Identification of Rothia Bacteria as Gluten-Degrading Natural Colonizers of the Upper Gastro-Intestinal Tract
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{"title"=>"Identification of rothia bacteria as gluten-degrading natural colonizers of the upper gastro-intestinal tract", "type"=>"journal", "authors"=>[{"first_name"=>"Maram", "last_name"=>"Zamakhchari", "scopus_author_id"=>"36877188600"}, {"first_name"=>"Guoxian", "last_name"=>"Wei", "scopus_author_id"=>"55747200700"}, {"first_name"=>"Floyd", "last_name"=>"Dewhirst", "scopus_author_id"=>"7005348138"}, {"first_name"=>"Jaeseop", "last_name"=>"Lee", "scopus_author_id"=>"53463749100"}, {"first_name"=>"Detlef", "last_name"=>"Schuppan", "scopus_author_id"=>"35448732000"}, {"first_name"=>"Frank G.", "last_name"=>"Oppenheim", "scopus_author_id"=>"7006254960"}, {"first_name"=>"Eva J.", "last_name"=>"Helmerhorst", "scopus_author_id"=>"7003843706"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "scopus"=>"2-s2.0-80053038305", "pui"=>"362600974", "doi"=>"10.1371/journal.pone.0024455", "isbn"=>"1932-6203", "sgr"=>"80053038305", "pmid"=>"21957450"}, "id"=>"a57f6379-f9cb-3fdd-bb6f-305a1d4806e6", "abstract"=>"BACKGROUND: Gluten proteins, prominent constituents of barley, wheat and rye, cause celiac disease in genetically predisposed subjects. Gluten is notoriously difficult to digest by mammalian proteolytic enzymes and the protease-resistant domains contain multiple immunogenic epitopes. The aim of this study was to identify novel sources of gluten-digesting microbial enzymes from the upper gastro-intestinal tract with the potential to neutralize gluten epitopes.\\n\\nMETHODOLOGY/PRINCIPAL FINDINGS: Oral microorganisms with gluten-degrading capacity were obtained by a selective plating strategy using gluten agar. Microbial speciations were carried out by 16S rDNA gene sequencing. Enzyme activities were assessed using gliadin-derived enzymatic substrates, gliadins in solution, gliadin zymography, and 33-mer α-gliadin and 26-mer γ-gliadin immunogenic peptides. Fragments of the gliadin peptides were separated by RP-HPLC and structurally characterized by mass spectrometry. Strains with high activity towards gluten were typed as Rothia mucilaginosa and Rothia aeria. Gliadins (250 µg/ml) added to Rothia cell suspensions (OD(620) 1.2) were degraded by 50% after ∼30 min of incubation. Importantly, the 33-mer and 26-mer immunogenic peptides were also cleaved, primarily C-terminal to Xaa-Pro-Gln (XPQ) and Xaa-Pro-Tyr (XPY). The major gliadin-degrading enzymes produced by the Rothia strains were ∼70-75 kDa in size, and the enzyme expressed by Rothia aeria was active over a wide pH range (pH 3-10).\\n\\nCONCLUSION/SIGNIFICANCE: While the human digestive enzyme system lacks the capacity to cleave immunogenic gluten, such activities are naturally present in the oral microbial enzyme repertoire. The identified bacteria may be exploited for physiologic degradation of harmful gluten peptides.", "link"=>"http://www.mendeley.com/research/identification-rothia-bacteria-glutendegrading-natural-colonizers-upper-gastrointestinal-tract", "reader_count"=>63, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>3, "Researcher"=>9, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>12, "Student > Postgraduate"=>2, "Student > Master"=>12, "Other"=>4, "Student > Bachelor"=>12, "Professor"=>5}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>3, "Researcher"=>9, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>12, "Student > Postgraduate"=>2, "Student > Master"=>12, "Other"=>4, "Student > Bachelor"=>12, "Professor"=>5}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>9, "Nursing and Health Professions"=>1, "Agricultural and Biological Sciences"=>29, "Medicine and Dentistry"=>10, "Sports and Recreations"=>1, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Chemistry"=>3, "Psychology"=>1, "Social Sciences"=>2, "Immunology and