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Volume 9, Issue 1

A bittersweet fate: detection of serotype switching in Open Access

Abstract

High-risk clone types in are problematic global multidrug-resistant clones. However, apart from their ability to resist antimicrobial treatment, not much is known about what sets these clones apart from the multitude of other clones. In high-risk clone ST111, it has previously been shown that replacement of the native serotype biosynthetic gene cluster (O4) by a different gene cluster (O12) by horizontal gene transfer and recombination may have contributed to the global success of this clone. However, the extent to which isolates undergo this type of serotype switching has not been adequately explored in . In the present study, a bioinformatics tool has been developed and utilized to provide a first estimate of serotype switching in groups of multidrug resistant (MDR) clinical isolates. The tool detects serotype switching by analysis of core-genome phylogeny and serotype. Analysis of a national survey of MDR isolates found a prevalence of 3.9 % of serotype-switched isolates in high-risk clone types ST111, ST244 and ST253. A global survey of MDR isolates was additionally analysed, and it was found that 2.3 % of isolates had undergone a serotype switch. To further understand this process, we determined the exact boundaries of the horizontally transferred serotype O12 island. We found that the size of the serotype island correlates with the clone type of the receiving isolate and additionally we found intra-clone type variations in size and boundaries. This suggests multiple serotype switch events. Moreover, we found that the housekeeping gene is co-transferred with the O12 serotype island, which prompted us to analyse this allele for all serotype O12 isolates. We found that 95 % of ST111 O12 isolates had a resistant allele and 86 % of all O12 isolates had a resistant allele. The rates of resistant alleles in isolates with other prevalent serotypes are all lower. Together, these results show that the transfer and acquisition of serotype O12 in high-risk clone ST111 has happened multiple times and may be facilitated by multiple donors, which clearly suggests a strong selection pressure for this process. However, gyrA-mediated antibiotic resistance may not be the only evolutionary driver.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Antibiotic resistance , HIRIC evolution , lipopolysaccharide , O antigen , Pseudomonas aeruginosa and serotype switch
Funding
This study was supported by the:
  • Danmarks Frie Forskningsfond (Award 9039-00350A)
    • Principle Award Recipient: LarsJelsbak
© 2023 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2023-01-11
2024-04-26
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References

  1. Rice LB. Federal funding for the study of antimicrobial resistance in nosocomial pathogens: no ESKAPE. J Infect Dis 2008; 197:1079–1081 [View Article]
     [Google Scholar]
  2. Oliver A, Mulet X, López-Causapé C, Juan C. The increasing threat of Pseudomonas aeruginosa high-risk clones. Drug Resist Updat 2015; 21–22:41–59 [View Article]
     [Google Scholar]
  3. Lyczak JB, Cannon CL, Pier GB. Establishment of Pseudomonas aeruginosa infection: lessons from a versatile opportunist. Microbes Infect 2000; 2:1051–1060 [View Article]
     [Google Scholar]
  4. King JD, Kocíncová D, Westman EL, Lam JS. Review: Lipopolysaccharide biosynthesis in Pseudomonas aeruginosa. Innate Immun 2009; 15:261–312 [View Article] [PubMed]
     [Google Scholar]
