Metatranscriptomic Profiling Reveals the Effect of Breed on Active Rumen Eukaryotic Composition in Beef Cattle With Varied Feed Efficiency

Abstract

Exploring the compositional characteristics of rumen eukaryotic community can expand our understanding of their role in rumen function and feed efficiency. In this study, we applied metatranscriptomics to characterize the active rumen eukaryotic community (protozoa and fungi) in beef cattle (n = 48) of three breeds [Angus (AN), Charolais (CH), and Kinsella Composite (KC)] and with divergent residual feed intake (RFI). The composition of active rumen eukaryotic microbiota was evaluated based on enriched 18S rRNAs from the metatranscriptomic datasets. At the phylum level, a total of four protozoal taxa (Ciliophora, Parabasalia, unclassified SAR, and unclassified Alveolata), six fungal taxa (Neocallimastigomycota, Basidiomycota, unclassified Fungi, Mucoromycota, Ascomycota, and Chytridiomycota), and one sister group of kingdom Fungi (unclassified Opisthokonta) were detected with relative abundances higher than 0.01% and in at least 50% of animals within each breed. Among these, Ciliophora, Parabasalia, unclassified Opisthokonta, and Neocallimastigomycota were the top four active eukaryotic phyla. At the genus level, a total of 8 ciliated protozoa, 5 flagellated protozoa, 5 anaerobic fungi, and 10 aerobic fungi taxa were detected, with unclassified Trichostomatia, Tetratrichomonas, unclassified Neocallimastigaceae, and Pleurotus being the most predominant taxa of ciliated protozoa, flagellated protozoa, anaerobic fungi, and aerobic fungi, respectively. Differential abundance analysis revealed that breed had a significant effect on the phylogenetic lineages of rumen eukaryotes, and seven fungal taxa were more abundant (linear discriminant analysis score > 2 with P < 0.05) in the rumen of KC steers than in the rumen of AN and CH steers. Although principal coordinate analysis (PCoA) revealed that the ruminal active eukaryotic profiles were not distinguishable between high-and low-RFI groups, the diversity indices, including Faith's phylogenetic diversity (PD), observed operational taxonomic units (OTUs), and Shannon index of rumen eukaryotes were higher in low-RFI steers than those in high-RFI steers. Meanwhile, the abundance of genus Entodinium and the kingdom Fungi was higher in low-RFI steers than that in high-RFI steers. This information on active rumen eukaryotic microbiota and identified differential abundance of taxa between high-and low-RFI animals suggests the possibility of improving feed efficiency through altering rumen eukaryotic microbiota.

Integrated meta-omics reveals new ruminal microbial features associated with feed efficiency in dairy cattle

“…Most of the published studies focused on the rumen prokaryotes, emphasizing the importance of bacteria and archaea in affecting feed efficiency [ 8 , 47 , 52 ]. Rumen fungi play important roles in feed digestion [ 53 , 54 ], but few studies have focused on their linkage to feed efficiency [ 9 , 21 ]. Using metatranscriptomics, Zhang et al [ 9 ] characterized the rumen eukaryotic community in beef cattle and found significant differences in protozoa and fungi among animals with different feed efficiencies [ 9 ].…”

“…Rumen fungi play important roles in feed digestion [ 53 , 54 ], but few studies have focused on their linkage to feed efficiency [ 9 , 21 ]. Using metatranscriptomics, Zhang et al [ 9 ] characterized the rumen eukaryotic community in beef cattle and found significant differences in protozoa and fungi among animals with different feed efficiencies [ 9 ]. The lack of difference in the fungal community between the two cow groups in our study contradicts the above study on beef cattle, but concur with a previous metagenomic study on dairy cattle [ 21 ].…”

“…The ability to digest various plant masses differs among individual cows and is largely dependent on the diverse microbiomes in their digestive tracts, particularly in the rumen [ 4 , 5 ]. In recent years, the advancement of understanding of the associations between the rumen microbiome and feed efficiency has led to novel strategies to select high-efficiency animals based on their rumen microbiomes [ 6 – 9 ]. The rumen microbiome is responsible for the deconstruction and fermentation of feed plant fibers and converts plant materials to volatile fatty acids (VFAs), which serve as the main energy source for ruminants [ 10 ].…”

Sporadic isolation ofTetratrichomonasspecies from the cattle urogenital tract

“…There are plausible sources for the isolated urogenital trichomonads from the bovine GIT; Tetratrichomonas spp. (Zhang et al ., 2020 ), such as Te. buttreyi (Dufernez et al ., 2007 ), are known to inhabit the cattle gut, and P. hominis is known to occupy the GIT of a very wide range of animals (Li et al ., 2016 ), including cattle (Li et al ., 2020 ).…”

Interrelationships of Fiber-Associated Anaerobic Fungi and Bacterial Communities in the Rumen of Bloated Cattle Grazing Alfalfa

“…These fungi may represent epiphytic fungal populations inhabiting forages and other feed components, and likely do not contribute directly to ruminal fermentation. However, in a recent study utilizing metatranscriptomic data to extract 18S rRNA genes [ 41 ], authors also detected members of the phyla Ascomycota and Basidiomycota in the rumen contents of cattle, and suggested that these fungi may play an active role in the scavenging of oxygen that enters the rumen during feed and water consumption. We identified eight distinct genera of the phylum Neocallimastigomycetes, including Neocallimastix, Caecomyces, Piromyces, Anaeromyces, Orpinomyces, Cyllamyces , and Buwchfawromyces in over 80% of the ruminal samples collected from steers on both baseline and alfalfa pasture.…”