Temperate Phages Acquire DNA from Defective Prophages by Relaxed Homologous Recombination: The Role of Rad52-Like Recombinases
Temperate bacteriophages (or phages) are bacterial viruses that, unlike virulent phages, have the ability to enter a prophage dormant state upon infection, in which they stably replicate with the bacterial genome. A majority of bacterial genomes contain multiple active or defective prophages, and numerous bacterial phenotypes are modified by these prophages, such as increased virulence. These mobile genetic elements are subject to high levels of genetic exchanges, through which new genes are constantly imported into bacterial genomes. Phage-encoded homologous recombination enzymes, or recombinases, are potentially key actors in phage genome shuffling. In this work, we show that gene acquisition in temperate phages is strongly dependent on the presence of sequence homology, but is highly tolerant to divergence. We report that gene exchanges are mainly catalyzed by recombinases found on temperate phages, and show that four different Rad52-like recombinases have a relaxed fidelity in vivo, compared to RecA. This high capacity of exchange speeds up evolution of phages, and indirectly also the evolution of bacteria.
Vyšlo v časopise:
Temperate Phages Acquire DNA from Defective Prophages by Relaxed Homologous Recombination: The Role of Rad52-Like Recombinases. PLoS Genet 10(3): e32767. doi:10.1371/journal.pgen.1004181
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1004181
Souhrn
Temperate bacteriophages (or phages) are bacterial viruses that, unlike virulent phages, have the ability to enter a prophage dormant state upon infection, in which they stably replicate with the bacterial genome. A majority of bacterial genomes contain multiple active or defective prophages, and numerous bacterial phenotypes are modified by these prophages, such as increased virulence. These mobile genetic elements are subject to high levels of genetic exchanges, through which new genes are constantly imported into bacterial genomes. Phage-encoded homologous recombination enzymes, or recombinases, are potentially key actors in phage genome shuffling. In this work, we show that gene acquisition in temperate phages is strongly dependent on the presence of sequence homology, but is highly tolerant to divergence. We report that gene exchanges are mainly catalyzed by recombinases found on temperate phages, and show that four different Rad52-like recombinases have a relaxed fidelity in vivo, compared to RecA. This high capacity of exchange speeds up evolution of phages, and indirectly also the evolution of bacteria.
Zdroje
1. D'HerelleF (1917) On an invisible microbe antagonistic toward dysenteric bacilli. Compte Rendu de l'Académie des Sciences 165: 373–375.
2. TwortFW (1915) An Investigation on the Nature of ultra-microscopic Viruses. The Lancet 2: 1241–1243.
3. KristensenDM, WallerAS, YamadaT, BorkP, MushegianAR, et al. (2013) Orthologous gene clusters and taxon signature genes for viruses of prokaryotes. J Bacteriol 195 (5) 941–50.
4. DuffyS, ShackeltonLA, HolmesEC (2008) Rates of evolutionary change in viruses: patterns and determinants. Nat Rev Genet 9: 267–276.
5. SanjuanR, NebotMR, ChiricoN, ManskyLM, BelshawR (2010) Viral mutation rates. J Virol 84: 9733–9748.
6. BakerJ, LimbergerR, SchneiderSJ, CampbellA (1991) Recombination and modular exchange in the genesis of new lambdoid phages. New Biol 3: 297–308.
7. van der WaltE, RybickiEP, VarsaniA, PolstonJE, BillharzR, et al. (2009) Rapid host adaptation by extensive recombination. J Gen Virol 90: 734–746.
8. MuylkensB, FarnirF, MeurensF, SchyntsF, VanderplasschenA, et al. (2009) Coinfection with two closely related alphaherpesviruses results in a highly diversified recombination mosaic displaying negative genetic interference. J Virol 83: 3127–3137.
9. HatfullGF (2008) Bacteriophage genomics. Curr Opin Microbiol 11: 447–453.
10. NiwaO, YamagishiH, OzekiH (1978) Sequence homology in DNA molecules of temperate phages phi81, phi80 and lambda. Mol Gen Genet 159: 259–268.
11. HendrixRW (2003) Bacteriophage genomics. Curr Opin Microbiol 6: 506–511.
12. CanchayaC, ProuxC, FournousG, BruttinA, BrussowH (2003) Prophage genomics. Microbiol Mol Biol Rev 67: 238–276 table of contents.
13. BotsteinD (1980) A theory of modular evolution for bacteriophages. Ann N Y Acad Sci 354: 484–490.
14. LawrenceJG, HatfullGF, HendrixRW (2002) Imbroglios of viral taxonomy: genetic exchange and failings of phenetic approaches. J Bacteriol 184: 4891–4905.
