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Volume 6, Issue 4

Comparative virulome analysis of four strains from human skin and platelet concentrates using whole genome sequencing Open Access

Graphical Abstract

Graphical Abstract

Virulome profile of four strains isolated from platelet concentrates and human skin.

Abstract

is one of the predominant bacterial contaminants in platelet concentrates (PCs), a blood component used to treat bleeding disorders. PCs are a unique niche that triggers biofilm formation, the main pathomechanism of infections. We performed whole genome sequencing of four strains isolated from skin of healthy human volunteers (AZ22 and AZ39) and contaminated PCs (ST10002 and ST11003) to unravel phylogenetic relationships and decipher virulence mechanisms compared to 24 complete genomes in GenBank. AZ39 and ST11003 formed a separate unique lineage with strains 14.1 .R1 and SE95, while AZ22 formed a cluster with 1457 and ST10002 closely grouped with FDAAGOS_161. The four isolates were assigned to sequence types ST1175, ST1174, ST73 and ST16, respectively. All four genomes exhibited biofilm-associated genes , , , and . Additionally, AZ22 had and , whereas ST10002 had and . Notably, AZ39 possesses truncated and and harbours a toxin-encoding gene. All isolates carry multiple antibiotic resistance genes conferring resistance to fosfomycin (), β-lactams () and fluoroquinolones (). This study reveales a unique lineage for and provides insight into the genetic basis of virulence and antibiotic resistance in transfusion-associated strains.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): biofilm , phylogeny , platelet concentrates , Staphylococcus epidermidis , virulome and whole genome sequencing
Funding
This study was supported by the:
  • Health Canada
    • Principle Award Recipient: SandraRamirez-Arcos
  • Canadian Blood Services
    • Principle Award Recipient: SandraRamirez-Arcos
© 2024 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2024-04-03
2024-04-30
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References

  1. Byrd AL, Belkaid Y, Segre JA. The human skin microbiome. Nat Rev Microbiol 2018; 16:143–155 [View Article] [PubMed]
     [Google Scholar]
  2. National Nosocomial Infections Surveillance System National Nosocomial Infections Surveillance (NNIS) System Report, data summary from January 1992 through June 2004, issued October 2004. Am J Infect Control 2004; 32:470–485 [View Article] [PubMed]
     [Google Scholar]
  3. Kou Y, Pagotto F, Hannach B, Ramirez-Arcos S. Fatal false-negative transfusion infection involving a buffy coat platelet pool contaminated with biofilm-positive Staphylococcus epidermidis: a case report. Transfusion 2015; 55:2384–2389 [View Article] [PubMed]
     [Google Scholar]
  4. Walther-Wenke G, Schrezenmeier H, Deitenbeck R, Geis G, Burkhart J et al. Screening of platelet concentrates for bacterial contamination: spectrum of bacteria detected, proportion of transfused units, and clinical follow-up. Ann Hematol 2010; 89:83–91 [View Article] [PubMed]
     [Google Scholar]
  5. Hong H, Xiao W, Lazarus HM, Good CE, Maitta RW et al. Detection of septic transfusion reactions to platelet transfusions by active and passive surveillance. Blood 2016; 127:496–502 [View Article] [PubMed]
     [Google Scholar]
  6. Ramirez-Arcos S, Goldman MC. Bacterial contamination of platelet components. AABB Trans React 2021115–164 [View Article]
     [Google Scholar]
  7. 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]
  8. Perez K, Patel R. Survival of Staphylococcus epidermidis in Fibroblasts and Osteoblasts. In Freitag NE. eds Infection and Immunity vol 86 2018 [View Article] [PubMed]
