1887

Abstract

Symmetric genomic rearrangements around replication axes in genomes are commonly observed in prokaryotic genomes, including Group A (GAS). However, asymmetric rearrangements are rare. Our previous studies showed that the hypervirulent invasive GAS strain, M23ND, containing an inactivated transcriptional regulator system, , exhibits unique extensive asymmetric rearrangements, which reconstructed a genomic structure distinct from other GAS genomes. In the current investigation, we identified the rearrangement events and examined the genetic consequences and evolutionary implications underlying the rearrangements. By comparison with a close phylogenetic relative, M18-MGAS8232, we propose a molecular model wherein a series of asymmetric rearrangements have occurred in M23ND, involving translocations, inversions and integrations mediated by multiple factors, , rRNA- (factor for late competence), transposons and phage-encoded gene segments. Assessments of the cumulative gene orientations and GC skews reveal that the asymmetric genomic rearrangements did not affect the general genomic integrity of the organism. However, functional distributions reveal re-clustering of a broad set of CovRS-regulated actively transcribed genes, including virulence factors and metabolic genes, to the same leading strand, with high confidence (-value ~10). The re-clustering of the genes suggests a potential selection advantage for the spatial proximity to the transcription complexes, which may contain the global transcriptional regulator, CovRS, and other RNA polymerases. Their proximities allow for efficient transcription of the genes required for growth, virulence and persistence. A new paradigm of survival strategies of GAS strains is provided through multiple genomic rearrangements, while, at the same time, maintaining genomic integrity.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000326
2016-08-01
2021-10-20
Loading full text...

Full text loading...

/deliver/fulltext/micro/162/8/1346.html?itemId=/content/journal/micro/10.1099/mic.0.000326&mimeType=html&fmt=ahah