15. BrussowH, DesiereF (2001) Comparative phage genomics and the evolution of Siphoviridae: insights from dairy phages. Mol Microbiol 39: 213–222.
16. HayashiT, MakinoK, OhnishiM, KurokawaK, IshiiK, et al. (2001) Complete genome sequence of enterohemorrhagic Escherichia coli O157:H7 and genomic comparison with a laboratory strain K-12. DNA Res 8: 11–22.
17. BobayLM, RochaEP, TouchonM (2013) The adaptation of temperate bacteriophages to their host genomes. Mol Biol Evol 30: 737–751.
18. TenaillonO, SkurnikD, PicardB, DenamurE (2010) The population genetics of commensal Escherichia coli. Nat Rev Microbiol 8: 207–217.
19. MartinsohnJT, RadmanM, PetitMA (2008) The lambda red proteins promote efficient recombination between diverged sequences: implications for bacteriophage genome mosaicism. PLoS Genet 4: e1000065.
20. ClarkAJ, InwoodW, CloutierT, DhillonTS (2001) Nucleotide sequence of coliphage HK620 and the evolution of lambdoid phages. J Mol Biol 311: 657–679.
21. HatfullGF, HendrixRW (2011) Bacteriophages and their genomes. Curr Opin Virol 1: 298–303.
22. MurphyKC (2012) Phage recombinases and their applications. Adv Virus Res 83: 367–414.
23. KuzminovA (1999) Recombinational repair of DNA damage in Escherichia coli and bacteriophage lambda. Microbiol Mol Biol Rev 63: 751–813 table of contents.
24. ShenP, HuangHV (1986) Homologous recombination in Escherichia coli: dependence on substrate length and homology. Genetics 112: 441–457.
25. MajewskiJ, CohanFM (1999) DNA sequence similarity requirements for interspecific recombination in Bacillus. Genetics 153: 1525–1533.
26. LopesA, Amarir-BouhramJ, FaureG, PetitMA, GueroisR (2010) Detection of novel recombinases in bacteriophage genomes unveils Rad52, Rad51 and Gp2.5 remote homologs. Nucleic Acids Res 38: 3952–3962.
27. DubocH, RajcaS, RainteauD, BenarousD, MaubertMA, et al. (2013) Connecting dysbiosis, bile-acid dysmetabolism and gut inflammation in inflammatory bowel diseases. Gut 62: 531–539.
28. TurpinW, HumblotC, NoordineML, WrzosekL, TomasJ, et al. Behavior of lactobacilli isolated from fermented slurry (ben-saalga) in gnotobiotic rats. PLoS One 8: e57711.
29. LiXT, ThomasonLC, SawitzkeJA, CostantinoN, CourtDL (2013) Bacterial DNA polymerases participate in oligonucleotide recombination. Mol Microbiol 88: 906–920.
30. MuyrersJP, ZhangY, BuchholzF, StewartAF (2000) RecE/RecT and Redalpha/Redbeta initiate double-stranded break repair by specifically interacting with their respective partners. Genes Dev 14: 1971–1982.
31. HayesS, AsaiK, ChuAM, HayesC (2005) NinR- and red-mediated phage-prophage marker rescue recombination in Escherichia coli: recovery of a nonhomologous immlambda DNA segment by infecting lambdaimm434 phages. Genetics 170: 1485–1499.
32. CurtisFA, ReedP, WilsonLA, BowersLY, YeoRP, et al. (2011) The C-terminus of the phage lambda Orf recombinase is involved in DNA binding. J Mol Recognit 24: 333–340.
33. SawitzkeJA, StahlFW (1997) Roles for lambda Orf and Escherichia coli RecO, RecR and RecF in lambda recombination. Genetics 147: 357–369.
34. TarkowskiTA, MooneyD, ThomasonLC, StahlFW (2002) Gene products encoded in the ninR region of phage lambda participate in Red-mediated recombination. Genes Cells 7: 351–363.
35. SharplesGJ, CurtisFA, McGlynnP, BoltEL (2004) Holliday junction binding and resolution by the Rap structure-specific endonuclease of phage lambda. J Mol Biol 340: 739–751.
36. PoteeteAR (2004) Modulation of DNA repair and recombination by the bacteriophage lambda Orf function in Escherichia coli K-12. J Bacteriol 186: 2699–2707.
37. AsadulghaniM, OguraY, OokaT, ItohT, SawaguchiA, et al. (2009) The defective prophage pool of Escherichia coli O157: prophage-prophage interactions potentiate horizontal transfer of virulence determinants. PLoS Pathog 5: e1000408.
