Abstract
Members of the genus Bifidobacterium are common inhabitants of the human gastrointestinal tract. Previously it was shown that arabino-oligosaccharides (AOS) might act as prebiotics and stimulate the bifidobacterial growth in the gut. However, despite the rapid accumulation of genomic data, the precise mechanisms by which these sugars are utilized and associated transcription control still remain unclear. In the current study, we used a comparative genomic approach to reconstruct arabinose and AOS utilization pathways in over 40 bacterial species belonging to the Bifidobacteriaceae family. The results indicate that the gene repertoire involved in the catabolism of these sugars is highly diverse, and even phylogenetically close species may differ in their utilization capabilities. Using bioinformatics analysis we identified potential DNA-binding motifs and reconstructed putative regulons for the arabinose and AOS utilization genes in the Bifidobacteriaceae genomes. Six LacI-family transcriptional factors (named AbfR, AauR, AauU1, AauU2, BauR1 and BauR2) and a TetR-family regulator (XsaR) presumably act as local repressors for AOS utilization genes encoding various α- or β-L-arabinofuranosidases and predicted AOS transporters. The ROK-family regulator AraU and the LacI-family regulator AraQ control adjacent operons encoding putative arabinose transporters and catabolic enzymes, respectively. However, the AraQ regulator is universally present in all Bifidobacterium species including those lacking the arabinose catabolic genes araBDA, suggesting its control of other genes. Comparative genomic analyses of prospective AraQ-binding sites allowed the reconstruction of AraQ regulons and a proposed binary repression/activation mechanism. The conserved core of reconstructed AraQ regulons in bifidobacteria includes araBDA, as well as genes from the central glycolytic and fermentation pathways (pyk, eno, gap, tkt, tal, galM, ldh). The current study expands the range of genes involved in bifidobacterial arabinose/AOS utilization and demonstrates considerable variations in associated metabolic pathways and regulons. Detailed comparative and phylogenetic analyses allowed us to hypothesize how the identified reconstructed regulons evolved in bifidobacteria. Our findings may help to improve carbohydrate catabolic phenotype prediction and metabolic modeling, while it may also facilitate rational development of novel prebiotics.
Highlights
Bifidobacteria are Gram-positive, non-motile, non-sporeforming, anaerobic saccharolytic microorganisms that represent one of the deepest branches within the Actinobacteria phylum (Ventura et al, 2007; Lugli et al, 2017)
In three Bifidobacterium species, the araBDA operon contains the arabinose transporter (araE) gene encoding a putative transporter from the Sugar Porter (SP) family, which shares 47% sequence identity with the arabinose-proton symporter AraE from Bacillus subtilis (Sá-Nogueira and Ramos, 1997)
It should be pointed out that the process of prebiotic development should consider metabolic connections of bifidobacteria with other members of the gut microbiota (GM), for example if they are dependent on glycoside hydrolase (GH) activities produced by other bacteria in order to gain access to certain carbohydrates
Summary
Bifidobacteria are Gram-positive, non-motile, non-sporeforming, anaerobic saccharolytic microorganisms that represent one of the deepest branches within the Actinobacteria phylum (Ventura et al, 2007; Lugli et al, 2017). The majority of known Bifidobacterium species inhabit the gastrointestinal tract of various animals (mostly mammals, though birds and insects), yet some species may be found in different ecological niches ranging from the oral cavity (Okamoto et al, 2008; Ventura et al, 2009) to fermented milk products (Watanabe et al, 2009) Since their first isolation from infant feces in 1899 by Henri Tissier (van den Broek et al, 2008; Lee and O’Sullivan, 2010), bifidobacteria have continued to be a subject of study, especially in the last two decades due to increased interest in the functionalities of the GM in (human) health and disease. Due to these claimed beneficial activities, several bifidobacterial species and strains, such as B. animalis subsp. lactis and B. longum subsp. longum, are commonly used as probiotics and are included in functional foods (Stanton et al, 2005; Russell et al, 2011)
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