Dataset Information

Novel molecular, structural and evolutionary characteristics of the phosphoketolases from bifidobacteria and Coriobacteriales.

ABSTRACT: Members from the order Bifidobacteriales, which include many species exhibiting health promoting effects, differ from all other organisms in using a unique pathway for carbohydrate metabolism, known as the "bifid shunt", which utilizes the enzyme phosphoketolase (PK) to carry out the phosphorolysis of both fructose-6-phosphate (F6P) and xylulose-5-phosphate (X5P). In contrast to bifidobacteria, the PKs found in other organisms (referred to XPK) are able to metabolize primarily X5P and show very little activity towards F6P. Presently, very little is known about the molecular or biochemical basis of the differences in the two forms of PKs. Comparative analyses of PK sequences from different organisms reported here have identified multiple high-specific sequence features in the forms of conserved signature inserts and deletions (CSIs) in the PK sequences that clearly distinguish the X5P/F6P phosphoketolases (XFPK) of bifidobacteria from the XPK homologs found in most other organisms. Interestingly, most of the molecular signatures that are specific for the XFPK from bifidobacteria are also shared by the PK homologs from the Coriobacteriales order of Actinobacteria. Similarly to the Bifidobacteriales, the order Coriobacteriales is also made up of commensal organisms, that are saccharolytic and able to metabolize wide variety of carbohydrates, producing lactate and other metabolites. Phylogenetic studies provide evidence that the XFPK from bifidobacteria are specifically related to those found in the Coriobacteriales and suggest that the gene for PK (XFPK) was horizontally transferred between these two groups. A number of the identified CSIs in the XFPK sequence, which serve to distinguish the XFPK homologs from XPK homologs, are located at the subunit interface in the structure of the XFPK dimer protein. The results of protein modelling and subunit docking studies indicate that these CSIs are involved in the formation/stabilization of the protein dimer. The significance of these observations regarding the differences in the activities of the XFPK and XPK homologs are discussed. Additionally, this work also discusses the significance of the XFPK-like homologs, similar to those found in bifidobacteria, in the order Coriobacteriales.

SUBMITTER: Gupta RS

PROVIDER: S-EPMC5315409 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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Novel molecular, structural and evolutionary characteristics of the phosphoketolases from bifidobacteria and Coriobacteriales.

Gupta Radhey S RS Nanda Anish A Khadka Bijendra B

PloS one 20170217 2

Members from the order Bifidobacteriales, which include many species exhibiting health promoting effects, differ from all other organisms in using a unique pathway for carbohydrate metabolism, known as the "bifid shunt", which utilizes the enzyme phosphoketolase (PK) to carry out the phosphorolysis of both fructose-6-phosphate (F6P) and xylulose-5-phosphate (X5P). In contrast to bifidobacteria, the PKs found in other organisms (referred to XPK) are able to metabolize primarily X5P and show very ...[more]

PMID: 28212383

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Project description:BACKGROUND:The assembly of animal microbiomes is influenced by multiple environmental factors and host genetics, although the relative importance of these factors remains unclear. Bifidobacteria (genus Bifidobacterium, phylum Actinobacteria) are common first colonizers of gut microbiomes in humans and inhabit other mammals, social insects, food, and sewages. In humans, the presence of bifidobacteria in the gut has been correlated with health-promoting benefits. Here, we compared the genome sequences of a subset of the over 400 Bifidobacterium strains publicly available to investigate the adaptation of bifidobacteria diversity. We tested 1) whether bifidobacteria show a phylogenetic signal with their isolation sources (hosts and environments) and 2) whether key traits encoded by the bifidobacteria genomes depend on the host or environment from which they were isolated. We analyzed Bifidobacterium genomes available in the PATRIC and NCBI repositories and identified the hosts and/or environment from which they were isolated. A multilocus phylogenetic analysis was conducted to compare the genetic relatedness the strains harbored by different hosts and environments. Furthermore, we examined differences in genomic traits and genes related to amino acid biosynthesis and degradation of carbohydrates. RESULTS:We found that bifidobacteria diversity appears to have evolved with their hosts as strains isolated from the same host were non-randomly associated with their phylogenetic relatedness. Moreover, bifidobacteria isolated from different sources displayed differences in genomic traits such as genome size and accessory gene composition and on particular traits related to amino acid production and degradation of carbohydrates. In contrast, when analyzing diversity within human-derived bifidobacteria, we observed no phylogenetic signal or differences on specific traits (amino acid biosynthesis genes and CAZymes). CONCLUSIONS:Overall, our study shows that bifidobacteria diversity is strongly adapted to specific hosts and environments and that several genomic traits were associated with their isolation sources. However, this signal is not observed in human-derived strains alone. Looking into the genomic signatures of bifidobacteria strains in different environments can give insights into how this bacterial group adapts to their environment and what types of traits are important for these adaptations.

Project description:Some probiotic bifidobacteria are highly robust and shelf-stable, whereas others are difficult to produce, due to their sensitivity to stressors. This limits their potential use as probiotics. Here, we investigate the molecular mechanisms underlying the variability in stress physiologies of Bifidobacterium animalis subsp. lactis BB-12 and Bifidobacterium longum subsp. longum BB-46, by applying a combination of classical physiological characterization and transcriptome profiling. The growth behavior, metabolite production, and global gene expression profiles differed considerably between the strains. BB-12 consistently showed higher expression levels of multiple stress-associated genes, compared to BB-46. This difference, besides higher cell surface hydrophobicity and a lower ratio of unsaturated to saturated fatty acids in the cell membrane of BB-12, should contribute to its higher robustness and stability. In BB-46, the expression of genes related to DNA repair and fatty acid biosynthesis was higher in the stationary than in the exponential phase, which was associated with enhanced stability of BB-46 cells harvested in the stationary phase. The results presented herein highlight important genomic and physiological features contributing to the stability and robustness of the studied Bifidobacterium strains. IMPORTANCE Probiotics are industrially and clinically important microorganisms. To exert their health-promoting effects, probiotic microorganisms must be administered at high counts, while maintaining their viability at the time of consumption. In addition, intestinal survival and bioactivity are important criteria for probiotics. Although bifidobacteria are among the most well-documented probiotics, the industrial-scale production and commercialization of some Bifidobacterium strains is challenged by their high sensitivity to environmental stressors encountered during manufacturing and storage. Through a comprehensive comparison of the metabolic and physiological characteristics of 2 Bifidobacterium strains, we identify key biological markers that can serve as indicators for robustness and stability in bifidobacteria.

Dataset Information

Novel molecular, structural and evolutionary characteristics of the phosphoketolases from bifidobacteria and Coriobacteriales.

Publications

Novel molecular, structural and evolutionary characteristics of the phosphoketolases from bifidobacteria and Coriobacteriales.

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