38. RuzinA, LindsayJ, NovickRP (2001) Molecular genetics of SaPI1–a mobile pathogenicity island in Staphylococcus aureus. Mol Microbiol 41: 365–377.
39. GalletR, ShaoY, WangIN (2009) High adsorption rate is detrimental to bacteriophage fitness in a biofilm-like environment. BMC Evol Biol 9: 241.
40. HendrixRW, DudaRL (1992) Bacteriophage lambda PaPa: not the mother of all lambda phages. Science 258: 1145–1148.
41. ThalerDS, StahlMM, StahlFW (1987) Double-chain-cut sites are recombination hotspots in the Red pathway of phage lambda. J Mol Biol 195: 75–87.
42. LiuX, JiangH, GuZ, RobertsJW (2013) High-resolution view of bacteriophage lambda gene expression by ribosome profiling. Proc Natl Acad Sci U S A 110: 11928–11933.
43. KolodnerR, HallSD, Luisi-DeLucaC (1994) Homologous pairing proteins encoded by the Escherichia coli recE and recT genes. Mol Microbiol 11: 23–30.
44. MillsS, ShanahanF, StantonC, HillC, CoffeyA, et al. (2013) Movers and shakers: influence of bacteriophages in shaping the mammalian gut microbiota. Gut Microbes 4: 4–16.
45. EllisHM, YuD, DiTizioT, CourtDL (2001) High efficiency mutagenesis, repair, and engineering of chromosomal DNA using single-stranded oligonucleotides. Proc Natl Acad Sci U S A 98: 6742–6746.
46. PoteeteAR, FentonAC, WangHR (2002) Recombination-promoting activity of the bacteriophage lambda Rap protein in Escherichia coli K-12. J Bacteriol 184: 4626–4629.
47. HollifieldWC, KaplanEN, HuangHV (1987) Efficient RecABC-dependent, homologous recombination between coliphage lambda and plasmids requires a phage ninR region gene. Mol Gen Genet 210: 248–255.
48. RotmanE, KouzminovaE, PlunkettG3rd, KuzminovA (2012) Genome of Enterobacteriophage Lula/phi80 and insights into its ability to spread in the laboratory environment. J Bacteriol 194: 6802–6817.
49. IyerLM, KooninEV, AravindL (2002) Classification and evolutionary history of the single-strand annealing proteins, RecT, Redbeta, ERF and RAD52. BMC Genomics 3: 8.
50. CampbellA (1994) Comparative molecular biology of lambdoid phages. Annu Rev Microbiol 48: 193–222.
51. BouchardJD, MoineauS (2000) Homologous recombination between a lactococcal bacteriophage and the chromosome of its host strain. Virology 270: 65–75.
52. DurmazE, KlaenhammerTR (2000) Genetic analysis of chromosomal regions of Lactococcus lactis acquired by recombinant lytic phages. Appl Environ Microbiol 66: 895–903.
53. HallSD, KolodnerRD (1994) Homologous pairing and strand exchange promoted by the Escherichia coli RecT protein. Proc Natl Acad Sci U S A 91: 3205–3209.
54. BobayLM, TouchonM, RochaEP (2013) Manipulating or superseding host recombination functions: a dilemma that shapes phage evolvability. PLoS Genet 9: e1003825.
55. SawitzkeJA, CostantinoN, LiXT, ThomasonLC, BubunenkoM, et al. (2011) Probing cellular processes with oligo-mediated recombination and using the knowledge gained to optimize recombineering. J Mol Biol 407: 45–59.
56. RadmanM, WagnerR (1993) DNA mismatch repair systems: mechanisms and applications in biotechnology. Biotechnol Genet Eng Rev 11: 357–366.
57. ElezM, RadmanM, MaticI (2007) The frequency and structure of recombinant products is determined by the cellular level of MutL. Proc Natl Acad Sci U S A 104: 8935–8940.
58. CostantinoN, CourtDL (2003) Enhanced levels of lambda Red-mediated recombinants in mismatch repair mutants. Proc Natl Acad Sci U S A 100: 15748–15753.
59. PoteeteAR (2001) What makes the bacteriophage lambda Red system useful for genetic engineering: molecular mechanism and biological function. FEMS Microbiol Lett 201: 9–14.
60. PloquinM, BransiA, PaquetER, StasiakAZ, StasiakA, et al. (2008) Functional and structural basis for a bacteriophage homolog of human RAD52. Curr Biol 18: 1142–1146.
61. SokolH, SeksikP (2010) The intestinal microbiota in inflammatory bowel diseases: time to connect with the host. Curr Opin Gastroenterol 26: 327–331.
