{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,18]],"date-time":"2026-01-18T11:19:08Z","timestamp":1768735148575,"version":"3.49.0"},"reference-count":58,"publisher":"Public Library of Science (PLoS)","issue":"9","license":[{"start":{"date-parts":[[2022,9,16]],"date-time":"2022-09-16T00:00:00Z","timestamp":1663286400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100002790","name":"Canadian Network for Research and Innovation in Machining Technology, Natural Sciences and Engineering Research Council of Canada","doi-asserted-by":"publisher","award":["RPGIN-2014-05018"],"award-info":[{"award-number":["RPGIN-2014-05018"]}],"id":[{"id":"10.13039\/501100002790","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002790","name":"Canadian Network for Research and Innovation in Machining Technology, Natural Sciences and Engineering Research Council of Canada","doi-asserted-by":"publisher","award":["DDG-2020-00007"],"award-info":[{"award-number":["DDG-2020-00007"]}],"id":[{"id":"10.13039\/501100002790","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100009056","name":"Canadian Glycomics Network","doi-asserted-by":"publisher","award":["AM-21"],"award-info":[{"award-number":["AM-21"]}],"id":[{"id":"10.13039\/501100009056","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"abstract":"<jats:p>Advanced periodontitis has been shown to have strong association with the residence of the bacterial consortia known as the red complex comprised by <jats:italic>Porphyromonas gingivalis<\/jats:italic>, <jats:italic>Tannerella forsythia<\/jats:italic>, and <jats:italic>Treponema denticola<\/jats:italic>. <jats:italic>T<\/jats:italic>. <jats:italic>forsythia<\/jats:italic> shares a distant genetic linkage to <jats:italic>Bacteroidetes thetaiotaomicron<\/jats:italic> and may therefore produce analogous polysaccharide utilization loci (PUL) which enable complex carbohydrate degradation, import, and use, although this capacity has yet to be demonstrated. Chondroitin sulfate A is a linear, sulfated carbohydrate linked to periodontal disease as the principal species of glycosaminoglycan appended on the surface of cortical bone of teeth and in supporting dental ligaments. Through genomic comparisons with <jats:italic>B<\/jats:italic>. <jats:italic>thetaiotaomicron<\/jats:italic>, a new PUL-like operon (Bfo2285-Bfo2295, and Bfo3043) was identified in <jats:italic>T<\/jats:italic>. <jats:italic>forsythia<\/jats:italic> and the crystal structure of two proteins from this PUL-like operon, Bfo2290 and Bfo2294, were reported using X-ray crystallography. Enzyme kinetics for Bfo2290 were reported using a pH-dependent assay and suggested a <jats:italic>K<\/jats:italic><jats:sub><jats:italic>m<\/jats:italic><\/jats:sub> of 0.75 mg\/ml \u00b1 0.60 mg\/ml, <jats:italic>K<\/jats:italic><jats:sub><jats:italic>cat<\/jats:italic><\/jats:sub> of 3.74 min<jats:sup>-1<\/jats:sup> \u00b1 0.88 min<jats:sup>-1<\/jats:sup>, and <jats:italic>V<\/jats:italic><jats:sub><jats:italic>max<\/jats:italic><\/jats:sub> of 7.48 \u03bcM\/min \u00b1 1.76 \u03bcM\/min with partially degraded chondroitin sulfate A. Fluorophore-assisted carbohydrate electrophoresis was used to show the processive degradation of chondroitin sulfate A by the proteins encoded in <jats:italic>T<\/jats:italic>. <jats:italic>forsythia<\/jats:italic> PUL-like operon, and revealed Bfo2291 and Bfo2290 to be an endolytic chondroitin sulfate A lyase and exolytic \u0394Di-4S chondroitin sulfate A sulfatase, respectively.<\/jats:p>","DOI":"10.1371\/journal.pone.0272904","type":"journal-article","created":{"date-parts":[[2022,9,16]],"date-time":"2022-09-16T17:46:05Z","timestamp":1663350365000},"page":"e0272904","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":8,"title":["Degradation of chondroitin sulfate A by a PUL-like operon in Tannerella forsythia"],"prefix":"10.1371","volume":"17","author":[{"given":"Peter","family":"Nguyen","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Rony","family":"Eshaque","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Barbara Anne","family":"Garland","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5431-0424","authenticated-orcid":true,"given":"Anthony","family":"Dang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2594-9162","authenticated-orcid":true,"given":"Michael D. L.","family":"Suits","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2022,9,16]]},"reference":[{"key":"pone.0272904.ref001","article-title":"The oral microbiome\u2014An update for oral healthcare professionals","author":"M Kilian","year":"2016","journal-title":"Br Dent J."