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Synergistic metabolism of salivary MUC5B in oral commensal bacteria during early biofilm formation
Malmö University, Faculty of Odontology (OD). Malmö University, Biofilms Research Center for Biointerfaces.ORCID iD: 0000-0001-9545-9161
Malmö University, Faculty of Odontology (OD). Malmö University, Biofilms Research Center for Biointerfaces.ORCID iD: 0000-0003-3173-7577
Malmö University, Faculty of Odontology (OD). Malmö University, Biofilms Research Center for Biointerfaces.ORCID iD: 0000-0001-5888-664X
Swedish NMR Centre, Gothenburg University, Gothenburg, Sweden.
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2023 (English)In: Microbiology Spectrum, E-ISSN 2165-0497, Vol. 11, no 6Article in journal (Refereed) Published
Abstract [en]

Bacterial metabolism in oral biofilms is comprised of complex networks of nutritional chains and biochemical regulations. These processes involve both intraspecies and interspecies networks as well as interactions with components from host saliva, gingival crevicular fluid, and dietary intake. In a previous paper, a large salivary glycoprotein, mucin MUC5B, was suggested to promote a dental health-related phenotype in the oral type strain of Streptococcus gordonii DL1, by regulating bacterial adhesion and protein expression. In this study, nuclear magnetic resonance-based metabolomics was used to examine the effects on the metabolic output of monospecies compared to dual species early biofilms of two clinical strains of oral commensal bacteria, S. gordonii and Actinomyces naeslundii, in the presence of MUC5B. The presence of S. gordonii increased colonization of A. naeslundii on salivary MUC5B, and both commensals were able to utilize MUC5B as a sole nutrient source during early biofilm formation. The metabolomes suggested that the bacteria were able to release mucin carbohydrates from oligosaccharide side chains as well as amino acids from the protein core. Synergistic effects were also seen in the dual species biofilm metabolome compared to the monospecies, indicating that A. naeslundii and S. gordonii cooperated in the degradation of salivary MUC5B. A better understanding of bacterial interactions and salivary-mediated regulation of early dental biofilm activity is meaningful for understanding oral biofilm physiology and may contribute to the development of future prevention strategies for biofilm-induced oral disease.

IMPORTANCE: The study of bacterial interactions and salivary-mediated regulation of early dental biofilm activity is of interest for understanding oral microbial adaptation to environmental cues and biofilm maturation. Findings in oral commensals can prove useful from the perspectives of both oral and systemic health of the host, as well as the understanding of general microbial biofilm physiology. The knowledge may provide a basis for the development of prognostic biomarkers, or development of new treatment strategies, related to oral health and disease and possibly also to other biofilm-induced conditions. The study is also an important step toward developing the methodology for similar studies in other species and/or growth conditions.

Place, publisher, year, edition, pages
ASM International, 2023. Vol. 11, no 6
Keywords [en]
MUC5B, NMR, actinomyces, bacterial metabolism, biofilm physiology, dental biofilm, metabolomics, oral microbiology, saliva, streptococci
National Category
Dentistry
Identifiers
URN: urn:nbn:se:mau:diva-63213DOI: 10.1128/spectrum.02704-23ISI: 001085549500001PubMedID: 37855449Scopus ID: 2-s2.0-85180007534OAI: oai:DiVA.org:mau-63213DiVA, id: diva2:1806711
Available from: 2023-10-23 Created: 2023-10-23 Last updated: 2024-01-10Bibliographically approved
In thesis
1. Responses to External Cues in Oral Bacteria
Open this publication in new window or tab >>Responses to External Cues in Oral Bacteria
2023 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

This thesis investigates responses to external cues in oral bacteria on a molecular level. Paper I maps Ser/Thr/Tyr phosphorylated proteins in relation to the general proteome in an oral commensal streptococcus (Streptococcus gordonii DL1). The identified phosphoproteins were involved in various bacterial processes, several associated to dysbiosis and development of biofilm-induced disease. Comparison against phosphoproteomes of other bacteria showed many similarities. This is of interest for the identification of shared phosphorylation profiles. 