Microbiology"=>4}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>10}, "Chemistry"=>{"Chemistry"=>3}, "Social Sciences"=>{"Social Sciences"=>2}, "Sports and Recreations"=>{"Sports and Recreations"=>1}, "Psychology"=>{"Psychology"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>4}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>29}, "Nursing and Health Professions"=>{"Nursing and Health Professions"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>9}, "Unspecified"=>{"Unspecified"=>2}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"Norway"=>1, "Denmark"=>1, "United Arab Emirates"=>1}, "group_count"=>5}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/733003"], "description"=>"<p>WSA-2B (<i>R. mucilaginosa</i>) or WSA-8 (<i>R. aeria</i>) cells were suspended in saliva ion buffer to a final cell concentration of OD<sub>620</sub> 0.15, 0.3, 0.6, and 1.2. Z-KPQ-pNA or Z-YPQ-pNA were added as enzymatic substrates to a final concentrations of 200 µM. Note that the rate of substrate hydrolysis increased with increasing cell density. As expected, boiled cell suspensions (OD<sub>620</sub> 1.2) were devoid of enzyme activities.</p>", "links"=>[], "tags"=>["proteolytic"], "article_id"=>403358, "categories"=>["Biochemistry", "Chemistry", "Microbiology"], "users"=>["Maram Zamakhchari", "Guoxian Wei", "Floyd Dewhirst", "Jaeseop Lee", "Detlef Schuppan", "Frank G. Oppenheim", "Eva J. Helmerhorst"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0024455.g002", "stats"=>{"downloads"=>3, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Relationship_between_cell_density_and_proteolytic_activity_/403358", "title"=>"Relationship between cell density and proteolytic activity.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-21 00:55:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/370555", "https://ndownloader.figshare.com/files/370622"], "description"=>"<div><h3>Background</h3><p>Gluten proteins, prominent constituents of barley, wheat and rye, cause celiac disease in genetically predisposed subjects. Gluten is notoriously difficult to digest by mammalian proteolytic enzymes and the protease-resistant domains contain multiple immunogenic epitopes. The aim of this study was to identify novel sources of gluten-digesting microbial enzymes from the upper gastro-intestinal tract with the potential to neutralize gluten epitopes.</p> <h3>Methodology/Principal Findings</h3><p>Oral microorganisms with gluten-degrading capacity were obtained by a selective plating strategy using gluten agar. Microbial speciations were carried out by 16S rDNA gene sequencing. Enzyme activities were assessed using gliadin-derived enzymatic substrates, gliadins in solution, gliadin zymography, and 33-mer α-gliadin and 26-mer γ-gliadin immunogenic peptides. Fragments of the gliadin peptides were separated by RP-HPLC and structurally characterized by mass spectrometry. Strains with high activity towards gluten were typed as <em>Rothia mucilaginosa</em> and <em>Rothia aeria</em>. Gliadins (250 µg/ml) added to <em>Rothia</em> cell suspensions (OD<sub>620</sub> 1.2) were degraded by 50% after ∼30 min of incubation. Importantly, the 33-mer and 26-mer immunogenic peptides were also cleaved, primarily C-terminal to Xaa-Pro-Gln (XPQ) and Xaa-Pro-Tyr (XPY). The major gliadin-degrading enzymes produced by the <em>Rothia</em> strains were ∼70–75 kDa in size, and the enzyme expressed by <em>Rothia aeria</em> was active over a wide pH range (pH 3–10).</p> <h3>Conclusion/Significance</h3><p>While the human digestive enzyme system lacks the capacity to cleave immunogenic gluten, such activities are naturally present in the oral microbial enzyme repertoire. The identified bacteria may be exploited for physiologic degradation of harmful gluten peptides.