},{"key":"pone.0272904.ref002","article-title":"Microbial ecology of dental plaque and its significance in health and disease","author":"PD Marsh","year":"1994","journal-title":"Advances in dental research"},{"key":"pone.0272904.ref003","article-title":"A search within the genera streptococcus, enterococcus and lactobacillus for organisms inhibitory to mutans streptococci.","author":"SM James","year":"1988","journal-title":"Microb Ecol Health Dis."},{"key":"pone.0272904.ref004","article-title":"Role of Streptococcus mutans in human dental decay","author":"WJ Loesche","year":"1986","journal-title":"Microbiological Reviews"},{"key":"pone.0272904.ref005","article-title":"Acute Gingival Infections","author":"MG Newman","year":"2007","journal-title":"Essentials of Clinical Periodontology and Periodontics"},{"key":"pone.0272904.ref006","article-title":"Production of bactericidal concentrations of hydrogen peroxide by Streptococcus sanguis","author":"K Holmberg","year":"1973","journal-title":"Arch Oral Biol"},{"key":"pone.0272904.ref007","article-title":"Community as the unit of pathogenicity: An emerging concept as to the microbial pathogenesis of apical periodontitis.","author":"JF Siqueira","year":"2009","journal-title":"Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology and Endodontology"},{"key":"pone.0272904.ref008","article-title":"Microbial complexes in subgingival plaque","author":"SS Socransky","year":"1998","journal-title":"J Clin Periodontol."},{"key":"pone.0272904.ref009","article-title":"Porphyromonas gingivalis vesicles enhance attachment, and the leucine-rich repeat BspA protein is required for invasion of epithelial cells by \u201cTannerella forsythia","author":"S Inagaki","year":"2006","journal-title":"Infect Immun"},{"key":"pone.0272904.ref010","article-title":"Stimulation of growth of Porphyromonas gingivalis by cell extracts from Tannerella forsythia","author":"M Yoneda","year":"2005","journal-title":"J Periodontal Res"},{"key":"pone.0272904.ref011","article-title":"Pathogenic potential of Porphyromonas gingivalis, Treponema denticola andTannerella forsythia, the red bacterial complex associated with periodontitis","author":"C Bodet","year":"2007","journal-title":"Pathol Biol (Paris)"},{"key":"pone.0272904.ref012","article-title":"Porphyromonas gingivalis invasion of gingival epithelial cells","author":"RJ Lamont","year":"1995","journal-title":"Infect Immun"},{"key":"pone.0272904.ref013","article-title":"Porphyromonas gingivalis-epithelial cell interactions in periodontitis","author":"E Andrian","year":"2006","journal-title":"Journal of Dental Research"},{"key":"pone.0272904.ref014","article-title":"In or out: The invasiveness of oral bacteria","author":"RJ Lamont","year":"2002","journal-title":"Periodontol 2000"},{"key":"pone.0272904.ref015","doi-asserted-by":"crossref","DOI":"10.1128\/IAI.74.1.703-710.2006","article-title":"Intercellular spreading of Porphyromonas gingivalis infection in primary gingival epithelial cells","author":"\u00d6 Yilmaz","year":"2006","journal-title":"Infect Immun"},{"key":"pone.0272904.ref016","article-title":"Caspase activation is involved in chronic periodontitis","author":"H Bantel","year":"2005","journal-title":"FEBS Lett"},{"key":"pone.0272904.ref017","article-title":"The Role of Gingipains in the Pathogenesis of Periodontal Disease","author":"T. Imamura","year":"2003","journal-title":"J Periodontol."},{"key":"pone.0272904.ref018","article-title":"The Treponema denticola surface protease dentilisin degrades interleukin-1\u03b2 (IL-1\u03b2), IL-6, and tumor necrosis factor alpha","author":"M Miyamoto","year":"2006","journal-title":"Infect Immun"},{"key":"pone.0272904.ref019","article-title":"Inflammatory responses of a macrophage\/epithelial cell co-culture model to mono and mixed infections with Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia","author":"C Bodet","year":"2006","journal-title":"Microbes Infect"},{"key":"pone.0272904.ref020","article-title":"Proteolytic inactivation of the leukocyte C5a receptor by proteinases derived from Porphyromonas gingivalis","author":"MA Jagels","year":"1996","journal-title":"Infect Immun"},{"key":"pone.0272904.ref021","article-title":"Role of dentilisin in Treponema denticola epithelial cell layer penetration","author":"B Chi","year":"2003","journal-title":"Res Microbiol"},{"key":"pone.0272904.ref022","article-title":"Proteoglycans of the periodontium: Structure, role and function","author":"PM Bartold","year":"1987","journal-title":"J Periodontal Res."