1887

Microbial Genomics logo

Volume 9, Issue 11

The intra-host evolutionary landscape and pathoadaptation of persistent in chronic rhinosinusitis Open Access

Abstract

Chronic rhinosinusitis (CRS) is a common chronic sinonasal mucosal inflammation associated with biofilm and relapsing infections. This study aimed to determine rates of persistence and pathoadaptation in CRS patients by investigating the genomic relatedness and antibiotic resistance/tolerance in longitudinally collected clinical isolates. A total of 68 . paired isolates (34 pairs) were sourced from 34 CRS patients at least 6 months apart. Isolates were grown into 48 h biofilms and tested for tolerance to antibiotics. A hybrid sequencing strategy was used to obtain high-quality reference-grade assemblies of all isolates. Single nucleotide variants (SNV) divergence in the core genome and sequence type clustering were used to analyse the relatedness of the isolate pairs. Single nucleotide and structural genome variations, plasmid similarity, and plasmid copy numbers between pairs were examined. Our analysis revealed that 41 % (14/34 pairs) of isolates were persistent, while 59 % (20/34 pairs) were non-persistent. Persistent isolates showed episode-specific mutational changes over time with a bias towards events in genes involved in adhesion to the host and mobile genetic elements such as plasmids, prophages, and insertion sequences. Furthermore, a significant increase in the copy number of conserved plasmids of persistent strains was observed. This was accompanied by a significant increase in biofilm tolerance against all tested antibiotics, which was linked to a significant increase in biofilm biomass over time, indicating a potential biofilm pathoadaptive process in persistent isolates. In conclusion, our study provides important insights into the mutational changes during persistence in CRS patients highlighting potential pathoadaptive mechanisms in persistent isolates culminating in increased biofilm biomass.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): S. aureus, Chronic Rhinosinusitis, Biofilm, Evolution, Plasmids
Funding
This study was supported by the:
  • University of Adelaide
    • Principle Award Recipient: GhaisHoutak
  • National Health and Medical Research Council (Award APP1196832)
    • Principle Award Recipient: Peter-JohnWormald
© 2023 The Authors
  • 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/mgen/10.1099/mgen.0.001128
2023-11-27
2024-12-14
Loading full text...

Full text loading...

/deliver/fulltext/mgen/9/11/mgen001128.html?itemId=/content/journal/mgen/10.1099/mgen.0.001128&mimeType=html&fmt=ahah

References

  1. Fokkens WJ, Lund VJ, Hopkins C, Hellings PW, Kern R et al. European position paper on rhinosinusitis and nasal polyps 2020. Rhinology 2020; 58:1–464 [View Article] [PubMed]
     [Google Scholar]
  2. Hastan D, Fokkens WJ, Bachert C, Newson RB, Bislimovska J et al. Chronic rhinosinusitis in Europe--an underestimated disease. A GA(2)LEN study. Allergy 2011; 66:1216–1223 [View Article] [PubMed]
     [Google Scholar]
  3. Hopkins C. Chronic rhinosinusitis with nasal polyps. N Engl J Med 2019; 381:55–63 [View Article] [PubMed]
     [Google Scholar]
  4. Okifo O, Ray A, Gudis DA. The microbiology of acute exacerbations in chronic rhinosinusitis - a systematic review. Front Cell Infect Microbiol 2022; 12:858196 [View Article] [PubMed]
     [Google Scholar]
  5. Vickery TW, Ramakrishnan VR, Suh JD. The role of Staphylococcus aureus in patients with chronic sinusitis and nasal polyposis. Curr Allergy Asthma Rep 2019; 19:21 [View Article] [PubMed]
     [Google Scholar]
