1887

Abstract

is a gut commensal of the gastro-digestive tract, but also known as nosocomial pathogen among hospitalized patients. Population genetics based on whole-genome sequencing has revealed that strains from hospitalized patients form a distinct clade, designated clade A1, and that plasmids are major contributors to the emergence of nosocomial . Here we further explored the adaptive evolution of using a genome-wide co-evolution study (GWES) to identify co-evolving single-nucleotide polymorphisms (SNPs). We identified three genomic regions harbouring large numbers of SNPs in tight linkage that are not proximal to each other based on the completely assembled chromosome of the clade A1 reference hospital isolate AUS0004. Close examination of these regions revealed that they are located at the borders of four different types of large-scale genomic rearrangements, insertion sites of two different genomic islands and an IS-like transposon. In non-clade A1 isolates, these regions are adjacent to each other and they lack the insertions of the genomic islands and IS-like transposon. Additionally, among the clade A1 isolates there is one group of pet isolates lacking the genomic rearrangement and insertion of the genomic islands, suggesting a distinct evolutionary trajectory. analysis of the biological functions of the genes encoded in three regions revealed a common link to a stress response. This suggests that these rearrangements may reflect adaptation to the stringent conditions in the hospital environment, such as antibiotics and detergents, to which bacteria are exposed. In conclusion, to our knowledge, this is the first study using GWES to identify genomic rearrangements, suggesting that there is considerable untapped potential to unravel hidden evolutionary signals from population genomic data.

Funding
This study was supported by the:
  • Joint Programming Initiative on Antimicrobial Resistance (Award JPIAMR2016-AC16)
    • Principle Award Recipient: RobJ.L. Willems
  • This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial License.
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2020-11-30
2021-10-24
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References

