Abstract
Butyrivibrio and Pseudobutyrivibrio dominate in anaerobic gastrointestinal microbiomes, particularly the rumen, where they play a key role in harvesting dietary energy. Within these genera, five rumen species have been classified ( Butyrivibrio fibrisolvens , Butyrivibrio hungatei , Butyrivibrio proteoclasticus , Pseudobutyrivibrio ruminis and Pseudobutyrivibrio xylanivorans ) and more recently an additional Butyrivibrio sp. group was added. Given the recent increase in available genomes, we re-investigated the phylogenetic systematics and evolution of Butyrivibrio and Pseudobutyrivibrio . Across 71 genomes, we show using 16S rDNA and 40 gene marker phylogenetic trees that the current six species designations ( P. ruminis , P. xylanivorans , B. fibrisolvens , Butyrivibrio sp., B. hungatei and B. proteclasticus) are found. However, pangenome analysis showed vast genomic variation and a high abundance of accessory genes (91.50–99.34 %), compared with core genes (0.66–8.50 %), within these six taxonomic groups, suggesting incorrectly assigned taxonomy. Subsequent pangenome accessory genomes under varying core gene cut-offs (%) and average nucleotide identity (ANI) analysis suggest the existence of 42 species within 32 genera. Pangenome analysis of those that still group within B. fibrisolvens , B. hungatei and P. ruminis , based on revised ANI phylogeny, also showed possession of very open genomes, illustrating the diversity that exists even within these groups. All strains of both Butyrivibrio and Pseudobutyrivibrio also shared a broad range of clusters of orthologous genes (COGs) (870), indicating recent evolution from a common ancestor. We also demonstrate that the carbohydrate-active enzymes (CAZymes) predominantly belong to glycosyl hydrolase (GH)2, 3, 5, 13 and 43, with numerous within family isoforms apparent, likely facilitating metabolic plasticity and resilience under dietary perturbations. This study provides a major advancement in our functional and evolutionary understanding of these important anaerobic bacteria.
Highlights
The definition of ‘species’ in bacteria or archaea is contentious, with some believing that the search for a single, natural way to divide bacteria into species is futile [1, 2]
Across 71 genomes, we show using 16S rDNA and 40 gene marker phylogenetic trees that the current six species designations (P. ruminis, P. xylanivorans, B. fibrisolvens, Butyrivibrio sp., B. hungatei and B. proteclasticus) are found
We have used genotypic analyses, multilocus sequence analyses, average nucleotide identity (ANI), whole- genome analyses, etc. [3, 4]. 16S rDNA became a popular metric in the 1980s, with organisms sharing greater than 97 % 16S rDNA being classified as a single species [5]
Summary
The definition of ‘species’ in bacteria or archaea is contentious, with some believing that the search for a single, natural way to divide bacteria into species is futile [1, 2]. At the beginning of the 20th century, more biochemical and physiological markers were added to this list, followed by chemotaxonomy, numerical taxonomy and. 16S rDNA became a popular metric in the 1980s, with organisms sharing greater than 97 % 16S rDNA being classified as a single species [5]. This was further developed to whole-genome alignments [6] and phylogenetic clustering [7], both facing scrutiny for their seemingly arbitrary cut-off values [8]. Pangenomic analyses (those which look at shared core genes, accessory genes that confer variability, and the combination of these as the pangenome) have been suggested as potential methods for defining bacterial species [12,13,14]
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