  6. Hoggard M, Wagner Mackenzie B, Jain R, Taylor MW, Biswas K et al. Chronic rhinosinusitis and the evolving understanding of microbial ecology in chronic inflammatory mucosal disease. Clin Microbiol Rev 2017; 30:321–348 [View Article] [PubMed]
     [Google Scholar]
  7. Psaltis AJ, Weitzel EK, Ha KR, Wormald PJ. The effect of bacterial biofilms on post-sinus surgical outcomes. Am J Rhinol 2008; 22:1–6 [View Article] [PubMed]
     [Google Scholar]
  8. Singhal D, Foreman A, Jervis-Bardy J, Wormald PJ. Staphylococcus aureus biofilms: Nemesis of endoscopic sinus surgery. Laryngoscope 2011; 121:1578–1583 [View Article] [PubMed]
     [Google Scholar]
  9. Barshak MB, Durand ML. The role of infection and antibiotics in chronic rhinosinusitis. Laryngoscope Investig Otolaryngol 2017; 2:36–42 [View Article] [PubMed]
     [Google Scholar]
  10. Hall CW, Mah TF. Molecular mechanisms of biofilm-based antibiotic resistance and tolerance in pathogenic bacteria. FEMS Microbiol Rev 2017; 41:276–301 [View Article] [PubMed]
     [Google Scholar]
  11. Drilling A, Coombs GW, Tan H, Pearson JC, Boase S et al. Cousins, siblings, or copies: the genomics of recurrent Staphylococcus aureus infections in chronic rhinosinusitis. Int Forum Allergy Rhinol 2014; 4:953–960 [View Article] [PubMed]
     [Google Scholar]
  12. Bachert C, Humbert M, Hanania NA, Zhang N, Holgate S et al. Staphylococcus aureus and its IgE-inducing enterotoxins in asthma: current knowledge. Eur Respir J 2020; 55:1901592 [View Article] [PubMed]
     [Google Scholar]
  13. Schechner V, Temkin E, Harbarth S, Carmeli Y, Schwaber MJ. Epidemiological interpretation of studies examining the effect of antibiotic usage on resistance. Clin Microbiol Rev 2013; 26:289–307 [View Article] [PubMed]
     [Google Scholar]
  14. Shaghayegh G, Cooksley C, Bouras GS, Panchatcharam BS, Idrizi R et al. Chronic rhinosinusitis patients display an aberrant immune cell localization with enhanced S aureus biofilm metabolic activity and biomass. J Allergy Clin Immunol 2023; 151:723–736 [View Article]
     [Google Scholar]
  15. Mölder F, Jablonski KP, Letcher B, Hall MB, Tomkins-Tinch CH et al. Sustainable data analysis with snakemake. F1000Res 2021; 10:33 [View Article] [PubMed]
     [Google Scholar]
  16. Roach MJ, Pierce-Ward NT, Suchecki R, Mallawaarachchi V, Papudeshi B et al. Ten simple rules and a template for creating workflows-as-applications. PLoS Comput Biol 2022; 18:e1010705 [View Article] [PubMed]
     [Google Scholar]
  17. Bouras G. hybracter hybracter. n.d https://github.com/gbouras13/hybracter
  18. Wick RR, Judd LM, Holt KE. Assembling the perfect bacterial genome using Oxford Nanopore and Illumina sequencing. PLoS Comput Biol 2023; 19:e1010905 [View Article] [PubMed]
     [Google Scholar]
  19. Hall M. Rasusa: randomly subsample sequencing reads to a specified coverage. JOSS 2022; 7:3941 [View Article]
     [Google Scholar]
  20. Wick RR. Filtlong Filtlong. n.d https://github.com/rrwick/Filtlong
  21. Wick RR. Porechop Porechop. n.d https://github.com/rrwick/Porechop
  22. 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]
  23. 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]
  24. ONT Medaka; 2022 https://github.com/nanoporetech/medaka
  25. Bouras G. dnaapler dnaapler. n.d https://github.com/gbouras13/dnaapler
  26. 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]
  27. Zimin AV, Salzberg SL. The genome polishing tool POLCA makes fast and accurate corrections in genome assemblies. PLoS Comput Biol 2020; 16:e1007981 [View Article] [PubMed]
     [Google Scholar]
  28. Bouras G, Sheppard AE, Mallawaarachchi V, Vreugde S. Plassembler: an automated bacterial plasmid assembly tool. Bioinformatics 2023; 39:btad409 [View Article] [PubMed]
     [Google Scholar]
