Evidence for a Xer/ System for Chromosome Resolution in Archaea
Homologous recombination events between circular chromosomes, occurring during or after replication, can generate dimers that need to be converted to monomers prior to their segregation at cell division. In Escherichia coli, chromosome dimers are converted to monomers by two paralogous site-specific tyrosine recombinases of the Xer family (XerC/D). The Xer recombinases act at a specific dif site located in the replication termination region, assisted by the cell division protein FtsK. This chromosome resolution system has been predicted in most Bacteria and further characterized for some species. Archaea have circular chromosomes and an active homologous recombination system and should therefore resolve chromosome dimers. Most archaea harbour a single homologue of bacterial XerC/D proteins (XerA), but not of FtsK. Therefore, the role of XerA in chromosome resolution was unclear. Here, we have identified dif-like sites in archaeal genomes by using a combination of modeling and comparative genomics approaches. These sites are systematically located in replication termination regions. We validated our in silico prediction by showing that the XerA protein of Pyrococcus abyssi specifically recombines plasmids containing the predicted dif site in vitro. In contrast to the bacterial system, XerA can recombine dif sites in the absence of protein partners. Whereas Archaea and Bacteria use a completely different set of proteins for chromosome replication, our data strongly suggest that XerA is most likely used for chromosome resolution in Archaea.
Vyšlo v časopise:
Evidence for a Xer/ System for Chromosome Resolution in Archaea. PLoS Genet 6(10): e32767. doi:10.1371/journal.pgen.1001166
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1001166
Souhrn
Homologous recombination events between circular chromosomes, occurring during or after replication, can generate dimers that need to be converted to monomers prior to their segregation at cell division. In Escherichia coli, chromosome dimers are converted to monomers by two paralogous site-specific tyrosine recombinases of the Xer family (XerC/D). The Xer recombinases act at a specific dif site located in the replication termination region, assisted by the cell division protein FtsK. This chromosome resolution system has been predicted in most Bacteria and further characterized for some species. Archaea have circular chromosomes and an active homologous recombination system and should therefore resolve chromosome dimers. Most archaea harbour a single homologue of bacterial XerC/D proteins (XerA), but not of FtsK. Therefore, the role of XerA in chromosome resolution was unclear. Here, we have identified dif-like sites in archaeal genomes by using a combination of modeling and comparative genomics approaches. These sites are systematically located in replication termination regions. We validated our in silico prediction by showing that the XerA protein of Pyrococcus abyssi specifically recombines plasmids containing the predicted dif site in vitro. In contrast to the bacterial system, XerA can recombine dif sites in the absence of protein partners. Whereas Archaea and Bacteria use a completely different set of proteins for chromosome replication, our data strongly suggest that XerA is most likely used for chromosome resolution in Archaea.
Zdroje
1. BlakelyG
MayG
McCullochR
ArciszewskaLK
BurkeM
1993 Two related recombinases are required for site-specific recombination at dif and cer in E. coli K12. Cell 75 351 361
2. BlakelyG
CollomsS
MayG
BurkeM
SherrattD
1991 Escherichia coli XerC recombinase is required for chromosomal segregation at cell division. New Biol 3 789 798
3. ClergetM
1991 Site-specific recombination promoted by a short DNA segment of plasmid R1 and by a homologous segment in the terminus region of the Escherichia coli chromosome. New Biol 3 780 788
4. KuempelPL
HensonJM
DircksL
TecklenburgM
LimDF
1991 dif, a recA-independent recombination site in the terminus region of the chromosome of Escherichia coli. New Biol 3 799 811
5. CarnoyC
RotenCA
2009 The dif/Xer recombination systems in proteobacteria. PLoS One 4 e6531 doi:10.1371/journal.pone.0006531
6. JensenRB
2006 Analysis of the terminus region of the Caulobacter crescentus chromosome and identification of the dif site. J Bacteriol 188 6016 6019