References

  1. Andersson S. G., Zomorodipour A., Andersson J. O., Sicheritz-Pontén T., Alsmark U. C., Podowski R. M., Näslund A. K., Eriksson A. S., Winkler H. H. et al. 1998; The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396:133–140 [View Article][PubMed]
    [Google Scholar]
  2. Banks D. J., Porcella S. F., Barbian K. D., Beres S. B., Philips L. E., Voyich J. M., DeLeo F. R., Martin J. M., Somerville G. A. et al. 2004; Progress toward characterization of the group A Streptococcus metagenome: complete genome sequence of a macrolide-resistant serotype M6 strain. J Infect Dis 190:727–738 [View Article][PubMed]
    [Google Scholar]
  3. Bao Y., Liang Z., Booyjzsen C., Mayfield J. A., Li Y., Lee S. W., Ploplis V. A., Song H., Castellino F. J. 2014; Unique genomic arrangements in an invasive serotype M23 strain of Streptococcus pyogenes identify genes that induce hypervirulence. J Bacteriol 196:4089–4102 [View Article][PubMed]
    [Google Scholar]
  4. Bao Y. J., Liang Z., Mayfield J. A., Lee S. W., Ploplis V. A., Castellino F. J. 2015; CovRS-regulated transcriptome analysis of a hypervirulent M23 strain of Group A Streptococcus pyogenes provides new insights into virulence determinants. J Bacteriol 197:3191–3205 [View Article][PubMed]
    [Google Scholar]
  5. Bartlett J., Blagojevic J., Carter D., Eskiw C., Fromaget M., Job C., Shamsher M., Trindade I. F., Xu M. et al. 2006; Specialized transcription factories. Biochem Soc Symp67–75 [View Article][PubMed]
    [Google Scholar]
  6. Berge A., Rasmussen M., Björck L. 1998; Identification of an insertion sequence located in a region encoding virulence factors of Streptococcus pyogenes. Infect Immun 66:3449–3453[PubMed]
    [Google Scholar]
  7. Bessen D. E., McShan W. M., Nguyen S., Shetty A., Agrawal S., Tettelin H. 2015; Molecular epidemiology and genomics of group A Streptococcus. Infect Genet Evol 33:393–418 [View Article][PubMed]
    [Google Scholar]
  8. Brewer B. J. 1988; When polymerases collide: replication and the transcriptional organization of the E. coli chromosome. Cell 53:679–686 [View Article][PubMed]
    [Google Scholar]
  9. Campbell A. M. 1992; Chromosomal insertion sites for phages and plasmids. J Bacteriol 174:7495–7499[PubMed]
    [Google Scholar]
  10. Canchaya C., Desiere F., McShan W. M., Ferretti J. J., Parkhill J., Brussow H. 2002; Genome analysis of an inducible prophage and prophage remnants integrated in the Streptococcus pyogenes strain SF370. Virology . 302245–258
  11. Carver T., Berriman M., Tivey A., Patel C., Böhme U., Barrell B. G., Parkhill J., Rajandream M. A. 2008; Artemis and ACT: viewing, annotating and comparing sequences stored in a relational database. Bioinformatics 24:2672–2676 [View Article][PubMed]
    [Google Scholar]
  12. Chakalova L., Debrand E., Mitchell J. A., Osborne C. S., Fraser P. 2005; Replication and transcription: shaping the landscape of the genome. Nat Rev Genet 6:669–677 [View Article][PubMed]
    [Google Scholar]
  13. Cook P. R. 2002; Predicting three-dimensional genome structure from transcriptional activity. Nat Genet 32:347–352 [View Article][PubMed]
    [Google Scholar]
  14. Cournac A., Plumbridge J. 2013; DNA looping in prokaryotes: experimental and theoretical approaches. J Bacteriol 195:1109–1119 [View Article][PubMed]
    [Google Scholar]
  15. Cui L., Neoh H. M., Iwamoto A., Hiramatsu K. 2012; Coordinated phenotype switching with large-scale chromosome flip-flop inversion observed in bacteria. Proc Natl Acad Sci U S A 109:E1647E1656 [View Article][PubMed]
    [Google Scholar]
  16. Darling A. C., Mau B., Blattner F. R., Perna N. T. 2004; Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14:1394–1403 [View Article][PubMed]
    [Google Scholar]
  17. Darling A. E., Miklós I., Ragan M. A. 2008; Dynamics of genome rearrangement in bacterial populations. PLoS Genet 4:e1000128 [View Article][PubMed]
    [Google Scholar]
  18. Delcher A. L., Phillippy A., Carlton J., Salzberg S. L. 2002; Fast algorithms for large-scale genome alignment and comparison. Nucleic Acids Res 30:2478–2483 [View Article][PubMed]
    [Google Scholar]
  19. Diruggiero J., Dunn D., Maeder D. L., Holley-Shanks R., Chatard J., Horlacher R., Robb F. T., Boos W., Weiss R. B. 2000; Evidence of recent lateral gene transfer among hyperthermophilic archaea. Mol Microbiol 38:684–693 [View Article][PubMed]
    [Google Scholar]
  20. Eisen J., Heidelberg J., White O., Salzberg S. 2000; Evidence for symmetric chromosomal inversions around the replication origin in bacteria. Genome Biol 1:research0011.0011–research0011.0019 [CrossRef]