  29. De Coster W, D’Hert S, Schultz DT, Cruts M, Van Broeckhoven C. NanoPack: visualizing and processing long-read sequencing data. Bioinformatics 2018; 34:2666–2669 [View Article] [PubMed]
     [Google Scholar]
  30. Li H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 2018; 34:3094–3100 [View Article] [PubMed]
     [Google Scholar]
  31. Li H. Aligning sequence reads, clone sequences and assembly Contigs with BWA-MEM. arXiv preprint arXiv 201313033997
     [Google Scholar]
  32. 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]
  33. Schwengers O, Jelonek L, Dieckmann MA, Beyvers S, Blom J et al. Bakta: rapid and standardized annotation of bacterial genomes via alignment-free sequence identification. Microb Genom 2021; 7:11 [View Article] [PubMed]
     [Google Scholar]
  34. Seemann T. mlst mlst. n.d https://github.com/tseemann/mlst
  35. 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]
  36. Lees JA, Harris SR, Tonkin-Hill G, Gladstone RA, Lo SW et al. Fast and flexible bacterial genomic epidemiology with PopPUNK. Genome Res 2019; 29:304–316 [View Article]
     [Google Scholar]
  37. Petit RA, Read TD. Staphylococcus aureus viewed from the perspective of 40,000+ genomes. PeerJ 2018; 6:e5261 [View Article] [PubMed]
     [Google Scholar]
  38. Xu S, Li L, Luo X, Chen M, Tang W et al. Ggtree: a serialized data object for visualization of a phylogenetic tree and annotation data. iMeta 2022; 1: [View Article]
     [Google Scholar]
  39. Tonkin-Hill G, MacAlasdair N, Ruis C, Weimann A, Horesh G et al. Producing polished prokaryotic pangenomes with the Panaroo pipeline. Genome Biol 2020; 21:180 [View Article] [PubMed]
     [Google Scholar]
  40. Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol 2020; 37:1530–1534 [View Article] [PubMed]
     [Google Scholar]
  41. Seemann T. Abricate Abricate. n.d https://github.com/tseemann/abricate
  42. Jia B, Raphenya AR, Alcock B, Waglechner N, Guo P et al. CARD 2017: expansion and model-centric curation of the comprehensive antibiotic resistance database. Nucleic Acids Res 2017; 45:D566–D573 [View Article] [PubMed]
     [Google Scholar]
  43. Liu B, Zheng D, Jin Q, Chen L, Yang J. VFDB 2019: a comparative pathogenomic platform with an interactive web interface. Nucleic Acids Res 2019; 47:D687–D692 [View Article] [PubMed]
     [Google Scholar]
  44. Brynildsrud O, Bohlin J, Scheffer L, Eldholm V. Rapid scoring of genes in microbial pan-genome-wide association studies with scoary. Genome Biol 2016; 17:262 [View Article] [PubMed]
     [Google Scholar]
  45. Seemann T. Snippy: fast bacterial variant calling from NGS reads; 2015 https://github.com/tseemann/snippy
  46. Khelik K, Lagesen K, Sandve GK, Rognes T, Nederbragt AJ. NucDiff: in-depth characterization and annotation of differences between two sets of DNA sequences. BMC Bioinformatics 2017; 18:338 [View Article] [PubMed]
     [Google Scholar]
  47. Sedlazeck FJ, Rescheneder P, Smolka M, Fang H, Nattestad M et al. Accurate detection of complex structural variations using single-molecule sequencing. Nat Methods 2018; 15:461–468 [View Article] [PubMed]
     [Google Scholar]
  48. Danecek P, Bonfield JK, Liddle J, Marshall J, Ohan V et al. Twelve years of SAMtools and BCFtools. Gigascience 2021; 10:giab008 [View Article] [PubMed]
     [Google Scholar]
  49. Hahne F, Ivanek R. Visualizing genomic data using gviz and bioconductor. In Mathé E, Davis S. eds Statistical Genomics: Methods and Protocols New York: Springer; 2016 pp 335–351 [View Article]
     [Google Scholar]
  50. Ankenbrand Th. gggenomes: a grammar of graphics for comparative genomics; 2022
  51. Robertson J, Nash JHE. MOB-suite: software tools for clustering, reconstruction and typing of plasmids from draft assemblies. Microb Genom 2018; 4: [View Article]
