Growth of Porphyromonas gingivalis on human serum albumin triggers programmed cell death

ABSTRACT

Aims

Gingival crevicular fluid (GCF) constitutes the primary growth substrate for Porphyromonas gingivalis in vivo. The goal of this work was to evaluate the growth of different strains of P. gingivalis on human serum albumin (HSA), a major constituent of GCF.

Methods

Growth of five different strains of P. gingivalis in the HSA medium was examined and, surprisingly, three of the strains underwent autolysis within 24 h. Comparative transcriptomic analysis was used to identify genes involved in autolysis.

Results

Two highly related reference strains (W50 and W83) differed dramatically in their survival when grown on HSA. Strain W83 grew fast and lysed within 24 h, while W50 survived for an additional 20 h. Differential gene expression analysis led us to a gene cluster containing enzymes involved in arginine metabolism and a gene predicted to be a lytic murein transglycosylase, which are known to play a role in autolysis. Deletion of this gene (PG0139) resulted in a mutant that did not lyse, and complementation restored the HSA lysis phenotype, indicating that this enzyme plays a central role in the autolysis of P. gingivalis.

Conclusions

P. gingivalis undergoes autolysis when provided with HSA as a substrate for growth.

KEYWORDS:

• Lytic transglycosylase
• polyamines
• autolysis
• p. gingivalis
• asRNA

Acknowledgments

We thank Dr. Frank Gibson for suggesting a comparison between BSA and HSA and the Gene Expression & Genotyping core of Interdisciplinary Center for Biotechnology Research at the University of Florida for library construction and DNA sequencing. The research reported in the manuscript was supported by the National Institute of Dental and Craniofacial Research of the National Institutes of Health under award numbers R01DEO24580 and R01DE019117 (MED).

Disclosure statement

No potential conflict of interest was reported by the author(s).

Author contribution

S.G., M.F.M., and M.E.D conceived the project. S.G. D.D., A.R.W, and M.F.M. performed experiments. S.G., M.F.M., D.D., and M.E.D. wrote the manuscript. All authors reviewed the manuscript.

Data availability statement

The authors declare that the data supporting the findings of this study are available within the paper and its supplementary information files. Raw sequencing data are available on the NCBI Sequence Read Archive (SRA) under accession number PRJNA911789. https://www.ncbi.nlm.nih.gov/bioproject/PRJNA911789

Supplementary material

Supplemental data for this article can be accessed online at https://doi.org/10.1080/20002297.2022.2161182.

Correction Statement

This article has been corrected with minor changes. These changes do not impact the academic content of the article.

Additional information

Funding

The work was supported by the the National Institute of Dental and Craniofacial Research of the National Institutes of Health [R01DEO24580, R01DE019117].