7. NeilsonL
BlakelyG
SherrattDJ
1999 Site-specific recombination at dif by Haemophilus influenzae XerC. Mol Microbiol 31 915 926
8. SciochettiSA
PiggotPJ
BlakelyGW
2001 Identification and characterization of the dif Site from Bacillus subtilis. J Bacteriol 183 1058 1068
9. ValME
KennedySP
El KarouiM
BonneL
ChevalierF
2008 FtsK-dependent dimer resolution on multiple chromosomes in the pathogen Vibrio cholerae. PLoS Genet 4 e1000201 doi:10.1371/journal.pgen.1000201
10. YenMR
LinNT
HungCH
ChoyKT
WengSF
2002 oriC region and replication termination site, dif, of the Xanthomonas campestris pv. campestris 17 chromosome. Appl Environ Microbiol 68 2924 2933
11. BlakelyGW
SherrattDJ
1994 Interactions of the site-specific recombinases XerC and XerD with the recombination site dif. Nucleic Acids Res 22 5613 5620
12. AusselL
BarreFX
AroyoM
StasiakA
StasiakAZ
2002 FtsK is a DNA motor protein that activates chromosome dimer resolution by switching the catalytic state of the XerC and XerD recombinases. Cell 108 195 205
13. BarreFX
AroyoM
CollomsSD
HelfrichA
CornetF
2000 FtsK functions in the processing of a Holliday junction intermediate during bacterial chromosome segregation. Genes Dev 14 2976 2988
14. IpSC
BreguM
BarreFX
SherrattDJ
2003 Decatenation of DNA circles by FtsK-dependent Xer site-specific recombination. EMBO J 22 6399 6407
15. SteinerW
LiuG
DonachieWD
KuempelP
1999 The cytoplasmic domain of FtsK protein is required for resolution of chromosome dimers. Mol Microbiol 31 579 583
16. BigotS
SalehOA
LesterlinC
PagesC
El KarouiM
2005 KOPS: DNA motifs that control E. coli chromosome segregation by orienting the FtsK translocase. EMBO J 24 3770 3780
17. CorreJ
LouarnJM
2002 Evidence from terminal recombination gradients that FtsK uses replichore polarity to control chromosome terminus positioning at division in Escherichia coli. J Bacteriol 184 3801 3807
18. LevyO
PtacinJL
PeasePJ
GoreJ
EisenMB
2005 Identification of oligonucleotide sequences that direct the movement of the Escherichia coli FtsK translocase. Proc Natl Acad Sci U S A 102 17618 17623
19. PeasePJ
LevyO
CostGJ
GoreJ
PtacinJL
2005 Sequence-directed DNA translocation by purified FtsK. Science 307 586 590
20. SivanathanV
AllenMD
de BekkerC
BakerR
ArciszewskaLK
2006 The FtsK gamma domain directs oriented DNA translocation by interacting with KOPS. Nat Struct Mol Biol 13 965 972
21. YatesJ
ZhekovI
BakerR
EklundB
SherrattDJ
2006 Dissection of a functional interaction between the DNA translocase, FtsK, and the XerD recombinase. Mol Microbiol 59 1754 1766
22. Le BourgeoisP
BugarelM
CampoN
Daveran-MingotML
LabonteJ
2007 The unconventional Xer recombination machinery of Streptococci/Lactococci. PLoS Genet 3 e117 doi:10.1371/journal.pgen.0030117
23. HaldenbyS
WhiteMF
AllersT
2009 RecA family proteins in archaea: RadA and its cousins. Biochem Soc Trans 37 102 107
24. SerreMC
DuguetM
2003 Enzymes that cleave and religate DNA at high temperature: the same story with different actors. Prog Nucleic Acid Res Mol Biol 74 37 81
25. KanehisaM
GotoS
KawashimaS
NakayaA
2002 The KEGG databases at GenomeNet. Nucleic Acids Res 30 42 46
26. SherrattDJ
WigleyDB
1998 Conserved themes but novel activities in recombinases and topoisomerases. Cell 93 149 152
27. CaoY
HalletB
SherrattDJ
HayesF
1997 Structure-function correlations in the XerD site-specific recombinase revealed by pentapeptide scanning mutagenesis. J Mol Biol 274 39 53
28. SpiersAJ
SherrattDJ
1997 Relating primary structure to function in the Escherichia coli XerD site-specific recombinase. Mol Microbiol 24 1071 1082
29. SubramanyaHS
ArciszewskaLK
BakerRA
BirdLE
SherrattDJ
1997 Crystal structure of the site-specific recombinase, XerD. EMBO J 16 5178 5187
30. LillestolRK
RedderP
GarrettRA
BruggerK
2006 A putative viral defence mechanism in archaeal cells. Archaea 2 59 72
31. MakarovaKS
GrishinNV
ShabalinaSA
WolfYI
KooninEV
2006 A putative RNA-interference-based immune system in prokaryotes: computational analysis of the predicted enzymatic machinery, functional analogies with eukaryotic RNAi, and hypothetical mechanisms of action. Biol Direct 1 7
32. ZivanovicY
LopezP
PhilippeH
ForterreP
2002 Pyrococcus genome comparison evidences chromosome shuffling-driven evolution. Nucleic Acids Res 30 1902 1910
33. MyllykallioH
LopezP
Lopez-GarciaP
HeiligR
SaurinW
2000 Bacterial mode of replication with eukaryotic-like machinery in a hyperthermophilic archaeon. Science 288 2212 2215
