remained in place, and their substitutes maintained significant presence. The rumen microbiome was distinct from previously reported faecal microbiomes. In summary, KY-31 and MaxQ were digested in the cattle rumen with distinct consortia and the KY-31-specific features were dominant. The study also identified candidate ergovaline transforming bacteria. It highlighted the importance of analysing sessile and planktonic fractions separately.

Evolving understanding of rumen methanogen ecophysiology

“…In most cases there is little information on the association of isolate genomes, MAGs, and even sometimes the metatranscriptomic and metaproteomic data for the methanogens with the following key parameters: (i) details of the feed; (ii) spatial location within the rumen, namely, fiber-associated, planktonic, and epimural microbiome; (iii) co-occurrence, such as association with the syntrophic partners, protozoa, and bacteria; (iv) timing of sampling with respect to feeding; and (v) comparison with free-living counterparts. In a recent study with cattle grazing tall fescue, a major perturbation of the microbiome by a toxic version of the grass was detected only when the sessile and planktonic fractions were analyzed separately (Khairunisa et al, 2022) and similar observations have been reported by others (Pitta et al, 2014).…”

Cellulose fermentation by the gut microbiota is likely not essential for the nutrition of millipedes

“…Various studies suggest that certain millipede gut bacteria possess enzymes for breaking down plant polysaccharides (20–24). If millipedes rely on cellulose for their nutrition, extensive fermentation followed by methanogenesis, similar to ruminants or wood-feeding termites, should occur in their guts (7, 25). However, methanogenesis has only been observed in some millipede species, but not others, with its occurrence correlated to the millipede size (26).…”