},{"key":"pone.0272904.ref023","article-title":"Glycosaminoglycans: Molecular properties, protein interactions, and role in physiological processes","author":"RL Jackson","year":"1991","journal-title":"Physiological Reviews"},{"key":"pone.0272904.ref024","article-title":"Characterization of proteoglycans from the calcified matrix of bovine bone","author":"A Franzen","year":"1984","journal-title":"Biochem J"},{"key":"pone.0272904.ref025","article-title":"Functional genomic and metabolic studies of the adaptations of a prominent adult human gut symbiont, Bacteroides thetaiotaomicron, to the suckling period","author":"MK Bjursell","year":"2006","journal-title":"J Biol Chem"},{"key":"pone.0272904.ref026","article-title":"Metabolism of multiple glycosaminoglycans by Bacteroides thetaiotaomicron is orchestrated by a versatile core genetic locus","author":"D Ndeh","year":"2020","journal-title":"Nat Commun"},{"key":"pone.0272904.ref027","article-title":"Carrageenan catabolism is encoded by a complex regulon in marine heterotrophic bacteria","author":"E Ficko-Blean","year":"2017","journal-title":"Nat Commun."},{"key":"pone.0272904.ref028","article-title":"Evolution of Symbiotic Bacteria in the Distal Human Intestine","author":"J Xu","year":"2007","journal-title":"PLoS Biol"},{"key":"pone.0272904.ref029","article-title":"Prostaglandin E 2 Is a Main Mediator in Receptor Activator of Nuclear Factor-\u03baB Ligand-Dependent Osteoclastogenesis Induced by Porphyromonas gingivalis, Treponema denticola, and Treponema socranskii","author":"K Choi B-","year":"2005","journal-title":"J Periodontol."},{"key":"pone.0272904.ref030","article-title":"Modulation of Host PGE 2 Secretion as a Determinant of Periodontal Disease Expression","author":"S Offenbacher","year":"1993","journal-title":"J Periodontol."},{"key":"pone.0272904.ref031","article-title":"Role of Matrix Metalloproteinases in Human Periodontal Diseases","author":"H. Birkedal-Hansen","year":"1993","journal-title":"J Periodontol"},{"key":"pone.0272904.ref032","article-title":"Mechanisms of connective tissue matrix destruction in periodontitis","author":"JJ Reynolds","year":"1997","journal-title":"Periodontol 2000"},{"key":"pone.0272904.ref033","article-title":"Cloning of the Tannerella forsythensis (Bacteroides forsythus) siaHI gene and purification of the sialidase enzyme","author":"H Ishikura","year":"2003","journal-title":"J Med Microbiol"},{"key":"pone.0272904.ref034","article-title":"An orthologue of Bacteroides fragilis NanH is the principal sialidase in Tannerella forsythia","author":"H Thompson","year":"2009","journal-title":"J Bacteriol"},{"key":"pone.0272904.ref035","article-title":"Sialidases from gut bacteria: A mini-review","author":"N Juge","year":"2016","journal-title":"Biochem Soc Trans"},{"key":"pone.0272904.ref036","article-title":"Cloning and expression of \u03b1-D-glucosidase and N-acetyl-\u03b2 -glucosaminidase from the periodontal pathogen, Tannerella forsythensis (Bacteroides forsythus)","author":"C V. Hughes","year":"2003","journal-title":"Oral Microbiol Immunol"},{"key":"pone.0272904.ref037","article-title":"NCBI","author":"J. Arnemann","year":"2018","journal-title":"In: Lexikon der Medizinischen Laboratoriumsdiagnostik"},{"key":"pone.0272904.ref038","article-title":"NCBI BLAST: a better web interface","author":"M Johnson","year":"2008","journal-title":"Nucleic Acids Res"},{"key":"pone.0272904.ref039","article-title":"Automatic annotation of bacterial community sequences and application to infections diagnostic","author":"V Solovyev","year":"2011","journal-title":"BIOINFORMATICS 2011\u2014Proceedings of the International Conference on Bioinformatics Models, Methods and Algorithms."