     [Google Scholar]
  52. Ondov BD, Treangen TJ, Melsted P, Mallonee AB, Bergman NH et al. Mash: fast genome and metagenome distance estimation using MinHash. Genome Biol 2016; 17:132 [View Article] [PubMed]
     [Google Scholar]
  53. Hawkey J, Wyres KL, Judd LM, Harshegyi T, Blakeway L et al. ESBL plasmids in Klebsiella pneumoniae: diversity, transmission and contribution to infection burden in the hospital setting. Genome Med 2022; 14:97 [View Article] [PubMed]
     [Google Scholar]
  54. Rocha EPC, Smith JM, Hurst LD, Holden MTG, Cooper JE et al. Comparisons of dN/dS are time dependent for closely related bacterial genomes. J Theor Biol 2006; 239:226–235 [View Article] [PubMed]
     [Google Scholar]
  55. Golubchik T, Batty EM, Miller RR, Farr H, Young BC et al. Within-host evolution of Staphylococcus aureus during asymptomatic carriage. PLoS One 2013; 8:e61319 [View Article] [PubMed]
     [Google Scholar]
  56. Holden MTG, Hsu L-Y, Kurt K, Weinert LA, Mather AE et al. A genomic portrait of the emergence, evolution, and global spread of a methicillin-resistant Staphylococcus aureus pandemic. Genome Res 2013; 23:653–664 [View Article] [PubMed]
     [Google Scholar]
  57. McAdam PR, Templeton KE, Edwards GF, Holden MTG, Feil EJ et al. Molecular tracing of the emergence, adaptation, and transmission of hospital-associated methicillin-resistant Staphylococcus aureus. Proc Natl Acad Sci U S A 2012; 109:9107–9112 [View Article] [PubMed]
     [Google Scholar]
  58. Nübel U, Dordel J, Kurt K, Strommenger B, Westh H et al. A timescale for evolution, population expansion, and spatial spread of an emerging clone of methicillin-resistant Staphylococcus aureus. PLoS Pathog 2010; 6:e1000855 [View Article] [PubMed]
     [Google Scholar]
  59. Ward MJ, Gibbons CL, McAdam PR, van Bunnik BAD, Girvan EK et al. Time-scaled evolutionary analysis of the transmission and antibiotic resistance dynamics of Staphylococcus aureus clonal complex 398. Appl Environ Microbiol 2014; 80:7275–7282 [View Article] [PubMed]
     [Google Scholar]
  60. Uhlemann A-C, Dordel J, Knox JR, Raven KE, Parkhill J et al. Molecular tracing of the emergence, diversification, and transmission of S. aureus sequence type 8 in a New York community. Proc Natl Acad Sci U S A 2014; 111:6738–6743 [View Article] [PubMed]
     [Google Scholar]
  61. Baines SL, Holt KE, Schultz MB, Seemann T, Howden BO et al. Convergent adaptation in the dominant global hospital clone ST239 of methicillin-resistant Staphylococcus aureus. mBio 2015; 6:e00080 [View Article] [PubMed]
     [Google Scholar]
  62. Harris SR, Feil EJ, Holden MTG, Quail MA, Nickerson EK et al. Evolution of MRSA during hospital transmission and intercontinental spread. Science 2010; 327:469–474 [View Article]
     [Google Scholar]
  63. Szafrańska AK, Junker V, Steglich M, Nübel U. Rapid cell division of Staphylococcus aureus during colonization of the human nose. BMC Genomics 2019; 20:229 [View Article] [PubMed]
     [Google Scholar]
  64. Wiegand I, Hilpert K, Hancock REW. Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat Protoc 2008; 3:163–175 [View Article]
     [Google Scholar]
  65. Mah TF. Establishing the minimal bactericidal concentration of an antimicrobial agent for planktonic cells (MBC-P) and biofilm cells (MBC-B). J Vis Exp 2014; 2014:e50854 [View Article] [PubMed]
     [Google Scholar]
  66. Pettit RK, Weber CA, Kean MJ, Hoffmann H, Pettit GR et al. Microplate Alamar blue assay for Staphylococcus epidermidis biofilm susceptibility testing. Antimicrob Agents Chemother 2005; 49:2612–2617 [View Article] [PubMed]
     [Google Scholar]
