1887

Abstract

The genus in the family consists 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 . 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 we propose three novel genera, gen. nov., gen. nov. and gen. nov., and an amended description of the genus . Furthermore, our genome-based analyses support the amounting evidence that the subdivision of 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.

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.001367
2016-11-01
2021-09-28
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/66/11/4422.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.001367&mimeType=html&fmt=ahah

References

  1. Abeijón Mukdsi M. C., Falentin H., Maillard M. B., Chuat V., Medina R. B., Parayre S., Thierry A. 2014; The secreted esterase of Propionibacterium freudenreichii has a major role in cheese lipolysis. Appl Environ Microbiol 80:751–756 [View Article][PubMed]
    [Google Scholar]
  2. Alikhan N.-F., Petty N. K., Ben Zakour N. L., Beatson S. A. 2011; blast Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics 12:402 [View Article][PubMed]
    [Google Scholar]
  3. Barta M. L., McWhorter W. J., Miziorko H. M., Geisbrecht B. V. 2012; Structural basis for nucleotide binding and reaction catalysis in mevalonate diphosphate decarboxylase. Biochemistry 51:5611–5621 [View Article][PubMed]
    [Google Scholar]
  4. Bernard K. A., Shuttleworth L., Munro C., Forbes-Faulkner J. C., Pitt D., Norton J. H., Thomas A. D. 2002; Propionibacterium australiense sp. nov. Derived from Granulomatous Bovine Lesions. Anaerobe 8:41–47 [View Article]
    [Google Scholar]
  5. Brüggemann H., Henne A., Hoster F., Liesegang H., Wiezer A., Strittmatter A., Hujer S., Dürre P., Gottschalk G. 2004; The complete genome sequence of Propionibacterium acnes, a commensal of human skin. Science 305:671–673 [View Article][PubMed]
    [Google Scholar]
  6. Butler-Wu S. M., Sengupta D. J., Kittichotirat W., Matsen F. A., Bumgarner R. E. 2011; Genome sequence of a novel species, Propionibacterium humerusii. J Bacteriol 193:3678 [View Article][PubMed]
    [Google Scholar]
  7. Camacho C., Coulouris G., Avagyan V., Ma N., Papadopoulos J., Bealer K., Madden T. L. 2009; blast+: architecture and applications. BMC Bioinformatics 10:421 [View Article][PubMed]
    [Google Scholar]
  8. Charfreitag O., Collins M. D., Stackebrandt E. 1988; Reclassification of Arachnia propionica as Propionibacterium propionicus comb. nov. Int J Syst Evol Microbiol 38:354–357 [View Article]
    [Google Scholar]
  9. Charfreitag O., Stackebrandt E. 1989; Inter- and intrageneric relationships of the genus Propionibacterium as determined by 16S rRNA sequences. J Gen Microbiol 135:2065–2070 [View Article][PubMed]
    [Google Scholar]
  10. Dalmasso M., Nicolas P., Falentin H., Valence F., Tanskanen J., Jatila H., Salusjärvi T., Thierry A. 2011; Multilocus sequence typing of Propionibacterium freudenreichii. Int J Food Microbiol 145:113–120 [View Article][PubMed]
    [Google Scholar]
  11. Dasen G., Smutny J., Teuber M., Meile L. 1998; Classification and identification of propionibacteria based on ribosomal RNA genes and PCR. Syst Appl Microbiol 21:251–259 [View Article][PubMed]
    [Google Scholar]
  12. de Freitas R., Madec M.-N., Chuat V., Maillard M.-B., Mukdsi M. C., Falentin H., de Carvalho A. F., Valence F., Thierry A. 2015; New insights about phenotypic heterogeneity within Propionibacterium freudenreichii argue against its division into subspecies. Dairy Sci Technol 95:465–477 [View Article][PubMed]
    [Google Scholar]
  13. Dekio I., Culak R., Misra R., Gaulton T., Fang M., Sakamoto M., Ohkuma M., Oshima K., Hattori M. et al. 2015; Dissecting the taxonomic heterogeneity within Propionibacterium acnes: proposal for Propionibacterium acnes subsp. acnes subsp. nov. and Propionibacterium acnes subsp. elongatum subsp. nov. Int J Syst Evol Microbiol 65:4776–4787 [View Article][PubMed]
    [Google Scholar]
  14. Downes J., Wade W. G. 2009; Propionibacterium acidifaciens sp. nov., isolated from the human mouth. Int J Syst Evol Microbiol 59:2778–2781 [View Article][PubMed]
    [Google Scholar]
  15. Droettboom M., Hunter J., Firing E., Caswell T. A., Elson P., Dale D., Lee J. J., McDougall D., Root B. et al. 2015 matplotlib: v1.4.3
    [Google Scholar]
  16. Edgar R. C. 2004; muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797 [View Article][PubMed]
    [Google Scholar]
  17. Francisco C. C., Chamberlain C. S., Waldner D. N., Wettemann R. P., Spicer L. J. 2002; Propionibacteria fed to dairy cows: effects on energy balance, plasma metabolites and hormones, and reproduction. J Dairy Sci 85:1738–1751 [View Article][PubMed]
