Dataset Information

The essential genomic landscape of the commensal Bifidobacterium breve UCC2003.

ABSTRACT: Bifidobacteria are common gut commensals with purported health-promoting effects. This has encouraged scientific research into bifidobacteria, though recalcitrance to genetic manipulation and scarcity of molecular tools has hampered our knowledge on the precise molecular determinants of their health-promoting attributes and gut adaptation. To overcome this problem and facilitate functional genomic analyses in bifidobacteria, we created a large Tn5 transposon mutant library of the commensal Bifidobacterium breve UCC2003 that was further characterized by means of a Transposon Directed Insertion Sequencing (TraDIS) approach. Statistical analysis of transposon insertion distribution revealed a set of 453 genes that are essential for or markedly contribute to growth of this strain under laboratory conditions. These essential genes encode functions involved in the so-called bifid-shunt, most enzymes related to nucleotide biosynthesis and a range of housekeeping functions. Comparison to the Bifidobacterium and B. breve core genomes highlights a high degree of conservation of essential genes at the species and genus level, while comparison to essential gene datasets from other gut bacteria identified essential genes that appear specific to bifidobacteria. This work establishes a useful molecular tool for scientific discovery of bifidobacteria and identifies targets for further studies aimed at characterizing essential functions not previously examined in bifidobacteria.

SUBMITTER: Ruiz L

PROVIDER: S-EPMC5514069 | biostudies-literature | 2017 Jul

REPOSITORIES: biostudies-literature

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The essential genomic landscape of the commensal Bifidobacterium breve UCC2003.

Ruiz Lorena L Bottacini Francesca F Boinett Christine J CJ Cain Amy K AK O'Connell-Motherway Mary M Lawley Trevor D TD van Sinderen Douwe D

Scientific reports 20170717 1

Bifidobacteria are common gut commensals with purported health-promoting effects. This has encouraged scientific research into bifidobacteria, though recalcitrance to genetic manipulation and scarcity of molecular tools has hampered our knowledge on the precise molecular determinants of their health-promoting attributes and gut adaptation. To overcome this problem and facilitate functional genomic analyses in bifidobacteria, we created a large Tn5 transposon mutant library of the commensal Bifid ...[more]

PMID: 28717159

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Project description:Bifidobacteria constitute a specific group of commensal bacteria typically found in the gastrointestinal tract (GIT) of humans and other mammals. Bifidobacterium breve strains are numerically prevalent among the gut microbiota of many healthy breastfed infants. In the present study, we investigated glycosulfatase activity in a bacterial isolate from a nursling stool sample, B. breve UCC2003. Two putative sulfatases were identified on the genome of B. breve UCC2003. The sulfated monosaccharide N-acetylglucosamine-6-sulfate (GlcNAc-6-S) was shown to support the growth of B. breve UCC2003, while N-acetylglucosamine-3-sulfate, N-acetylgalactosamine-3-sulfate, and N-acetylgalactosamine-6-sulfate did not support appreciable growth. By using a combination of transcriptomic and functional genomic approaches, a gene cluster designated ats2 was shown to be specifically required for GlcNAc-6-S metabolism. Transcription of the ats2 cluster is regulated by a repressor open reading frame kinase (ROK) family transcriptional repressor. This study represents the first description of glycosulfatase activity within the Bifidobacterium genus.ImportanceBifidobacteria are saccharolytic organisms naturally found in the digestive tract of mammals and insects. Bifidobacterium breve strains utilize a variety of plant- and host-derived carbohydrates that allow them to be present as prominent members of the infant gut microbiota as well as being present in the gastrointestinal tract of adults. In this study, we introduce a previously unexplored area of carbohydrate metabolism in bifidobacteria, namely, the metabolism of sulfated carbohydrates. B. breve UCC2003 was shown to metabolize N-acetylglucosamine-6-sulfate (GlcNAc-6-S) through one of two sulfatase-encoding gene clusters identified on its genome. GlcNAc-6-S can be found in terminal or branched positions of mucin oligosaccharides, the glycoprotein component of the mucous layer that covers the digestive tract. The results of this study provide further evidence of the ability of this species to utilize mucin-derived sugars, a trait which may provide a competitive advantage in both the infant gut and adult gut.

Project description:The 190 kb megaplasmid pMP7017 of Bifidobacterium breve JCM7017 represents the first conjugative and largest plasmid characterised within this genus to date. In the current study, we adopted an integrated approach combining transcriptomics, whole genome comparative analysis and metagenomic data mining to understand the biology of pMP7017 and related megaplasmids, and to assess the impact of plasmid-carriage on the host strain. The data generated revealed variations within basic features of promoter elements which correlate with a high level of transcription on the plasmid and highlight the transcriptional activity of genes encoding both offensive and defensive adaptations, including a Type IIL restriction-modification system, an anti-restriction system and four Type II toxin-antitoxin systems. Furthermore, a highly transcribed tmRNA, which likely provides translational support to the host strain, was identified, making pMP7017 the first plasmid of the Bifidobacterium genus and the smallest plasmid known to express a tmRNA. Analyses of synteny and variability among pMP7017 and related plasmids indicate substantial diversity in gene organisation and accessory gene cargo highlighting diverse (co-)evolution and potential host-specific rearrangements and adaptations. Systematic analysis of the codon usage profile of transcriptionally active pMP7017-encoded genes suggests that pMP7017 originated from (sub)species of Bifidobacterium longum. Furthermore, mining of metagenomic data suggests the presence of pMP7017-homologues in ~10% of microbiome samples, mostly infants and/or mothers from various geographical locations. Comparative transcriptome analysis of the B. breve UCC2003 chromosome in the presence or absence of pMP7017 revealed differential expression of genes representing 8% of the total gene pool. Genes involved in genetic information processing were exclusively upregulated, while altered expression of genes involved in biofilm production and polysaccharide biosynthesis was also observed.

Dataset Information

The essential genomic landscape of the commensal Bifidobacterium breve UCC2003.

Publications

The essential genomic landscape of the commensal Bifidobacterium breve UCC2003.

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