  1. Weiner LM, Webb AK, Limbago B, Dudeck MA, Patel J et al. Antimicrobial-Resistant pathogens associated with healthcare-associated infections: summary of data reported to the National healthcare safety network at the centers for disease control and prevention, 2011-2014. Infect Control Hosp Epidemiol 2016; 37:1288–1301 [View Article][PubMed]
    [Google Scholar]
  2. Lebreton F, Willems RJL, Gilmore MS. Enterococcus diversity, origins in nature, and gut colonization. In: Enterococci: from commensals to leading causes of drug resistant infection [Internet]; 20141–56
  3. Gilmore MS, Lebreton F, van Schaik W. Genomic transition of enterococci from gut commensals to leading causes of multidrug-resistant hospital infection in the antibiotic era. Curr Opin Microbiol 2013; 16:10–16 p. [View Article][PubMed]
    [Google Scholar]
  4. Guzman Prieto AM, van Schaik W, Rogers MRC, Coque TM, Baquero F et al. Global emergence and dissemination of enterococci as nosocomial pathogens: attack of the clones?. Front Microbiol 2016; 7:788 [View Article][PubMed]
    [Google Scholar]
  5. Galloway-Peña J, Roh JH, Latorre M, Qin X, Murray BE. Genomic and SNP analyses demonstrate a distant separation of the hospital and community-associated clades of Enterococcus faecium . PLoS One 2012; 7:e30187 [View Article][PubMed]
    [Google Scholar]
  6. Palmer KL, Godfrey P, Griggs A, Kos VN, Zucker J et al. Comparative genomics of enterococci: variation in Enterococcus faecalis, clade structure in E. faecium and defining characteristics of E.gallinarum and E.casseliflavus . MBio 2012; 3:1–11 [View Article]
    [Google Scholar]
  7. Lebreton F, van Schaik W, McGuire AM, Godfrey P, Griggs A et al. Emergence of epidemic multidrug-resistant Enterococcus faecium from animal and commensal strains. mBio 2013; 4:e00534-13 20 Aug 2013 [View Article][PubMed]
    [Google Scholar]
  8. Raven KE, Reuter S, Reynolds R, Brodrick HJ, Russell JE et al. A decade of genomic history for healthcare-associated Enterococcus faecium in the United Kingdom and Ireland. Genome Res 2016; 26:1388–1396 [View Article][PubMed]
    [Google Scholar]
  9. Arredondo-Alonso S, Top J, McNally A, Puranen S, Pesonen M et al. Plasmids shaped the recent emergence of the major nosocomial pathogen Enterococcus faecium . mBio 2020; 11:1–17 [View Article][PubMed]
    [Google Scholar]
  10. Rios R, Reyes J, Carvajal LP, Rincon S, Panesso D et al. Genomic epidemiology of Vancomycin-Resistant Enterococcus faecium (VREfm) in Latin America: revisiting the global VRE population structure. Sci Rep 2020; 10:5636 Available from [View Article][PubMed]
    [Google Scholar]
  11. Arredondo-Alonso S, Rogers MRC, Braat JC, Verschuuren TD, Top J et al. mlplasmids: a user-friendly tool to predict plasmid- and chromosome-derived sequences for single species. Microb Genom 2018; 4: 01 11 2018 [View Article][PubMed]
    [Google Scholar]
  12. Lagator M, Colegrave N, Neve P. Selection history and epistatic interactions impact dynamics of adaptation to novel environmental stresses. Proc Biol Sci 2014; 281:20141679 Available from [View Article][PubMed]
    [Google Scholar]
  13. Puranen S, Pesonen M, Pensar J, Xu YY, Lees JA et al. SuperDCA for genome-wide epistasis analysis. Microb Genom 2018; 4: 29 05 2018 [View Article][PubMed]
    [Google Scholar]
  14. Lam MMC, Seemann T, Bulach DM, Gladman SL, Chen H et al. Comparative analysis of the first complete Enterococcus faecium genome. J Bacteriol 2012; 194:2334–2341 [View Article][PubMed]
    [Google Scholar]
  15. Wang E, Bauer MC, Rogstam A, Linse S, Logan DT et al. Structure and functional properties of the Bacillus subtilis transcriptional repressor Rex. Mol Microbiol 2008; 69:466–478 [View Article][PubMed]
    [Google Scholar]
  16. Elsholz AKW, Birk MS, Charpentier E, Turgay K. Functional diversity of AAA+ protease complexes in Bacillus subtilis . Front Mol Biosci 2017; 4:1–15 [View Article]
    [Google Scholar]
  17. Hurme R, Berndt KD, Namork E, Rhen M. DNA binding exerted by a bacterial gene regulator with an extensive coiled-coil domain. J Biol Chem 1996; 271:12626–12631 [View Article][PubMed]
    [Google Scholar]
  18. Hurme R, Berndt KD, Normark SJ, Rhen M. A proteinaceous gene regulatory thermometer in Salmonella . Cell 1997; 90:55–64 [View Article][PubMed]
    [Google Scholar]
  19. Alves MS, Dadalto SP, Gonçalves AB, de Souza GB, Barros VA et al. Transcription factor functional protein-protein interactions in plant defense responses. Proteomes 2014; 2:85–106 [View Article][PubMed]
    [Google Scholar]
  20. Maruyama A, Kumagai Y, Morikawa K, Taguchi K, Hayashi H et al. Oxidative-stress-inducible qorA encodes an NADPH-dependent quinone oxidoreductase catalysing a one-electron reduction in Staphylococcus aureus . Microbiology 2003; 149:389–398 [View Article][PubMed]
    [Google Scholar]
  21. Shah P, Romero DG, Swiatlo E. Role of polyamine transport in Streptococcus pneumoniae response to physiological stress and murine septicemia. Microb Pathog 2008; 45:167–172 [View Article][PubMed]
    [Google Scholar]
  22. Murata T, Kawano M, Igarashi K, Yamato I, Kakinuma Y. Catalytic properties of Na(+)-translocating V-ATPase in Enterococcus hirae . Biochim Biophys Acta 2001; 1505:75–81 [View Article][PubMed]
    [Google Scholar]
  23. Heikens E, van Schaik W, Leavis HL, Bonten MJM, Willems RJL. Identification of a novel genomic island specific to hospital-acquired clonal complex 17 Enterococcus faecium isolates. Appl Environ Microbiol 2008; 74:7094–7097 [View Article][PubMed]
    [Google Scholar]
  24. Zhang X, Top J, de Been M, Bierschenk D, Rogers M et al. Identification of a genetic determinant in clinical Enterococcus faecium strains that contributes to intestinal colonization during antibiotic treatment. J Infect Dis 2013; 207:1780–1786 [View Article][PubMed]
    [Google Scholar]
  25. Yan W, Wei S, Wang Q, Xiao X, Zeng Q et al. Genome rearrangement shapes Prochlorococcus ecological adaptation. Appl Environ Microbiol 2018; 84:e01178–18 [View Article][PubMed]
    [Google Scholar]
  26. Wu X, Monchy S, Taghavi S, Zhu W, Ramos J et al. Comparative genomics and functional analysis of niche-specific adaptation in Pseudomonas putida . FEMS Microbiol Rev 2011; 35:299–323 [View Article][PubMed]
    [Google Scholar]
  27. Qin X, Galloway-Peña JR, Sillanpaa J, Roh JH, Nallapareddy SR et al. Complete genome sequence of Enterococcus faecium strain TX16 and comparative genomic analysis of Enterococcus faecium genomes. BMC Microbiol 2012; 12:1 [View Article][PubMed]
    [Google Scholar]
  28. Lam MMC, Seemann T, Tobias NJ, Chen H, Haring V et al. Comparative analysis of the complete genome of an epidemic hospital sequence type 203 clone of vancomycin-resistant Enterococcus faecium . BMC Genomics 2013; 14:1 [View Article][PubMed]
    [Google Scholar]
  29. Repar J, Warnecke T. Non-Random inversion landscapes in prokaryotic genomes are shaped by heterogeneous selection pressures. Mol Biol Evol 2017; 34:1902–1911 [View Article][PubMed]
    [Google Scholar]
  30. Hegstad K, Mikalsen T, Coque TM, Werner G, Sundsfjord A. Mobile genetic elements and their contribution to the emergence of antimicrobial resistant Enterococcus faecalis and Enterococcus faecium . Clin Microbiol Infect 2010; 16:541–554 Available from [View Article][PubMed]
    [Google Scholar]
  31. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017; 13:e1005595–22 [View Article]
    [Google Scholar]
  32. Yu G, Smith DK, Zhu H, Guan Y, Lam Tommy Tsan‐Yuk. ggtree : an r package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol Evol 2017; 8:28–36 [View Article]
    [Google Scholar]
  33. 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]
  34. 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]
  35. Krumsiek J, Arnold R, Rattei T. Gepard: a rapid and sensitive tool for creating dotplots on genome scale. Bioinformatics 2007; 23:1026–1028 [View Article][PubMed]
    [Google Scholar]
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