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  • 1.
    Boyd, Hannah
    et al.
    Malmö University, Faculty of Health and Society (HS), Department of Biomedical Science (BMV). Malmö University, Biofilms Research Center for Biointerfaces.
    Gonzalez-Martinez, Juan F
    Malmö University, Faculty of Health and Society (HS), Department of Biomedical Science (BMV). Malmö University, Biofilms Research Center for Biointerfaces.
    Welbourn, Rebecca J L
    ISIS Facility, STFC, Rutherford Appleton Laboratory, Chilton, Didcot, Oxon OX11 0QX, UK.
    Gutfreund, Philipp
    Institut Laue Langevin, 71 avenue des Martyrs, Grenoble 38000, France.
    Klechikov, Alexey
    Institut Laue Langevin, 71 avenue des Martyrs, Grenoble 38000, France; Department of Physics and Astronomy, Uppsala University, 75120 Uppsala, Sweden.
    Robertsson, Carolina
    Malmö University, Faculty of Odontology (OD). Malmö University, Biofilms Research Center for Biointerfaces.
    Wickström, Claes
    Malmö University, Faculty of Odontology (OD). Malmö University, Biofilms Research Center for Biointerfaces.
    Arnebrant, Thomas
    Malmö University, Faculty of Health and Society (HS), Department of Biomedical Science (BMV). Malmö University, Biofilms Research Center for Biointerfaces.
    Barker, Robert
    School of Physical Sciences, University of Kent, Canterbury, Kent CT2 7NH, UK.
    Sotres, Javier
    Malmö University, Faculty of Health and Society (HS), Department of Biomedical Science (BMV). Malmö University, Biofilms Research Center for Biointerfaces.
    A comparison between the structures of reconstituted salivary pellicles and oral mucin (MUC5B) films.2021In: Journal of Colloid and Interface Science, ISSN 0021-9797, E-ISSN 1095-7103, Vol. 584, p. 660-668, article id S0021-9797(20)31464-8Article in journal (Refereed)
    Abstract [en]

    HYPOTHESIS: Salivary pellicles i.e., thin films formed upon selective adsorption of saliva, protect oral surfaces against chemical and mechanical insults. Pellicles are also excellent aqueous lubricants. It is generally accepted that reconstituted pellicles have a two-layer structure, where the outer layer is mainly composed of MUC5B mucins. We hypothesized that by comparing the effect of ionic strength on reconstituted pellicles and MUC5B films we could gain further insight into the pellicle structure.

    EXPERIMENTS: Salivary pellicles and MUC5B films reconstituted on solid surfaces were investigated at different ionic strengths by Force Spectroscopy, Quartz Crystal Microbalance with Dissipation, Null Ellipsometry and Neutron Reflectometry.

    FINDINGS: Our results support the two-layer structure for reconstituted salivary pellicles. The outer layer swelled when ionic strength decreased, indicating a weak polyelectrolyte behavior. While initially the MUC5B films exhibited a similar tendency, this was followed by a drastic collapse indicating an interaction between exposed hydrophobic domains. This suggests that mucins in the pellicle outer layer form complexes with other salivary components that prevent this interaction. Lowering ionic strength below physiological values also led to a partial removal of the pellicle inner layer. Overall, our results highlight the importance that the interactions of mucins with other pellicle components play on their structure.

  • 2.
    Gonzalez-Martinez, Juan F
    et al.
    Malmö University, Faculty of Health and Society (HS), Department of Biomedical Science (BMV). Malmö University, Biofilms Research Center for Biointerfaces.
    Boyd, Hannah
    Malmö University, Faculty of Health and Society (HS), Department of Biomedical Science (BMV). Malmö University, Biofilms Research Center for Biointerfaces.
    Gutfreund, Philipp
    Institut Laue Langevin, 71 avenue des Martyrs, Grenoble 38000, France.
    Welbourn, Rebecca J L
    ISIS Facility, STFC, Rutherford Appleton Laboratory, Chilton, Didcot, Oxon OX11 0QX, United Kingdom.
    Robertsson, Carolina
    Malmö University, Faculty of Odontology (OD). Malmö University, Biofilms Research Center for Biointerfaces.
    Wickström, Claes
    Malmö University, Faculty of Odontology (OD). Malmö University, Biofilms Research Center for Biointerfaces.
    Arnebrant, Thomas
    Malmö University, Biofilms Research Center for Biointerfaces. Malmö University, Faculty of Health and Society (HS), Department of Biomedical Science (BMV).
    Richardson, Robert M
    School of Physics, University of Bristol, Tyndall Avenue, BS8 1TL Bristol, United Kingdom.
    Prescott, Stuart W
    School of Chemical Engineering, University of New South Wales, Sydney, NSW 2052, Australi.
    Barker, Robert
    School of Physical Sciences, University of Kent, Canterbury, Kent CT2 7NH, United Kingdom.
    Sotres, Javier
    Malmö University, Biofilms Research Center for Biointerfaces. Malmö University, Faculty of Health and Society (HS), Department of Biomedical Science (BMV).
    MUC5B mucin films under mechanical confinement: A combined neutron reflectometry and atomic force microscopy study.2022In: Journal of Colloid and Interface Science, ISSN 0021-9797, E-ISSN 1095-7103, Vol. 614, p. 120-129, article id S0021-9797(22)00109-6Article in journal (Refereed)
    Abstract [en]

