Streptococcus mutans extracellular DNA is upregulated during growth in biofilms, actively released via membrane vesicles, and influenced by components of the protein secretion machinery
Autor(a) principal: | |
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Data de Publicação: | 2014 |
Outros Autores: | , , , , , , , , |
Tipo de documento: | Artigo |
Idioma: | eng |
Título da fonte: | Repositório Institucional da UNESP |
Texto Completo: | http://dx.doi.org/10.1128/JB.01493-14 http://hdl.handle.net/11449/171587 |
Resumo: | Streptococcus mutans, a major etiological agent of human dental caries, lives primarily on the tooth surface in biofilms. Limited information is available concerning the extracellular DNA (eDNA) as a scaffolding matrix in S. mutans biofilms. This study demonstrates that S. mutans produces eDNA by multiple avenues, including lysis-independent membrane vesicles. Unlike eDNAs from cell lysis that were abundant and mainly concentrated around broken cells or cell debris with floating open ends, eDNAs produced via the lysis-independent pathway appeared scattered but in a structured network under scanning electron microscopy. Compared to eDNA production of planktonic cultures, eDNA production in 5- and 24-h biofilms was increased by >3- and >1.6-fold, respectively. The addition of DNase I to growth medium significantly reduced biofilm formation. In an in vitro adherence assay, added chromosomal DNA alone had a limited effect on S. mutans adherence to saliva-coated hydroxylapatite beads, but in conjunction with glucans synthesized using purified glucosyltransferase B, the adherence was significantly enhanced. Deletion of sortase A, the transpeptidase that covalently couples multiple surface-associated proteins to the cell wall peptidoglycan, significantly reduced eDNA in both planktonic and biofilm cultures. Sortase A deficiency did not have a significant effect on membrane vesicle production; however, the protein profile of the mutant membrane vesicles was significantly altered, including reduction of adhesin P1 and glucan-binding proteins B and C. Relative to the wild type, deficiency of protein secretion and membrane protein insertion machinery components, including Ffh, YidC1, and YidC2, also caused significant reductions in eDNA. © 2014, American Society for Microbiology. |
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Streptococcus mutans extracellular DNA is upregulated during growth in biofilms, actively released via membrane vesicles, and influenced by components of the protein secretion machineryStreptococcus mutans, a major etiological agent of human dental caries, lives primarily on the tooth surface in biofilms. Limited information is available concerning the extracellular DNA (eDNA) as a scaffolding matrix in S. mutans biofilms. This study demonstrates that S. mutans produces eDNA by multiple avenues, including lysis-independent membrane vesicles. Unlike eDNAs from cell lysis that were abundant and mainly concentrated around broken cells or cell debris with floating open ends, eDNAs produced via the lysis-independent pathway appeared scattered but in a structured network under scanning electron microscopy. Compared to eDNA production of planktonic cultures, eDNA production in 5- and 24-h biofilms was increased by >3- and >1.6-fold, respectively. The addition of DNase I to growth medium significantly reduced biofilm formation. In an in vitro adherence assay, added chromosomal DNA alone had a limited effect on S. mutans adherence to saliva-coated hydroxylapatite beads, but in conjunction with glucans synthesized using purified glucosyltransferase B, the adherence was significantly enhanced. Deletion of sortase A, the transpeptidase that covalently couples multiple surface-associated proteins to the cell wall peptidoglycan, significantly reduced eDNA in both planktonic and biofilm cultures. Sortase A deficiency did not have a significant effect on membrane vesicle production; however, the protein profile of the mutant membrane vesicles was significantly altered, including reduction of adhesin P1 and glucan-binding proteins B and C. Relative to the wild type, deficiency of protein secretion and membrane protein insertion machinery components, including