Skip to content
1887

Abstract

is a bacterial skin commensal that is often isolated during routine testing of blood products like platelet concentrates (PCs). Due to the slow-growing nature of this bacterium in culture media, contaminated PCs are often transfused into vulnerable patients before retrieval of these units can be initiated. This study aimed at obtaining the whole-genome sequence of six isolates derived from contaminated PCs, comparing and assessing their genetic backgrounds. Furthermore, the whole genomes of the PC isolates were compared to clinical isolates obtained from different sites and types of infection. The results indicate that these PC isolates assessed belong to four phylotypes, namely IA, IB, II and III. Whole-genome comparisons identified differences in the virulence profiles of the isolates and provide a foundation for future studies aimed at evaluating the risk to transfusion patients by determining whether the expression of virulence factors is impacted in the PC storage environment.

Funding
This study was supported by the:
  • Health Canada
    • Principle Award Recipient: NotApplicable
  • Canadian Blood Services
    • Principle Award Recipient: NotApplicable
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/acmi/10.1099/acmi.0.000938.v3
2025-04-08
2025-04-21
Loading full text...

Full text loading...

/deliver/fulltext/acmi/7/4/acmi000938.v3.html?itemId=/content/journal/acmi/10.1099/acmi.0.000938.v3&mimeType=html&fmt=ahah