Paper II studies differences between the S. gordonii DL1 general proteomes in planktonic and biofilm growth phases, and the regulatory effects of salivary mucin MUC5B on protein expression in the biofilm cells. Regulations in protein expression between the different growth conditions provides insights in bacterial mechanisms for adaptation to the biofilm lifestyle. 

Paper III examines the regulatory roles of salivary MUC5B on biofilm attachment and metabolic output in two clinical isolates of oral commensals, S. gordonii CW and Actinomyces naeslundii CW. S. gordonii facilitated adhesion of A. naeslundii to MUC5B during early attachment. Both bacteria were also able to utilize MUC5B as a sole nutrient source during early biofilm formation, individually and synergistically in a dual species biofilm. The specific responses elicited by MUC5B in paper II-III seem to promote commensal colonization while down-regulating dysbiosis-related biofilm activities. 

Microbiological studies are often focused on dysbiosis and development of disease. However, mechanisms that promote eubiosis are equally important to understand how health can be maintained. Findings associated with responses to external cues in oral bacteria may contribute to future development of novel preventative strategies and identification of predictive biomarkers for oral health. 

Abstract [sv]

Avhandlingen undersöker orala bakteriers svar till utifrån kommande signaler på en molekylärbiologisk nivå. I delarbete I kartläggs proteiner med serin/treonin/ tyrosin fosforylering i relation till det generella proteomet hos en oral streptokock (Streptococcus gordonii DL1). De identifierade fosfoproteinerna kunde kopplas till olika bakteriella processer, varav flera av intresse ur kariessynpunkt. Jämförelse mot andra bakteriers fosfoproteom visade många likheter, vilket är av intresse för identifiering av delade fosforyleringsprofiler. 

I delarbete II undersöks skillnader i det generella proteomet hos S. gordonii DL1 mellan tillväxtfaserna planktonisk och biofilm, samt reglerande effekter av salivmucinet MUC5B på biofilmscellerna proteinuttryck. Skillnaderna i proteinuttryck mellan tillväxtfaser ger ledtrådar om bakteriernas mekanismer för anpassning till biofilmstillväxt. 

Delarbete III studeras salivmucinet MUC5Bs reglerande roll på vidhäftning och metabolism i biofilmer med kliniska isolat av S. gordonii CW samt Actinomyces naeslundii CW. S. gordonii ökade vidhäftningen av A. naeslundii till MUC5B. Båda arterna kunde också använda MUC5B som enda näringskälla under tidig biofilmsbildning, både enskilt och tillsammans. Responserna som MUC5B framkallade i biofilmerna (paper II och III) verkar främja kolonisering av kommensaler och samtidigt nedreglera kariesrelaterade aktiviteter. 

Mikrobiologiska studier fokuserar ofta på dysbiosis och sjukdomsutveckling, men mekanismer som bibehåller eubiosis är minst lika viktiga för att förstå hur oral hälsa kan främjas. Resultat kopplade till orala bakteriers svar på utifrån kommande signaler kan bidra till framtida utveckling av nya strategier för prevention och identifiering av prediktiva biomarkörer för oral hälsa. 

Place, publisher, year, edition, pages
Malmö: Malmö University Press, 2023. p. 105
Series
Malmö University Odontological Dissertations, ISSN 1650-6065
Keywords
Oral Microbiology, Oral Biofilms, Saliva, Salivary mucin MUC5B, Streptococcus, Actinomyces
National Category
Microbiology Biochemistry and Molecular Biology Cell and Molecular Biology Dentistry
Identifiers
urn:nbn:se:mau:diva-62571 (URN)10.24834/isbn.9789178774180 (DOI)978-91-7877-417-3 (ISBN)978-91-7877-418-0 (ISBN)
Public defence
2023-12-08, KL:2370, Carl Gustafs väg 34, Malmö, 09:00 (English)
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Supervisors
Projects
Foresight
Funder
Swedish Research Council, 201601994NIH (National Institutes of Health), P005403501
Available from: 2023-10-27 Created: 2023-10-26 Last updated: 2024-02-23Bibliographically approved

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Robertsson, CarolinaSvensäter, GunnelDavies, Julia RWickström, Claes

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