1887

Abstract

Rearrangements of large genome fragments occur in bacteria between repeat sequences and can impact on growth and gene expression. Homologous recombination resulting in inversion between indirect repeats and excision/translocation between direct repeats enables these structural changes. One form of rearrangement occurs around ribosomal operons, found in multiple copies across many bacteria, but identification of these rearrangements by sequencing requires reads of several thousand bases to span the ribosomal operons. With long-read sequencing aiding the routine generation of complete bacterial assemblies, we have developed , a typing method for the order and orientation of genome fragments between ribosomal operons. It allows for a single identifier to convey the order and orientation of genome-level structure and we have successfully applied this typing to 433 of the most common bacterial species. In a focused analysis, we observed the presence of multiple structural genotypes in nine bacterial pathogens, underscoring the importance of routinely assessing this form of variation alongside traditional single-nucleotide polymorphism (SNP) typing.

Funding
This study was supported by the:
  • Biotechnology and Biological Sciences Research Council (Award BB/CCG1860/1)
    • Principle Award Recipient: Andrew J. Page
  • Biotechnology and Biological Sciences Research Council (Award BBS/E/F/000PR10352)
    • Principle Award Recipient: Emma V. Ainsworth
  • Biotechnology and Biological Sciences Research Council (Award BBS/E/F/000PR10352)
    • Principle Award Recipient: Gemma C. Langridge
  • Biotechnology and Biological Sciences Research Council (Award BB/R012504/1)
    • Principle Award Recipient: Emma V. Ainsworth
  • Biotechnology and Biological Sciences Research Council (Award BB/R012504/1)
    • Principle Award Recipient: Gemma C. Langridge
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000396
2020-06-25
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/mgen/6/7/mgen000396.html?itemId=/content/journal/mgen/10.1099/mgen.0.000396&mimeType=html&fmt=ahah

References

  1. Brüssow H, Canchaya C, Hardt W-D. Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol Mol Biol Rev 2004; 68:560–602 [View Article][PubMed]
    [Google Scholar]
  2. Sanderson KE, Liu SL. Chromosomal rearrangements in enteric bacteria. Electrophoresis 1998; 19:569–572 [View Article][PubMed]
    [Google Scholar]
  3. Belda E, Moya A, Silva FJ. Genome rearrangement distances and gene order phylogeny in gamma-Proteobacteria. Mol Biol Evol 2005; 22:1456–1467 [View Article][PubMed]
    [Google Scholar]
  4. Chen P, den Bakker HC, Korlach J, Kong N, Storey DB et al. Comparative genomics reveals the diversity of restriction-modification systems and DNA methylation sites in Listeria monocytogenes . Appl Environ Microbiol 2017; 83:e02091–02016 [View Article][PubMed]
    [Google Scholar]
  5. Liu W-Y, Wong C-F, Chung KM-K, Jiang J-W, Leung FC-C. Comparative genome analysis of Enterobacter cloacae . PLoS One 2013; 8:e74487 [View Article][PubMed]
    [Google Scholar]
  6. Tsuru T, Kawai M, Mizutani-Ui Y, Uchiyama I, Kobayashi I. Evolution of paralogous genes: Reconstruction of genome rearrangements through comparison of multiple genomes within Staphylococcus aureus . Mol Biol Evol 2006; 23:1269–1285 [View Article][PubMed]
    [Google Scholar]
  7. Matthews TD, Rabsch W, Maloy S. Chromosomal rearrangements in Salmonella enterica serovar Typhi strains isolated from asymptomatic human carriers. mBio 2011; 2:e00060–00011 [View Article][PubMed]
    [Google Scholar]
  8. Matthews TD, Edwards R, Maloy S. Chromosomal rearrangements formed by rrn recombination do not improve replichore balance in host-specific Salmonella enterica serovars. PLoS One 2010; 5:e13503 [View Article][PubMed]
    [Google Scholar]
  9. Soler-Bistué A, Mondotte JA, Bland MJ, Val M-E, Saleh M-C et al. Genomic location of the major ribosomal protein gene locus determines Vibrio cholerae global growth and infectivity. PLoS Genet 2015; 11:e1005156 [View Article][PubMed]
    [Google Scholar]
  10. Blom J, Kreis J, Spänig S, Juhre T, Bertelli C et al. EDGAR 2.0: an enhanced software platform for comparative gene content analyses. Nucleic Acids Res 2016; 44:W22–W28 [View Article][PubMed]
    [Google Scholar]
  11. Darling AE, Mau B, Perna NT. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 2010; 5:e11147 [View Article][PubMed]
    [Google Scholar]
  12. Carver TJ, Rutherford KM, Berriman M, Rajandream M-A, Barrell BG et al. ACT: the Artemis comparison tool. Bioinformatics 2005; 21:3422–3423 [View Article][PubMed]
    [Google Scholar]
  13. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R et al. Circos: an information aesthetic for comparative genomics. Genome Res 2009; 19:1639–1645 [View Article][PubMed]
    [Google Scholar]
  14. 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][PubMed]
    [Google Scholar]
  15. Ramos PIP, Picão RC, Almeida LGPde, Lima NCB, Girardello R et al. Comparative analysis of the complete genome of KPC-2-producing Klebsiella pneumoniae Kp13 reveals remarkable genome plasticity and a wide repertoire of virulence and resistance mechanisms. BMC Genomics 2014; 15:54 [View Article]
    [Google Scholar]
  16. Fluit AC, Jansen MD, Bosch T, Jansen WTM, Schouls L et al. rRNA operon copy number can explain the distinct epidemiology of hospital-associated methicillin-resistant Staphylococcus aureus . Antimicrob Agents Chemother 2016; 60:7313–7320 [View Article][PubMed]
    [Google Scholar]
  17. Guérillot R, Kostoulias X, Donovan L, Li L, Carter GP et al. Unstable chromosome rearrangements in Staphylococcus aureus cause phenotype switching associated with persistent infections. Proc Natl Acad Sci U S A 2019; 116:20135–20140 [View Article][PubMed]
    [Google Scholar]
  18. Lewis K, cells P. Persister cells.. Annu Rev Microbiol 2010; 64:357–372 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000396
Loading
/content/journal/mgen/10.1099/mgen.0.000396
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL
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