References

  1. Callum JL, Yeh CH, Petrosoniak A, McVey MJ, Cope S et al. A regional massive hemorrhage protocol developed through a modified Delphi technique. CMAJ Open 2019; 7:E546–E561 [View Article] [PubMed]
    [Google Scholar]
  2. Panuganti S, Schlinker AC, Lindholm PF, Papoutsakis ET, Miller WM. Three-stage ex vivo expansion of high-ploidy megakaryocytic cells: toward large-scale platelet production. Tissue Eng Part A 2013; 19:998–1014 [View Article] [PubMed]
    [Google Scholar]
  3. Suddock JT, Crookston KP. Transfusion reactions. Pubmed. Treasure Island (FL): StatPearls Publishing; 2023 https://pubmed.ncbi.nlm.nih.gov/29489247/#:~:text=The%20most%20common%20signs%20and accessed 3 March 2024
  4. Ramírez‐Arcos S, Goldman M. Bacterial contamination. In Practical Transfusion Medicine 2017 pp 168–175 [View Article]
    [Google Scholar]
  5. Hillyer CD, Josephson CD, Blajchman MA, Vostal JG, Epstein JS et al. Bacterial contamination of blood components: risks, strategies, and regulation: joint ASH and AABB educational session in transfusion medicine. Hematology Am Soc Hematol Educ Program 2003; 2003:575–589 [View Article] [PubMed]
    [Google Scholar]
  6. Ramirez-Arcos S, DiFranco C, McIntyre T, Goldman M. Residual risk of bacterial contamination of platelets: six years of experience with sterility testing. Transfusion 2017; 57:2174–2181 [View Article] [PubMed]
    [Google Scholar]
  7. Störmer M, Kleesiek K, Dreier J. Propionibacterium acnes lacks the capability to proliferate in platelet concentrates. Vox Sang 2008; 94:193–201 [View Article] [PubMed]
    [Google Scholar]
  8. Jacobs MR, Good CE, Lazarus HM, Yomtovian RA. Relationship between bacterial load, species virulence, and transfusion reaction with transfusion of bacterially contaminated platelets. Clin Infect Dis 2008; 46:1214–1220 [View Article] [PubMed]
    [Google Scholar]
  9. Lodhi SH, Abbasi A, Ahmed T, Chan A. Acne on the valve: two intriguing cases of Cutibacterium acnes endocarditis. Cureus 2020; 12:e8532 [View Article] [PubMed]
    [Google Scholar]
  10. Boisrenoult P. Cutibacterium acnes prosthetic joint infection: diagnosis and treatment. OTSR 2018; 104:S19–S24 [View Article]
    [Google Scholar]
  11. Schmid B, Hausmann O, Hitzl W, Achermann Y, Wuertz-Kozak K. The role of Cutibacterium acnes in intervertebral disc inflammation. Biomedicines 2020; 8:186 [View Article] [PubMed]
    [Google Scholar]
  12. Pietropaoli C, Cavalli Z, Jouanneau E, Tristan A, Conrad A et al. Cerebral empyema and abscesses due to Cutibacterium acnes. Med Mal Infect 2020; 50:274–279 [View Article] [PubMed]
    [Google Scholar]
  13. Davidsson S, Mölling P, Rider JR, Unemo M, Karlsson MG et al. Frequency and typing of Propionibacterium acnes in prostate tissue obtained from men with and without prostate cancer. Infect Agents Cancer 2016; 11: [View Article]
    [Google Scholar]
  14. Chen S, Zhou Y, Chen Y, Gu J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 2018; 34:i884–i890 [View Article] [PubMed]
    [Google Scholar]
  15. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017; 13:e1005595 [View Article] [PubMed]
    [Google Scholar]
  16. Wick RR, Holt KE. Polypolish: short-read polishing of long-read bacterial genome assemblies. PLoS Comput Biol 2022; 18:e1009802 [View Article] [PubMed]
    [Google Scholar]
  17. Barnard E, Nagy I, Hunyadkürti J, Patrick S, McDowell A. Multiplex touchdown PCR for rapid typing of the opportunistic pathogen Propionibacterium acnes. J Clin Microbiol 2015; 53:1149–1155 [View Article] [PubMed]
    [Google Scholar]
  18. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article] [PubMed]
    [Google Scholar]
  19. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J et al. BLAST+: architecture and applications. BMC Bioinf 2009; 10:421 [View Article] [PubMed]
    [Google Scholar]
  20. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 2013; 30:2725–2729 [View Article] [PubMed]
    [Google Scholar]
  21. Li H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 2018; 34:3094–3100 [View Article] [PubMed]
    [Google Scholar]
  22. Ankenbrand MJ, Hohlfeld S, Hackl T, Förster F. AliTV—interactive visualization of whole genome comparisons. PeerJ Comput Sci 2017; 3:e116 [View Article]
    [Google Scholar]
  23. Feldgarden M, Brover V, Gonzalez-Escalona N, Frye JG, Haendiges J et al. AMRFinderPlus and the Reference Gene Catalog facilitate examination of the genomic links among antimicrobial resistance, stress response, and virulence. Sci Rep 2021; 11:12728 [View Article] [PubMed]
    [Google Scholar]
  24. Chen LJ, Yang J, Yu Z, Yao L, Sun Y. VFDB: a reference database for bacterial virulence factors. Nucleic Acids Research 2004; 33:D325–D328 [View Article]
    [Google Scholar]
  25. Treangen TJ, Ondov BD, Koren S, Phillippy AM. The Harvest suite for rapid core-genome alignment and visualization of thousands of intraspecific microbial genomes. Genome Biol 2014; 15:524 [View Article] [PubMed]
    [Google Scholar]
  26. O’Neill AM, Cavagnero KJ, Seidman JS, Zaramela L, Chen Y et al. Genetic and functional analyses of Cutibacterium acnes isolates reveal the association of a linear plasmid with skin inflammation. J Invest Dermatol 2024; 144:116–124 [View Article] [PubMed]
    [Google Scholar]
  27. Koizumi J, Nakase K, Nakaminami H. Identification of a transferable linear plasmid carrying the macrolide-clindamycin resistance gene erm (X) in a Cutibacterium acnes isolate from a patient with acne vulgaris in Japan. Microbiol Resour Announc 2022; 11:e0009422 [View Article] [PubMed]
