Literature DB >> 28778894

Veillonella Catalase Protects the Growth of Fusobacterium nucleatum in Microaerophilic and Streptococcus gordonii-Resident Environments.

Peng Zhou1, Xiaoli Li2, I-Hsiu Huang3, Fengxia Qi2,4.   

Abstract

The oral biofilm is a multispecies community in which antagonism and mutualism coexist among friends and foes to keep an ecological balance of community members. The pioneer colonizers, such as Streptococcus gordonii, produce H2O2 to inhibit the growth of competitors, like the mutans streptococci, as well as strict anaerobic middle and later colonizers of the dental biofilm. Interestingly, Veillonella species, as early colonizers, physically interact (coaggregate) with S. gordonii A putative catalase gene (catA) is found in most sequenced Veillonella species; however, the function of this gene is unknown. In this study, we characterized the ecological function of catA from Veillonella parvula PK1910 by integrating it into the only transformable strain, Veillonella atypica OK5, which is catA negative. The strain (OK5-catA) became more resistant to H2O2 Further studies demonstrated that the catA gene expression is induced by the addition of H2O2 or coculture with S. gordonii Mixed-culture experiments further revealed that the transgenic OK5-catA strain not only enhanced the growth of Fusobacterium nucleatum, a strict anaerobic periodontopathogen, under microaerophilic conditions, but it also rescued F. nucleatum from killing by S. gordonii A potential role of catalase in veillonellae in biofilm ecology and pathogenesis is discussed here.IMPORTANCEVeillonella species, as early colonizers, can coaggregate with many bacteria, including the initial colonizer Streptococcus gordonii and periodontal pathogen Fusobacterium nucleatum, during various stages of oral biofilm formation. In addition to providing binding sites for many microbes, our previous study also showed that Veillonella produces nutrients for the survival and growth of periodontal pathogens. These findings indicate that Veillonella plays an important "bridging" role in the development of oral biofilms and the ecology of the human oral cavity. In this study, we demonstrated that the reducing activity of Veillonella can rescue the growth of Fusobacterium nucleatum not only under microaerophilic conditions, but also in an environment in which Streptococcus gordonii is present. Thus, this study will provide a new insight for future studies on the mechanisms of human oral biofilm formation and the control of periodontal diseases.
Copyright © 2017 American Society for Microbiology.

Entities:  

Keywords:  Fusobacterium nucleatum; Streptococcus gordonii; anaerobes; oxidative stress; transformable strain; veillonellae

Mesh:

Substances:

Year:  2017        PMID: 28778894      PMCID: PMC5601340          DOI: 10.1128/AEM.01079-17

Source DB:  PubMed          Journal:  Appl Environ Microbiol        ISSN: 0099-2240            Impact factor:   4.792


  49 in total

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Authors:  Paul E Kolenbrander; Robert J Palmer; Alexander H Rickard; Nicholas S Jakubovics; Natalia I Chalmers; Patricia I Diaz
Journal:  Periodontol 2000       Date:  2006       Impact factor: 7.589

Review 2.  Bacterial interactions in dental biofilm.

Authors:  Ruijie Huang; Mingyun Li; Richard L Gregory
Journal:  Virulence       Date:  2011-09-01       Impact factor: 5.882

3.  A role for rubredoxin in oxidative stress protection in Desulfovibrio vulgaris: catalytic electron transfer to rubrerythrin and two-iron superoxide reductase.

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Journal:  Arch Biochem Biophys       Date:  2001-10-01       Impact factor: 4.013

4.  Molecular characterization of subject-specific oral microflora during initial colonization of enamel.

Authors:  Patricia I Diaz; Natalia I Chalmers; Alexander H Rickard; Colin Kong; Craig L Milburn; Robert J Palmer; Paul E Kolenbrander
Journal:  Appl Environ Microbiol       Date:  2006-04       Impact factor: 4.792

5.  Anaerobic microbes: oxygen detoxification without superoxide dismutase.

Authors:  F E Jenney; M F Verhagen; X Cui; M W Adams
Journal:  Science       Date:  1999-10-08       Impact factor: 47.728

Review 6.  Fusobacterium nucleatum in periodontal health and disease.

