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Glycerol metabolism supports oral commensal interactions

The ISME Journal volume 17, pages 1116–1127 (2023)Cite this article

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Abstract

During oral biofilm development, interspecies interactions drive species distribution and biofilm architecture. To understand what molecular mechanisms determine these interactions, we used information gained from recent biogeographical investigations demonstrating an association of corynebacteria with streptococci. We previously reported that Streptococcus sanguinis and Corynebacterium durum have a close relationship through the production of membrane vesicle and fatty acids leading to S. sanguinis chain elongation and overall increased fitness supporting their commensal state. Here we present the molecular mechanisms of this interspecies interaction. Coculture experiments for transcriptomic analysis identified several differentially expressed genes in S. sanguinis. Due to its connection to fatty acid synthesis, we focused on the glycerol-operon. We further explored the differentially expressed type IV pili genes due to their connection to motility and biofilm adhesion. Gene inactivation of the glycerol kinase glpK had a profound impact on the ability of S. sanguinis to metabolize C. durum secreted glycerol and impaired chain elongation important for their interaction. Investigations on the effect of type IV pili revealed a reduction of S. sanguinis twitching motility in the presence of C. durum, which was caused by a decrease in type IV pili abundance on the surface of S. sanguinis as determined by SEM. In conclusion, we identified that the ability to metabolize C. durum produced glycerol is crucial for the interaction of C. durum and S. sanguinis. Reduced twitching motility could lead to a closer interaction of both species, supporting niche development in the oral cavity and potentially shaping symbiotic health-associated biofilm communities.

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Fig. 1: Interspecies interaction of S. sanguinis and C. durum on the phenotypic and genotypic level.
Fig. 2: Glycerol consumption of S. sanguinis.
Fig. 3: Effect of glycerol on SK36 chain morphological alteration via the glpK metabolic pathway.
Fig. 4: Total glycerol production under the influence of glucose.
Fig. 5: Effect of glpK in bacteria-phagocytic interactions.
Fig. 6: Differences in surface twitching/swarming motility phenotypes of S. sanguinis SK strains under the influence of Cd.
Fig. 7: Comparison of type IV pilus gene expression in S. sanguinis SK strains ± Cd.
Fig. 8: Scanning electron micrographs (SEM) of type IV pilus morphology in the SK strains.

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Data availability

All data are available in the main text and the supplementary materials. Raw and processed sequencing data can be found under GSE230560 in the NCBI GEO data repository.

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Acknowledgements

This work was supported by an NIH-NIDCR grant DE021726, DE029492, and DE029612 to JK and NIH-NIDCR grant DE028252 to JM. We thank Prof. Todd Kitten for kindly providing S. sanguinis SK strains, and Dr. Claudia S. López (Multiscale Microscopy Core, OHSU) for expert assistance in performing SEM with technical support from Center for Spatial Systems Biomedicine (OCSSB).

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Authors and Affiliations

  1. Department of Restorative Dentistry, School of Dentistry, Oregon Health & Science University (OHSU), Portland, OR, 97239, USA

    Puthayalai Treerat, David Anderson, Justin Merritt & Jens Kreth

  2. Cariology Unit, Department of Oral Rehabilitation, Faculty of Dentistry, University of Talca, Talca, Chile

    Rodrigo A. Giacaman

  3. Department of Molecular Microbiology and Immunology, School of Medicine, Oregon Health & Science University (OHSU), Portland, OR, 97239, USA

    Justin Merritt & Jens Kreth

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PT, DA, JM and JK designed and conceptualized the research project. PT and DA performed experimental work and PT, DA, RAG and JK performed data analysis. All authors were involved in drafting, revising and finalizing the manuscript.

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Treerat, P., Anderson, D., Giacaman, R.A. et al. Glycerol metabolism supports oral commensal interactions. ISME J 17, 1116–1127 (2023). https://doi.org/10.1038/s41396-023-01426-9

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