  5. Valero A, Rodríguez-Gascón A, Isla A, Barrasa H, Del Barrio-Tofiño E et al. Pseudomonas aeruginosa susceptibility in Spain: antimicrobial activity and resistance suppression evaluation by PK/PD analysis. Pharmaceutics 2021; 13:1899 [View Article]
     [Google Scholar]
  6. Woodford N, Turton JF, Livermore DM. Multiresistant Gram-negative bacteria: the role of high-risk clones in the dissemination of antibiotic resistance. FEMS Microbiol Rev 2011; 35:736–755 [View Article]
     [Google Scholar]
  7. Del Barrio-Tofiño E, López-Causapé C, Oliver A. Pseudomonas aeruginosa epidemic high-risk clones and their association with horizontally-acquired β-lactamases: 2020 update. Int J Antimicrob Agents 2020; 56:106196 [View Article]
     [Google Scholar]
  8. Huszczynski SM, Lam JS, Khursigara CM. The role of Pseudomonas aeruginosa lipopolysaccharide in bacterial pathogenesis and physiology. Pathogens 2019; 9:E6 [View Article]
     [Google Scholar]
  9. Rocchetta HL, Burrows LL, Lam JS. Genetics of O-antigen biosynthesis in Pseudomonas aeruginosa. Microbiol Mol Biol Rev 1999; 63:523–553 [View Article] [PubMed]
     [Google Scholar]
  10. Cryz SJ Jr, Pitt TL, Fürer E, Germanier R. Role of lipopolysaccharide in virulence of Pseudomonas aeruginosa. Infect Immun 1984; 44:508–513 [View Article] [PubMed]
     [Google Scholar]
  11. Makin SA, Beveridge TJ. The influence of A-band and B-band lipopolysaccharide on the surface characteristics and adhesion of Pseudomonas aeruginosa to surfaces. Microbiology 1996; 142 (Pt 2):299–307 [View Article]
     [Google Scholar]
  12. Collins MS, Ladehoff DK, Mehton NS, Noonan JS. Opsonic and protective activity of five human IgM monoclonal antibodies reactive with lipopolysaccharide antigen of Pseudomonas aeruginosa. FEMS Microbiol Immunol 1990; 2:263–268 [View Article] [PubMed]
     [Google Scholar]
  13. Engels W, Endert J, Kamps MA, van Boven CP. Role of lipopolysaccharide in opsonization and phagocytosis of Pseudomonas aeruginosa. Infect Immun 1985; 49:182–189 [View Article] [PubMed]
     [Google Scholar]
  14. Nobrega FL, Vlot M, de Jonge PA, Dreesens LL, Beaumont HJE et al. Targeting mechanisms of tailed bacteriophages. Nat Rev Microbiol 2018; 16:760–773 [View Article]
     [Google Scholar]
  15. Köhler T, Donner V, van Delden C. Lipopolysaccharide as shield and receptor for R-pyocin-mediated killing in Pseudomonas aeruginosa. J Bacteriol 2010; 192:1921–1928 [View Article]
     [Google Scholar]
  16. Kintz E, Scarff JM, DiGiandomenico A, Goldberg JB. Lipopolysaccharide O-antigen chain length regulation in Pseudomonas aeruginosa serogroup O11 strain PA103. J Bacteriol 2008; 190:2709–2716 [View Article]
     [Google Scholar]
  17. Hancock REW, Mutharia LM, Chan L, Darveau RP, Speert DP et al. Pseudomonas aeruginosa isolates from patients with cystic fibrosis: a class of serum-sensitive, nontypable strains deficient in lipopolysaccharide O side chains. Infect Immun 1983; 42:170–177 [View Article] [PubMed]
     [Google Scholar]
  18. Lam JS, Taylor VL, Islam ST, Hao Y, Kocíncová D. Genetic and functional diversity of Pseudomonas aeruginosa lipopolysaccharide. Front Microbiol 2011; 2:118 [View Article]
     [Google Scholar]
  19. Klockgether J, Cramer N, Wiehlmann L, Davenport CF, Tümmler B. Pseudomonas aeruginosa genomic structure and diversity. Front Microbiol 2011; 2:150 [View Article]
     [Google Scholar]
  20. Raymond CK, Sims EH, Kas A, Spencer DH, Kutyavin TV et al. Genetic variation at the O-antigen biosynthetic locus in Pseudomonas aeruginosa. J Bacteriol 2002; 184:3614–3622 [View Article] [PubMed]