Ffh, YidC1, and YidC2, also caused significant reductions in eDNA. © 2014, American Society for Microbiology.National Institutes of HealthCenter of Excellence in Oral and Craniofacial Biology, School of Dentistry, Louisiana State University Health Sciences Center, New Orleans, LACenter for Oral Biology, University of Rochester School of Medicine and Dentistry, Rochester, NYDepartment of Oral Biology, University of Florida School of Dentistry, Gainesville, FLDepartment of Comprehensive Dentistry and Biomaterials, School of Dentistry, Louisiana State University Health Sciences Center, New Orleans, LADepartment of Orthodontics, University of Pennsylvania School of Dental Medicine, Philadelphia, PADepartment of Microbiology, Immunology and Parasitology, School of Medicine, Louisiana State University Health Sciences Center, New Orleans, LADepartment of Dental Materials and Prosthodontics, Araraquara Dental School, Universidade Estadual Paulista, UNESP, Sao PauloDepartment of Microbiology and Immunology, Tulane University School of Medicine, New Orleans, LADepartment of Dental Materials and Prosthodontics, Araraquara Dental School, Universidade Estadual Paulista, UNESP, Sao PauloNational Institutes of Health: DE08007National Institutes of Health: DE19452National Institutes of Health: DE21789National Institutes of Health: DE22529National Institutes of Health: EFRI-1137186Center of Excellence in Oral and Craniofacial Biology, School of Dentistry, Louisiana State University Health Sciences CenterCenter for Oral Biology, University of Rochester School of Medicine and DentistryUniversidade Estadual Paulista (Unesp)Liao, SumeiKlein, Marlise I. [UNESP]Heim, Kyle P.Fan, YuweiBitoun, Jacob P.Ahn, San-JoonBurne, Robert A.Koo, HyunBrady, L. JeannineWen, Zezhang T.2018-12-11T16:56:07Z2018-12-11T16:56:07Z2014-01-01info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/article2355-2366application/pdfhttp://dx.doi.org/10.1128/JB.01493-14Journal of Bacteriology, v. 196, n. 13, p. 2355-2366, 2014.1098-55300021-9193http://hdl.handle.net/11449/17158710.1128/JB.01493-142-s2.0-849020076662-s2.0-84902007666.pdfScopusreponame:Repositório Institucional da UNESPinstname:Universidade Estadual Paulista (UNESP)instacron:UNESPengJournal of Bacteriology1,8851,885info:eu-repo/semantics/openAccess2024-01-23T07:05:21Zoai:repositorio.unesp.br:11449/171587Repositório InstitucionalPUBhttp://repositorio.unesp.br/oai/requestopendoar:29462024-01-23T07:05:21Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)false |
dc.title.none.fl_str_mv |
Streptococcus mutans extracellular DNA is upregulated during growth in biofilms, actively released via membrane vesicles, and influenced by components of the protein secretion machinery |
title |
Streptococcus mutans extracellular DNA is upregulated during growth in biofilms, actively released via membrane vesicles, and influenced by components of the protein secretion machinery |
spellingShingle |
Streptococcus mutans extracellular DNA is upregulated during growth in biofilms, actively released via membrane vesicles, and influenced by components of the protein secretion machinery Liao, Sumei |
title_short |
Streptococcus mutans extracellular DNA is upregulated during growth in biofilms, actively released via membrane vesicles, and influenced by components of the protein secretion machinery |
title_full |
Streptococcus mutans extracellular DNA is upregulated during growth in biofilms, actively released via membrane vesicles, and influenced by components of the protein secretion machinery |
title_fullStr |
Streptococcus mutans extracellular DNA is upregulated during growth in biofilms, actively released via membrane vesicles, and influenced by components of the protein secretion machinery |
title_full_unstemmed |
Streptococcus mutans extracellular DNA is upregulated during growth in biofilms, actively released via membrane vesicles, and influenced by components of the protein secretion machinery |
title_sort |
Streptococcus mutans extracellular DNA is upregulated during growth in biofilms, actively released via membrane vesicles, and influenced by components of the protein secretion machinery |
author |
Liao, Sumei |
author_facet |