34. LopezP
PhilippeH
MyllykallioH
ForterreP
1999 Identification of putative chromosomal origins of replication in Archaea. Mol Microbiol 32 883 886
35. EddySR
1998 Profile hidden Markov models. Bioinformatics 14 755 763
36. LundgrenM
AnderssonA
ChenL
NilssonP
BernanderR
2004 Three replication origins in Sulfolobus species: synchronous initiation of chromosome replication and asynchronous termination. Proc Natl Acad Sci U S A 101 7046 7051
37. RobinsonNP
DionneI
LundgrenM
MarshVL
BernanderR
2004 Identification of two origins of replication in the single chromosome of the archaeon Sulfolobus solfataricus. Cell 116 25 38
38. HoebekeM
SchbathS
2006 R'MES: Finding Exceptional Motifs, version 3. User guide http://genome.jouy.inra.fr/ssb/rmes
39. SerreMC
LetzelterC
GarelJR
DuguetM
2002 Cleavage properties of an archaeal site-specific recombinase, the SSV1 integrase. J Biol Chem 277 16758 16767
40. HayesF
SherrattDJ
1997 Recombinase binding specificity at the chromosome dimer resolution site dif of Escherichia coli. J Mol Biol 266 525 537
41. CornetF
HalletB
SherrattDJ
1997 Xer recombination in Escherichia coli. Site-specific DNA topoisomerase activity of the XerC and XerD recombinases. J Biol Chem 272 21927 21931
42. ConstantinescoF
ForterreP
KooninEV
AravindL
ElieC
2004 A bipolar DNA helicase gene, herA, clusters with rad50, mre11 and nurA genes in thermophilic archaea. Nucleic Acids Res 32 1439 1447
43. QuaiserA
ConstantinescoF
WhiteMF
ForterreP
ElieC
2008 The Mre11 protein interacts with both Rad50 and the HerA bipolar helicase and is recruited to DNA following gamma irradiation in the archaeon Sulfolobus acidocaldarius. BMC Mol Biol 9 25
44. ZhangS
WeiT
HouG
ZhangC
LiangP
2008 Archaeal DNA helicase HerA interacts with Mre11 homologue and unwinds blunt-ended double-stranded DNA and recombination intermediates. DNA Repair (Amst) 7 380 391
45. IyerLM
MakarovaKS
KooninEV
AravindL
2004 Comparative genomics of the FtsK-HerA superfamily of pumping ATPases: implications for the origins of chromosome segregation, cell division and viral capsid packaging. Nucleic Acids Res 32 5260 5279
46. CollomsSD
AlenC
SherrattDJ
1998 The ArcA/ArcB two-component regulatory system of Escherichia coli is essential for Xer site-specific recombination at psi. Mol Microbiol 28 521 530
47. CornetF
MortierI
PatteJ
LouarnJM
1994 Plasmid pSC101 harbors a recombination site, psi, which is able to resolve plasmid multimers and to substitute for the analogous chromosomal Escherichia coli site dif. J Bacteriol 176 3188 3195
48. StirlingCJ
CollomsSD
CollinsJF
SzatmariG
SherrattDJ
1989 xerB, an Escherichia coli gene required for plasmid ColE1 site-specific recombination, is identical to pepA, encoding aminopeptidase A, a protein with substantial similarity to bovine lens leucine aminopeptidase. EMBO J 8 1623 1627
49. StirlingCJ
SzatmariG
StewartG
SmithMC
SherrattDJ
1988 The arginine repressor is essential for plasmid-stabilizing site-specific recombination at the ColE1 cer locus. EMBO J 7 4389 4395
50. LundgrenM
BernanderR
2007 Genome-wide transcription map of an archaeal cell cycle. Proc Natl Acad Sci U S A 104 2939 2944
51. ForterreP
1999 Displacement of cellular proteins by functional analogues from plasmids or viruses could explain puzzling phylogenies of many DNA informational proteins. Mol Microbiol 33 457 465
52. ForterreP
2002 The origin of DNA genomes and DNA replication proteins. Curr Opin Microbiol 5 525 532
53. CrooksGE
HonG
ChandoniaJM
BrennerSE
2004 WebLogo: a sequence logo generator. Genome Res 14 1188 1190
54. GuindonS
GascuelO
2003 A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52 696 704
55. KimJ
ZwiebC
WuC
AdhyaS
1989 Bending of DNA by gene-regulatory proteins: construction and use of a DNA bending vector. Gene 85 15 23
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2010 Číslo 10
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Genome-Wide Identification of Targets and Function of Individual MicroRNAs in Mouse Embryonic Stem Cells
- Common Genetic Variants and Modification of Penetrance of -Associated Breast Cancer
- Allele-Specific Down-Regulation of Expression Induced by Retinoids Contributes to Climate Adaptations
- Simultaneous Disruption of Two DNA Polymerases, Polη and Polζ, in Avian DT40 Cells Unmasks the Role of Polη in Cellular Response to Various DNA Lesions