     [Google Scholar]
  9. Greco C, Mastronardi C, Pagotto F, Mack D, Ramirez-Arcos S. Assessment of biofilm-forming ability of coagulase-negative staphylococci isolated from contaminated platelet preparations in Canada. Transfusion 2008; 48:969–977 [View Article] [PubMed]
     [Google Scholar]
  10. Greco C, Martincic I, Gusinjac A, Kalab M, Yang A-F et al. Staphylococcus epidermidis forms biofilms under simulated platelet storage conditions. Transfusion 2007; 47:1143–1153 [View Article] [PubMed]
     [Google Scholar]
  11. Rogers KL, Rupp ME, Fey PD. The presence of icaADBC is detrimental to the colonization of human skin by Staphylococcus epidermidis . Appl Environ Microbiol 2008; 74:6155–6157 [View Article] [PubMed]
     [Google Scholar]
  12. Rohde H, Burdelski C, Bartscht K, Hussain M, Buck F et al. Induction of Staphylococcus epidermidis biofilm formation via proteolytic processing of the accumulation-associated protein by staphylococcal and host proteases. Mol Microbiol 2005; 55:1883–1895 [View Article] [PubMed]
     [Google Scholar]
  13. Christner M, Franke GC, Schommer NN, Wendt U, Wegert K et al. The giant extracellular matrix-binding protein of Staphylococcus epidermidis mediates biofilm accumulation and attachment to fibronectin. Mol Microbiol 2010; 75:187–207 [View Article] [PubMed]
     [Google Scholar]
  14. Schommer NN, Christner M, Hentschke M, Ruckdeschel K, Aepfelbacher M et al. Staphylococcus epidermidis uses distinct mechanisms of biofilm formation to interfere with phagocytosis and activation of mouse macrophage-like cells 774A.1. In Bliska JB. eds Infection and Immunity vol 79 2011 pp 2267–2276 [View Article] [PubMed]
     [Google Scholar]
  15. Qin Z, Ou Y, Yang L, Zhu Y, Tolker-Nielsen T et al. Role of autolysin-mediated DNA release in biofilm formation of Staphylococcus epidermidis . Microbiology 2007; 153:2083–2092 [View Article] [PubMed]
     [Google Scholar]
  16. Stevens NT, Tharmabala M, Dillane T, Greene CM, O’Gara JP et al. Biofilm and the role of the ICA operon and AAP in Staphylococcus epidermidis isolates causing neurosurgical meningitis. Clin Microbiol Infect 2008; 14:719–722 [View Article] [PubMed]
     [Google Scholar]
  17. Hodgson SD, Greco-Stewart V, Jimenez CS, Sifri CD, Brassinga AKC et al. Enhanced pathogenicity of biofilm-negative Staphylococcus epidermidis isolated from platelet preparations. Transfusion 2014; 54:461–470 [View Article] [PubMed]
     [Google Scholar]
  18. Alabdullatif M, Atreya CD, Ramirez-Arcos S. Antimicrobial peptides: an effective approach to prevent bacterial biofilm formation in platelet concentrates. Transfusion 2018; 58:2013–2021 [View Article] [PubMed]
     [Google Scholar]
  19. Loza-Correa M, Ayala JA, Perelman I, Hubbard K, Kalab M et al. The peptidoglycan and biofilm matrix of Staphylococcus epidermidis undergo structural changes when exposed to human platelets. In Das S. eds PLoS One vol 14 2019 p e0211132 [View Article] [PubMed]
     [Google Scholar]
  20. 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]
  21. Miragaia M, Thomas JC, Couto I, Enright MC, de Lencastre H. Inferring a population structure for Staphylococcus epidermidis from multilocus sequence typing data. J Bacteriol 2007; 189:2540–2552 [View Article] [PubMed]
     [Google Scholar]
  22. Lee JYH, Monk IR, Gonçalves da Silva A, Seemann T, Chua KYL et al. Global spread of three multidrug-resistant lineages of Staphylococcus epidermidis . Nat Microbiol 2018; 3:1175–1185 [View Article] [PubMed]
     [Google Scholar]
