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Synergism between Corynebacterium and Streptococcus sanguinis reveals new interactions between oral commensals

Abstract

The oral microbiome engages in a diverse array of highly sophisticated ecological interactions that are crucial for maintaining symbiosis with the host. Streptococci and corynebacteria are among the most abundant oral commensals and their interactions are critical for normal biofilm development. In this study, we discovered that Streptococcus sanguinis specifically responds to the presence of Corynebacterium durum by dramatically altering its chain morphology and improving its overall fitness. By employing gas chromatography-mass spectrometry (GC-MS) analysis, specific fatty acids were identified in C. durum supernatants that are responsible for the observed effect. Membrane vesicles (MVs) containing these fatty acids were isolated from C. durum supernatants and were able to replicate the chain morphology phenotype in S. sanguinis, suggesting MV as a mediator of interspecies interactions. Furthermore, S. sanguinis responds to C. durum lipids by decreasing the expression of key FASII genes involved in fatty acid synthesis. Several of these genes are also essential for the chain elongation phenotype, which implicates a regulatory connection between lipid metabolism and chain elongation. In addition, C. durum was found to affect the growth, cell aggregation, and phagocytosis of S. sanguinis, revealing a complex association of these species that likely supports oral commensal colonization and survival.

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Fig. 1: Effect of C. durum JJ1 [1] on S. sanguinis SK36 (SK36) chain morphology.
Fig. 2: Strain-specific interactions between Corynebacterium spp. and S. sanguinis.
Fig. 3: Role of fatty acids in S. sanguinis chain elongation.
Fig. 4: Involvement of SK36 lipid metabolism and cell division genes in the elongated chain phenotype induced by Cd.
Fig. 5: Influence of glucose on the SK36 chain elongated phenotype.
Fig. 6: Transmission electron micrograph of MVs prepared from Cd.
Fig. 7: Effect of Cd on SK36 survivability and phagocytosis.

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Acknowledgements

This work was supported by an NIH-NIDCR grant DE021726 to JK and NIH-NIDCR grants DE018893 and DE022083 to JM. We thank Prof. Todd Kitten for kindly providing S. sanguinis SK strains, Dr Stefanie K. Petrie (Advanced Light Microscopy Core, OHSU) for expert assistance with LSM 780 confocal microscope, Prof. Dennis Koop (Bioanalytical Shared Resource/Pharmacokinetics Core, OHSU) for fatty acid identification, Dr Claudia S. López (Multiscale Microscopy Core, OHSU) for expert assistance in performing TEM with technical support from Center for Spatial Systems Biomedicine (OCSSB). We also thank Dr Nyssa Cullin for constructing SK36 ldh-gfp.

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Treerat, P., Redanz, U., Redanz, S. et al. Synergism between Corynebacterium and Streptococcus sanguinis reveals new interactions between oral commensals. ISME J 14, 1154–1169 (2020). https://doi.org/10.1038/s41396-020-0598-2

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