    [Google Scholar]
  21. French S. 1992; Consequences of replication fork movement through transcription units in vivo. Science 258:1362–1365 [View Article][PubMed]
    [Google Scholar]
  22. Graham M. R., Smoot L. M., Migliaccio C. A., Virtaneva K., Sturdevant D. E., Porcella S. F., Federle M. J., Adams G. J., Scott J. R. et al. 2002; Virulence control in group A Streptococcus by a two-component gene regulatory system: global expression profiling and in vivo infection modeling. Proc Natl Acad Sci U S A 99:13855–13860 [View Article][PubMed]
    [Google Scholar]
  23. Green N. M., Zhang S., Porcella S. F., Nagiec M. J., Barbian K. D., Beres S. B., LeFebvre R. B., Musser J. M. 2005; Genome sequence of a serotype M28 strain of group a streptococcus: potential new insights into puerperal sepsis and bacterial disease specificity. J Infect Dis 192:760–770 [View Article][PubMed]
    [Google Scholar]
  24. Grigoriev A. 2000; Graphical genome comparison: rearrangements and replication origin of Helicobacter pylori. Trends Genet 16:376–378 [View Article][PubMed]
    [Google Scholar]
  25. Haack K. R., Roth J. R. 1995; Recombination between chromosomal IS200 elements supports frequent duplication formation in Salmonella typhimurium. Genetics 141:1245–1252[PubMed]
    [Google Scholar]
  26. Hatfull G. F. 2008; Bacteriophage genomics. Curr Opin Microbiol 11:447–453 [View Article][PubMed]
    [Google Scholar]
  27. Helmrich A., Ballarino M., Nudler E., Tora L. 2013; Transcription-replication encounters, consequences and genomic instability. Nat Struct Mol Biol 20:412–418 [View Article][PubMed]
    [Google Scholar]
  28. Holden M. T., Scott A., Cherevach I., Chillingworth T., Churcher C., Cronin A., Dowd L., Feltwell T., Hamlin N. et al. 2007; Complete genome of acute rheumatic fever-associated serotype M5 Streptococcus pyogenes strain manfredo. J Bacteriol 189:1473–1477 [View Article][PubMed]
    [Google Scholar]
  29. Horstmann N., Sahasrabhojane P., Saldaña M., Ajami N. J., Flores A. R., Sumby P., Liu C. G., Yao H., Su X. et al. 2015; Characterization of the effect of the histidine kinase CovS on response regulator phosphorylation in group A Streptococcus. Infect Immun 83:1068–1077 [View Article][PubMed]
    [Google Scholar]
  30. Komoda Y., Enomoto M., Tominaga A. 1991; Large inversion in Escherichia coli K-12 1485IN between inversely oriented IS3 elements near lac and cdd. Genetics 129:639–645[PubMed]
    [Google Scholar]
  31. Kunst F., Ogasawara N., Moszer I., Albertini A. M., Alloni G., Azevedo V., Bertero M. G., Bessières P., Bolotin A. et al. 1997; The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 390:249–256 [View Article][PubMed]
    [Google Scholar]
  32. Lee M. S., Morrison D. A. 1999; Identification of a new regulator in Streptococcus pneumoniae linking quorum sensing to competence for genetic transformation. J Bacteriol 181:5004–5016[PubMed]
    [Google Scholar]
  33. Liu S. L., Sanderson K. E. 1995; Rearrangements in the genome of the bacterium Salmonella typhi. Proc Natl Acad Sci U S A 92:1018–1022 [View Article][PubMed]
    [Google Scholar]
  34. Lobry J. R. 1996; Asymmetric substitution patterns in the two DNA strands of bacteria. Mol Biol Evol 13:660–665 [View Article][PubMed]
    [Google Scholar]
  35. Mahillon J., Chandler M. 1998; Insertion sequences. Microbiol Mol Biol Rev 62:725–774[PubMed]
    [Google Scholar]
  36. McShan W. M., Ferretti J. J. 1997; Genetic diversity in temperate bacteriophages of Streptococcus pyogenes: identification of a second attachment site for phages carrying the erythrogenic toxin A gene. J Bacteriol 179:6509–6511[PubMed]
    [Google Scholar]
  37. McShan W. M., Tang Y. F., Ferretti J. J. 1997; Bacteriophage T12 of Streptococcus pyogenes integrates into the gene encoding a serine tRNA. Mol Microbiol 23:719–728 [View Article][PubMed]
    [Google Scholar]
  38. Merrikh H., Zhang Y., Grossman A. D., Wang J. D. 2012; Replication-transcription conflicts in bacteria. Nat Rev Microbiol 10:449–458 [View Article][PubMed]
    [Google Scholar]
  39. Nakagawa I., Kurokawa K., Yamashita A., Nakata M., Tomiyasu Y., Okahashi N., Kawabata S., Yamazaki K., Shiba T. et al. 2003; Genome sequence of an M3 strain of Streptococcus pyogenes reveals a large-scale genomic rearrangement in invasive strains and new insights into phage evolution. Genome Res 13:1042–1055 [View Article][PubMed]