</p> </div>", "links"=>[], "tags"=>["gluten-degrading", "colonizers", "gastro-intestinal", "tract"], "article_id"=>133211, "categories"=>["Biochemistry", "Chemistry", "Microbiology"], "users"=>["Maram Zamakhchari", "Guoxian Wei", "Floyd Dewhirst", "Jaeseop Lee", "Detlef Schuppan", "Frank G. Oppenheim", "Eva J. Helmerhorst"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0024455.s001", "https://dx.doi.org/10.1371/journal.pone.0024455.s002"], "stats"=>{"downloads"=>0, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Identification_of_Rothia_Bacteria_as_Gluten_Degrading_Natural_Colonizers_of_the_Upper_Gastro_Intestinal_Tract/133211", "title"=>"Identification of <em>Rothia</em> Bacteria as Gluten-Degrading Natural Colonizers of the Upper Gastro-Intestinal Tract", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-09-21 00:53:31"}
  • {"files"=>["https://ndownloader.figshare.com/files/732890"], "description"=>"<p>Twenty different microbial strains collected from dental plaque were cultured on agar media containing gluten as the sole protein source (GA, left) and on the same agar formulation not containing gluten (control, right). After 24 h incubation, among these twenty analyzed strains, one strain (WSA-8) was found to be capable of growing on the gluten agar (indicated by an arrow). Note the presence of small, undissolved gluten particles appearing as white flakes in the gluten agar.</p>", "links"=>[], "tags"=>["bacterial", "gluten-limited"], "article_id"=>403240, "categories"=>["Biochemistry", "Chemistry", "Microbiology"], "users"=>["Maram Zamakhchari", "Guoxian Wei", "Floyd Dewhirst", "Jaeseop Lee", "Detlef Schuppan", "Frank G. Oppenheim", "Eva J. Helmerhorst"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0024455.g001", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Assessment_of_bacterial_growth_on_gluten_limited_agar_/403240", "title"=>"Assessment of bacterial growth on gluten-limited agar.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-21 00:54:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/733565"], "description"=>"<p>In the zymogram gels 150 µl cells (OD<sub>620</sub> 5.0) were applied per lane. Lane 1, strain WSA-2B (<i>R. mucilaginosa</i>); lanes 2: strain WSA-8 (<i>R. aeria</i>), lane 3: strain WSA-26 (<i>R. mucilaginosa</i>); lane 4: strain ATCC 25296 (<i>R. mucilaginosa</i>). A, gel developed at pH 7.0; B, gel developed at pH 3.0. C, Z-YPQ-pNA (200 µM) hydrolysis by WSA-8 cells (OD<sub>620</sub> 1.2) measured in 20 mM Tris solutions ranging in pH from 2.0 to 10.0. Measurements at 405 nm were carried out hourly for the first 6 hours and after 24 h and 72 h.</p>", "links"=>[], "tags"=>["zymography", "strains", "ph"], "article_id"=>403921, "categories"=>["Biochemistry", "Chemistry", "Microbiology"], "users"=>["Maram Zamakhchari", "Guoxian Wei", "Floyd Dewhirst", "Jaeseop Lee", "Detlef Schuppan", "Frank G. Oppenheim", "Eva J. Helmerhorst"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0024455.g006", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Gliadin_zymography_6_of_Rothia_strains_and_pH_activity_analysis_/403921", "title"=>"Gliadin zymography (6%) of <i>Rothia</i> strains and pH activity analysis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-21 01:05:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/733385"], "description"=>"<p>Gliadin 33-mer (250 µg/ml) was incubated in a suspension of WSA-8 (<i>R. aeria</i>) cells (OD<sub>620</sub> 1.2). Incubation aliquots removed after 0 h, 2 h and 5 h were analyzed by RP-HPLC (A). Degradation peaks labeled 1 to 11 were collected and sequenced by LC-ESI-MS/MS (B). Large arrows: cleavage after QPQ; small solid arrows: cleavage after LPY; small dotted arrows: other cleavages.