Liao, Sumei Klein, Marlise I. [UNESP] Heim, Kyle P. Fan, Yuwei Bitoun, Jacob P. Ahn, San-Joon Burne, Robert A. Koo, Hyun Brady, L. Jeannine Wen, Zezhang T. |
author_role |
author |
author2 |
Klein, Marlise I. [UNESP] Heim, Kyle P. Fan, Yuwei Bitoun, Jacob P. Ahn, San-Joon Burne, Robert A. Koo, Hyun Brady, L. Jeannine Wen, Zezhang T. |
author2_role |
author author author author author author author author author |
dc.contributor.none.fl_str_mv |
Center of Excellence in Oral and Craniofacial Biology, School of Dentistry, Louisiana State University Health Sciences Center Center for Oral Biology, University of Rochester School of Medicine and Dentistry Universidade Estadual Paulista (Unesp) |
dc.contributor.author.fl_str_mv |
Liao, Sumei Klein, Marlise I. [UNESP] Heim, Kyle P. Fan, Yuwei Bitoun, Jacob P. Ahn, San-Joon Burne, Robert A. Koo, Hyun Brady, L. Jeannine Wen, Zezhang T. |
description |
Streptococcus mutans, a major etiological agent of human dental caries, lives primarily on the tooth surface in biofilms. Limited information is available concerning the extracellular DNA (eDNA) as a scaffolding matrix in S. mutans biofilms. This study demonstrates that S. mutans produces eDNA by multiple avenues, including lysis-independent membrane vesicles. Unlike eDNAs from cell lysis that were abundant and mainly concentrated around broken cells or cell debris with floating open ends, eDNAs produced via the lysis-independent pathway appeared scattered but in a structured network under scanning electron microscopy. Compared to eDNA production of planktonic cultures, eDNA production in 5- and 24-h biofilms was increased by >3- and >1.6-fold, respectively. The addition of DNase I to growth medium significantly reduced biofilm formation. In an in vitro adherence assay, added chromosomal DNA alone had a limited effect on S. mutans adherence to saliva-coated hydroxylapatite beads, but in conjunction with glucans synthesized using purified glucosyltransferase B, the adherence was significantly enhanced. Deletion of sortase A, the transpeptidase that covalently couples multiple surface-associated proteins to the cell wall peptidoglycan, significantly reduced eDNA in both planktonic and biofilm cultures. Sortase A deficiency did not have a significant effect on membrane vesicle production; however, the protein profile of the mutant membrane vesicles was significantly altered, including reduction of adhesin P1 and glucan-binding proteins B and C. Relative to the wild type, deficiency of protein secretion and membrane protein insertion machinery components, including Ffh, YidC1, and YidC2, also caused significant reductions in eDNA. © 2014, American Society for Microbiology. |
publishDate |
2014 |
dc.date.none.fl_str_mv |
2014-01-01 2018-12-11T16:56:07Z 2018-12-11T16:56:07Z |
dc.type.status.fl_str_mv |
info:eu-repo/semantics/publishedVersion |
dc.type.driver.fl_str_mv |
info:eu-repo/semantics/article |
format |
article |
status_str |
publishedVersion |
dc.identifier.uri.fl_str_mv |
http://dx.doi.org/10.1128/JB.01493-14 Journal of Bacteriology, v. 196, n. 13, p. 2355-2366, 2014. 1098-5530 0021-9193 http://hdl.handle.net/11449/171587 10.1128/JB.01493-14 2-s2.0-84902007666 2-s2.0-84902007666.pdf |
url |
http://dx.doi.org/10.1128/JB.01493-14 http://hdl.handle.net/11449/171587 |
identifier_str_mv |
Journal of Bacteriology, v. 196, n. 13, p. 2355-2366, 2014. 1098-5530 0021-9193 10.1128/JB.01493-14 2-s2.0-84902007666 2-s2.0-84902007666.pdf |
dc.language.iso.fl_str_mv |
eng |
language |
eng |
dc.relation.none.fl_str_mv |
Journal of Bacteriology 1,885 1,885 |
dc.rights.driver.fl_str_mv |
info:eu-repo/semantics/openAccess |
eu_rights_str_mv |
openAccess |
dc.format.none.fl_str_mv |
2355-2366 application/pdf |
dc.source.none.fl_str_mv |
Scopus reponame:Repositório Institucional da UNESP instname:Universidade Estadual Paulista (UNESP) instacron:UNESP |
instname_str |
Universidade Estadual Paulista (UNESP) |
instacron_str |
UNESP |
institution |
UNESP |
reponame_str |
Repositório Institucional da UNESP |
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Repositório Institucional da UNESP |
repository.name.fl_str_mv |
Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP) |
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1799965701348261888 |