Phylogenetic systematics of Butyrivibrio and Pseudobutyrivibrio pure culture and metagenomically assembled genomes suggest existence of 59 genera and 75 species, alongside possession of open pangenomes with an abundance of carbohydrate-active enzyme family isoforms

Abstract

Abstract Background Gut microbiomes are crucial for host nutrition due to their feed energy-harvesting capacity. In the rumen microbiome Butyrivibrio and Pseudobutyrivibrio dominate and play a key role in harvesting dietary energy. Within these genera, five rumen species have been classified (Butyrivibrio fibrisolvens, B. hungatei, B. proteoclasticus, Pseudobutyrivibrio ruminis and P. xylanivorans) and more recently an additional sixth Butyrivibrio sp. group was added. Nonetheless, in recent years the explosion in available metagenomically assembled genomes (MAGs) offer a new insight into their taxonomy and function. Consequently, in this study we analysed the pangenome and function of 64 MAGs and 71 culture representatives of Butyrivibrio and Pseudobutyrivibrio. Results Using MASH and ANI we demonstrate that the 135 Butyrivibrio and Pseudobutyrivibrio genomes from MAGs and pure culture cluster into 59 genera and 75 species. Pangenome analysis of 8 groups containing > 4 strains showed average core genome percentages of between 38.49–76.67%. In turn, the accessory genome percentages for the 8 groups were between 23.33% and 65.39%. The most abundant GH families found in the 8 groups were GH13, GH3, GH43, GH2, GH25, GH31, GH36, and GH5 in descending order. Dendograms of the GH families show extensive variation, and expression of 20.45–47.11% of the genes is observed in metatranscriptome datasets. Conclusions Our findings demonstrate that Butyrivibrio and Pseudobutyrivibrio genomes cluster into 59 genera and 75 species. The 8 groups containing 4 or more genomes that were carried forward possess open genomes with extensive genomic diversity. The MAGs, alongside genomes for cultured isolates, contained an expansive repertoire of glycosyl hydrolase isoforms, which likely facilitate the symbiotic breakdown of plant matter under dietary perturbations allowing a competitive advantage and driving niche specialisation. This study has enabled a substantial enhancement in our understanding of the functional capacity and taxonomy of the dominant rumen isolates, Butyrivibrio and Pseudobutyrivibrio by utilising all recently published rumen MAGs.