Comparative genomics reveals distinct host-interacting traits of three major human-associated propionibacteria

Abstract

BackgroundPropionibacteria are part of the human microbiota. Many studies have addressed the predominant colonizer of sebaceous follicles of the skin, Propionibacterium acnes, and investigated its association with the skin disorder acne vulgaris, and lately with prostate cancer. Much less is known about two other propionibacterial species frequently found on human tissue sites, Propionibacterium granulosum and Propionibacterium avidum. Here we analyzed two and three genomes of P. granulosum and P. avidum, respectively, and compared them to two genomes of P. acnes; we further highlight differences among the three cutaneous species with proteomic and microscopy approaches.ResultsElectron and atomic force microscopy revealed an exopolysaccharide (EPS)-like structure surrounding P. avidum cells, that is absent in P. acnes and P. granulosum. In contrast, P. granulosum possesses pili-like appendices, which was confirmed by surface proteome analysis. The corresponding genes were identified; they are clustered with genes encoding sortases. Both, P. granulosum and P. avidum lack surface or secreted proteins for predicted host-interacting factors of P. acnes, including several CAMP factors, sialidases, dermatan-sulphate adhesins, hyaluronidase and a SH3 domain-containing lipoprotein; accordingly, only P. acnes exhibits neuraminidase and hyaluronidase activities. These functions are encoded on previously unrecognized island-like regions in the genome of P. acnes.ConclusionsDespite their omnipresence on human skin little is known about the role of cutaneous propionibacteria. All three species are associated with a variety of diseases, including postoperative and device-related abscesses and infections. We showed that the three organisms have evolved distinct features to interact with their human host. Whereas P. avidum and P. granulosum produce an EPS-like surface structure and pili-like appendices, respectively, P. acnes possesses a number of unique surface-exposed proteins with host-interacting properties. The different surface properties of the three cutaneous propionibacteria are likely to determine their colonizing ability and pathogenic potential on the skin and at non-skin sites.

TLR-2 Recognizes Propionibacterium acnes CAMP Factor 1 from Highly Inflammatory Strains

“…In this study, we extracted surface proteins from washed bacterial pellets by lithium stripping. Our results are consistent with the CAMP factor 1 protein being associated with the surface but not firmly bound to it, as it can be removed from whole bacteria by trypsin cleavage [46]. Previous studies have reported the presence of P .…”

The balance of metagenomic elements shapes the skin microbiome in acne and health

“…After removal of human DNA sequences and low-quality reads, we obtained an average of 1.08 gigabase pairs (Gbp) per sample (6.9 × 10 7  bp – 4.8 × 10 9  bp), sufficient to cover the microbial diversity of skin samples24. We mapped the cleaned sequencing reads to our reference genome set, which consists of 1,252 bacterial and 272 fungal genomes from the HMP reference genome database and several additional genomes of skin microorganisms: Propionibacterium avidum 2526 , Propionibacterium granulosum 26 , Propionibacterium humerusii 27, and P. acnes bacteriophage2829. To cover different P. acnes strains, we also included the P. acnes pan-genome in the reference19.…”

“…Limited genomic information exists for P. granulosum . Previous comparative analysis based on two draft genomes revealed that, compared to P. acnes, P. granulosum lacks virulence-related factors such as CAMP factors and sialidases, and exhibits no neuraminidase and hyaluronidase activities26. The bacterium may provide protection to the skin with less production of virulence-associated elements.…”

A Novel High-Resolution Single Locus Sequence Typing Scheme for Mixed Populations of Propionibacterium acnes In Vivo

“…Previous research has shown an abundance of CAMP1 as surface-exposed factor [19], [30], [31]. In contrast to other CAMP factors, such as CAMP2 and CAMP4, the gene encoding CAMP1 is not located on an island-like genomic region [32]. It is possible that differences in the SLST target region are important for the transcription of CAMP1 resulting in clade-specific differences.…”