Authors:  Benoit Signat; Christine Roques; Pierre Poulet; Danielle Duffaut
Journal:  Curr Issues Mol Biol       Date:  2011-01-10       Impact factor: 2.081

7.  Identification and characterization of a haem biosynthesis locus in Veillonella.

Authors:  Peng Zhou; Xiaoli Li; Fengxia Qi
Journal:  Microbiology (Reading)       Date:  2016-08-26       Impact factor: 2.777

8.  Coaggregation properties of human oral Veillonella spp.: relationship to colonization site and oral ecology.

Authors:  C V Hughes; P E Kolenbrander; R N Andersen; L V Moore
Journal:  Appl Environ Microbiol       Date:  1988-08       Impact factor: 4.792

9.  Streptococcal antagonism in oral biofilms: Streptococcus sanguinis and Streptococcus gordonii interference with Streptococcus mutans.

Authors:  Jens Kreth; Yongshu Zhang; Mark C Herzberg
Journal:  J Bacteriol       Date:  2008-04-25       Impact factor: 3.490

10.  Complete Genome Sequence of Veillonella atypica OK5, the First Transformable Strain in the Species.

Authors:  Peng Zhou; Gary Xie; Xiaoli Li; Jinman Liu; Fengxia Qi
Journal:  Genome Announc       Date:  2017-06-01
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1.  Magnesium-Dependent Promotion of H2O2 Production Increases Ecological Competitiveness of Oral Commensal Streptococci.

Authors:  X Cheng; S Redanz; P Treerat; H Qin; D Choi; X Zhou; X Xu; J Merritt; J Kreth
Journal:  J Dent Res       Date:  2020-03-20       Impact factor: 6.116

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3.  The Predominant Oral Microbiota Is Acquired Early in an Organized Pattern.

Authors:  Rosalyn M Sulyanto; Zachary A Thompson; Clifford J Beall; Eugene J Leys; Ann L Griffen
Journal:  Sci Rep       Date:  2019-07-22       Impact factor: 4.379

4.  Fusobacterium Species and Subspecies Differentially Affect the Composition and Architecture of Supra- and Subgingival Biofilms Models.

Authors:  Thomas Thurnheer; Lamprini Karygianni; Manuela Flury; Georgios N Belibasakis
Journal:  Front Microbiol       Date:  2019-07-30       Impact factor: 5.640

5.  Transcriptional profiling of coaggregation interactions between Streptococcus gordonii and Veillonella parvula by Dual RNA-Seq.

Authors:  Naresh V R Mutha; Waleed K Mohammed; Natalio Krasnogor; Geok Y A Tan; Wei Yee Wee; Yongming Li; Siew Woh Choo; Nicholas S Jakubovics
Journal:  Sci Rep       Date:  2019-05-21       Impact factor: 4.379

6.  The Oral Microbiome in Periodontal Health.

Authors:  Magdalena Lenartova; Barbora Tesinska; Tatjana Janatova; Ondrej Hrebicek; Jaroslav Mysak; Jiri Janata; Lucie Najmanova
Journal:  Front Cell Infect Microbiol       Date:  2021-03-22       Impact factor: 5.293

7.  Comparison of antibacterial and antibiofilm activity of bioactive glass compounds S53P4 and 45S5.

Authors:  Peng Zhou; Brittny L Garcia; Georgios A Kotsakis
Journal:  BMC Microbiol       Date:  2022-09-02       Impact factor: 4.465

8.  Fecal Microbiome Alteration May Be a Potential Marker for Gastric Cancer.

Authors:  Juan Wu; Cong Zhang; Shuo Xu; Chunjie Xiang; Ruiping Wang; Dongqing Yang; Bin Lu; Liyun Shi; Ruimin Tong; Yuhao Teng; Wei Dong; Junfeng Zhang
Journal:  Dis Markers       Date:  2020-09-15       Impact factor: 3.434

Review 9.  Veillonellae: Beyond Bridging Species in Oral Biofilm Ecology.

Authors:  Peng Zhou; Daniel Manoil; Georgios N Belibasakis; Georgios A Kotsakis
Journal:  Front Oral Health       Date:  2021-10-29
  9 in total

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