  67. Stiefel P, Rosenberg U, Schneider J, Mauerhofer S, Maniura-Weber K et al. Is biofilm removal properly assessed? Comparison of different quantification methods in a 96-well plate system. Appl Microbiol Biotechnol 2016; 100:4135–4145 [View Article] [PubMed]
     [Google Scholar]
  68. R Core Team R: A Language and Environment for Statistical Computing Vienna, Austria: R Foundation for Statistical Computing; 2017
     [Google Scholar]
  69. Key FM, Khadka VD, Romo-González C, Blake KJ, Deng L et al. On-person adaptive evolution of Staphylococcus aureus during treatment for atopic dermatitis. Cell Host Microbe 2023; 31:593–603 [View Article] [PubMed]
     [Google Scholar]
  70. Krysko O, Teufelberger A, Van Nevel S, Krysko DV, Bachert C. Protease/antiprotease network in allergy: the role of Staphylococcus aureus protease-like proteins. Allergy 2019; 74:2077–2086 [View Article] [PubMed]
     [Google Scholar]
  71. Nepal R, Houtak G, Shaghayegh G, Bouras G, Shearwin K et al. Prophages encoding human immune evasion cluster genes are enriched in Staphylococcus aureus isolated from chronic rhinosinusitis patients with nasal polyps. Microb Genom 2021; 7:12 [View Article] [PubMed]
     [Google Scholar]
  72. Mazmanian SK, Liu G, Ton-That H, Schneewind O. Staphylococcus aureus sortase, an enzyme that anchors surface proteins to the cell wall. Science 1999; 285:760–763 [View Article] [PubMed]
     [Google Scholar]
  73. Foster TJ, Geoghegan JA, Ganesh VK, Höök M. Adhesion, invasion and evasion: the many functions of the surface proteins of Staphylococcus aureus. Nat Rev Microbiol 2014; 12:49–62 [View Article] [PubMed]
     [Google Scholar]
  74. Malachowa N, DeLeo FR. Mobile genetic elements of Staphylococcus aureus. Cell Mol Life Sci 2010; 67:3057–3071 [View Article] [PubMed]
     [Google Scholar]
  75. Sollid JUE, Furberg AS, Hanssen AM, Johannessen M. Staphylococcus aureus: determinants of human carriage. Infect Genet Evol 2014; 21:531–541 [View Article] [PubMed]
     [Google Scholar]
  76. Price JR, Cole K, Bexley A, Kostiou V, Eyre DW et al. Transmission of Staphylococcus aureus between health-care workers, the environment, and patients in an intensive care unit: a longitudinal cohort study based on whole-genome sequencing. Lancet Infect Dis 2017; 17:207–214 [View Article] [PubMed]
     [Google Scholar]
  77. Muthukrishnan G, Lamers RP, Ellis A, Paramanandam V, Persaud AB et al. Longitudinal genetic analyses of Staphylococcus aureus nasal carriage dynamics in a diverse population. BMC Infect Dis 2013; 13:221 [View Article] [PubMed]
     [Google Scholar]
  78. Thunberg U, Hugosson S, Ehricht R, Monecke S, Müller E et al. Long-term sinonasal carriage of Staphylococcus aureus and anti-staphylococcal humoral immune response in patients with chronic rhinosinusitis. Microorganisms 2021; 9:256 [View Article] [PubMed]
     [Google Scholar]
  79. Lagos AC, Sundqvist M, Dyrkell F, Stegger M, Söderquist B et al. Evaluation of within-host evolution of methicillin-resistant Staphylococcus aureus (MRSA) by comparing cgMLST and SNP analysis approaches. Sci Rep 2022; 12:10541 [View Article] [PubMed]
     [Google Scholar]
  80. Coll F, Raven KE, Knight GM, Blane B, Harrison EM et al. Definition of a genetic relatedness cutoff to exclude recent transmission of meticillin-resistant Staphylococcus aureus: a genomic epidemiology analysis. Lancet Microbe 2020; 1:e328–e335 [View Article] [PubMed]
     [Google Scholar]
  81. Giulieri SG, Baines SL, Guerillot R, Seemann T, Gonçalves da Silva A et al. Genomic exploration of sequential clinical isolates reveals a distinctive molecular signature of persistent Staphylococcus aureus bacteraemia. Genome Med 2018; 10:65 [View Article] [PubMed]
     [Google Scholar]
