Alternative Sigma Factor σ Modulates Prophage Integration and Excision in

English version České info

The prophage is one of the most important components of variable regions in bacterial genomes. Some prophages carry additional genes that may enhance the toxicity and survival ability of their host bacteria. This phenomenon is predominant in Staphylococcus aureus, a very common human pathogen. Bioinformatics analysis of several staphylococcal prophages revealed a highly conserved 40-bp untranslated region upstream of the int gene. A small transcript encoding phage integrase was identified to be initiated from the region, demonstrating that the untranslated region contained a promoter for int. No typical recognition sequence for either σ^A or σ^B was identified in the 40-bp region. Experiments both in vitro and in vivo demonstrated that σ^H recognized the promoter and directed transcription. Genetic deletion of sigH altered the int expression, and subsequently, the excision proportion of prophage DNAs. Phage assays further showed that sigH affected the ability of spontaneous lysis and lysogenization in S. aureus, suggesting that sigH plays a role in stabilizing the lysogenic state. These findings revealed a novel mechanism of prophage integration specifically regulated by a host-source alternative sigma factor. This mechanism suggests a co-evolution strategy of staphylococcal prophages and their host bacteria.

Vyšlo v časopise: Alternative Sigma Factor σ Modulates Prophage Integration and Excision in. PLoS Pathog 6(5): e32767. doi:10.1371/journal.ppat.1000888
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1000888

Souhrn

Zdroje

1. BoydEF

M.DavisB

HochhutB

2001 Bacteriophage–bacteriophage interactions in the evolution of pathogenic bacteria. Trends Microbiol 9 137 144

2. CanchayaC

FournousG

BrüssowH

2004 The impact of prophages on bacterial chromosomes. Mol Microbiol 53 9 18

3. GoerkeC

PantucekR

HoltfreterS

SchulteB

ZinkM

2009 Diversity of prophages in dominant Staphylococcus aureus clonal lineages. J Bacteriol 191 3462 3468

4. BabaT

BaeT

SchneewindO

TakeuchiF

HiramatsuK

2008 Genome Sequence of Staphylococcus aureus Strain Newman and Comparative Analysis of Staphylococcal Genomes: Polymorphism and Evolution of Two Major Pathogenicity Islands. J Bacteriol 190 300 310

5. BaeT

BabaT

HiramatsuK

SchneewindO

2006 Prophages of Staphylococcus aureus Newman and their contribution to virulence. Mol Microbiol 62 1035 1047

6. Bru″ssowH

CanchayaC

HardtW-D

2004 Phages and the Evolution of Bacterial Pathogens: from Genomic Rearrangements to Lysogenic Conversion. Microbiol Mol Biol Rev 68 560 602

7. HoldenMTG

FeilEJ

LindsayJA

PeacockSJ

DayNPJ

2004 Complete genomes of two clinical Staphylococcus aureus strains: Evidence for the rapid evolution of virulence and drug resistance. PNAS 101 9786 9791

8. ChenJ

NovickRP

2009 Phage-Mediated Intergeneric Transfer of Toxin Genes. Science 323 139 141

9. UbedaC

OlivarezNP

BarryP

WangH

KongX

2009 Specificity of staphylococcal phage and SaPI DNA packaging as revealed by integrase and terminase mutations. Mol Microbiol 72 98 108

10. WuS

HdLencastre

TomaszA

1996 Sigma-B, a putative operon encoding alternate sigma factor of Staphylococcus aureus RNA polymerase: molecular cloning and DNA sequencing. J Bacteriol 178 6036 6042

11. MorikawaK

InoseY

OkamuraH

MaruyamaA

HayashiH

2003 A new staphylococcal sigma factor in the conserved gene cassette: functional significance and implication for the evolutionary processes. Genes Cells 8 699 712

12. ShawLN

LindholmC

PrajsnarTK

MillerHK

BrownMC

2008 Identification and Characterization of sigmaS, a Novel Component of the Staphylococcus aureus Stress and Virulence Responses. PLoS ONE 3 e3844