},{"key":"pone.0272904.ref040","article-title":"DOOR 2.0: Presenting operons and their functions through dynamic and integrated views","author":"X Mao","year":"2014","journal-title":"Nucleic Acids Res"},{"key":"pone.0272904.ref041","article-title":"PSORTb 3.0: Improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes","author":"NY Yu","year":"2010","journal-title":"Bioinformatics"},{"key":"pone.0272904.ref042","article-title":"SignalP 5.0 improves signal peptide predictions using deep neural networks","author":"JJ Almagro Armenteros","year":"2019","journal-title":"Nat Biotechnol"},{"key":"pone.0272904.ref043","article-title":"The InterPro protein families database: The classification resource after 15 years","author":"A Mitchell","year":"2015","journal-title":"Nucleic Acids Res"},{"key":"pone.0272904.ref044","article-title":"The Phyre2 web portal for protein modeling, prediction and analysis","author":"LA Kelley","year":"2015","journal-title":"Nat Protoc"},{"key":"pone.0272904.ref045","article-title":"SWISS-MODEL: Homology modelling of protein structures and complexes","author":"A Waterhouse","year":"2018","journal-title":"Nucleic Acids Res"},{"key":"pone.0272904.ref046","article-title":"STRING v11: Protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets","author":"D Szklarczyk","year":"2019","journal-title":"Nucleic Acids Res"},{"key":"pone.0272904.ref047","article-title":"The I-TASSER suite: Protein structure and function prediction","author":"J Yang","year":"2014","journal-title":"Nature Methods"},{"key":"pone.0272904.ref048","article-title":"Protein identification and analysis tools in the ExPASy server","author":"MR Wilkins","year":"1999","journal-title":"Methods in molecular biology (Clifton, N.J.)"},{"key":"pone.0272904.ref049","article-title":"UniProt: The universal protein knowledgebase","author":"R Apweiler","year":"2004","journal-title":"Nucleic Acids Res"},{"key":"pone.0272904.ref050","article-title":"Transformation of Plasmid DNA into E. Coli using the heat shock method","author":"A Froger","year":"2007","journal-title":"J Vis Exp"},{"key":"pone.0272904.ref051","article-title":"SDS-PAGE","author":"K. Nybo","year":"2014","journal-title":"Biotechniques"},{"key":"pone.0272904.ref052","article-title":"Fluorophore-assisted carbohydrate electrophoresis (FACE) of glycosaminoglycans","author":"A Calabro","year":"2001","journal-title":"Osteoarthr Cartil."},{"key":"pone.0272904.ref053","article-title":"The Molecular Basis of Polysaccharide Sulfatase Activity and a Nomenclature for Catalytic Subsites in this Class of Enzyme","author":"AG Hettle","year":"2018","journal-title":"Structure"},{"key":"pone.0272904.ref054","article-title":"Structural and Mechanistic Analysis of the Choline Sulfatase from Sinorhizobium melliloti: A Class I Sulfatase Specific for an Alkyl Sulfate Ester","author":"B van Loo","year":"2018","journal-title":"J Mol Biol"},{"key":"pone.0272904.ref055","volume-title":"Initial Functional characterization of Bfo2291 and Bfo2294 from Tannerella forsythia; degraders of chondroitin sulfate A","author":"R. Eshaque","year":"2018"},{"key":"pone.0272904.ref056","article-title":"Comparative Study of Two Chondroitin Sulfate\/Dermatan Sulfate 4-O-Sulfatases With High Identity","author":"S Wang","year":"2019","journal-title":"Front Microbiol"},{"key":"pone.0272904.ref057","article-title":"Comprehensive Natural Products II: Chemistry and Biology","author":"L Mander","year":"2010","journal-title":"Comprehensive Natural Products II: Chemistry and Biology"},{"key":"pone.0272904.ref058","article-title":"1.3 \u00c5 structure of arylsulfatase from Pseudomonas aeruginosa establishes the catalytic mechanism of sulfate ester cleavage in the sulfatase family","author":"I Boltes","year":"2001","journal-title":"Structure"}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0272904","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,9,16]],"date-time":"2022-09-16T17:46:59Z","timestamp":1663350419000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0272904"}},"subtitle":[],"editor":[{"given":"Nikos K.","family":"Karamanos","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2022,9,16]]},"references-count":58,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2022,9,16]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0272904","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,9,16]]}}}