Insights into the bovine rumen plasmidome

Abstract

Plasmids are self-replicating genetic elements capable of mobilization between different hosts. Plasmids often serve as mediators of lateral gene transfer, a process considered to be a strong and sculpting evolutionary force in microbial environments. Our aim was to characterize the overall plasmid population in the environment of the bovine rumen, which houses a complex and dense microbiota that holds enormous significance for humans. We developed a procedure for the isolation of total rumen plasmid DNA, termed rumen plasmidome, and subjected it to deep sequencing using the Illumina paired-end protocol and analysis using public and custom-made bioinformatics tools. A large number of plasmidome contigs aligned with plasmids of rumen bacteria isolated from different locations and at various time points, suggesting that not only the bacterial taxa, but also their plasmids, are defined by the ecological niche. The bacterial phylum distribution of the plasmidome was different from that of the rumen bacterial taxa. Nevertheless, both shared a dominance of the phyla Firmicutes, Bacteroidetes, and Proteobacteria. Evidently, the rumen plasmidome is of a highly mosaic nature that can cross phyla. Interestingly, when we compared the functional profile of the rumen plasmidome to two plasmid databases and two recently published rumen metagenomes, it became apparent that the rumen plasmidome codes for functions, which are enriched in the rumen ecological niche and could confer advantages to their hosts, suggesting that the functional profiles of mobile genetic elements are associated with their environment, as has been previously implied for viruses.

Temporal Metagenomic and Metabolomic Characterization of Fresh Perennial Ryegrass Degradation by Rumen Bacteria

“…The rumen, via it's complex microbiome is responsible for the breakdown of plant material and the functional capacity of the microbiome defines the amount, quality, and composition of meat and milk produced, whilst also defining the release of nitrogen and greenhouse gases to the environment (Edwards et al, 2008a; Kim et al, 2009; Kingston-Smith et al, 2010; Brown Kav et al, 2012; Huws et al, 2014a). The process of colonizing ingested plant material by the rumen microbiome is rapid (Cheng et al, 1980; Miron et al, 2001; Russell and Rychlik, 2001; Koike et al, 2003a; Edwards et al, 2007, 2008b; Huws et al, 2013, 2014b, 2016), and eventually these populations form mature biofilms encompassed in self-produced polymeric substances (EPS) (Akin, 1976; Cheng et al, 1980, 1981; McAllister et al, 1994; Huws et al, 2013; Leng, 2014).…”

Comparison of Four Comamonas Catabolic Plasmids Reveals the Evolution of pBHB To Catabolize Haloaromatics

“…In addition to the conserved backbone, which is important for DNA replication and mobilization, plasmids usually carry highly variable regions of accessory genes that are responsible for the phenotypic diversity of their hosts, such as the capability to catabolize organic pollutants and to resist heavy metals (13,16). Furthermore, the plasmid-meditated horizontal transfer of catabolic genes contributes to the evolution of catabolic pathways in recipients (9,16). Given the important role of plasmids in shaping microbial phenotypes and adaptation to changing environments, understanding their biology is central to understanding microbial evolution and ecology (17).…”

The rumen plasmidome

“…These findings from our exploration of the metagenomic plasmid population within the complex microbial habitat of the rumen 1 suggest that in this habitat, the plasmids have certain hereditary characteristics—as they recur and are acquired at different locations and time points, while serving as a channel for the exchange of rumen-advantageous functions between the rumen microbes (Fig. 1).…”

“…These traits include amino acid metabolism, protein metabolism, respiration and carbohydrate metabolism, which are needed within the rumen ecosystem 1 , 4 . This suggests that the accessory functions carried by plasmids could reflect the most advantageous functions within a given ecological niche.…”