     [Google Scholar]
  21. Kaluzny K, Abeyrathne PD, Lam JS. Coexistence of two distinct versions of O-antigen polymerase, Wzy-alpha and Wzy-beta, in Pseudomonas aeruginosa serogroup O2 and their contributions to cell surface diversity. J Bacteriol 2007; 189:4141–4152 [View Article] [PubMed]
     [Google Scholar]
  22. Huszczynski SM, Hao Y, Lam JS, Khursigara CM. Identification of the Pseudomonas aeruginosa O17 and O15 O-specific antigen biosynthesis loci reveals an ABC transporter-dependent synthesis pathway and mechanisms of genetic diversity. J Bacteriol 2020; 202:e00347-20 [View Article]
     [Google Scholar]
  23. Thrane SW, Taylor VL, Lund O, Lam JS, Jelsbak L. Application of whole-genome sequencing data for o-specific antigen analysis and in silico serotyping of Pseudomonas aeruginosa isolates. J Clin Microbiol 2016; 54:1782–1788 [View Article]
     [Google Scholar]
  24. Thrane SW, Taylor VL, Freschi L, Kukavica-Ibrulj I, Boyle B et al. The widespread multidrug-resistant serotype O12 Pseudomonas aeruginosa clone emerged through concomitant horizontal transfer of serotype antigen and antibiotic resistance gene clusters. mBio 2015; 6:e01396-15 [View Article]
     [Google Scholar]
  25. Del Barrio-Tofiño E, Zamorano L, Cortes-Lara S, López-Causapé C, Sánchez-Diener I et al. Spanish nationwide survey on Pseudomonas aeruginosa antimicrobial resistance mechanisms and epidemiology. J Antimicrob Chemother 2019; 74:1825–1835 [View Article] [PubMed]
     [Google Scholar]
  26. Kos VN, Déraspe M, McLaughlin RE, Whiteaker JD, Roy PH et al. The resistome of Pseudomonas aeruginosa in relationship to phenotypic susceptibility. Antimicrob Agents Chemother 2015; 59:427–436 [View Article]
     [Google Scholar]
  27. Recio R, Sánchez-Diener I, Viedma E, Meléndez-Carmona MÁ, Villa J et al. Pathogenic characteristics of Pseudomonas aeruginosa bacteraemia isolates in a high-endemicity setting for ST175 and ST235 high-risk clones. Eur J Clin Microbiol Infect Dis 2020; 39:671–678 [View Article]
     [Google Scholar]
  28. Abdouchakour F, Aujoulat F, Licznar-Fajardo P, Marchandin H, Toubiana M et al. Intraclonal variations of resistance and phenotype in Pseudomonas aeruginosa epidemic high-risk clone ST308: a key to success within a hospital?. Int J Med Microbiol 2018; 308:279–289 [View Article]
     [Google Scholar]
  29. Miyoshi-Akiyama T, Tada T, Ohmagari N, Viet Hung N, Tharavichitkul P et al. Emergence and spread of epidemic multidrug-resistant Pseudomonas aeruginosa. Genome Biol Evol 2017; 9:3238–3245 [View Article]
     [Google Scholar]
  30. Sekiguchi J-I, Asagi T, Miyoshi-Akiyama T, Kasai A, Mizuguchi Y et al. Outbreaks of multidrug-resistant Pseudomonas aeruginosa in community hospitals in Japan. J Clin Microbiol 2007; 45:979–989 [View Article]
     [Google Scholar]
  31. Miyoshi-Akiyama T, Kuwahara T, Tada T, Kitao T, Kirikae T. Complete genome sequence of highly multidrug-resistant Pseudomonas aeruginosa NCGM2.S1, a representative strain of a cluster endemic to Japan. J Bacteriol 2011; 193:7010 [View Article]
     [Google Scholar]
  32. National Center for Biotechnology Information (NCBI) Datasets - NCBI [Internet]. [cited 2021 Oct 22]. Available from. n.d https://www.ncbi.nlm.nih.gov/datasets/
  33. van Belkum A, Soriaga LB, LaFave MC, Akella S, Veyrieras JB et al. Phylogenetic distribution of CRISPR-Cas systems in antibiotic- resistant pseudomonas aeruginosa. MBio [Internet]. 2015 Nov 24 [cited 2021 Jun 2];6(6). Available from. n.d https://pubmed.ncbi.nlm.nih.gov/26604259/
