Phylogenetic systematics of Butyrivibrio and Pseudobutyrivibrio genomes illustrate vast taxonomic diversity, open genomes and an abundance of carbohydrate-active enzyme family isoforms

• Published in: Microbial genomics Vol. 7; no. 10
• Main Authors: Pidcock, Sara E, Skvortsov, Timofey, Santos, Fernanda G, Courtney, Stephen J, Sui-Ting, Karen, Creevey, Christopher J, Huws, Sharon A
• Format: Journal Article
• Language: English
• Published: England Microbiology Society 01-10-2021
• Subjects: Animals; Base Composition; Butyrivibrio - classification; Butyrivibrio - genetics; Carbohydrates; Clostridiales - classification; Clostridiales - genetics; DNA, Ribosomal; Genome, Bacterial; Haplotypes; Phylogeny; Protein Isoforms; Rumen - microbiology; Butyrivibrio; pangenome; evolution; taxonomy; Pseudobutyrivibrio; rumen
• ISSN: 2057-5858; 2057-5858
• DOI: 10.1099/mgen.0.000638

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.