  23. Bouchami O, de Lencastre H, Miragaia M. Impact of Insertion Sequences and Recombination on the Population Structure of Staphylococcus haemolyticus. In Schaik van W. eds PLoS One vol 11 2016 p e0156653 [View Article] [PubMed]
     [Google Scholar]
  24. Rolo J, Worning P, Nielsen JB, Bowden R, Bouchami O et al. Evolutionary origin of the Staphylococcal cassette Chromosome MEC (SCC MEC). Antimicrob Agents Chemother 2017; 61: [View Article]
     [Google Scholar]
  25. Onishi M, Urushibara N, Kawaguchiya M, Ghosh S, Shinagawa M et al. Prevalence and genetic diversity of arginine catabolic mobile element (ACME) in clinical isolates of coagulase-negative staphylococci: identification of ACME type I variants in Staphylococcus epidermidis . Infect Genet Evol 2013; 20:381–388 [View Article] [PubMed]
     [Google Scholar]
  26. O’Connor AM, McManus BA, Kinnevey PM, Brennan GI, Fleming TE et al. Significant enrichment and diversity of the Staphylococcal arginine catabolic mobile element ACME in Staphylococcus epidermidis isolates from subgingival peri-implantitis sites and periodontal pockets. Front Microbiol 2018; 9:1558 [View Article] [PubMed]
     [Google Scholar]
  27. Taha M, Kohnen C, Mallya S, Kou Y, Zapata A et al. Comparative characterisation of the biofilm-production abilities of Staphylococcus epidermidis isolated from human skin and platelet concentrates. J Med Microbiol 2018; 67:190–197 [View Article] [PubMed]
     [Google Scholar]
  28. 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]
  29. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: Resolving bacterial genome assemblies from short and long sequencing reads. In Phillippy AM. eds PLOS Computational Biology vol 13 2017 p e1005595 [View Article] [PubMed]
     [Google Scholar]
  30. Kolmogorov M, Yuan J, Lin Y, Pevzner PA. Assembly of long, error-prone reads using repeat graphs. Nat Biotechnol 2019; 37:540–546 [View Article] [PubMed]
     [Google Scholar]
  31. Wick RR, Holt KE. Benchmarking of long-read assemblers for prokaryote whole genome sequencing. F1000Res 2019; 8:2138 [View Article] [PubMed]
     [Google Scholar]
  32. Ruan J, Li H. Fast and accurate long-read assembly with wtdbg2. Nat Methods 2020; 17:155–158 [View Article] [PubMed]
     [Google Scholar]
  33. Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One 2014; 9:e112963 [View Article] [PubMed]
     [Google Scholar]
  34. 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]
  35. 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]
  36. Grissa I, Vergnaud G, Pourcel C. CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res 2007; 35:W52–W57 [View Article] [PubMed]
     [Google Scholar]
  37. Alcock BP, Raphenya AR, Lau TTY, Tsang KK, Bouchard M et al. CARD 2020: antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Res 2020; 48:D517–D525 [View Article] [PubMed]
     [Google Scholar]
  38. Arndt D, Grant JR, Marcu A, Sajed T, Pon A et al. PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res 2016; 44:W16–W21 [View Article] [PubMed]
     [Google Scholar]
  39. Chen L, Zheng D, Liu B, Yang J, Jin Q. VFDB 2016: hierarchical and refined dataset for big data analysis--10 years on. Nucleic Acids Res 2016; 44:D694–D697 [View Article] [PubMed]
     [Google Scholar]
  40. Herbig A, Nieselt K. nocoRNAc: characterization of non-coding RNAs in prokaryotes. BMC Bioinformatics 2011; 12:1–13 [View Article] [PubMed]
     [Google Scholar]
  41. Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP et al. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 2016; 44:6614–6624 [View Article] [PubMed]
     [Google Scholar]
  42. Jolley KA, Bray JE, Maiden MCJ. Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications. Wellcome Open Res 2018; 3:124 [View Article] [PubMed]
     [Google Scholar]