    [Google Scholar]
  18. Giraud M.-F., Naismith J. H. 2000; The rhamnose pathway. Curr Opin Struct Biol 10:687–696 [View Article][PubMed]
    [Google Scholar]
  19. Goodfellow M., Whitman W. B., Bergey D. H. 2012 Bergey’s Manual of Systematic Bacteriology: Volume 5, The Actinobacteria, 2 edn. New York, NY: Springer; [CrossRef]
    [Google Scholar]
  20. Kanehisa M., Goto S., Sato Y., Kawashima M., Furumichi M., Tanabe M. 2014; Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res 42:D199–D205 [View Article][PubMed]
    [Google Scholar]
  21. Kilian M., Scholz C. F., Lomholt H. B. 2012; Multilocus sequence typing and phylogenetic analysis of Propionibacterium acnes. J Clin Microbiol 50:1158–1165 [View Article][PubMed]
    [Google Scholar]
  22. Koussémon M., Combet-Blanc Y., Patel B. K., Cayol J. L., Thomas P., Garcia J. L., Ollivier B. 2001; Propionibacterium microaerophilum sp. nov., a microaerophilic bacterium isolated from olive mill wastewater. Int J Syst Evol Microbiol 51:1373–1382 [View Article][PubMed]
    [Google Scholar]
  23. Kumar S., Stecher G., Tamura K. 2016; mega7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874 [View Article][PubMed]
    [Google Scholar]
  24. Kusano K., Yamada H., Niwa M., Yamasato K. 1997; Propionibacterium cyclohexanicum sp. nov., a new acid-tolerant ω-cyclohexyl fatty acid-containing Propionibacterium isolated from spoiled orange juice. Int J Syst Evol Microbiol 47:825–831 [View Article]
    [Google Scholar]
  25. Lomholt H. B., Kilian M. 2010; Population genetic analysis of Propionibacterium acnes identifies a subpopulation and epidemic clones associated with acne. PLoS One 5:e12277 [View Article][PubMed]
    [Google Scholar]
  26. Loux V., Mariadassou M., Almeida S., Chiapello H., Hammani A., Buratti J., Gendrault A., Barbe V., Aury J.-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]
    [Google Scholar]
  27. Lucena-Padrós H., González J. M., Caballero-Guerrero B., Ruiz-Barba J. L., Maldonado-Barragán A. 2014; Propionibacterium olivae sp. nov. and Propionibacterium damnosum sp. nov., isolated from spoiled packaged Spanish-style green olives. Int J Syst Evol Microbiol 64:2980–2985 [View Article][PubMed]
    [Google Scholar]
  28. Martin I., Débarbouillé M., Ferrari E., Klier A., Rapoport G. 1987; Characterization of the levanase gene of Bacillus subtilis which shows homology to yeast invertase. Mol Gen Genet 208:177–184 [View Article][PubMed]
    [Google Scholar]
  29. McDowell A., Valanne S., Ramage G., Tunney M. M., Glenn J. V., McLorinan G. C., Bhatia A., Maisonneuve J. F., Lodes M. et al. 2005; Propionibacterium acnes types I and II represent phylogenetically distinct groups. J Clin Microbiol 43:326–334 [View Article][PubMed]
    [Google Scholar]
  30. McDowell A., Perry A. L., Lambert P. A., Patrick S. 2008; A new phylogenetic group of Propionibacterium acnes. J Med Microbiol 57:218–224 [View Article][PubMed]
    [Google Scholar]
  31. Mollerup S., Friis-Nielsen J., Vinner L., Hansen T. A., Richter S. R., Fridholm H., Herrera J. A., Lund O., Brunak S. 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]
    [Google Scholar]
  32. Orla-Jensen S. 1909; Die hauptlinien der natürlichen bakterienssystems. Zentralbl bakteriol parasitenk infektionskr Hyg Abt 2:305–346
    [Google Scholar]
  33. Peng M., Smith A. H., Rehberger T. 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]
    [Google Scholar]
  34. Skerman V. B. D., McGowan V., Sneath P. H. A. 1980; Approved lists of bacterial names. Int J Syst Evol Microbiol 30:225–420 [View Article]
    [Google Scholar]
  35. Stackebrandt E., Schumann P., Schaal K. P., Weiss N. 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]
    [Google Scholar]
  36. Stackebrandt E., Cummins C. S., Johnson J. L. 2006; Family Propionibacteriaceae: The genus Propionibacterium. In The Prokaryotes pp. 400–418 Edited by Dworkin M., Falkow S., Rosenberg E., Schleifer K.-H., Stackebrandt E. New York: Springer; [CrossRef]
    [Google Scholar]
  37. Suzuki M., Chatterton N. J. 1993 Science and Technology of Fructans Florida, USA: CRC Press;
    [Google Scholar]
  38. Thierry A., Deutsch S.-M., Falentin H., Dalmasso M., Cousin F. J., Jan G. 2011; New insights into physiology and metabolism of Propionibacterium freudenreichii. Int J Food Microbiol 149:19–27 [View Article][PubMed]
    [Google Scholar]
  39. Williams H. C., Dellavalle R. P., Garner S. 2012; Acne vulgaris. Lancet 379:361–372 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.001367
Loading
/content/journal/ijsem/10.1099/ijsem.0.001367
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error