Genomic and phenotypic comparison of Prevotella intermedia strains possessing different virulence in vivo

ABSTRACT

Prevotella intermedia readily colonizes healthy dental biofilm and is associated with periodontal diseases. The viscous exopolysaccharide (EPS)-producing capability is known as a major virulence factor of P. intermedia 17 (Pi17). However, the inter-strain difference in P. intermedia regarding virulence-associated phenotype is not well studied. We compared in vivo virulence and whole genome sequences using five wild-type strains: ATCC 49046 (Pi49046), ATCC 15032 (Pi15032), ATCC 15033 (Pi15033), ATCC 25611 (Pi25611), and Pi17. Non-EPS producing Pi25611 was the least virulent in insect and mammalian models. Unexpectedly, Pi49046 did not produce viscous EPS but was the most virulent, followed by Pi17. Genomes of the five strains were quite similar but revealed subtle differences such as copy number variations and single nucleotide polymorphisms. Variations between strains were found in genes encoding glycosyltransferases and genes involved in the acquisition of carbohydrates and iron/haem. Based on these genetic variations, further analyses were performed. Phylogenetic and structural analyses discovered phosphoglycosyltransferases of Pi49046 and Pi17 have evolved to contain additional loops that may confer substrate specificity. Pi17, Pi15032, and Pi15033 displayed increased growth by various carbohydrates. Meanwhile, Pi49046 exhibited the highest activities for haemolysis and haem accumulation, as well as co-aggregation with Porphyromonas gingivalis harbouring fimA type II, which is more tied to periodontitis than other fimA types. Collectively, subtle genetic differences related to glycosylation and acquisition of carbohydrates and iron/haem may contribute to the diversity of virulence and phenotypic traits among P. intermedia strains. These variations may also reflect versatile strategies for within-host adaptation of P. intermedia.

KEYWORDS:

• P. intermedia
• inter-strain difference
• virulence
• genome
• phenotype
• within-host adaptation

Disclosure statement

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

Author’s contributions

K.H. Kwack contributed to data acquisition and drafted the manuscript. E.Y. Jang and S.B. Yang contributed to data acquisition. J.H. Lee contributed to conception, design, data analysis, interpretation, and critically revised the manuscript. J.H. Moon contributed to conception, design, data analysis and interpretation, drafted, and critically revised the manuscript. All authors gave final approval and agreed to be accountable for all aspects of the work.

Data availability statement

The authors confirm that the data supporting the findings of this study are available within the article and its supplementary materials.

Supplementary material

Supplemental data for this article can be accessed online at https://doi.org/10.1080/21505594.2022.2095718

Additional information

Funding

This research was supported by the National Research Foundation of Korea (NRF) funded by the Ministry of Science & ICT (2021R1A2C2008180).