The natural history of cutaneous propionibacteria, and reclassification of selected species within the genus Propionibacterium to the proposed novel genera Acidipropionibacterium gen. nov., Cutibacterium gen. nov. and Pseudopropionibacterium gen. nov.
The genus Propionibacterium in the family Propionibacteriaceaeconsists of species of various habitats, including mature cheese, cattle rumen and human skin. Traditionally, these species have been grouped as either classical or cutaneous propionibacteria based on characteristic phenotypes and source of isolation. To re-evaluate the taxonomy of the family and to elucidate the interspecies relatedness we compared 162 public whole-genome sequences of strains representing species of the family Propionibacteriaceae. We found substantial discrepancies between the phylogenetic signals of 16S rRNA gene sequence analysis and our high-resolution core-genome analysis. To accommodate these discrepancies, and to address the long-standing issue of the taxonomically problematic Propionibacterium propionicum, we propose three novel genera, Acidipropionibacterium gen. nov., Cutibacterium gen. nov. and Pseudopropionibacterium gen. nov., and an amended description of the genus Propionibacterium. Furthermore, our genome-based analyses support the amounting evidence that the subdivision of Propionibacterium freudenreichii into subspecies is not warranted. Our proposals are supported by phylogenetic analyses, DNA G+C content, peptidoglycan composition and patterns of the gene losses and acquisitions in the cutaneous propionibacteria during their adaptation to the human host.
Abeijón MukdsiM. C., FalentinH., MaillardM. B., ChuatV., MedinaR. B., ParayreS., ThierryA.2014; The secreted esterase of Propionibacterium freudenreichii has a major role in cheese lipolysis. Appl Environ Microbiol 80:751–756 [View Article][PubMed]
BrüggemannH., HenneA., HosterF., LiesegangH., WiezerA., StrittmatterA., HujerS., DürreP., GottschalkG.2004; The complete genome sequence of Propionibacterium acnes, a commensal of human skin. Science 305:671–673 [View Article][PubMed]
CharfreitagO., StackebrandtE.1989; Inter- and intrageneric relationships of the genus Propionibacterium as determined by 16S rRNA sequences. J Gen Microbiol 135:2065–2070 [View Article][PubMed]
DasenG., SmutnyJ., TeuberM., MeileL.1998; Classification and identification of propionibacteria based on ribosomal RNA genes and PCR. Syst Appl Microbiol 21:251–259 [View Article][PubMed]
de FreitasR., MadecM.-N., ChuatV., MaillardM.-B., MukdsiM. C., FalentinH., de CarvalhoA. F., ValenceF., ThierryA.2015; New insights about phenotypic heterogeneity within Propionibacterium freudenreichii argue against its division into subspecies. Dairy Sci Technol 95:465–477 [View Article][PubMed]
DownesJ., WadeW. G.2009; Propionibacterium acidifaciens sp. nov., isolated from the human mouth. Int J Syst Evol Microbiol 59:2778–2781 [View Article][PubMed]
GoodfellowM., WhitmanW. B., BergeyD. H.2012Bergey’s Manual of Systematic Bacteriology: Volume 5, The Actinobacteria, 2 edn. New York, NY: Springer; [CrossRef]
KanehisaM., GotoS., SatoY., KawashimaM., FurumichiM., TanabeM.2014; Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res 42:D199–D205 [View Article][PubMed]
LomholtH. B., KilianM.2010; Population genetic analysis of Propionibacterium acnes identifies a subpopulation and epidemic clones associated with acne. PLoS One 5:e12277 [View Article][PubMed]
LouxV., MariadassouM., AlmeidaS., ChiapelloH., HammaniA., BurattiJ., GendraultA., BarbeV., AuryJ.-M. et al.2015; Mutations and genomic islands can explain the strain dependency of sugar utilization in 21 strains of Propionibacterium freudenreichii. BMC Genomics 16:296 [View Article][PubMed]
MartinI., DébarbouilléM., FerrariE., KlierA., RapoportG.1987; Characterization of the levanase gene of Bacillus subtilis which shows homology to yeast invertase. Mol Gen Genet 208:177–184 [View Article][PubMed]
McDowellA., PerryA. L., LambertP. A., PatrickS.2008; A new phylogenetic group of Propionibacterium acnes. J Med Microbiol 57:218–224 [View Article][PubMed]
MollerupS., Friis-NielsenJ., VinnerL., HansenT. A., RichterS. R., FridholmH., HerreraJ. A., LundO., BrunakS. et al.2016; Propionibacterium acnes: Disease-causing agent or common contaminant? detection in diverse patient samples by next-generation sequencing. J Clin Microbiol 54:980–987 [View Article][PubMed]
PengM., SmithA. H., RehbergerT. G.2011; Quantification of Propionibacterium acidipropionici P169 bacteria in environmental samples by use of strain-specific primers derived by suppressive subtractive hybridization. Appl Environ Microbiol 77:3898–3902 [View Article][PubMed]
StackebrandtE., SchumannP., SchaalK. P., WeissN.2002; Propionim3icrobium gen. nov., a new genus to accommodate Propionibacterium lymphophilum (Torrey 1916) Johnson and Cummins 1972, 1057AL as Propionimicrobium lymphophilum comb. nov. Int J Syst Evol Microbiol 52:1925–1927 [View Article][PubMed]
StackebrandtE., CumminsC. S., JohnsonJ. L.2006; Family Propionibacteriaceae: The genus Propionibacterium. In The Prokaryotes pp. 400–418 Edited by DworkinM., FalkowS., RosenbergE., SchleiferK.-H., StackebrandtE. New York: Springer; [CrossRef]
ThierryA., DeutschS.-M., FalentinH., DalmassoM., CousinF. J., JanG.2011; New insights into physiology and metabolism of Propionibacterium freudenreichii. Int J Food Microbiol 149:19–27 [View Article][PubMed]
The natural history of cutaneous propionibacteria, and reclassification of selected species within the genus Propionibacterium to the proposed novel genera Acidipropionibacterium gen. nov., Cutibacterium gen. nov. and Pseudopropionibacterium gen. nov.