13. SennMM

GiachinoP

HomerovaD

SteinhuberA

StrassnerJ

2005 Molecular Analysis and Organization of the sigB Operon in Staphylococcus aureus. J Bacteriol 8006 8019

14. Pane'-Farre'J

JonasB

Fo″rstnerK

EngelmannS

HeckerM

2006 The sigmaB regulon in Staphylococcus aureus and its regulation. Int J Medic Microbiol 296 237 258

15. WeirJ

PredichM

DubnauE

NairG

SmithI

1991 Regulation of spo0H, a Gene Coding for the Bacillus subtilis sigmaH Factor. J Bacteriol 173 521 529

16. HatfullGF

2008 Bacteriophage genomics. Curr Opin Microbiol 11 447 453

17. KanekoJ

KimuraT

NaritaS

TomitaT

KamioY

1998 Complete nucleotide sequence and molecular characterization of the temperate staphylococcal bacteriophage φPVL carrying Panton–Valentine leukocidin genes. Gene 215 57 67

18. KwanT

LiuJ

DuBowM

GrosP

PelletierJ

2005 The complete genomes and proteomes of 27 Staphylococcus aureus bacteriophages. PNAS 102 5174 5179

19. NaritaaS

KanekoaJ

ChibaaJ

PiémontbY

JarraudcS

2001 Phage conversion of Panton-Valentine leukocidin in Staphylococcus aureus: molecular analysis of a PVL-converting phage, φSLT. Gene 268 195 206

20. TallentSM

LangstonTB

MoranRG

ChristieGE

2007 Transducing Particles of Staphylococcus aureus Pathogenicity Island SaPI1 Are Comprised of Helper Phage-Encoded Proteins. J Bacteriol 189 7520 7524

21. YamaguchiT

HayashiT

TakamiH

NakasoneK

OhnishiM

2000 Phage conversion of exfoliative toxin A production in Staphylococcus aureus. Mol Microbiol 38 694 705

22. MaXX

ItoT

ChongtrakoolP

HiramatsuK

2006 Predominance of Clones Carrying Panton-Valentine Leukocidin Genes among Methicillin-Resistant Staphylococcus aureus Strains Isolated in Japanese Hospitals from 1979 to 1985. J Clin Microbiol 44 4515 4527

23. LucchiniS

DesiereF

BrussowH

1999 Similarly organized lysogeny modules in temperate Siphoviridae from low GC content gram-positive bacteria. Virology 263 427 435

24. IandoloJJ

WorrellV

GroicherKH

QianY

TianR

2002 Comparative analysis of the genomes of the temperate bacteriophages phi11, phi12 and phi13 of Staphylococcus aureus 8325. Gene 289 109 118

25. ZouD

KanekoJ

NaritaS

KamioY

2000 Prophage, ФPV83-pro, Carrying Panton-Valentine Leukocidin Genes, on the Staphylococcus aureus P83 Chromosome: Comparative Analysis of the Genome Structures of ФPV83-pro, ФPVL, Ф11, and Other Phages. Biosci Biotechnol Biochem 64 2631 2643

26. BabaT

TakeuchiF

Makoto KurodaHY

AokiK

OguchiA

2002 Genome and virulence determinants of high virulence community-acquired MRSA. Lancet 359 1819 1827

27. NovickR

1967 Properties of a cryptic high-frequency transducing phage in Staphylococcus aureus. Virology 33 155 166

28. SumbyP

WaldorMK

2003 Transcription of the Toxin Genes Present within the Staphylococcal Phage ΦSa3ms is Intimately Linked with the Phage's Life Cycle. J Bacteriol 185 6841 6851

29. HaldimannA

WannerBL

2001 Conditional-Replication, Integration, Excision, and Retrieval Plasmid-Host Systems for Gene Structure-Function Studies of Bacteria. J Bacteriol 183 6384 6393

30. ConnellN

HanZ

MorenoF

Kolter.R

1987 An E. coli promoter induced by the cessation of growth. Mol Microbiol 1 195

31. HasanN

KoobM

SzybalskW

1994 Escherichia coli genome targeting, I. Cre-lox-mediated in vitro generation of ori- plasmids and their in vivo chromosomal integration and retrieval. Gene 150 51 56

