Genomic architecture of three newly isolated unclassified Butyrivibrio species elucidate their potential role in the rumen ecosystem

Sengupta, Kriti; Hivarkar, Sai Suresh; Palevich, Nikola; Chaudhary, Prem Prashant; Dhakephalkar, Prashant K.; Dagar, Sumit Singh

doi:10.1016/j.ygeno.2022.110281

Cited by 11 publications

(7 citation statements)

References 104 publications

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“…This is more likely to be the case in "open" pangenomes (whereby each new addition is likely to add an abundance of accessory genes) than in "closed" pangenomes (in which new genomes will introduce very few new genes). Given that Butyrivibrio are considered to have an open pangnome [31], our nding that they have a smaller core genome than, for example, Staphylococcus lugdunensis, whose core genes represent 86-88% of the entire genome [21] corroborates our hypothesis that these genera have very open genomes. An open pangenome is proposed to be typical of organisms that colonise multiple environments, and are more likely to exchange genetic information [32]; given that Butyrivibrio have been isolated from ruminants worldwide, regardless of geography, host animal, host feed, etc.…”

Section: Discussionsupporting

confidence: 77%

“…GH family 3 enzymes were also present in high abundance; GH3 enzymes are primarily β-glucosidases, which are capable of hydrolysing the β-glucosidic linkages in complex carbohydrate molecules. GH3 enzymes are mostly intracellular [40], and have also been found to be abundantly present in newly isolated Butyrivibrio strains CB08, XB500-5, and X503, which it is suggested facilitates their high levels of cellobiohydrolase and xylobiohydrolase activity [31]. Alongside endo-and exoglucanases, β-glucosidases play a key role in the metabolism of cellulose, the most abundant organic biopolymer in the biosphere; endo-and exoglucanases act synergistically to hydrolyse glucosidic bonds to generate various oligosaccharides.…”

Section: Discussionmentioning

confidence: 99%

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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

Pidcock

Skvortsov

Courtney

et al. 2022

Preprint

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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.

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Section: Discussionsupporting

confidence: 77%

Section: Discussionmentioning

confidence: 99%

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

Pidcock

Skvortsov

Courtney

et al. 2022

Preprint

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“…s_Butyrivibrio fibrisolvens and s_Ruminococcus albus are bacteria that are good for ruminants. s_Butyrivibrio fibrisolvens can increase the content of conjugated linoleic acid in the intestine and adipose tissue (Srivastava et al, 2021) and produce diverse carbohydrate-active enzymes that hydrolyze cellulose and other plant-derived macromolecular polymers (Sengupta et al, 2022). This bacterium is similar to s_Ruminococcus albus, which can also synthesize some types of hydrolytic enzymes that help ruminants digest plant-based feed (Storani et al, 2020;Ortiz-Chura et al, 2021).…”

Section: Discussionmentioning

confidence: 99%

A preliminary study on the possibility of fermented pineapple peel residue partially replacing whole corn silage in feeding Chuanzhong black goats

et al. 2022

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This study aims to assess the effects of the partial replacement of whole corn silage (WCS) with fermented pineapple peel residue (FPPR) on growth, serological parameters, muscle quality, rumen microorganisms, and fecal microorganisms. A total of 24 Chuanzhong black goats weighing 10.23 ± 1.42 kg were evaluated in a randomized complete trial design in accordance with the following treatments: (1) 0% FPPR in the diet, (2) 25% FPPR in the diet, and (3) 50% FPPR in the diet. In goats, the partial substitution of FPPR for WCS increased the abundance of probiotics, such as Blautia, Butyrivibrio fibrisolvens, and Ruminococcus albus, and did not exert significant effects on overall serological parameters and muscle quality. In conclusion, the partial substitution of FPPR for WCS in the diet did not impair or affect the productive performance of goats.

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“…Butyrivibrio play important roles in plant fibre breakdown, protein digestion, and the biohydrogenation of fatty acids but also contribute significantly to methanol formation in the rumen [ 16 , 17 , 18 , 19 , 20 ]. Butyrivibrio proteoclasticus B316 T and Butyrivibrio fibrisolvens D1 T are well-characterised rumen bacteria known for their ability to degrade pectins into various monosaccharides that are metabolized and fermented to butyrate, formate, and acetate [ 21 , 22 , 23 , 24 , 25 , 26 , 27 , 28 , 29 , 30 , 31 ].…”

Section: Introductionmentioning

confidence: 99%

Crystal Structures of Bacterial Pectin Methylesterases Pme8A and PmeC2 from Rumen Butyrivibrio

Carbone,

Reilly,

Sang

et al. 2023

IJMS

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Pectin is a complex polysaccharide that forms a substantial proportion of the plant’s middle lamella of forage ingested by grazing ruminants. Methanol in the rumen is derived mainly from methoxy groups released from pectin by the action of pectin methylesterase (PME) and is subsequently used by rumen methylotrophic methanogens that reduce methanol to produce methane (CH4). Members of the genus Butyrivibrio are key pectin-degrading rumen bacteria that contribute to methanol formation and have important roles in fibre breakdown, protein digestion, and the biohydrogenation of fatty acids. Therefore, methanol release from pectin degradation in the rumen is a potential target for CH4 mitigation technologies. Here, we present the crystal structures of PMEs belonging to the carbohydrate esterase family 8 (CE8) from Butyrivibrio proteoclasticus and Butyrivibrio fibrisolvens, determined to a resolution of 2.30 Å. These enzymes, like other PMEs, are right-handed β-helical proteins with a well-defined catalytic site and reaction mechanisms previously defined in insect, plant, and other bacterial pectin methylesterases. Potential substrate binding domains are also defined for the enzymes.

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Genomic architecture of three newly isolated unclassified Butyrivibrio species elucidate their potential role in the rumen ecosystem

Cited by 11 publications

References 104 publications

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

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

A preliminary study on the possibility of fermented pineapple peel residue partially replacing whole corn silage in feeding Chuanzhong black goats

Crystal Structures of Bacterial Pectin Methylesterases Pme8A and PmeC2 from Rumen Butyrivibrio

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