  43. Thomas JC, Vargas MR, Miragaia M, Peacock SJ, Archer GL et al. Improved multilocus sequence typing scheme for Staphylococcus epidermidis . J Clin Microbiol 2007; 45:616–619 [View Article] [PubMed]
     [Google Scholar]
  44. Rosenstein R, Götz F. What distinguishes highly pathogenic Staphylococci from medium- and non-pathogenic?. In Between Pathogenicity and Commensalism Berlin Heidelberg: Springer; 2012 pp 33–89 [View Article] [PubMed]
     [Google Scholar]
  45. Raue S, Fan S-H, Rosenstein R, Zabel S, Luqman A et al. The genome of Staphylococcus epidermidis O47. Front Microbiol 2020; 11: [View Article]
     [Google Scholar]
  46. Schoenfelder SMK, Lange C, Prakash SA, Marincola G, Lerch MF et al. The small non-coding RNA RsaE influences extracellular matrix composition in Staphylococcus epidermidis biofilm communities. PLoS Pathog 2019; 15:e1007618 [View Article] [PubMed]
     [Google Scholar]
  47. Marraffini LA, Sontheimer EJ. CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science 2008; 322:1843–1845 [View Article] [PubMed]
     [Google Scholar]
  48. Cave R, Misra R, Chen J, Wang S, Mkrtchyan HV. Comparative genomics analysis demonstrated a link between Staphylococci isolated from different sources: a possible public health risk. Front Microbiol 2021; 12:576696 [View Article] [PubMed]
     [Google Scholar]
  49. Büttner H, Mack D, Rohde H. Structural basis of Staphylococcus epidermidis biofilm formation: mechanisms and molecular interactions. Front Cell Infect Microbiol 2015; 5:14 [View Article] [PubMed]
     [Google Scholar]
  50. Foster TJ. Surface proteins of Staphylococcus epidermidis . Front Microbiol 2020; 11: [View Article]
     [Google Scholar]
  51. Zhang Y-Q, Ren S-X, Li H-L, Wang Y-X, Fu G et al. Genome-based analysis of virulence genes in a non-biofilm-forming Staphylococcus epidermidis strain (ATCC 12228). Mol Microbiol 2003; 49:1577–1593 [View Article] [PubMed]
     [Google Scholar]
  52. Galac MR, Stam J, Maybank R, Hinkle M, Mack D et al. Complete genome sequence of Staphylococcus epidermidis 1457. Genome Announc 2017; 5:e00450-17 [View Article] [PubMed]
     [Google Scholar]
  53. Le KY, Park MD, Otto M. Immune evasion mechanisms of Staphylococcus epidermidis biofilm infection. Front Microbiol 2018; 9:359 [View Article] [PubMed]
     [Google Scholar]
  54. Cao Z, Casabona MG, Kneuper H, Chalmers JD, Palmer T. The type VII secretion system of Staphylococcus aureus secretes a nuclease toxin that targets competitor bacteria. Nat Microbiol 2016; 2:16183 [View Article] [PubMed]
     [Google Scholar]
  55. Bowman L, Palmer T. The type VII secretion system of Staphylococcus . Annu Rev Microbiol 2021; 75:471–494
     [Google Scholar]
  56. Lassen SB, Lomholt HB, Brüggemann H. Complete genome sequence of a Staphylococcus epidermidis strain with exceptional antimicrobial activity. Genome Announc 2017; 5:e00004-17 [View Article] [PubMed]
     [Google Scholar]
  57. Argemi X, Nanoukon C, Affolabi D, Keller D, Hansmann Y et al. Comparative genomics and identification of an enterotoxin-bearing pathogenicity Island, SEPI-1/SECI-1, in Staphylococcus epidermidis pathogenic strains. Toxins 2018; 10:93 [View Article] [PubMed]
     [Google Scholar]
  58. Schilcher K, Horswill AR. Staphylococcal biofilm development: structure, regulation, and treatment strategies. Microbiol Mol Biol Rev 2020; 84:e00026-19 [View Article] [PubMed]
     [Google Scholar]
  59. Brunskill EW, Bayles KW. Identification and molecular characterization of a putative regulatory locus that affects autolysis in Staphylococcus aureus . J Bacteriol 1996; 178:611–618 [View Article] [PubMed]
     [Google Scholar]
