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Identification of a Novel N-Acetylmuramic Acid Transporter in Tannerella forsythia
Identification of a Novel N-Acetylmuramic Acid Transporter in Tannerella forsythia
- Source :
- Journal of bacteriology. 198(22)
- Publication Year :
- 2016
-
Abstract
- Tannerella forsythia is a Gram-negative periodontal pathogen lacking the ability to undergo de novo synthesis of amino sugars N -acetylmuramic acid (MurNAc) and N -acetylglucosamine (GlcNAc) that form the disaccharide repeating unit of the peptidoglycan backbone. T. forsythia relies on the uptake of these sugars from the environment, which is so far unexplored. Here, we identified a novel transporter system of T. forsythia involved in the uptake of MurNAc across the inner membrane and characterized a homolog of the Escherichia coli MurQ etherase involved in the conversion of MurNAc-6-phosphate (MurNAc-6-P) to GlcNAc-6-P. The genes encoding these components were identified on a three-gene cluster spanning Tanf_08375 to Tanf_08385 located downstream from a putative peptidoglycan recycling locus. We show that the three genes, Tanf_08375, Tanf_08380, and Tanf_08385, encoding a MurNAc transporter, a putative sugar kinase, and a MurQ etherase, respectively, are transcriptionally linked. Complementation of the Tanf_08375 and Tanf_08380 genes together in trans , but not individually, rescued the inability of an E. coli mutant deficient in the phosphotransferase (PTS) system-dependent MurNAc transporter MurP as well as that of a double mutant deficient in MurP and components of the PTS system to grow on MurNAc. In addition, complementation with this two-gene construct in E. coli caused depletion of MurNAc in the medium, further confirming this observation. Our results show that the products of Tanf_08375 and Tanf_08380 constitute a novel non-PTS MurNAc transporter system that seems to be widespread among bacteria of the Bacteroidetes phylum. To the best of our knowledge, this is the first identification of a PTS-independent MurNAc transporter in bacteria. IMPORTANCE In this study, we report the identification of a novel transporter for peptidoglycan amino sugar N -acetylmuramic acid (MurNAc) in the periodontal pathogen T. forsythia . It has been known since the late 1980s that T. forsythia is a MurNAc auxotroph relying on environmental sources for this essential sugar. Most sugar transporters, and the MurNAc transporter MurP in particular, require a PTS phosphorelay to drive the uptake and concurrent phosphorylation of the sugar through the inner membrane in Gram-negative bacteria. Our study uncovered a novel type of PTS-independent MurNAc transporter, and although so far, it seems to be unique to T. forsythia , it may be present in a range of bacteria both of the oral cavity and gut, especially of the phylum Bacteroidetes .
- Subjects :
- 0301 basic medicine
Glycoside Hydrolases
030106 microbiology
Mutant
Peptidoglycan
medicine.disease_cause
Microbiology
Phosphotransferase
03 medical and health sciences
chemistry.chemical_compound
Forsythia
Bacterial Proteins
medicine
Escherichia coli
Tannerella forsythia
Molecular Biology
biology
Membrane Transport Proteins
Articles
biology.organism_classification
Complementation
carbohydrates (lipids)
stomatognathic diseases
030104 developmental biology
Biochemistry
chemistry
N-Acetylmuramic acid
Muramic Acids
Subjects
Details
- ISSN :
- 10985530
- Volume :
- 198
- Issue :
- 22
- Database :
- OpenAIRE
- Journal :
- Journal of bacteriology
- Accession number :
- edsair.doi.dedup.....149c56946d276864115fad7267ffe59b