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.
The genus Bifidobacterium represents one of the major components of the intestinal microbiota of breastfed infants (1-5) while also typically constituting between 2% and 10% of the adult intestinal microbiota (6-11). Bifidobacteria are saccharolytic microorganisms whose ability to colonize and survive in the large intestine is presumed to depend on the ability to metabolize complex carbohydrates present in this environment (12, 13). Certain bifidobacterial species, including Bifidobacterium longum subsp. longum, Bifidobacterium adolescentis, and Bifidobacterium breve, utilize a range of plant/diet-derived oligosaccharides such as raffinose, arabinoxylan, galactan, and cellodextrins (14-20). Bifidobacterial metabolism of human milk oligosaccharides (HMOs) is also well described, with the typically infant-derived species B. longum subsp. infantis and Bifidobacterium bifidum ...