  60. Cheung GYC, Rigby K, Wang R, Queck SY, Braughton KR et al. Staphylococcus epidermidis strategies to avoid killing by human neutrophils. PLoS Pathog 2010; 6:e1001133 [View Article] [PubMed]
     [Google Scholar]
  61. Cheung GYC, Joo H-S, Chatterjee SS, Otto M. Phenol-soluble modulins--critical determinants of staphylococcal virulence. FEMS Microbiol Rev 2014; 38:698–719 [View Article] [PubMed]
     [Google Scholar]
  62. Otto M. Phenol-soluble modulins. Int J Med Microbiol 2014; 304:164–169 [View Article] [PubMed]
     [Google Scholar]
  63. Le KY, Villaruz AE, Zheng Y, He L, Fisher EL et al. Role of phenol-soluble modulins in Staphylococcus epidermidis biofilm formation and infection of indwelling medical devices. J Mol Biol 2019; 431:3015–3027 [View Article] [PubMed]
     [Google Scholar]
  64. Nanoukon C, Affolabi D, Keller D, Tollo R, Riegel P et al. Characterization of human type C enterotoxin produced by clinical S. epidermidis isolates. Toxins (Basel) 2018; 10:139 [View Article] [PubMed]
     [Google Scholar]
  65. Li M, Lai Y, Villaruz AE, Cha DJ, Sturdevant DE et al. Gram-positive three-component antimicrobial peptide-sensing system. Proc Natl Acad Sci U S A 2007; 104:9469–9474 [View Article] [PubMed]
     [Google Scholar]
  66. Joo HS, Otto M. Mechanisms of resistance to antimicrobial peptides in staphylococci. Biochim Biophys Acta 2015; 1848:3055–3061 [View Article] [PubMed]
     [Google Scholar]
  67. Liu Q, Liu Q, Meng H, Lv H, Liu Y et al. Staphylococcus epidermidis contributes to healthy maturation of the nasal microbiome by stimulating antimicrobial peptide production. Cell Host Microbe 2020; 27:68–78 [View Article] [PubMed]
     [Google Scholar]
  68. PrabhuDas M, Adkins B, Gans H, King C, Levy O et al. Challenges in infant immunity: implications for responses to infection and vaccines. Nat Immunol 2011; 12:189–194 [View Article] [PubMed]
     [Google Scholar]
  69. Naik S, Bouladoux N, Linehan JL, Han S-J, Harrison OJ et al. Commensal-dendritic-cell interaction specifies a unique protective skin immune signature. Nature 2015; 520:104–108 [View Article] [PubMed]
     [Google Scholar]
  70. Fitzgerald JR, Foster TJ, Cox D. The interaction of bacterial pathogens with platelets. Nat Rev Microbiol 2006; 4:445–457 [View Article] [PubMed]
     [Google Scholar]
  71. Taha M, Kyluik-Price D, Kumaran D, Scott MD, Toyofuku W et al. Bacterial survival in whole blood depends on plasma sensitivity and resistance to neutrophil killing. Transfusion 2019; 59:3674–3682 [View Article] [PubMed]
     [Google Scholar]
  72. Stepanović S, Vuković D, Hola V, Di Bonaventura G, Djukić S et al. Quantification of biofilm in microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. APMIS 2007; 115:891–899 [View Article] [PubMed]
     [Google Scholar]
  73. Loza-Correa M, Kalab M, Yi Q-L, Eltringham-Smith LJ, Sheffield WP et al. Comparison of bacterial attachment to platelet bags with and without preconditioning with plasma. Vox Sang 2017; 112:401–407 [View Article] [PubMed]
     [Google Scholar]
  74. Yousuf B, Pasha R, Pineault N, Ramirez-Arcos S. Contamination of platelet concentrates with Staphylococcus aureus induces significant modulations in platelet functionality. Vox Sang 2022; 117:1318–1322 [View Article] [PubMed]
     [Google Scholar]
  75. Grande R, Nistico L, Sambanthamoorthy K, Longwell M, Iannitelli A et al. Temporal expression of agrB, cidA, and alsS in the early development of Staphylococcus aureus UAMS-1 biofilm formation and the structural role of extracellular DNA and carbohydrates. Pathog Dis 2014; 70:414–422 [View Article] [PubMed]
     [Google Scholar]