    HYPOTHESIS: Among other functions, mucins hydrate and protect biological interfaces from mechanical challenges. Mucins also attract interest as biocompatible coatings with excellent lubrication performance. Therefore, it is of high interest to understand the structural response of mucin films to mechanical challenges. We hypothesized that this could be done with Neutron Reflectometry using a novel sample environment where mechanical confinement is achieved by inflating a membrane against the films.

    EXPERIMENTS: Oral MUC5B mucin films were investigated by Force Microscopy/Spectroscopy and Neutron Reflectometry both at solid-liquid interfaces and under mechanical confinement.

    FINDINGS: NR indicated that MUC5B films were almost completely compressed and dehydrated when confined at 1 bar. This was supported by Force Microscopy/Spectroscopy investigations. Force Spectroscopy also indicated that MUC5B films could withstand mechanical confinement by means of steric interactions for pressures lower than ∼ 0.5 bar i.e., mucins could protect interfaces from mechanical challenges of this magnitude while keeping them hydrated. To investigate mucin films under these pressures by means of the employed sample environment for NR, further technological developments are needed. The most critical would be identifying or developing more flexible membranes that would still meet certain requirements like chemical homogeneity and very low roughness.

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  • 3.
    Neilands, Jessica
    et al.
    Malmö University, Faculty of Odontology (OD).
    Svensäter, Gunnel
    Malmö University, Faculty of Odontology (OD).
    Boisen, Gabriella
    Malmö University, Faculty of Odontology (OD).
    Robertsson, Carolina
    Malmö University, Faculty of Odontology (OD).
    Wickström, Claes
    Malmö University, Faculty of Odontology (OD).
    Davies, Julia R
    Malmö University, Faculty of Odontology (OD).
    Formation and Analysis of Mono-species and Polymicrobial Oral Biofilms in Flow-Cell Models2023In: Bacterial Pathogenesis: Methods and Protocols,, Springer, 2023, p. 33-52Chapter in book (Refereed)
    Abstract [en]

    The oral microbiota, which is known to include at least 600 different bacterial species, is found on the teethand mucosal surfaces as multi-species communities or biofilms. The oral surfaces are covered with a pellicleof proteins absorbed from saliva, and biofilm formation is initiated when primary colonizers, which expresssurface adhesins that bind to specific salivary components, attach to the oral tissues. Further developmentthen proceeds through co-aggregation of additional species. Over time, the composition of oral biofilms,which varies between different sites throughout the oral cavity, is determined by a combination ofenvironmental factors such as the properties of the underlying surface, nutrient availability and oxygenlevels, and bacterial interactions within the community. A complex equilibrium between biofilm communities and the host is responsible for the maintenance of a healthy biofilm phenotype (eubiosis). In the faceof sustained environmental perturbation, however, biofilm homeostasis can break down giving rise todysbiosis, which is associated with the development of oral diseases such as caries and periodontitis.In vitro models have an important part to play in increasing our understanding of the complex processesinvolved in biofilm development in oral health and disease, and the requirements for experimental system,microbial complexity, and analysis techniques will necessarily vary depending on the question posed. In thischapter we describe some current and well-established methods used in our laboratory for studying oralbacteria in biofilm models which can be adapted to suit the needs of individual users. 

  • 4.
    Robertsson, Carolina
    Malmö University, Faculty of Odontology (OD). Malmö University, Biofilms Research Center for Biointerfaces.
    Responses to External Cues in Oral Bacteria2023Doctoral 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. 