</p>", "links"=>[], "tags"=>["33-mer", "incubated"], "article_id"=>403739, "categories"=>["Biochemistry", "Chemistry", "Microbiology"], "users"=>["Maram Zamakhchari", "Guoxian Wei", "Floyd Dewhirst", "Jaeseop Lee", "Detlef Schuppan", "Frank G. Oppenheim", "Eva J. Helmerhorst"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0024455.g005", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Degradation_and_fragment_analysis_of_the_33_mer_incubated_with_R_aeria_/403739", "title"=>"Degradation and fragment analysis of the 33-mer incubated with <i>R. aeria</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-21 01:02:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/733156"], "description"=>"<p>Gliadin (250 µg/ml) was incubated in a suspension of WSA-8 (<i>R. aeria</i>). The final OD<sub>620</sub> was 1.0. Incubation sample aliquots were analyzed by Bis-Tris PAGE. A, lane 1: molecular weight standard; lanes 2–7, WSA-8/gliadin mixtures incubated for 0, 2, 4, 6, 24 and 48 h, respectively. B, lane 1: molecular weight standard, lanes 2–7: WSA-8/gliadin mixture incubated for 0, 5, 15, 30, 60 and 120 min, respectively. Lanes 8 and 9: gliadins incubated for 0 and 120 min in boiled bacterial cell suspensions; lanes 10 and 11: cell suspensions without added gliadins; Lanes 12 and 13: gliadins incubated for 0 and 120 min in saliva ion buffer only. Arrow points to the major protein constituent in the gliadin mixture.</p>", "links"=>[], "tags"=>["gliadins"], "article_id"=>403511, "categories"=>["Biochemistry", "Chemistry", "Microbiology"], "users"=>["Maram Zamakhchari", "Guoxian Wei", "Floyd Dewhirst", "Jaeseop Lee", "Detlef Schuppan", "Frank G. Oppenheim", "Eva J. Helmerhorst"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0024455.g003", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Degradation_of_gliadins_by_R_aeria_/403511", "title"=>"Degradation of gliadins by <i>R. aeria</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-21 00:58:31"}
  • {"files"=>["https://ndownloader.figshare.com/files/733674"], "description"=>"a<p>Speciation was carried out by partial 16S rDNA gene sequencing. All sequences were greater than 99% similar reference sequences at the Human Oral Microbiome Database (<a href=\"http://www.homd.org\" target=\"_blank\">www.homd.org</a>).</p>b<p>Substrates (final concentration 200 µM) were mixed with bacterial suspensions in saliva ion buffer (OD<sub>620</sub> 1.2). Hydrolysis was measured spectrophotometrically at 405 nm after 24 h incubation.</p>", "links"=>[], "tags"=>["characteristics", "microorganisms", "cultured", "gluten"], "article_id"=>404022, "categories"=>["Biochemistry", "Chemistry", "Microbiology"], "users"=>["Maram Zamakhchari", "Guoxian Wei", "Floyd Dewhirst", "Jaeseop Lee", "Detlef Schuppan", "Frank G. Oppenheim", "Eva J. Helmerhorst"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0024455.t001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Enzymatic_characteristics_of_selected_oral_microorganisms_cultured_on_gluten_agar_/404022", "title"=>"Enzymatic characteristics of selected oral microorganisms cultured on gluten agar.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-09-21 01:07:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/733266"], "description"=>"<p>The 33-mer peptide was incubated with pepsin (A), trypsin (B), chymotrypsin (C) (each 1 µg/ml) sampled at t = 0 and t = 24 h or in a suspension of WSA-8 (<i>R. aeria</i>) cells (D; OD<sub>620</sub> 1.2) sampled at t = 0, 30 min, 60 min and 120 min. Degradation of the 33-mer in incubation aliquots was monitored by RP-HPLC.</p>", "links"=>[], "tags"=>["33-mer", "mammalian", "enzymes"], "article_id"=>403615, "categories"=>["Biochemistry", "Chemistry", "Microbiology"], "users"=>["Maram Zamakhchari", "Guoxian Wei", "Floyd Dewhirst", "Jaeseop Lee", "Detlef Schuppan", "Frank G. Oppenheim", "Eva J. Helmerhorst"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0024455.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Degradation_of_the_33_mer_by_mammalian_enzymes_and_by_enzymes_associated_with_R_aeria_/403615", "title"=>"Degradation of the 33-mer by mammalian enzymes and by enzymes associated with <i>R. aeria</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-21 01:00:15"}

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