  76. Lou Q, Zhu T, Hu J, Ben H, Yang J et al. Role of the SaeRS two-component regulatory system in Staphylococcus epidermidis autolysis and biofilm formation. BMC Microbiol 2011; 11:146 [View Article] [PubMed]
     [Google Scholar]
  77. Bayles KW. The biological role of death and lysis in biofilm development. Nat Rev Microbiol 2007; 5:721–726 [View Article] [PubMed]
     [Google Scholar]
  78. Rice KC, Mann EE, Endres JL, Weiss EC, Cassat JE et al. The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus . Proc Natl Acad Sci U S A 2007; 104:8113–8118 [View Article] [PubMed]
     [Google Scholar]
  79. Sadykov MR, Bayles KW. The control of death and lysis in staphylococcal biofilms: a coordination of physiological signals. Curr Opin Microbiol 2012; 15:211–215 [View Article] [PubMed]
     [Google Scholar]
  80. Shelburne SA, Dib RW, Endres BT, Reitzel R, Li X et al. Whole-genome sequencing of Staphylococcus epidermidis bloodstream isolates from a prospective clinical trial reveals that complicated bacteraemia is caused by a limited number of closely related sequence types. Clin Microbiol Infect 2020; 26:646 [View Article] [PubMed]
     [Google Scholar]
  81. Espadinha D, Sobral RG, Mendes CI, Méric G, Sheppard SK et al. Distinct phenotypic and genomic signatures underlie contrasting pathogenic potential of Staphylococcus epidermidis clonal lineages. Front Microbiol 2019; 10:1971 [View Article] [PubMed]
     [Google Scholar]
  82. Conlan S, Mijares LA, Becker J, Blakesley RW, Bouffard GG et al. Staphylococcus epidermidis pan-genome sequence analysis reveals diversity of skin commensal and hospital infection-associated isolates. Genome Biol 2012; 13:R64 [View Article] [PubMed]
     [Google Scholar]
  83. Méric G, Miragaia M, de Been M, Yahara K, Pascoe B et al. Ecological overlap and horizontal gene transfer in Staphylococcus aureus and Staphylococcus epidermidis . Genome Biol Evol 2015; 7:1313–1328 [View Article] [PubMed]
     [Google Scholar]
  84. Lai Y, Villaruz AE, Li M, Cha DJ, Sturdevant DE et al. The human anionic antimicrobial peptide dermcidin induces proteolytic defence mechanisms in staphylococci. Mol Microbiol 2007; 63:497–506 [View Article] [PubMed]
     [Google Scholar]
  85. Christensen GJM, Scholz CFP, Enghild J, Rohde H, Kilian M et al. Antagonism between Staphylococcus epidermidis and propionibacterium acnes and its genomic basis. BMC Genomics 2016; 17:152 [View Article] [PubMed]
     [Google Scholar]
  86. Thurlow LR, Joshi GS, Clark JR, Spontak JS, Neely CJ et al. Functional modularity of the arginine catabolic mobile element contributes to the success of USA300 methicillin-resistant Staphylococcus aureus . Cell Host Microbe 2013; 13:100–107 [View Article] [PubMed]
     [Google Scholar]
  87. Lindgren JK, Thomas VC, Olson ME, Chaudhari SS, Nuxoll AS et al. Arginine deiminase in Staphylococcus epidermidis functions to augment biofilm maturation through pH homeostasis. J Bacteriol 2014; 196:2277–2289 [View Article] [PubMed]
     [Google Scholar]
  88. Park JY, Kim JW, Moon BY, Lee J, Fortin YJ et al. Characterization of a novel two-component regulatory system, HptRS, the regulator for the hexose phosphate transport system in Staphylococcus aureus . Infect Immun 2015; 83:1620–1628 [View Article] [PubMed]
     [Google Scholar]
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Comparative virulome analysis of four Staphylococcus epidermidis strains from human skin and platelet concentrates using whole genome sequencing
Access Microbiology 6, 000780.v3 (2024); https://doi.org/10.1099/acmi.0.000780.v3
/content/journal/acmi/10.1099/acmi.0.000780.v3
/content/journal/acmi/10.1099/acmi.0.000780.v3
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