    [Google Scholar]
  28. Kumaran D, Ramirez-Arcos S. Sebum components dampen the efficacy of skin disinfectants against Cutibacterium acnes biofilms. Microorganisms 2024; 12:271 [View Article] [PubMed]
    [Google Scholar]
  29. Both A, Huang J, Hentschke M, Tobys D, Christner M et al. Genomics of invasive Cutibacterium acnes isolates from deep-seated infections. Microbiol Spectr 2023; 11:e0474022 [View Article] [PubMed]
    [Google Scholar]
  30. Mayslich C, Grange PA, Dupin N. Cutibacterium acnes as an opportunistic pathogen: an update of its virulence-associated factors. Microorganisms 2021; 9:303 [View Article] [PubMed]
    [Google Scholar]
  31. Loza-Correa M, Yousuf B, Ramirez-Arcos S. Staphylococcus epidermidis undergoes global changes in gene expression during biofilm maturation in platelet concentrates. Transfusion 2021; 61:2146–2158 [View Article] [PubMed]
    [Google Scholar]
  32. Chi SI, Ramirez-Arcos S. Staphylococcal enterotoxins enhance biofilm formation by Staphylococcus aureus in platelet concentrates. Microorganisms 2022; 11:89 [View Article] [PubMed]
    [Google Scholar]
  33. Kasimatis G, Fitz-Gibbon S, Tomida S, Wong M, Li H. Analysis of complete genomes of Propionibacterium acnes reveals a novel plasmid and increased pseudogenes in an acne associated strain. Biomed Res Int 2013; 2013:918320 [View Article] [PubMed]
    [Google Scholar]
  34. Irvine S, Bunk B, Bayes HK, Spröer C, Connolly JPR et al. Genomic and transcriptomic characterization of Pseudomonas aeruginosa small colony variants derived from a chronic infection model. Microb Genom 2019; 5:e000262 [View Article] [PubMed]
    [Google Scholar]
  35. Hou X, Wang M, Wen Y, Ni T, Guan X et al. Quinone skeleton as a new class of irreversible inhibitors against Staphylococcus aureus sortase A. Bioorg Med Chem Lett 2018; 28:1864–1869 [View Article]
    [Google Scholar]
  36. Zhu H, Lee C, Zhang D, Wu W, Wang L et al. Surface-associated GroEL facilitates the adhesion of Escherichia coli to macrophages through lectin-like oxidized low-density lipoprotein receptor-1. Microbes Infect 2013; 15:172–180 [View Article] [PubMed]
    [Google Scholar]
  37. Nanra JS, Buitrago SM, Crawford S, Ng J, Fink PS et al. Capsular polysaccharides are an important immune evasion mechanism for Staphylococcus aureus. Hum Vaccin Immunother 2013; 9:480–487 [View Article] [PubMed]
    [Google Scholar]
  38. Cerca N, Jefferson KK, Oliveira R, Pier GB, Azeredo J. Comparative antibody-mediated phagocytosis of Staphylococcus epidermidis cells grown in a biofilm or in the planktonic state. Infect Immun 2006; 74:4849–4855 [View Article] [PubMed]
    [Google Scholar]
  39. Pasquali F, Palma F, Guillier L, Lucchi A, De Cesare A et al. Listeria monocytogenes sequence types 121 and 14 repeatedly isolated within one year of sampling in a rabbit meat processing plant: persistence and ecophysiology. Front Microbiol 2018; 9:596 [View Article] [PubMed]
    [Google Scholar]
  40. Dutta V, Elhanafi D, Kathariou S. Conservation and distribution of the benzalkonium chloride resistance cassette bcrABC in Listeria monocytogenes. Appl Environ Microbiol 2013; 79:6067–6074 [View Article] [PubMed]
    [Google Scholar]
  41. Camejo A, Buchrieser C, Couvé E, Carvalho F, Reis O et al. In vivo transcriptional profiling of Listeria monocytogenes and mutagenesis identify new virulence factors involved in infection. PLoS Pathog 2009; 5:e1000449 [View Article] [PubMed]
    [Google Scholar]
  42. Huemer M, Mairpady Shambat S, Brugger SD, Zinkernagel AS. Antibiotic resistance and persistence-Implications for human health and treatment perspectives. EMBO Rep 2020; 21:e51034 [View Article] [PubMed]
    [Google Scholar]
  43. Ladomersky E, Petris MJ. Copper tolerance and virulence in bacteria. Metallomics 2015; 7:957–964 [View Article] [PubMed]
    [Google Scholar]
  44. Khasheii B, Mahmoodi P, Mohammadzadeh A. Siderophores: importance in bacterial pathogenesis and applications in medicine and industry. Microbiol Res 2021; 250:126790 [View Article] [PubMed]
    [Google Scholar]
  45. M. Daly K, D. Cotter P, Hill C, Paul Ross R. Lantibiotic production by pathogenic microorganisms. Curr Protein Pept Sci 2012; 13:509–523 [View Article]
    [Google Scholar]
  46. Matilla MA, Krell T. The effect of bacterial chemotaxis on host infection and pathogenicity. FEMS Microbiol Rev 2018; 42: [View Article]
    [Google Scholar]
  47. Chalker AF, Ingraham KA, Lunsford RD, Bryant AP, Bryant J et al. The bacA gene, which determines bacitracin susceptibility in Streptococcus pneumoniae and Staphylococcus aureus, is also required for virulence The GenBank accession number for the sequence reported in this paper is AF228662. Microbiology 2000; 146:1547–1553 [View Article]
    [Google Scholar]
  48. Irsch J, Lin L. Pathogen inactivation of platelet and plasma blood components for transfusion using the INTERCEPT Blood SystemTM. Transfus Med Hemother 2011; 38:19–31 [View Article] [PubMed]
    [Google Scholar]
  49. Kumaran D, Ramirez-Arcos S. Nutrient supplementation of culture media improves the detection of Cutibacterium acnes in platelet components by an automated culture system. Vox Sang 2023; 118:930–937 [View Article] [PubMed]
    [Google Scholar]
/content/journal/acmi/10.1099/acmi.0.000938.v3
Loading
/content/journal/acmi/10.1099/acmi.0.000938.v3
Loading

Data & Media loading...

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