    [Google Scholar]
  40. Novick R. P., Christie G. E., Penadés J. R. 2010; The phage-related chromosomal islands of Gram-positive bacteria. Nat Rev Microbiol 8:541–551 [View Article][PubMed]
    [Google Scholar]
  41. Okazaki R., Okazaki T., Sakabe K., Sugimoto K. 1967; Mechanism of DNA replication possible discontinuity of DNA chain growth. Jpn J Med Sci Biol 20:255–260[PubMed]
    [Google Scholar]
  42. Osborne C. S., Chakalova L., Brown K. E., Carter D., Horton A., Debrand E., Goyenechea B., Mitchell J. A., Lopes S. et al. 2004; Active genes dynamically colocalize to shared sites of ongoing transcription. Nat Genet 36:1065–1071 [View Article][PubMed]
    [Google Scholar]
  43. Papantonis A., Cook P. R. 2013; Transcription factories: genome organization and gene regulation. Chem Rev 113:8683–8705 [View Article][PubMed]
    [Google Scholar]
  44. Parkhill J., Wren B. W., Thomson N. R., Titball R. W., Holden M. T., Prentice M. B., Sebaihia M., James K. D., Churcher C. et al. 2001; Genome sequence of Yersinia pestis, the causative agent of plague. Nature 413:523–527 [View Article][PubMed]
    [Google Scholar]
  45. Read T. D., Brunham R. C., Shen C., Gill S. R., Heidelberg J. F., White O., Hickey E. K., Peterson J., Utterback T. et al. 2000; Genome sequences of Chlamydia trachomatis MoPn and Chlamydia pneumoniae AR39. Nucleic Acids Res 28:1397–1406 [View Article][PubMed]
    [Google Scholar]
  46. Roberts J. W., Roberts C. W. 1975; Proteolytic cleavage of bacteriophage lambda repressor in induction. Proc Natl Acad Sci U S A 72:147–151 [View Article][PubMed]
    [Google Scholar]
  47. Rocha E. P., Danchin A., Viari A. 1999; Universal replication biases in bacteria. Mol Microbiol 32:11–16 [View Article][PubMed]
    [Google Scholar]
  48. Rocha E. 2002; Is there a role for replication fork asymmetry in the distribution of genes in bacterial genomes?. Trends Microbiol 10:393–395 [View Article][PubMed]
    [Google Scholar]
  49. Sakabe K., Okazaki R. 1966; A unique property of the replicating region of chromosomal DNA. Biochim Biophys Acta 129:651–654 [View Article][PubMed]
    [Google Scholar]
  50. Scott J., Thompson-Mayberry P., Lahmamsi S., King C. J., McShan W. M. 2008; Phage-associated mutator phenotype in group A streptococcus. J Bacteriol 190:6290–6301 [View Article][PubMed]
    [Google Scholar]
  51. Smoot J. C., Barbian K. D., Van Gompel J. J., Smoot L. M., Chaussee M. S., Sylva G. L., Sturdevant D. E., Ricklefs S. M., Porcella S. F. et al. 2002; Genome sequence and comparative microarray analysis of serotype M18 group A Streptococcus strains associated with acute rheumatic fever outbreaks. Proc Natl Acad Sci U S A 99:4668–4673 [View Article][PubMed]
    [Google Scholar]
  52. Tillier E. R., Collins R. A. 2000a; The contributions of replication orientation, gene direction, and signal sequences to base-composition asymmetries in bacterial genomes. J Mol Evol 50:249–257
    [Google Scholar]
  53. Tillier E. R. M., Collins R. A. 2000b; Genome rearrangement by replication-directed translocation. Nature Genetics 26:195–197 [View Article]
    [Google Scholar]
  54. Tse H., Bao J. Y., Davies M. R., Maamary P., Tsoi H. W., Tong A. H., Ho T. C., Lin C. H., Gillen C. M. et al. 2012; Molecular characterization of the 2011 Hong Kong scarlet fever outbreak. J Infect Dis 206:341–351 [View Article][PubMed]
    [Google Scholar]
  55. Wang W., Li G. W., Chen C., Xie X. S., Zhuang X. 2011; Chromosome organization by a nucleoid-associated protein in live bacteria. Science 333:1445–1449 [View Article][PubMed]
    [Google Scholar]
  56. Zawilak A., Cebrat S., Mackiewicz P., Król-Hulewicz A., Jakimowicz D., Messer W., Gosciniak G., Zakrzewska-Czerwinska J. 2001; Identification of a putative chromosomal replication origin from Helicobacter pylori and its interaction with the initiator protein DnaA. Nucleic Acids Res 29:2251–2259 [View Article][PubMed]
    [Google Scholar]
  57. Zhang Z., Schwartz S., Wagner L., Miller W. 2000; A greedy algorithm for aligning DNA sequences. J Comput Biol 7:203–214 [View Article][PubMed]
    [Google Scholar]
  58. Zivanovic Y., Lopez P., Philippe H., Forterre P. 2002; Pyrococcus genome comparison evidences chromosome shuffling-driven evolution. Nucleic Acids Res 30:1902–1910 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000326
Loading
/content/journal/micro/10.1099/mic.0.000326
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

Most cited this month 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