  82. Giulieri SG, Guérillot R, Duchene S, Hachani A, Daniel D et al. Niche-specific genome degradation and CONVERGENT evolution shaping Staphylococcus aureus adaptation during severe infections. Elife 2022; 11:e77195 [View Article] [PubMed]
     [Google Scholar]
  83. Altman DR, Sullivan MJ, Chacko KI, Balasubramanian D, Pak TR et al. Genome plasticity of agr-defective Staphylococcus aureus during clinical infection. Infect Immun 2018; 86:10 [View Article] [PubMed]
     [Google Scholar]
  84. Jenul C, Horswill AR. Regulation of Staphylococcus aureus virulence. Microbiol Spectr 2019; 7:
     [Google Scholar]
  85. Didelot X, Walker AS, Peto TE, Crook DW, Wilson DJ. Within-host evolution of bacterial pathogens. Nat Rev Microbiol 2016; 14:150–162 [View Article] [PubMed]
     [Google Scholar]
  86. Foster TJ. The MSCRAMM family of cell-wall-anchored surface proteins of gram-positive cocci. Trends Microbiol 2019; 27:927–941 [View Article]
     [Google Scholar]
  87. Raafat D, Otto M, Reppschlager K, Iqbal J, Holtfreter S. Fighting Staphylococcus aureus biofilms with monoclonal antibodies. Trends Microbiol 2019; 27:303–322
     [Google Scholar]
  88. Howden BP, Giulieri SG, Wong Fok Lung T, Baines SL, Sharkey LK et al. Staphylococcus aureus host interactions and adaptation. Nat Rev Microbiol 2023; 21:380–395 [View Article] [PubMed]
     [Google Scholar]
  89. McCarthy AJ, Lindsay JA. Staphylococcus aureus innate immune evasion is lineage-specific: a bioinfomatics study. Infect Genet Evol 2013; 19:7–14 [View Article] [PubMed]
     [Google Scholar]
  90. Thammavongsa V, Kim HK, Missiakas D, Schneewind O. Staphylococcal manipulation of host immune responses. Nat Rev Microbiol 2015; 13:529–543 [View Article] [PubMed]
     [Google Scholar]
  91. Haim MS, Zaheer R, Bharat A, Di Gregorio S, Di Conza J et al. Comparative genomics of ST5 and ST30 methicillin-resistant Staphylococcus aureus sequential isolates recovered from paediatric patients with cystic fibrosis. Microb Genom 2021; 7:mgen000510 [View Article] [PubMed]
     [Google Scholar]
  92. Solis N, Parker BL, Kwong SM, Robinson G, Firth N et al. Staphylococcus aureus surface proteins involved in adaptation to oxacillin identified using a novel cell shaving approach. J Proteome Res 2014; 13:2954–2972 [View Article] [PubMed]
     [Google Scholar]
  93. Ajayi C, Åberg E, Askarian F, Sollid JUE, Johannessen M et al. Genetic variability in the sdrD gene in Staphylococcus aureus from healthy nasal carriers. BMC Microbiol 2018; 18:34 [View Article] [PubMed]
     [Google Scholar]
  94. Barbu EM, Mackenzie C, Foster TJ, Höök M. SdrC induces staphylococcal biofilm formation through a homophilic interaction. Mol Microbiol 2014; 94:172–185 [View Article] [PubMed]
     [Google Scholar]
  95. Wick RR, Judd LM, Wyres KL, Holt KE. Recovery of small plasmid sequences via Oxford Nanopore sequencing. Microb Genom 2021; 7:000631 [View Article] [PubMed]
     [Google Scholar]
  96. Shearer JES, Wireman J, Hostetler J, Forberger H, Borman J et al. Major families of multiresistant plasmids from geographically and epidemiologically diverse staphylococci. G3 2011; 1:581–591 [View Article] [PubMed]
     [Google Scholar]
  97. Firth N, Jensen SO, Kwong SM, Skurray RA, Ramsay JP. Staphylococcal plasmids, transposable and integrative elements. Microbiol Spectr 2018; 6: [View Article] [PubMed]
     [Google Scholar]
  98. McCarthy AJ, Lindsay JA. The distribution of plasmids that carry virulence and resistance genes in Staphylococcus aureus is lineage associated. BMC Microbiol 2012; 12:104 [View Article] [PubMed]
     [Google Scholar]
  99. Turner NA, Sharma-Kuinkel BK, Maskarinec SA, Eichenberger EM, Shah PP et al. Methicillin-resistant Staphylococcus aureus: an overview of basic and clinical research. Nat Rev Microbiol 2019; 17:203–218 [View Article] [PubMed]
     [Google Scholar]
