Analysis of complete genomes of Propionibacterium acnes reveals a novel plasmid and increased pseudogenes in an acne associated strain

Gabriela Kasimatis, Sorel Fitz-Gibbon, Shuta Tomida, Marthew Wong, Huiying Li, Gabriela Kasimatis, Sorel Fitz-Gibbon, Shuta Tomida, Marthew Wong, Huiying Li

Abstract

The human skin harbors a diverse community of bacteria, including the Gram-positive, anaerobic bacterium Propionibacterium acnes. P. acnes has historically been linked to the pathogenesis of acne vulgaris, a common skin disease affecting over 80% of all adolescents in the US. To gain insight into potential P. acnes pathogenic mechanisms, we previously sequenced the complete genome of a P. acnes strain HL096PA1 that is highly associated with acne. In this study, we compared its genome to the first published complete genome KPA171202. HL096PA1 harbors a linear plasmid, pIMPLE-HL096PA1. This is the first described P. acnes plasmid. We also observed a five-fold increase of pseudogenes in HL096PA1, several of which encode proteins in carbohydrate transport and metabolism. In addition, our analysis revealed a few island-like genomic regions that are unique to HL096PA1 and a large genomic inversion spanning the ribosomal operons. Together, these findings offer a basis for understanding P. acnes virulent properties, host adaptation mechanisms, and its potential role in acne pathogenesis at the strain level. Furthermore, the plasmid identified in HL096PA1 may potentially provide a new opportunity for P. acnes genetic manipulation and targeted therapy against specific disease-associated strains.

Figures

Figure 1
Figure 1
Circular representation of P. acnes HL096PA1 chromosome. From the outer circle to the inner circle are circle 1, ORFs on the positive strand (blue); circle 2, ORFs on the negative strand (green); circle 3, pseudogenes (red); circle 4, tRNA (gold) and rRNA (purple); circle 5, GC content (light/dark grey); circle 6, GC skew (light/dark grey). DNA Plotter [46] was used in making the figure.
Figure 2
Figure 2
The homologous regions among P. acnes pIMPLE-HL096PA1, P. humerusii HL044PA1, and C. leptum DSM 753. (a) The 74 ORFs encoded on the plasmid pIMPLE-HL096PA1 are shown. ORFs PAGK_2344–PAGK_2378 (blue), including the Tad locus (pink), are shared among all three genomes. In addition, several ORFs are shared between P. acnes and P. humerusii (orange). ORFs unique to P. acnes are shown in grey. Absence of P. acnes homologous ORFs in P. humerusii or C. leptum is shown in white. (b) Organizations of the ORFs shared among all three genomes. (c) The sequence coverage of the contigs in three P. humerusii strains (HL037PA2, HL037PA3, and HL044PA1) that share homologous genes with pIMPLE-HL096PA1 is 3–5-folds higher than the contigs that do not share homologous genes with pIMPLE-HL096PA1.
Figure 3
Figure 3
Genomic inversion in HL096PA1. (a) Genomic inversions observed in P. acnes strains HL096PA1 and ATCC11828 compared to P. acnes strain KPA171202. (b) Primer sets I–V designed to verify the genomic inversion in HL096PA1. (c) PCR amplified DNA fragments of the inverted regions shown on an agarose gel. Primers, target genomes, and the predicted sizes of the amplicons are shown in the table. HL, strain HL096PA1; KPA, strain KPA171202.

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