  34. Pirnay J-P, Bilocq F, Pot B, Cornelis P, Zizi M et al. Pseudomonas aeruginosa population structure revisited. PLoS ONE 2009; 4:e7740 [View Article]
     [Google Scholar]
  35. Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P et al. Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 2000; 406:959–964 [View Article]
     [Google Scholar]
  36. Roy PH, Tetu SG, Larouche A, Elbourne L, Tremblay S et al. Complete genome sequence of the multiresistant taxonomic outlier pseudomonas aeruginosa PA7. PLoS One 2010
     [Google Scholar]
  37. Cain AK, Nolan LM, Sullivan GJ, Whitchurch CB, Filloux A et al. Complete genome sequence of Pseudomonas aeruginosa reference strain PAK. Microbiol Resour Announc 2019; 8:e00865-19 [View Article]
     [Google Scholar]
  38. Winstanley C, Langille MGI, Fothergill JL, Kukavica-Ibrulj I, Paradis-Bleau C et al. Newly introduced genomic prophage islands are critical determinants of in vivo competitiveness in the liverpool epidemic strain of Pseudomonas aeruginosa. Genome Res 2009; 19:12–23 [View Article]
     [Google Scholar]
  39. Lee DG, Urbach JM, Wu G, Liberati NT, Feinbaum RL et al. Genomic analysis reveals that Pseudomonas aeruginosa virulence is combinatorial. Genome Biol 2006; 7:R90 [View Article]
     [Google Scholar]
  40. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J et al. BLAST+: architecture and applications. BMC Bioinformatics 2009; 10:421 [View Article]
     [Google Scholar]
  41. Curran B, Jonas D, Grundmann H, Pitt T, Dowson CG. Development of a multilocus sequence typing scheme for the opportunistic pathogen Pseudomonas aeruginosa. J Clin Microbiol 2004; 42:5644–5649 [View Article]
     [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]
     [Google Scholar]
  43. 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]
     [Google Scholar]
  44. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article]
     [Google Scholar]
  45. Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 2000; 17:540–552 [View Article]
     [Google Scholar]
  46. Price MN, Dehal PS, Arkin AP. FastTree 2--approximately maximum-likelihood trees for large alignments. PLoS One 2010; 5:e9490 [View Article]
     [Google Scholar]
  47. Yu G, Smith DK, Zhu H, Guan Y, Lam TTY. Ggtree: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol Evol 2017
     [Google Scholar]
  48. R Core Team R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2020 https://www.R-project.org/
  49. Valero-Mora PM. ggplot2: Elegant Graphics for Data Analysis. Journal of Statistical Software. Springer-Verlag New York; 2010 https://ggplot2.tidyverse.org
  50. Pedersen TL, Shemanarev M, Juricic T, Marusinec M, Garett S. Graphic Devices Based on AGG [R package ragg version 1.2.1]. n.d https://cran.r-project.org/package=ragg
  51. Kassambara A. ggplot2” Based Publication Ready Plots [R package ggpubr version 0.4.0]. n.d https://cran.r-project.org/package=ggpubr
  52. Wang L-G, Lam TT-Y, Xu S, Dai Z, Zhou L et al. Treeio: an R package for phylogenetic tree input and output with richly annotated and associated data. Mol Biol Evol 2020; 37:599–603 [View Article]
     [Google Scholar]
  53. Yu G. A Tidy Tool for Phylogenetic Tree Data Manipulation [R package tidytree version 0.3.6]; 2021 https://cran.r-project.org/package=tidytree
  54. Garnier S, Ross N, Rudis R et al. {viridis} - Colorblind-Friendly Color Maps for R; 2021 https://sjmgarnier.github.io/viridis/
  55. Paradis E, Schliep K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 2019; 35:526–528 [View Article]
     [Google Scholar]
  56. Campitelli E. Multiple Fill and Colour Scales in “ggplot2" [R package ggnewscale version 0.4.5]; 2021Jan11 https://cran.r-project.org/package=ggnewscale