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  • 5.
    Robertsson, Carolina
    et al.
    Malmö University, Faculty of Odontology (OD).
    Svensäter, Gunnel
    Malmö University, Faculty of Odontology (OD).
    Blum, Zoltan
    Malmö University, Faculty of Health and Society (HS), Department of Biomedical Science (BMV).
    Jakobsson, Magnus E.
    Lund Univ, Dept Immunotechnol, Lund, Sweden..
    Wickström, Claes
    Malmö University, Faculty of Odontology (OD).
    Proteomic response in Streptococcus gordonii DL1 biofilm cells during attachment to salivary MUC5B2021In: Journal of Oral Microbiology, ISSN 2000-2297, E-ISSN 2000-2297, Vol. 13, no 1, article id 1967636Article in journal (Refereed)
    Abstract [en]

    Background Salivary mucin MUC5B seems to promote biodiversity in dental biofilms, and thereby oral health, for example, by inducing synergistic 'mucolytic' activities in a variety of microbial species that need to cooperate for the release of nutrients from the complex glycoprotein. Knowledge of how early colonizers interact with host salivary proteins is integral to better understand the maturation of putatively harmful oral biofilms and could provide key insights into biofilm physiology. Methods The early oral colonizer Streptococcus gordonii DL1 was grown planktonically and in biofilm flow cell systems with uncoated, MUC5B or low-density salivary protein (LDP) coated surfaces. Bacterial cell proteins were extracted and analyzed using a quantitative mass spectrometry-based workflow, and differentially expressed proteins were identified. Results and conclusions Overall, the proteomic profiles of S. gordonii DL1 were similar across conditions. Six novel biofilm cell proteins and three planktonic proteins absent in all biofilm cultures were identified. These differences may provide insights into mechanisms for adaptation to biofilm growth in this species. Salivary MUC5B also elicited specific responses in the biofilm cell proteome. These regulations may represent mechanisms by which this mucin could promote colonization of the commensal S. gordonii in oral biofilms.

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  • 6.
    Robertsson, Carolina
    et al.
    Malmö University, Faculty of Odontology (OD). Malmö University, Biofilms Research Center for Biointerfaces.
    Svensäter, Gunnel
    Malmö University, Faculty of Odontology (OD). Malmö University, Biofilms Research Center for Biointerfaces.
    Blum, Zoltan
    Malmö University, Faculty of Health and Society (HS), Department of Biomedical Science (BMV).
    Wickström, Claes
    Malmö University, Faculty of Odontology (OD). Malmö University, Biofilms Research Center for Biointerfaces.
    Intracellular Ser/Thr/Tyr phosphoproteome of the oral commensal Streptococcus gordonii DL12020In: BMC Microbiology, E-ISSN 1471-2180, Vol. 20, no 1, article id 280Article in journal (Refereed)
    Abstract [en]

    BACKGROUND: To respond and adapt to environmental challenges, prokaryotes regulate cellular processes rapidly and reversibly through protein phosphorylation and dephosphorylation. This study investigates the intracellular proteome and Ser/Thr/Tyr phosphoproteome of the oral commensal Streptococcus gordonii. Intracellular proteins from planktonic cells of S. gordonii DL1 were extracted and subjected to 2D-gel electrophoresis. Proteins in general were visualized using Coomassie Brilliant Blue and T-Rex staining. Phosphorylated proteins were visualized with Pro-Q Diamond Phosphoprotein Gel Stain. Proteins were identified by LC-MS/MS and sequence analysis.

    RESULTS: In total, sixty-one intracellular proteins were identified in S. gordonii DL1, many of which occurred at multiple isoelectric points. Nineteen of these proteins were present as one or more Ser/Thr/Tyr phosphorylated form. The identified phosphoproteins turned out to be involved in a variety of cellular processes.

    CONCLUSION: Nineteen phosphoproteins involved in various cellular functions were identified in S. gordonii. This is the first time the global intracellular Ser/Thr/Tyr phosphorylation profile has been analysed in an oral streptococcus. Comparison with phosphoproteomes of other species from previous studies showed many similarities. Proteins that are consistently found in a phosphorylated state across several species and growth conditions may represent a core phosphoproteome profile shared by many bacteria.

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  • 7.
    Robertsson, Carolina
    et al.
    Malmö University, Faculty of Odontology (OD). Malmö University, Biofilms Research Center for Biointerfaces.
    Svensäter, Gunnel
    Malmö University, Faculty of Odontology (OD). Malmö University, Biofilms Research Center for Biointerfaces.
    Davies, Julia R
    Malmö University, Faculty of Odontology (OD). Malmö University, Biofilms Research Center for Biointerfaces.
    Bay Nord, Anders
    Swedish NMR Centre, Gothenburg University, Gothenburg, Sweden.
    Malmodin, Daniel
    Swedish NMR Centre, Gothenburg University, Gothenburg, Sweden.
    Wickström, Claes
    Malmö University, Faculty of Odontology (OD). Malmö University, Biofilms Research Center for Biointerfaces.
    Synergistic metabolism of salivary MUC5B in oral commensal bacteria during early biofilm formation2023In: Microbiology Spectrum, E-ISSN 2165-0497, Vol. 11, no 6Article in journal (Refereed)
    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.

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