  100. Brantl S. Plasmid replication control by antisense RNAs. Microbiol Spectr 2014; 2:LAS–0001 [View Article] [PubMed]
     [Google Scholar]
  101. Ruiz-Masó JA, MachóN C, Bordanaba-Ruiseco L, Espinosa M, Coll M et al. Plasmid rolling-circle replication. Microbiol Spectr 2015; 3:LAS–0035 [View Article] [PubMed]
     [Google Scholar]
  102. San Millan A, MacLean RC. Fitness costs of plasmids: a limit to plasmid transmission. Microbiol Spectr 2017; 5: [View Article] [PubMed]
     [Google Scholar]
  103. Bhattacharyya N, Kepnes LJ. Assessment of trends in antimicrobial resistance in chronic rhinosinusitis. Ann Otol Rhinol Laryngol 2008; 117:448–452 [View Article]
     [Google Scholar]
  104. Singhal D, Psaltis AJ, Foreman A, Wormald PJ. The impact of biofilms on outcomes after endoscopic sinus surgery. Am J Rhinol Allergy 2010; 24:169–174 [View Article] [PubMed]
     [Google Scholar]
  105. Foreman A, Psaltis AJ, Tan LW, Wormald PJ. Characterization of bacterial and fungal biofilms in chronic rhinosinusitis. Allergy Rhinol 2010; 1:10 [View Article] [PubMed]
     [Google Scholar]
  106. Kim JS, Kwon SH. Mupirocin in the treatment of staphylococcal infections in chronic rhinosinusitis: a meta-analysis. PLoS One 2016; 11:e0167369 [View Article] [PubMed]
     [Google Scholar]
  107. Percival SL. Importance of biofilm formation in surgical infection. Br J Surg 2017; 104:e85–e94 [View Article] [PubMed]
     [Google Scholar]
  108. Rossi E, La Rosa R, Bartell JA, Marvig RL, Haagensen JAJ et al. Pseudomonas aeruginosa adaptation and evolution in patients with cystic fibrosis. Nat Rev Microbiol 2021; 19:331–342 [View Article] [PubMed]
     [Google Scholar]
  109. Krismer B, Liebeke M, Janek D, Nega M, Rautenberg M et al. Nutrient limitation governs Staphylococcus aureus metabolism and niche adaptation in the human nose. PLoS Pathog 2014; 10:e1003862 [View Article] [PubMed]
     [Google Scholar]
  110. Flemming HC, Wingender J, Szewzyk U, Steinberg P, Rice SA et al. Biofilms: an emergent form of bacterial life. Nat Rev Microbiol 2016; 14:563–575 [View Article] [PubMed]
     [Google Scholar]
  111. Karygianni L, Ren Z, Koo H, Thurnheer T. Biofilm matrixome: extracellular components in structured microbial communities. Trends Microbiol 2020; 28:668–681 [View Article] [PubMed]
     [Google Scholar]
  112. Votintseva AA, Miller RR, Fung R, Knox K, Godwin H et al. Multiple-strain colonization in nasal carriers of Staphylococcus aureus. J Clin Microbiol 2014; 52:1192–1200 [View Article] [PubMed]
     [Google Scholar]
  113. Thunberg U, Hugosson S, Ehricht R, Monecke S, Müller E et al. Long-term sinonasal carriage of Staphylococcus aureus and anti-staphylococcal humoral immune response in patients with chronic rhinosinusitis. Microorganisms 2021; 9:256 [View Article] [PubMed]
     [Google Scholar]
  114. Howden BP, Giulieri SG, Wong Fok Lung T, Baines SL, Sharkey LK et al. Staphylococcus aureus host interactions and adaptation. Nat Rev Microbiol 2023; 21:380–395 [View Article] [PubMed]
     [Google Scholar]
  115. Azarian T, Ridgway JP, Yin Z, David MZ. Long-term intrahost evolution of methicillin resistant Staphylococcus aureus among cystic fibrosis patients with respiratory carriage. Front Genet 2019; 10:546 [View Article] [PubMed]
     [Google Scholar]
/content/journal/mgen/10.1099/mgen.0.001128
Loading
The intra-host evolutionary landscape and pathoadaptation of persistent Staphylococcus aureus in chronic rhinosinusitis
M Gen 9, 001128 (2023); https://doi.org/10.1099/mgen.0.001128
/content/journal/mgen/10.1099/mgen.0.001128
/content/journal/mgen/10.1099/mgen.0.001128
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited 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