  57. Charif D, Lobry JR. SeqinR 1.0-2: A Contributed Package to the R Project for Statistical Computing Devoted to Biological Sequences Retrieval and Analysis; 2007 https://link.springer.com/chapter/10.1007/978-3-540-35306-5_10
  58. Hadley W, Jim H, Jennifer B. Read Rectangular Text Data [R package readr version 2.1.1]; 2021Nov30 https://cran.r-project.org/package=readr
  59. Neuwirth E. ColorBrewer Palettes [R package RColorBrewer version 1.1-2]; 2014Dec7 https://cran.r-project.org/package=RColorBrewer
  60. Freschi L, Vincent AT, Jeukens J, Emond-Rheault J-G, Kukavica-Ibrulj I et al. The Pseudomonas aeruginosa pan-genome provides new insights on its population structure, horizontal gene transfer, and pathogenicity. Genome Biol Evol 2019; 11:109–120 [View Article]
     [Google Scholar]
  61. Yonezawa M, Takahata M, Matsubara N, Watanabe Y, Narita H. DNA gyrase gyrA mutations in quinolone-resistant clinical isolates of Pseudomonas aeruginosa. Antimicrob Agents Chemother 1995; 39:1970–1972 [View Article]
     [Google Scholar]
  62. Akasaka T, Tanaka M, Yamaguchi A, Sato K. Type II topoisomerase mutations in fluoroquinolone-resistant clinical strains of Pseudomonas aeruginosa isolated in 1998 and 1999: role of target enzyme in mechanism of fluoroquinolone resistance. Antimicrob Agents Chemother 2001; 45:2263–2268 [View Article]
     [Google Scholar]
  63. Watts SC, Holta KE. In silico serotyping of the haemophilus influenzae capsule locus. J Clin Microbiol 2019; 57(6):
     [Google Scholar]
  64. Croucher NJ, Kagedan L, Thompson CM, Parkhill J, Bentley SD et al. Selective and genetic constraints on pneumococcal serotype switching. PLoS Genet 2015; 11:e1005095 [View Article]
     [Google Scholar]
  65. Wyres KL, Lambertsen LM, Croucher NJ, McGee L, von Gottberg A et al. Pneumococcal capsular switching: a historical perspective. J Infect Dis 2013; 207:439–449 [View Article]
     [Google Scholar]
  66. Swartley JS, Marfin AA, Edupuganti S, Liu LJ, Cieslak P et al. Capsule switching of Neisseria meningitidis. Proc Natl Acad Sci 1997; 94:271–276 [View Article]
     [Google Scholar]
  67. Beddek AJ, Li MS, Kroll JS, Jordan TW, Martin DR. Evidence for capsule switching between carried and disease-causing Neisseria meningitidis strains. Infect Immun 2009; 77:2989–2994 [View Article]
     [Google Scholar]
  68. Wyres KL, Gorrie C, Edwards DJ, Wertheim HFL, Hsu LY et al. Extensive capsule locus variation and large-scale genomic recombination within the Klebsiella pneumoniae clonal group 258. Genome Biol Evol 2015; 7:1267–1279 [View Article]
     [Google Scholar]
  69. Haudiquet M, Buffet A, Rendueles O, Rocha EPC. Interplay between the cell envelope and mobile genetic elements shapes gene flow in populations of the nosocomial pathogen Klebsiella pneumoniae. PLoS Biol 2021; 19:e3001276 [View Article]
     [Google Scholar]
  70. HOLLOWAY BW, COOPER GN. Lysogenic conversion in Pseudomonas aeruginosa. J Bacteriol 1962; 84:1321–1324 [View Article]
     [Google Scholar]
  71. Kuzio J, Kropinski AM. O-antigen conversion in Pseudomonas aeruginosa PAO1 by bacteriophage D3. J Bacteriol 1983; 155:203–212 [View Article]
     [Google Scholar]
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A bittersweet fate: detection of serotype switching in Pseudomonas aeruginosa
M Gen 9, 000919 (2023); https://doi.org/10.1099/mgen.0.000919
/content/journal/mgen/10.1099/mgen.0.000919
/content/journal/mgen/10.1099/mgen.0.000919
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