32. VenturaM

CanchayaC

PridmoreRD

Bru″ssowH

2004 The prophages of Lactobacillus johnsonii NCC 533: comparative genomics and transcription analysis. Virology 320 229 242

33. VenturaM

CanchayaC

BerniniV

AltermannE

BarrangouR

2006 Comparative Genomics and Transcriptional Analysis of Prophages Identified in the Genomes of Lactobacillus gasseri, Lactobacillus salivarius, and Lactobacillus casei. Appl Environ Microbiol 72 3130 3146

34. NeveH

FreudenbergW

Diestel-FeddersenF

EhlertR

HellerKJ

2003 Biology of the temperate Streptococcus thermophilus bacteriophage TP-J34 and physical characterization of the phage genome. Virology 315 184 194

35. DenouE

PridmoreRD

VenturaM

PittetA-C

ZwahlenM-C

2008 The Role of Prophage for Genome Diversification within a Clonal Lineage of Lactobacillus johnsonii: Characterization of the Defective Prophage LJ771. J Bacteriol 190 5806 5813

36. LundeM

BlatnyJM

LillehaugD

AastveitAH

NesIF

2003 Use of Real-Time Quantitative PCR for the Analysis of phiLC3 Prophage Stability in Lactococci. Appl Environ Microbiol 69 41 48

37. NashHA

1981 Integration and Excision of Bacteriophage Lambda: The Mechanism of Conservative Site Specific Recombination. Annu Rev Genet 15 143 167

38. QiuX

GurkarAU

LoryS

2006 Interstrain transfer of the large pathogenicity island (PAPI-1) of Pseudomonas aeruginosa. PNAS 103 19830 19835

39. CraigNL

1988 The Mechanism of Conservative Site-specific Recombination. Annu Rev Genet 22 77 105

40. CasjensS

2003 Prophages and bacterial genomics: what have we learned so far? Mol Microbiol 49 277 300

41. MizuuchiM

MizuuchiK

1980 Integrative recombination of bacteriophage lambda: Extent of the DNA sequence involved in attachment site function. PNAS 77 3220 3224

42. Nunes-DübySE

KwonHJ

TirumalaiRS

EllenbergerT

LandyA

1998 Similarities and differences among 105 members of the Int family of site-specific recombinases. Nucleic Acids Res 26 391 406

43. CarrollD

KehoeMA

CavanaghD

ColemanDC

1995 Novel organization of the site–specific recombination functions of the Staphylococcus aureus serotype F virulence-converting phages phi13 and phi42. Mol Microbiol 16 877 893

44. DubnauD

1991 Genetic Competence in Bacillus subtilis. Microbiol Rev 55 395 424

45. KatzirN

OppenheimA

BerfortM

OppenheimAB

1976 Activation of the Lambda int gene by the cii and ciii gene products. Virology 74 324 331

46. HoY-S

WulffDL

RosenbergM

1983 Bacteriophage λ protein cII binds promoters on the opposite face of the DNA helix from RNA polymerase. Nature 304 703 708

47. OppenheimAB

KobilerO

StavansJ

CourtDL

AdhyaS

2005 Switches in Bacteriophage Lambda Development. Annu Rev Genet 39 409 429

48. KreiswirthBN

LofdahlS

BetleyMJ

O'ReillyM

SchlievertPM

1983 The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature 305 709 712

49. ArnaudM

ChastanetA

De'barbouilleM

2004 New Vector for Efficient Allelic Replacement in Naturally Nontransformable, Low-GC-Content, Gram-Positive Bacteria. Appl Environ Microbiol 70 6887 6891

50. GerhardtP

KriegNR

MurrayRGE

WoodWA

1994 Methods for General and Molecular Bacteriology: Washington, D.C.: American Society for Microbiology

51. ThompsonJK

HartMGR

1981 Novel Patterns of Ultraviolet Mutagenesis and Weigle Reactivation in Staphylococcus aureus and Phage Ф11. J Gen Microbiol 124 147 157

52. HersheyAD

KalmansonG

BronfenbrennerJ

1943 Quantitative Method in the Study of the Phage-Antiphage Reaction. J Immunol 46 267 279