62. SokolH, VasquezN, Hoyeau-IdrissiN, SeksikP, BeaugerieL, et al. (2010) Crypt abscess-associated microbiota in inflammatory bowel disease and acute self-limited colitis. World J Gastroenterol 16: 583–587.
63. MottC, SymingtonLS (2011) RAD51-independent inverted-repeat recombination by a strand-annealing mechanism. DNA Repair (Amst) 10: 408–415.
64. WrzosekL, MiquelS, NoordineML, BouetS, Chevalier-CurtMJ, et al. (2013) Bacteroides thetaiotaomicron and Faecalibacterium prausnitzii influence the production of mucus glycans and the development of goblet cells in the colonic epithelium of a gnotobiotic model rodent. BMC Biol 11: 61.
65. CourtDL, SawitzkeJA, ThomasonLC (2002) Genetic engineering using homologous recombination. Annu Rev Genet 36: 361–388.
66. PoteeteAR (2008) Involvement of DNA replication in phage lambda Red-mediated homologous recombination. Mol Microbiol 68: 66–74.
67. MarescaM, ErlerA, FuJ, FriedrichA, ZhangY, et al. (2010) Single-stranded heteroduplex intermediates in lambda Red homologous recombination. BMC Mol Biol 11: 54.
68. MosbergJA, LajoieMJ, ChurchGM (2010) Lambda red recombineering in Escherichia coli occurs through a fully single-stranded intermediate. Genetics 186: 791–799.
69. NoirotP, KolodnerRD (1998) DNA strand invasion promoted by Escherichia coli RecT protein. J Biol Chem 273: 12274–12280.
70. RybalchenkoN, GolubEI, BiB, RaddingCM (2004) Strand invasion promoted by recombination protein beta of coliphage lambda. Proc Natl Acad Sci U S A 101: 17056–17060.
71. MontagD, SchwarzH, HenningU (1989) A component of the side tail fiber of Escherichia coli bacteriophage lambda can functionally replace the receptor-recognizing part of a long tail fiber protein of the unrelated bacteriophage T4. J Bacteriol 171: 4378–4384.
72. Haggard-LjungquistE, HallingC, CalendarR (1992) DNA sequences of the tail fiber genes of bacteriophage P2: evidence for horizontal transfer of tail fiber genes among unrelated bacteriophages. J Bacteriol 174: 1462–1477.
73. SandmeierH, IidaS, ArberW (1992) DNA inversion regions Min of plasmid p15B and Cin of bacteriophage P1: evolution of bacteriophage tail fiber genes. J Bacteriol 174: 3936–3944.
74. SandmeierH (1994) Acquisition and rearrangement of sequence motifs in the evolution of bacteriophage tail fibres. Mol Microbiol 12: 343–350.
75. ChopinA, BolotinA, SorokinA, EhrlichSD, ChopinM (2001) Analysis of six prophages in Lactococcus lactis IL1403: different genetic structure of temperate and virulent phage populations. Nucleic Acids Res 29: 644–651.
76. MiquelS, MartinR, RossiO, Bermudez-HumaranLG, ChatelJM, et al. (2013) Faecalibacterium prausnitzii and human intestinal health. Curr Opin Microbiol 16: 255–261.
77. LongM, BetranE, ThorntonK, WangW (2003) The origin of new genes: glimpses from the young and old. Nat Rev Genet 4: 865–875.
78. SorekR, LawrenceCM, WiedenheftB (2013) CRISPR-mediated Adaptive Immune Systems in Bacteria and Archaea. Annu Rev Biochem 82: 237–66.
79. LwoffA (1953) Lysogeny. Bacteriol Rev 17: 269–337.
80. BrussowH, CanchayaC, HardtWD (2004) Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol Mol Biol Rev 68: 560–602 table of contents.
81. PanisG, FrancheN, MejeanV, AnsaldiM (2012) Insights into the functions of a prophage recombination directionality factor. Viruses 4: 2417–2431.
82. WangX, KimY, MaQ, HongSH, PokusaevaK, et al. (2010) Cryptic prophages help bacteria cope with adverse environments. Nat Commun 1: 147.
83. RabinovichL, SigalN, BorovokI, Nir-PazR, HerskovitsAA (2012) Prophage Excision Activates Listeria Competence Genes that Promote Phagosomal Escape and Virulence. Cell 150: 792–802.
84. DatsenkoKA, WannerBL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97: 6640–6645.
85. BabaT, AraT, HasegawaM, TakaiY, OkumuraY, et al. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2: 2006 0008.
86. GorisJ, KonstantinidisKT, KlappenbachJA, CoenyeT, VandammeP, et al. (2007) DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57: 81–91.
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